More stories

  • in

    The genomic basis of the plant island syndrome in Darwin’s giant daisies

    Darwin, C. On the origin of species by means of natural selection, or, The preservation of favoured races in the struggle for life. (1859).Wallace, A. R. The Malay Archipelago: The Land of the Orang-utan and the Bird of Paradise; a Narrative of Travel, with Studies of Man and Nature (Courier Corporation, 1962).Mayr, E. Systematics and the Origin of Species from the Viewpoint of a Zoologist (Columbia Uni. Press, 1942).Emerson, B. C. Speciation on islands: what are we learning? Biol. J. Linn. Soc. Lond. 95, 47–52 (2008).
    Google Scholar 
    Lomolino, M. V., Riddle, B. R., Whittaker, R. J., Brown, J. H. & Lomolino, M. V. Biogeography (Sunderland, Mass: Sinauer Associates, 2017).Baeckens, S. & Van Damme, R. The island syndrome. Curr. Biol. 30, R338–R339 (2020).CAS 

    Google Scholar 
    Burns, K. C. Evolution in Isolation: The Search for an Island Syndrome in Plants (Cambridge University Press, 2019).Blaschke, J. D. & Sanders, R. W. Preliminary insights into the phylogeny and speciation of scalesia (asteraceae), galápagos islands. J. Bot. Res. Inst. Tex. 3, 177–191 (2009).
    Google Scholar 
    Fernández-Mazuecos, M. et al. The radiation of Darwin’s giant daisies in the Galápagos Islands. Curr. Biol. 30, 4989–4998.e7 (2020).
    Google Scholar 
    Crawford, D. J. et al. Genetic diversity in Asteraceae endemic to oceanic islands: Baker’s Law and polyploidy. Syst. Evol. Biogeogr. Compos 139, 151 (2009).
    Google Scholar 
    Eliasson, U. Studies in Galápagos plants. XIV. The genus Scalesia Arn. Opera Bot. 36, 1–117 (1974).
    Google Scholar 
    Itow, S. Phytogeography and ecology of Scalesia (compositae) endemic to the Galapagos islands! Pac. Sci. 49, 17–30 (1995).
    Google Scholar 
    Stöcklin, J. Darwin and the plants of the Galápagos-Islands. Bauhinia 21, 33–48 (2009).
    Google Scholar 
    Ono, M. Chromosome number of Scalesia (Compositae), an endemic genus of the Galapagos Islands. J. Jpn. Bot. 42, 353–360 (1967).
    Google Scholar 
    Eliasson, U. Studies in Galapagos plants. XIV. The genus Scalesia Arn. Opera Bot. 36, 1–117 (1974).
    Google Scholar 
    Meudt, H. M. et al. Polyploidy on islands: its emergence and importance for diversification. Front. Plant Sci. 12, 637214 (2021).PubMed Central 

    Google Scholar 
    Spring, O., Heil, N. & Vogler, B. Sesquiterpene lactones and flavanones in Scalesia species. Phytochemistry 46, 1369–1373 (1997).CAS 

    Google Scholar 
    Schilling, E. E., Panero, J. L. & Eliasson, U. H. Evidence from chloroplast DNA restriction site analysis on the relationships of Scalesia (Asteraceae: Heliantheae). Am. J. Bot. 81, 248–254 (1994).
    Google Scholar 
    Peona, V., Weissensteiner, M. H. & Suh, A. How complete are ‘complete’ genome assemblies?-An avian perspective. Mol. Ecol. Resour. 18, 1188–1195 (2018).CAS 

    Google Scholar 
    Badouin, H. et al. The sunflower genome provides insights into oil metabolism, flowering and Asterid evolution. Nature 546, 148–152 (2017).ADS 
    CAS 

    Google Scholar 
    Reyes-Chin-Wo, S. et al. Genome assembly with in vitro proximity ligation data and whole-genome triplication in lettuce. Nat. Commun. 8, 14953 (2017).ADS 
    CAS 
    PubMed Central 

    Google Scholar 
    Bellinger, M. R., Datlof, E., Selph, K. E., Gallaher, T. J. & Knope, M. L. A genome for Bidens hawaiensis: a member of a hexaploid Hawaiian plant adaptive radiation. J. Hered. https://doi.org/10.1093/jhered/esab077 (2022).Edger, P. P., McKain, M. R., Bird, K. A. & VanBuren, R. Subgenome assignment in allopolyploids: challenges and future directions. Curr. Opin. Plant Biol. 42, 76–80 (2018).CAS 

    Google Scholar 
    Session, A. M. et al. Genome evolution in the allotetraploid frog Xenopus laevis. Nature 538, 336–343 (2016).ADS 
    CAS 
    PubMed Central 

    Google Scholar 
    Mitros, T. et al. Genome biology of the paleotetraploid perennial biomass crop Miscanthus. Nat. Commun. 11, 5442 (2020).ADS 
    CAS 
    PubMed Central 

    Google Scholar 
    Funk, V. A. Systematics, Evolution, and Biogeography of Compositae (International Association for Plant Taxonomy, 2009).Julca, I. et al. Genomic evidence for recurrent genetic admixture during the domestication of Mediterranean olive trees (Olea europaea L.). BMC Biol 18, 148 (2020).PubMed Central 

    Google Scholar 
    te Beest, M. et al. The more the better? The role of polyploidy in facilitating plant invasions. Ann Bot. 109, 19–45 (2012).
    Google Scholar 
    Mandel, J. R. et al. A fully resolved backbone phylogeny reveals numerous dispersals and explosive diversifications throughout the history of Asteraceae. Proc. Natl Acad. Sci. USA 116, 14083–14088 (2019).CAS 
    PubMed Central 

    Google Scholar 
    Whittaker, R. J., School of Geography Robert J Whittaker & Fernandez-Palacios, J. M. Island Biogeography: Ecology, Evolution, and Conservation (OUP Oxford, 2007).Diop, S. I. et al. A pseudomolecule-scale genome assembly of the liverwort Marchantia polymorpha. Plant J. 101, 1378–1396 (2020).CAS 

    Google Scholar 
    Li, F.-W. et al. Anthoceros genomes illuminate the origin of land plants and the unique biology of hornworts. Nat. Plants 6, 259–272 (2020).CAS 
    PubMed Central 

    Google Scholar 
    Lang, D. et al. ThePhyscomitrella patenschromosome-scale assembly reveals moss genome structure and evolution. Plant J. 93, 515–533 (2018).CAS 

    Google Scholar 
    Bird, K. A., VanBuren, R., Puzey, J. R. & Edger, P. P. The causes and consequences of subgenome dominance in hybrids and recent polyploids. N. Phytol. 220, 87–93 (2018).
    Google Scholar 
    Freeling, M., Scanlon, M. J. & Fowler, J. E. Fractionation and subfunctionalization following genome duplications: mechanisms that drive gene content and their consequences. Curr. Opin. Genet. Dev. 35, 110–118 (2015).CAS 

    Google Scholar 
    Wolfe, K. H. Yesterday’s polyploids and the mystery of diploidization. Nat. Rev. Genet. 2, 333–341 (2001).CAS 

    Google Scholar 
    Bird, K. A. et al. Replaying the evolutionary tape to investigate subgenome dominance in allopolyploid Brassica napus. N. Phytol. 230, 354–371 (2021).CAS 

    Google Scholar 
    Alger, E. I. & Edger, P. P. One subgenome to rule them all: underlying mechanisms of subgenome dominance. Curr. Opin. Plant Biol. 54, 108–113 (2020).CAS 

    Google Scholar 
    Renny-Byfield, S., Gong, L., Gallagher, J. P. & Wendel, J. F. Persistence of subgenomes in paleopolyploid cotton after 60 my of evolution. Mol. Biol. Evol. 32, 1063–1071 (2015).CAS 

    Google Scholar 
    Douglas, G. M. et al. Hybrid origins and the earliest stages of diploidization in the highly successful recent polyploid Capsella bursa-pastoris. Proc. Natl Acad. Sci. USA 112, 2806–2811 (2015).ADS 
    CAS 
    PubMed Central 

    Google Scholar 
    Barrier, M., Baldwin, B. G., Robichaux, R. H. & Purugganan, M. D. Interspecific hybrid ancestry of a plant adaptive radiation: allopolyploidy of the Hawaiian silversword alliance (Asteraceae) inferred from floral homeotic gene duplications. Mol. Biol. Evol. 16, 1105–1113 (1999).CAS 

    Google Scholar 
    Catchen, J. M., Conery, J. S. & Postlethwait, J. H. Automated identification of conserved synteny after whole-genome duplication. Genome Res. 19, 1497–1505 (2009).CAS 
    PubMed Central 

    Google Scholar 
    Őszi, E. et al. E2FB interacts with RETINOBLASTOMA RELATED and regulates cell proliferation during leaf development. Plant Physiol. 182, 518–533 (2020).
    Google Scholar 
    Berckmans, B. et al. Light-dependent regulation of DEL1 is determined by the antagonistic action of E2Fb and E2Fc. Plant Physiol. 157, 1440–1451 (2011).CAS 
    PubMed Central 

    Google Scholar 
    Kojima, S. et al. Asymmetric leaves2 and Elongator, a histone acetyltransferase complex, mediate the establishment of polarity in leaves of Arabidopsis thaliana. Plant Cell Physiol. 52, 1259–1273 (2011).CAS 

    Google Scholar 
    Husbands, A. Y., Benkovics, A. H., Nogueira, F. T. S., Lodha, M. & Timmermans, M. C. P. The ASYMMETRIC LEAVES complex employs multiple modes of regulation to affect adaxial-abaxial patterning and leaf complexity. Plant Cell 27, 3321–3335 (2016).
    Google Scholar 
    Crane, R. A. et al. Negative regulation of age-related developmental leaf senescence by the IAOx pathway, PEN1, and PEN3. Front. Plant Sci. 10, 1202 (2019).PubMed Central 

    Google Scholar 
    Fu, M. et al. AtWDS1 negatively regulates age-dependent and dark-induced leaf senescence in Arabidopsis. Plant Sci. 285, 44–54 (2019).CAS 

    Google Scholar 
    Zhang, B., Jia, J., Yang, M., Yan, C. & Han, Y. Overexpression of a LAM domain containing RNA-binding protein LARP1c induces precocious leaf senescence in Arabidopsis. Mol. Cells 34, 367–374 (2012).PubMed Central 

    Google Scholar 
    Ma, Z., Wu, W., Huang, W. & Huang, J. Down-regulation of specific plastid ribosomal proteins suppresses thf1 leaf variegation, implying a role of THF1 in plastid gene expression. Photosynth. Res. 126, 301–310 (2015).CAS 

    Google Scholar 
    Wang, Z. et al. Two chloroplast proteins suppress drought resistance by affecting ROS production in guard cells. Plant Physiol. 172, 2491–2503 (2016).CAS 
    PubMed Central 

    Google Scholar 
    Meurer, J. et al. PALE CRESS binds to plastid RNAs and facilitates the biogenesis of the 50S ribosomal subunit. Plant J. 92, 400–413 (2017).CAS 

    Google Scholar 
    Holding, D. The chloroplast and leaf developmental mutant, pale cress, exhibits light-conditional severity and symptoms characteristic of its ABA deficiency. Ann. Bot. 86, 953–962 (2000).CAS 

    Google Scholar 
    Meurer, J., Grevelding, C., Westhoff, P. & Reiss, B. The PAC protein affects the maturation of specific chloroplast mRNAs in Arabidopsis thaliana. Mol. Gen. Genet. MGG 258, 342–351 (1998).CAS 

    Google Scholar 
    Lawesson, J. E. Stand-level dieback and regeneration of forests in the Galápagos Islands. Temporal and Spatial Patterns of Vegetation Dynamics 87–93. https://doi.org/10.1007/978-94-009-2275-4_10 (1988).Endo, M., Kudo, D., Koto, T., Shimizu, H. & Araki, T. Light-dependent destabilization of PHL in Arabidopsis. Plant Signal. Behav. 9, e28118 (2014).PubMed Central 

    Google Scholar 
    Endo, M., Tanigawa, Y., Murakami, T., Araki, T. & Nagatani, A. PHYTOCHROME-DEPENDENT LATE-FLOWERING accelerates flowering through physical interactions with phytochrome B and CONSTANS. Proc. Natl Acad. Sci. USA 110, 18017–18022 (2013).ADS 
    CAS 
    PubMed Central 

    Google Scholar 
    Li, G. et al. Coordinated transcriptional regulation underlying the circadian clock in Arabidopsis. Nat. Cell Biol. 13, 616–622 (2011).CAS 

    Google Scholar 
    Basset, G. J. C. et al. Folate synthesis in plants: the last step of the p-aminobenzoate branch is catalyzed by a plastidial aminodeoxychorismate lyase. Plant J. 40, 453–461 (2004).CAS 

    Google Scholar 
    Smeekens, S. Faculty Opinions recommendation of Large-scale analysis of mRNA translation states during sucrose starvation in arabidopsis cells identifies cell proliferation and chromatin structure as targets of translational control. Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature. https://doi.org/10.3410/f.1032260.373846 (2006).Oravecz, A. et al. CONSTITUTIVELY PHOTOMORPHOGENIC1 is required for the UV-B response in Arabidopsis. Plant Cell 18, 1975–1990 (2006).CAS 
    PubMed Central 

    Google Scholar 
    Dal Bosco, C. et al. Inactivation of the chloroplast ATP synthase gamma subunit results in high non-photochemical fluorescence quenching and altered nuclear gene expression in Arabidopsis thaliana. J. Biol. Chem. 279, 1060–1069 (2004).CAS 

    Google Scholar 
    Tan, Y.-F., O’Toole, N., Taylor, N. L. & Millar, A. H. Divalent metal ions in plant mitochondria and their role in interactions with proteins and oxidative stress-induced damage to respiratory function. Plant Physiol. 152, 747–761 (2010).CAS 
    PubMed Central 

    Google Scholar 
    Kim, J. Y. et al. Functional characterization of a glycine-rich RNA-binding protein 2 in Arabidopsis thaliana under abiotic stress conditions. Plant J. 50, 439–451 (2007).CAS 

    Google Scholar 
    ten Hove, C. A. et al. Probing the roles of LRR RLK genes in Arabidopsis thaliana roots using a custom T-DNA insertion set. Plant Mol. Biol. 76, 69–83 (2011).PubMed Central 

    Google Scholar 
    Jakoby, M. J. et al. Transcriptional profiling of mature Arabidopsis trichomes reveals that NOECK encodes the MIXTA-like transcriptional regulator MYB106. Plant Physiol. 148, 1583–1602 (2008).CAS 
    PubMed Central 

    Google Scholar 
    Fox, A. R. et al. Plasma membrane aquaporins interact with the endoplasmic reticulum resident VAP27 proteins at ER-PM contact sites and endocytic structures. N. Phytol. 228, 973–988 (2020).CAS 

    Google Scholar 
    Wang, P. et al. Plant AtEH/Pan1 proteins drive autophagosome formation at ER-PM contact sites with actin and endocytic machinery. Nat. Commun. 10, 5132 (2019).ADS 
    PubMed Central 

    Google Scholar 
    Bittner, A., Hause, B. & Baier, M. Cold-priming causes oxylipin dampening during the early cold and light response of Arabidopsis thaliana. J. Exp. Bot. https://doi.org/10.1093/jxb/erab314 (2021).Kuki, Y., Ohno, R., Yoshida, K. & Takumi, S. Heterologous expression of wheat WRKY transcription factor genes transcriptionally activated in hybrid necrosis strains alters abiotic and biotic stress tolerance in transgenic Arabidopsis. Plant Physiol. Biochem. 150, 71–79 (2020).CAS 

    Google Scholar 
    Czarnocka, W. et al. FMO1 is involved in excess light stress-induced signal transduction and cell death signaling. Cells 9, 2163 (2020).Kleine, T., Kindgren, P., Benedict, C., Hendrickson, L. & Strand, A. Genome-wide gene expression analysis reveals a critical role for CRYPTOCHROME1 in the response of Arabidopsis to high irradiance. Plant Physiol. 144, 1391–1406 (2007).CAS 
    PubMed Central 

    Google Scholar 
    Castells, E. et al. The conserved factor DE-ETIOLATED 1 cooperates with CUL4-DDB1DDB2 to maintain genome integrity upon UV stress. EMBO J. 30, 1162–1172 (2011).CAS 
    PubMed Central 

    Google Scholar 
    Lahari, T., Lazaro, J., Marcus, J. M. & Schroeder, D. F. RAD7 homologues contribute to Arabidopsis UV tolerance. Plant Sci. 277, 267–277 (2018).CAS 

    Google Scholar 
    Kim, A. et al. Non-intrinsic ATP-binding cassette proteins ABCI19, ABCI20 and ABCI21 modulate cytokinin response at the endoplasmic reticulum in Arabidopsis thaliana. Plant Cell Rep. 39, 473–487 (2020).CAS 
    PubMed Central 

    Google Scholar 
    Chen, D., Molitor, A., Liu, C. & Shen, W.-H. The Arabidopsis PRC1-like ring-finger proteins are necessary for repression of embryonic traits during vegetative growth. Cell Res. 20, 1332–1344 (2010).CAS 

    Google Scholar 
    Shen, L. et al. The putative PRC1 RING-finger protein AtRING1A regulates flowering through repressing MADS AFFECTING FLOWERING genes in Arabidopsis. Development 141, 1303–1312 (2014).CAS 

    Google Scholar 
    Li, J., Wang, Z., Hu, Y., Cao, Y. & Ma, L. Polycomb group proteins RING1A and RING1B regulate the vegetative phase transition in Arabidopsis. Front. Plant Sci. 8, 867 (2017).PubMed Central 

    Google Scholar 
    An, Z. et al. The histone methylation readers MRG1/MRG2 and the histone chaperones NRP1/NRP2 associate in fine-tuning Arabidopsis flowering time. Plant J. 103, 1010–1024 (2020).CAS 

    Google Scholar 
    Gómez-Zambrano, Á. et al. Arabidopsis SWC4 binds DNA and recruits the SWR1 complex to modulate histone H2A.Z deposition at key regulatory genes. Mol. Plant 11, 815–832 (2018).
    Google Scholar 
    Glass, M., Barkwill, S., Unda, F. & Mansfield, S. D. Endo-β−1,4-glucanases impact plant cell wall development by influencing cellulose crystallization. J. Integr. Plant Biol. 57, 396–410 (2015).CAS 

    Google Scholar 
    Markakis, M. N. et al. Identification of genes involved in the ACC-mediated control of root cell elongation in Arabidopsis thaliana. BMC Plant Biol. 12, 1–11 (2012).Noutoshi, Y. et al. Loss of necrotic spotted lesions 1 associates with cell death and defense responses in Arabidopsis thaliana. Plant Mol. Biol. 62, 29–42 (2006).CAS 

    Google Scholar 
    Fukunaga, S. et al. Dysfunction of Arabidopsis MACPF domain protein activates programmed cell death via tryptophan metabolism in MAMP-triggered immunity. Plant J. 89, 381–393 (2017).CAS 

    Google Scholar 
    Singh, S., Kailasam, S., Lo, J. & Yeh, K. Histone H3 lysine4 trimethylation‐regulated GRF11 expression is essential for the iron‐deficiency response in Arabidopsis thaliana. N. Phytologist 230, 244–258 (2021).CAS 

    Google Scholar 
    Fal, K. et al. Phyllotactic regularity requires the Paf1 complex in Arabidopsis. Development https://doi.org/10.1242/dev.154369 (2017).He, Y. PAF1-complex-mediated histone methylation of FLOWERING LOCUS C chromatin is required for the vernalization-responsive, winter-annual habit in Arabidopsis. Genes Dev. 18, 2774–2784 (2004).CAS 
    PubMed Central 

    Google Scholar 
    Hoson, T. et al. Growth stimulation in inflorescences of an Arabidopsis tubulin mutant under microgravity conditions in space. Plant Biol. 16, 91–96 (2014).
    Google Scholar 
    Xiong, X., Xu, D., Yang, Z., Huang, H. & Cui, X. A single amino-acid substitution at lysine 40 of an Arabidopsis thaliana α-tubulin causes extensive cell proliferation and expansion defects. J. Integr. Plant Biol. 55, 209–220 (2013).CAS 

    Google Scholar 
    Whitewoods, C. D. et al. CLAVATA was a genetic novelty for the morphological innovation of 3D growth in land plants. Curr. Biol. 30, 2645–2648 (2020).CAS 
    PubMed Central 

    Google Scholar 
    Galbraith, D. W. et al. Rapid flow cytometric analysis of the cell cycle in intact plant tissues. Science 220, 1049–1051 (1983).ADS 
    CAS 

    Google Scholar 
    Dolezel, J., Sgorbati, S. & Lucretti, S. Comparison of three DNA fluorochromes for flow cytometric estimation of nuclear DNA content in plants. Physiologia Plant. 85, 625–631 (1992).CAS 

    Google Scholar 
    Loureiro, J., Rodriguez, E., Dolezel, J. & Santos, C. Two new nuclear isolation buffers for plant DNA flow cytometry: a test with 37 species. Ann. Bot. 100, 875–888 (2007).CAS 
    PubMed Central 

    Google Scholar 
    Suda, J. et al. Genome size variation and species relationships in Hieracium sub-genus Pilosella (Asteraceae) as inferred by flow cytometry. Ann. Bot. 100, 1323–1335 (2007).PubMed Central 

    Google Scholar 
    Greilhuber, J., Dolezel, J., Lysák, M. A. & Bennett, M. D. The origin, evolution and proposed stabilization of the terms ‘genome size’ and ‘C-value’ to describe nuclear DNA contents. Ann. Bot. 95, 255–260 (2005).CAS 
    PubMed Central 

    Google Scholar 
    Dolezel, J., Bartos, J., Voglmayr, H. & Greilhuber, J. Nuclear DNA content and genome size of trout and human. Cytom. Part A: J. Int. Soc. Anal. Cytol. 51, 127–128 (2003).CAS 

    Google Scholar 
    Putnam, N. H. et al. Chromosome-scale shotgun assembly using an in vitro method for long-range linkage. Genome Res. 26, 342–350 (2016).CAS 
    PubMed Central 

    Google Scholar 
    Ruan, J. & Li, H. Fast and accurate long-read assembly with wtdbg2. Nat. Methods 17, 155–158 (2020).CAS 

    Google Scholar 
    Laetsch, D. R. & Blaxter, M. L. BlobTools: Interrogation of genome assemblies. F1000Res. 6, 1287 (2017).
    Google Scholar 
    Guan, D. et al. Identifying and removing haplotypic duplication in primary genome assemblies. Bioinformatics 36, 2896–2898 (2020).CAS 
    PubMed Central 

    Google Scholar 
    Bradnam, K. R. et al. Assemblathon 2: evaluating de novo methods of genome assembly in three vertebrate species. Gigascience 2, 10 (2013).PubMed Central 

    Google Scholar 
    Smit, A., Hubley, R. & Green, P. RepeatMasker 4.0 (Institute for Systems Biology, 2013).Flynn, J. M. et al. RepeatModeler2 for automated genomic discovery of transposable element families. Proc. Natl Acad. Sci. USA 117, 9451–9457 (2020).CAS 
    PubMed Central 

    Google Scholar 
    Tardaguila, M. et al. Corrigendum: SQANTI: extensive characterization of long-read transcript sequences for quality control in full-length transcriptome identification and quantification. Genome Res. 28, 1096 (2018).CAS 
    PubMed Central 

    Google Scholar 
    Holt, C. & Yandell, M. MAKER2: an annotation pipeline and genome-database management tool for second-generation genome projects. BMC Bioinforma. 12, 491 (2011).
    Google Scholar 
    Moore, B., Holt, C., Alvarado, A. S. & Yandell, M. MAKER: an easy-to-use annotation pipeline designed for emerging model organism genomes. Genome 18, 188–196 (2008).Parra, G., Bradnam, K. & Korf, I. CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics 23, 1061–1067 (2007).CAS 

    Google Scholar 
    Korf, I. Gene finding in novel genomes. BMC Bioinforma. 5, 59 (2004).
    Google Scholar 
    Keller, O., Kollmar, M., Stanke, M. & Waack, S. A novel hybrid gene prediction method employing protein multiple sequence alignments. Bioinformatics 27, 757–763 (2011).CAS 

    Google Scholar 
    Simão, F. A., Waterhouse, R. M., Ioannidis, P., Kriventseva, E. V. & Zdobnov, E. M. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31, 3210–3212 (2015).
    Google Scholar 
    Waterhouse, R. M. et al. BUSCO applications from quality assessments to gene prediction and phylogenomics. Mol. Biol. Evol. 35, 543–548 (2018).CAS 

    Google Scholar 
    Seppey, M., Manni, M. & Zdobnov, E. M. BUSCO: assessing genome assembly and annotation completeness. Methods Mol. Biol. 1962, 227–245 (2019).CAS 

    Google Scholar 
    Andrews, S. FastQC: A Quality Control Tool for High Throughput Sequence Data [Online]. Available online at: http://www.bioinformatics.babraham.ac.uk/projects/fastqc/ (2010).Schubert, M., Lindgreen, S. & Orlando, L. AdapterRemoval v2: rapid adapter trimming, identification, and read merging. BMC Res. Notes 9, 88 (2016).PubMed Central 

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

    Google Scholar 
    Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754–1760 (2009).CAS 
    PubMed Central 

    Google Scholar 
    Li, H. & Durbin, R. Inference of human population history from individual whole-genome sequences. Nature 475, 493–496 (2011).CAS 
    PubMed Central 

    Google Scholar 
    Danecek, P. et al. Twelve years of SAMtools and BCFtools. Gigascience 10, giab008 (2021).Mandel, J. R. et al. A target enrichment method for gathering phylogenetic information from hundreds of loci: an example from the Compositae. Appl. Plant Sci. 2, 1300085 (2014).Faircloth, B. C. PHYLUCE is a software package for the analysis of conserved genomic loci. Bioinformatics 32, 786–788 (2016).CAS 

    Google Scholar 
    Faircloth, B. C. et al. Ultraconserved elements anchor thousands of genetic markers spanning multiple evolutionary timescales. Syst. Biol. 61, 717–726 (2012).
    Google Scholar 
    Marçais, G. & Kingsford, C. A fast, lock-free approach for efficient parallel counting of occurrences of k-mers. Bioinformatics 27, 764–770 (2011).PubMed Central 

    Google Scholar 
    Delcher, A. L. et al. Alignment of whole genomes. Nucleic Acids Res. 27, 2369–2376 (1999).CAS 
    PubMed Central 

    Google Scholar 
    Kurtz, S. et al. Versatile and open software for comparing large genomes. Genome Biol. 5, R12 (2004).PubMed Central 

    Google Scholar 
    Krzywinski, M. et al. Circos: an information aesthetic for comparative genomics. Genome Res. 19, 1639–1645 (2009).CAS 
    PubMed Central 

    Google Scholar 
    Allen, M., Poggiali, D., Whitaker, K., Marshall, T. R. & Kievit, R. A. Raincloud plots: a multi-platform tool for robust data visualization. Wellcome Open Res. 4, 63 (2019).PubMed Central 

    Google Scholar 
    Hao, Z. et al. RIdeogram: drawing SVG graphics to visualize and map genome-wide data on the idiograms. PeerJ Comput Sci. 6, e251 (2020).PubMed Central 

    Google Scholar 
    Laforest, M. et al. A chromosome-scale draft sequence of the Canada fleabane genome. Pest Manag. Sci. 76, 2158–2169 (2020).CAS 

    Google Scholar 
    Liu, B. et al. Mikania micrantha genome provides insights into the molecular mechanism of rapid growth. Nat. Commun. 11, 340 (2020).ADS 
    CAS 
    PubMed Central 

    Google Scholar 
    Emms, D. M. & Kelly, S. OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol. 16, 157 (2015).PubMed Central 

    Google Scholar 
    Cerca, J. et al. The Tetragnatha kauaiensis genome sheds light on the origins of genomic novelty in spiders. Genome Biol. Evol. 13, evab262 (2021).Laetsch, D. R. & Blaxter, M. L. KinFin: software for taxon-aware analysis of clustered protein sequences. G3 7, 3349–3357 (2017).CAS 
    PubMed Central 

    Google Scholar 
    Conway, J. R., Lex, A. & Gehlenborg, N. UpSetR: an R package for the visualization of intersecting sets and their properties. Bioinformatics 33, 2938–2940 (2017).CAS 
    PubMed Central 

    Google Scholar 
    Sanderson, M. J. r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics 19, 301–302 (2003).CAS 

    Google Scholar 
    Lovell, J. T. et al. Genomic mechanisms of climate adaptation in polyploid bioenergy switchgrass. Nature 590, 438–444 (2021).ADS 
    CAS 
    PubMed Central 

    Google Scholar 
    Ellinghaus, D., Kurtz, S. & Willhoeft, U. LTRharvest, an efficient and flexible software for de novo detection of LTR retrotransposons. BMC Bioinforma. 9, 18 (2008).
    Google Scholar 
    Steinbiss, S., Willhoeft, U., Gremme, G. & Kurtz, S. Fine-grained annotation and classification of de novo predicted LTR retrotransposons. Nucleic Acids Res. 37, 7002–7013 (2009).CAS 
    PubMed Central 

    Google Scholar 
    Eddy, S. HMMER user’s guide. Dep. Genet., Wash. Univ. Sch. Med. 2, 13 (1992).
    Google Scholar 
    Llorens, C. et al. The Gypsy Database (GyDB) of mobile genetic elements: release 2.0. Nucleic Acids Res. 39, D70–D74 (2011).CAS 

    Google Scholar 
    Castresana, J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17, 540–552 (2000).CAS 

    Google Scholar 
    Talavera, G. & Castresana, J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst. Biol. 56, 564–577 (2007).CAS 

    Google Scholar 
    De Bie, T., Cristianini, N., Demuth, J. P. & Hahn, M. W. CAFE: a computational tool for the study of gene family evolution. Bioinformatics 22, 1269–1271 (2006).
    Google Scholar 
    Mendes, F. K., Vanderpool, D., Fulton, B. & Hahn, M. W. CAFE 5 models variation in evolutionary rates among gene families. Bioinformatics https://doi.org/10.1093/bioinformatics/btaa1022 (2020).Jones, P. et al. InterProScan 5: genome-scale protein function classification. Bioinformatics 30, 1236–1240 (2014).CAS 
    PubMed Central 

    Google Scholar 
    Alexa, A. & Rahnenfuhrer, J. topGO: enrichment analysis for gene ontology. R. Package Version 2, 2010 (2010).
    Google Scholar 
    Alexa, A. & Rahnenführer, J. Gene set enrichment analysis with topGO. Bioconductor Improv 27, 1–26 (2009).
    Google Scholar 
    Supek, F., Bošnjak, M., Škunca, N. & Šmuc, T. REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS ONE 6, e21800 (2011).ADS 
    CAS 
    PubMed Central 

    Google Scholar 
    Löytynoja, A. Phylogeny-aware alignment with PRANK. Methods Mol. Biol. 1079, 155–170 (2014).
    Google Scholar 
    Wu, M., Chatterji, S. & Eisen, J. A. Accounting for alignment uncertainty in phylogenomics. PLoS ONE 7, e30288 (2012).ADS 
    CAS 
    PubMed Central 

    Google Scholar 
    Smith, M. D. et al. Less is more: an adaptive branch-site random effects model for efficient detection of episodic diversifying selection. Mol. Biol. Evol. 32, 1342–1353 (2015).CAS 
    PubMed Central 

    Google Scholar 
    Pond, S. L. K., Frost, S. D. W. & Muse, S. V. HyPhy: hypothesis testing using phylogenies. Bioinformatics 21, 676–679 (2005).CAS 

    Google Scholar 
    Szklarczyk, D. et al. STRING v10: protein-protein interaction networks, integrated over the tree of life. Nucleic Acids Res. 43, D447–D452 (2015).CAS 

    Google Scholar  More

  • in

    Unique metabolism of different glucosinolates in larvae and adults of a leaf beetle specialised on Brassicaceae

    War, A. R. et al. Mechanisms of plant defense against insect herbivores. Plant Signal. Behav. 7, 1306–1320 (2012).Article 

    Google Scholar 
    Pentzold, S., Zagrobelny, M., Roelsgaard, P. S., Møller, B. L. & Bak, S. The multiple strategies of an insect herbivore to overcome plant cyanogenic glucoside defence. PLoS ONE 9, e91337. https://doi.org/10.1371/journal.pone.0091337 (2014).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Abdalsamee, M. K., Giampa, M., Niehaus, K. & Müller, C. Rapid incorporation of glucosinolates as a strategy used by a herbivore to prevent activation by myrosinases. Insect Biochem. Mol. Biol. 52, 115–123. https://doi.org/10.1016/j.ibmb.2014.07.002 (2014).CAS 
    Article 
    PubMed 

    Google Scholar 
    Winde, I. & Wittstock, U. Insect herbivore counteradaptations to the plant glucosinolate-myrosinase system. Phytochemistry 72, 1566–1575. https://doi.org/10.1016/j.phytochem.2011.01.016 (2011).CAS 
    Article 
    PubMed 

    Google Scholar 
    Sporer, T., Körnig, J. & Beran, F. Ontogenetic differences in the chemical defence of flea beetles influence their predation risk. Funct Ecol. 34, 1370–1379. https://doi.org/10.1111/1365-2435.13548 (2020).Article 

    Google Scholar 
    Hammer, T. J. & Moran, N. A. Links between metamorphosis and symbiosis in holometabolous insects. Philos. Trans. R. Soc. B-Biol. Sci. 374, 20190068. https://doi.org/10.1098/rstb.2019.0068 (2019).CAS 
    Article 

    Google Scholar 
    Wäckers, F. L., Romeis, J. & van Rijn, P. Nectar and pollen feeding by insect herbivores and implications for multitrophic interactions. Annu. Rev. Entomol. 52, 301–323. https://doi.org/10.1146/annurev.ento.52.110405.091352 (2007).CAS 
    Article 
    PubMed 

    Google Scholar 
    Altermatt, F. & Pearse, I. S. Similarity and specialization of the larval versus adult diet of european butterflies and moths. Am. Nat. 178, 372–382. https://doi.org/10.1086/661248 (2011).Article 
    PubMed 

    Google Scholar 
    Hammer, T. J., McMillan, W. O. & Fierer, N. Metamorphosis of a butterfly-associated bacterial community. PLoS ONE 9, e86995. https://doi.org/10.1371/journal.pone.0086995 (2014).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Shukla, S. P., Sanders, J. G., Byrne, M. J. & Pierce, N. E. Gut microbiota of dung beetles correspond to dietary specializations of adults and larvae. Mol. Ecol. 25, 6092–6106. https://doi.org/10.1111/mec.13901 (2016).CAS 
    Article 
    PubMed 

    Google Scholar 
    Blažević, I. et al. Glucosinolate structural diversity, identification, chemical synthesis and metabolism in plants. Phytochemistry 169, 112100. https://doi.org/10.1016/j.phytochem.2019.112100 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    Halkier, B. A. & Gershenzon, J. Biology and biochemistry of glucosinolates. Annu. Rev. Plant Biol. 57, 303–333. https://doi.org/10.1146/annurev.arplant.57.032905.105228 (2006).CAS 
    Article 
    PubMed 

    Google Scholar 
    Wittstock, U., Kurzbach, E., Herfurth, A. M. & Stauber, E. J. Glucosinolate breakdown. Adv. Botanical Res. – Glucosinolates 80, 125–169. https://doi.org/10.1016/bs.abr.2016.06.006 (2016).CAS 
    Article 

    Google Scholar 
    Jeschke, V., Gershenzon, J. & Vassão, D. G. in Glucosinolates Vol. 80 Advances in Botanical Research (ed S. Kopriva), 199–245 (2016).Sun, R. et al. Tritrophic metabolism of plant chemical defenses and its effects on herbivore and predator performance. eLife 9, e51029, doi:https://doi.org/10.7554/eLife.51029 (2019).Malka, O. et al. Glucosinolate desulfation by the phloem-feeding insect Bemisia tabaci. J. Chem. Ecol. 42, 230–235. https://doi.org/10.1007/s10886-016-0675-1 (2016).CAS 
    Article 
    PubMed 

    Google Scholar 
    Schramm, K., Vassão, D. G., Reichelt, M., Gershenzon, J. & Wittstock, U. Metabolism of glucosinolate-derived isothiocyanates to glutathione conjugates in generalist lepidopteran herbivores. Insect Biochem. Mol. Biol. 42, 174–182. https://doi.org/10.1016/j.ibmb.2011.12.002 (2012).CAS 
    Article 
    PubMed 

    Google Scholar 
    Beran, F. et al. Phyllotreta striolata flea beetles use host plant defense compounds to create their own glucosinolate-myrosinase system. Proc. Natl. Acad. Sci. USA 111, 7349–7354. https://doi.org/10.1073/pnas.1321781111 (2014).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Beran, F. et al. One pathway is not enough: The cabbage stem flea beetle Psylliodes chrysocephala uses multiple strategies to overcome the glucosinolate-myrosinase defense in its host plants. Front. Plant Sci. 9, 1754. https://doi.org/10.3389/fpls.2018.01754 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Müller, C. et al. Sequestration of host plant glucosinolates in the defensive hemolymph of the sawfly Athalia rosae. J. Chem. Ecol. 27, 2505–2516 (2001).Article 

    Google Scholar 
    Ratzka, A., Vogel, H., Kliebenstein, D. J., Mitchell-Olds, T. & Kroymann, J. Disarming the mustard oil bomb. Proc. Natl. Acad. Sci. USA. 99, 11223–11228 (2002).ADS 
    CAS 
    Article 

    Google Scholar 
    Wittstock, U. et al. Successful herbivore attack due to metabolic diversion of a plant chemical defense. Proc. Natl. Acad. Sci. USA. 101, 4859–4864 (2004).ADS 
    CAS 
    Article 

    Google Scholar 
    Falk, K. L. & Gershenzon, J. The desert locust, Schistocerca gregaria, detoxifies the glucosinolates of Schouwia purpurea by desulfation. J. Chem. Ecol. 33, 1542–1555. https://doi.org/10.1007/s10886-007-9331-0 (2007).CAS 
    Article 
    PubMed 

    Google Scholar 
    Vanhaelen, N., Haubruge, E., Lognay, G. & Francis, F. Hoverfly glutathione S-transferases and effect of Brassicaceae secondary metabolites. Pestic. Biochem. Phys. 71, 170–177 (2001).CAS 
    Article 

    Google Scholar 
    Friedrichs, J. et al. Novel glucosinolate metabolism in larvae of the leaf beetle Phaedon cochleariae. Insect Biochem. Mol. Biol. 124, 103431. https://doi.org/10.1016/j.ibmb.2020.103431 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    Reifenrath, K., Riederer, M. & Müller, C. Leaf surface wax layers of Brassicaceae lack feeding stimulants for Phaedon cochleariae. Entomol. Exp. Appl. 115, 41–50 (2005).CAS 
    Article 

    Google Scholar 
    Cataldi, T. R. I., Lelario, F., Orlando, D. & Bufo, S. A. Collision-induced dissociation of the A+2 isotope ion facilitates glucosinolates structure elucidation by electrospray Ionization-Tandem Mass Spectrometry with a linear Quadrupole Ion Trap. Anal. Chem. 82, 5686–5696. https://doi.org/10.1021/ac100703w (2010).CAS 
    Article 
    PubMed 

    Google Scholar 
    Cataldi, T. R. I., Rubino, A., Lelario, F. & Bufo, S. A. Naturally occuring glucosinolates in plant extracts of rocket salad (Eruca sativa L.) identified by liquid chromatography coupled with negative ion electrospray ionization and quadrupole ion-trap mass spectrometry. Rapid Commun. Mass Spectrom. 21, 2374–2388, doi:https://doi.org/10.1002/rcm.3101 (2007).Yang, Z. L., Kunert, G., Sporer, T., Kornig, J. & Beran, F. Glucosinolate abundance and composition in Brassicaceae influence sequestration in a specialist flea beetle. J. Chem. Ecol. 46, 186–197. https://doi.org/10.1007/s10886-020-01144-y (2020).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Smirnoff, N. Ascorbic acid metabolism and functions: a comparison of plants and mammals. Free Radical Biol. and Medic. 122, 116–129. https://doi.org/10.1016/j.freeradbiomed.2018.03.033 (2018).CAS 
    Article 

    Google Scholar 
    Agerbirk, N., De Vos, M., Kim, J. H. & Jander, G. Indole glucosinolate breakdown and its biological effects. Phytochem. Rev. 8, 101–120. https://doi.org/10.1007/s11101-008-9098-0 (2009).CAS 
    Article 

    Google Scholar 
    Goggin, F. L., Avila, C. A. & Lorence, A. Vitamin C content in plants is modified by insects and influences susceptibility to herbivory. BioEssays 32, 777–790. https://doi.org/10.1002/bies.200900187 (2010).CAS 
    Article 
    PubMed 

    Google Scholar 
    Kim, J. H., Lee, B. W., Schroeder, F. C. & Jander, G. Identification of indole glucosinolate breakdown products with antifeedant effects on Myzus persicae (green peach aphid). Plant J. 54, 1015–1026 (2008).CAS 
    Article 

    Google Scholar 
    Liu, T. T. & Yang, T. S. Stability and antimicrobial activity of allyl isothiocyanate during long-term storage in an oil-in-water emulsion. J. Food Sci. 75, C445–C451. https://doi.org/10.1111/j.1750-3841.2010.01645.x (2010).CAS 
    Article 
    PubMed 

    Google Scholar 
    Luang-In, V. & Rossiter, J. T. Stability studies of isothiocyanates and nitriles in aqueous media. Songklanakarin J. Sci. Technol. 37, 625–630 (2015).CAS 

    Google Scholar 
    Tsao, R., Yu, Q., Friesen, I., Potter, J. & Chiba, M. Factors affecting the dissolution and degradation of oriental mustard-derived sinigrin and allyl isothiocyanate in aqueous media. J. Agric. Food Chem. 48, 1898–1902. https://doi.org/10.1021/jf9906578 (2000).CAS 
    Article 
    PubMed 

    Google Scholar 
    Brodbeck, B. & Strong, D. in Insect Outbreaks (eds P. Barbosa & J. C. Schultz) Ch. 14, 347–363 (Academic Press, INC., 1987).Kumar, V. et al. Differential distribution of amino acids in plants. Amino Acids 49, 821–869. https://doi.org/10.1007/s00726-017-2401-x (2017).CAS 
    Article 
    PubMed 

    Google Scholar 
    Millar, K. A., Gallagher, E., Burke, R., McCarthy, S. & Barry-Ryan, C. Proximate composition and anti-nutritional factors of fava-bean (Vicia faba), green-pea and yellow-pea (Pisum sativum) flour. J. Food Compos. Anal. 82, doi:https://doi.org/10.1016/j.jfca.2019.103233 (2019).Miller, R. W., McGrew, C., Wolff, I. A., Jones, Q. & Vanetten, C. H. Seed meal amino acids – amino acid composition of seed meals from 41 species of Cruciferae. J. Agric. Food Chem. 10, 426-430. https://doi.org/10.1021/jf60123a023 (1962).Article 

    Google Scholar 
    Fischer, W. N. et al. Low and high affinity amino acid H+-cotransporters for cellular import of neutral and charged amino acids. Plant J. 29, 717–731. https://doi.org/10.1046/j.1365-313X.2002.01248.x (2002).CAS 
    Article 
    PubMed 

    Google Scholar 
    Lea, P. J., Sodek, L., Parry, M. A. J., Shewry, R. & Halford, N. G. Asparagine in plants. Ann. Appl. Biol. 150, 1–26. https://doi.org/10.1111/j.1744-7348.2006.00104.x (2007).CAS 
    Article 

    Google Scholar 
    Leroy, P. D. et al. Aphid-host plant interactions: does aphid honeydew exactly reflect the host plant amino acid composition? Arthropod-Plant Inte. 5, 193–199. https://doi.org/10.1007/s11829-011-9128-5 (2011).Article 

    Google Scholar 
    Shukla, S. P. & Beran, F. Gut microbiota degrades toxic isothiocyanates in a flea beetle pest. Mol. Ecol. 29, 4692–4705. https://doi.org/10.1111/mec.15657 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    Angelino, D. et al. Myrosinase-dependent and -independent formation and control of isothiocyanate products of glucosinolate hydrolysis. Front. Plant Sci. 6, 831. https://doi.org/10.3389/fpls.2015.00831 (2015).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Liou, C. S. et al. A metabolic pathway for activation of dietary glucosinolates by a human gut symbiont. Cell 180, 717–729. https://doi.org/10.1016/j.cell.2020.01.023 (2020).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Liu, X. J. et al. Dietary broccoli alters rat cecal microbiota to improve glucoraphanin hydrolysis to bioactive isothiocyanates. Nutrients 9, 262. https://doi.org/10.3390/nu9030262 (2017).CAS 
    Article 
    PubMed Central 

    Google Scholar 
    Sikorska-Zimny, K. & Beneduce, L. The metabolism of glucosinolates by gut microbiota. Nutrients 13, 2750. https://doi.org/10.3390/nu13082750 (2021).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Müller, C., Vogel, H. & Heckel, D. G. Transcriptional responses to short-term and long-term host plant experience and parasite load in an oligophagous beetle. Mol. Ecol. 26, 6370–6383. https://doi.org/10.1111/mec.14349 (2017).CAS 
    Article 
    PubMed 

    Google Scholar 
    Rueckert, S., Betts, E. L. & Tsaousis, A. D. The symbiotic spectrum: where do the gregarines fit? Trends Parasitol. 35, 687–694. https://doi.org/10.1016/j.pt.2019.06.013 (2019).Article 
    PubMed 

    Google Scholar 
    Kühnle, A. & Müller, C. Responses of an oligophagous beetle species to rearing for several generations on alternative host plant species. Ecol. Entomol. 36, 125–134. https://doi.org/10.1111/j.1365-2311.2010.01256.x (2011).Article 

    Google Scholar 
    Sporer, T. et al. Hijacking the mustard-oil bomb: How a glucosinolate-sequestering flea beetle copes with plant myrosinases. Front. Plant Sci. 12, 645030. https://doi.org/10.3389/fpls.2021.645030 (2021).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Kallenbach, M. et al. A robust, simple, high-throughput technique for time-resolved plant volatile analysis in field experiments. Plant J. 78, 1060–1072. https://doi.org/10.1111/tpj.12523 (2014).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Kallenbach, M., Veit, D., Eilers, E. J. & Schuman, M. C. Application of silicone tubing for robust, simple, high-throughput, and time-resolved analysis of plant volatiles in field experiments. Bioprotocol 5, e1391 (2015).
    Google Scholar 
    Ruttkies, C., Schymanski, E. L., Wolf, S., Hollender, J. & Neumann, S. MetFrag relaunched: incorporating strategies beyond in silico fragmentation. J. Cheminf. 8, 3. https://doi.org/10.1186/s13321-016-0115-9 (2016).CAS 
    Article 

    Google Scholar 
    Kováts, E. Characterization of organic compounds by gas chromatography. Part 1. Retention indices of aliphatic halides, alcohols, aldehydes and ketones. Helv. Chim. Acta 41, 1915–1932, doi:https://doi.org/10.1002/hlca.19580410703 (1958).El-Sayed, A. M. The Pherobase: Database of Pheromones and Semiochemicals. (2012).McDanell, R., McLean, A. E. M., Hanley, A. B., Heaney, R. K. & Fenwick, G. R. Chemical and biological properties of indole glucosinolates (glucobrassicins): a review. Food Chem. Toxicol. 26, 59–70. https://doi.org/10.1016/0278-6915(88)90042-7 (1988).CAS 
    Article 
    PubMed 

    Google Scholar 
    Weber, G., Oswald, S. & Zöllner, U. Suitability of rapae cultivars with a different glucosinolate content for Brevicoryne brassicae (L) and Myzus persicae (Sulzer) (Hemiptera, Aphididae). Z. Pflanzenk. Pflanzenschutz 93, 113–124 (1986).CAS 

    Google Scholar 
    Wadleigh, R. W. & Yu, S. J. Detoxification of isothiocynante allelochemicals by glutathione transferase in three lepidopterous species. J. Chem. Ecol. 14, 1279–1288. https://doi.org/10.1007/bf01019352 (1988).CAS 
    Article 
    PubMed 

    Google Scholar 
    Francis, F., Lognay, G., Wathelet, J. P. & Haubruge, E. Effects of allelochemicals from first (Brassicaceae) and second (Myzus persicae and Brevicoryne brassicae) trophic levels on Adalia bipunctata. J. Chem. Ecol. 27, 243–256. https://doi.org/10.1023/A:1005672220342 (2001).CAS 
    Article 
    PubMed 

    Google Scholar 
    Aliabadi, A., Renwick, J. A. A. & Whitman, D. W. Sequestration of glucosinolates by harlequin bug Murgantia histrionica. J. Chem. Ecol. 28, 1749–1762. https://doi.org/10.1023/a:1020505016637 (2002).CAS 
    Article 
    PubMed 

    Google Scholar 
    Bridges, M. et al. Spatial organization of the glucosinolate-myrosinase system in brassica specialist aphids is similar to that of the host plant. Proc. R. Soc. B-Biol. Sci. 269, 187–191. https://doi.org/10.1098/rspb.2001.1861 (2002).CAS 
    Article 

    Google Scholar 
    Müller, C., Agerbirk, N. & Olsen, C. E. Lack of sequestration of host plant glucosinolates in Pieris rapae and P. brassicae. Chemoecology 13, 47–54, doi: https://doi.org/10.1007/s000490300005 (2003).Francis, F., Vanhaelen, N. & Haubruge, E. Glutathione S-transferases in the adaptation to plant secondary metabolites in the Myzus persicae aphid. Arch. Insect Biochem. Physiol. 58, 166–174. https://doi.org/10.1002/arch.20049 (2005).CAS 
    Article 
    PubMed 

    Google Scholar 
    Müller, C. & Wittstock, U. Uptake and turn-over of glucosinolates sequestered in the sawfly Athalia rosae. Insect Biochem. Mol. Biol. 35, 1189–1198. https://doi.org/10.1016/j.ibmb.2005.06.001 (2005).CAS 
    Article 
    PubMed 

    Google Scholar 
    Agerbirk, N., Müller, C., Olsen, C. E. & Chew, F. S. A common pathway for metabolism of 4-hydroxybenzylglucosinolate in Pieris and Anthocaris (Lepidoptera: Pieridae). Biochem. Syst. Ecol. 34, 189–198. https://doi.org/10.1016/j.bse.2005.09.005 (2006).CAS 
    Article 

    Google Scholar 
    Vergara, F. et al. Glycine conjugates in a lepidopteran insect herbivore: the metabolism of benzylglucosinolate in the cabbage white butterfly Pieris rapae. ChemBioChem 7, 1982–1989. https://doi.org/10.1002/cbic.200600280 (2006).Article 
    PubMed 

    Google Scholar 
    Agerbirk, N., Olsen, C. E., Topbjerg, H. B. & Sørensen, J. C. Host plant-dependent metabolism of 4-hydroxybenzylglucosinolate in Pieris rapae: Substrate specificity and effects of genetic modification and plant nitrile hydratase. Insect Biochem. Mol. Biol. 37, 1119–1130. https://doi.org/10.1016/j.ibmb.2007.06.009 (2007).CAS 
    Article 
    PubMed 

    Google Scholar 
    Kazana, E. et al. The cabbage aphid: a walking mustard oil bomb. Proc. R. Soc. B-Biol. Sci. 274, 2271–2277 (2007).CAS 
    Article 

    Google Scholar 
    Agerbirk, N., Olsen, C. E., Poulsen, E., Jacobsen, N. & Hansen, P. R. Complex metabolism of aromatic glucosinolates in Pieris rapae caterpillars involving nitrile formation, hydroxylation, demethylation, sulfation, and host plant dependent carboxylic acid formation. Insect Biochem. Mol. Biol. 40, 126–137. https://doi.org/10.1016/j.ibmb.2010.01.003 (2010).CAS 
    Article 
    PubMed 

    Google Scholar 
    Opitz, S. E. W., Jensen, S. R. & Muller, C. Sequestration of glucosinolates and iridoid glucosides in sawfly species of the genus Athalia and their role in defense against ants. J. Chem. Ecol. 36, 148–157. https://doi.org/10.1007/s10886-010-9740-3 (2010).CAS 
    Article 
    PubMed 

    Google Scholar 
    Opitz, S. E. W., Mix, A., Winde, I. B. & Müller, C. Desulfation followed by sulfation: metabolism of benzylglucosinolate in Athalia rosae (Hymenoptera: Tenthredinidae). ChemBioChem 12, 1252–1257. https://doi.org/10.1002/cbic.201100053 (2011).CAS 
    Article 
    PubMed 

    Google Scholar 
    Elbaz, M. et al. Asymmetric adaptation to indolic and aliphatic glucosinolates in the B and Q sibling species of Bemisia tabaci (Hemiptera: Aleyrodidae). Mol. Ecol. 21, 4533–4546. https://doi.org/10.1111/j.1365-294X.2012.05713.x (2012).CAS 
    Article 
    PubMed 

    Google Scholar 
    Opitz, S. E. W. et al. Host shifts from Lamiales to Brassicaceae in the sawfly genus Athalia. PLoS ONE 7, e33649. https://doi.org/10.1371/journal.pone.0033649 (2012).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Stauber, E. J. et al. Turning the “Mustard oil bomb” into a “Cyanide bomb”: aromatic glucosinolate metabolism in a specialist insect herbivore. PLoS ONE 7, e35545. https://doi.org/10.1371/journal.pone.0035545 (2012).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Gloss, A. D. et al. Evolution in an ancient detoxification pathway is coupled with a transition to herbivory in the Drosophilidae. Mol. Biol. Evol. 31, 2441–2456. https://doi.org/10.1093/molbev/msu201 (2014).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Goodey, N. A., Florance, H. V., Smirnoff, N. & Hodgson, D. J. Aphids pick their poison: selective sequestration of plant chemicals affects host plant use in a specialist herbivore. J. Chem. Ecol. 41, 956–964. https://doi.org/10.1007/s10886-015-0634-2 (2015).CAS 
    Article 
    PubMed 

    Google Scholar 
    Jeschke, V. et al. How glucosinolates affect generalist lepidopteran larvae: growth, development and glucosinolate metabolism. Front. Plant Sci. 8, doi:https://doi.org/10.3389/fpls.2017.01995 (2017).Steiner, A. M., Busching, C., Vogel, H. & Wittstock, U. Molecular identification and characterization of rhodaneses from the insect herbivore Pieris rapae. Sci. Rep. 8, 10819. https://doi.org/10.1038/s41598-018-29148-5 (2018).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ahn, S. J. et al. Identification and evolution of glucosinolate sulfatases in a specialist flea beetle. Sci. Rep. 9, 15725. https://doi.org/10.1038/s41598-019-51749-x (2019).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Malka, O. et al. Glucosylation prevents plant defense activation in phloem-feeding insects. Nat. Chem. Biol. 16, 1420–1426. https://doi.org/10.1038/s41589-020-00658-6 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    Sun, R. et al. Detoxification of plant defensive glucosinolates by an herbivorous caterpillar is beneficial to its endoparasitic wasp. Mol. Ecol. 29, 4014–4031. https://doi.org/10.1111/mec.15613 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    Manivannan, A. et al. Identification of a sulfatase that detoxifies glucosinolates in the phloem-feeding insect Bemisia tabaci and prefers indolic glucosinolates. Front. Plant Sci. 12, 671286. https://doi.org/10.3389/fpls.2021.671286 (2021).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Yang, Z. L. et al. Sugar transporters enable a leaf beetle to accumulate plant defense compounds. Nat. Commun. 12, 2658. https://doi.org/10.1038/s41467-021-22982-8 (2021).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar  More

  • in

    Natural forest growth and human induced ecosystem disturbance influence water yield in forests

    Forest complexity increases hydrological resistance to disturbancesIn general, natural forests, old forests, forests with high coverage, and forests located in low aridity regions (P/PET ≥ 1) are characterized by higher ecosystem complexity than planted forests, young forests, forests with low coverage, and forests located in arid regions (P/PET  More

  • in

    Manure amendment can reduce rice yield loss under extreme temperatures

    Zhu, C. et al. Carbon dioxide (CO2) levels this century will alter the protein, micronutrients, and vitamin content of rice grains with potential health consequences for the poorest rice-dependent countries. Sci. Adv. 4, eaaq1012 (2018).
    Google Scholar 
    Alexandratos, N. & Bruinsma, J. World Agriculture Towards 2030/2050: The 2012 Revision (FAO Agricultural Development Economics Division, 2012).Arunrat, N., Pumijumnong, N., Sereenonchai, S., Chareonwong, U. & Wang, C. Assessment of climate change impact on rice yield and water footprint of large-scale and individual farming in Thailand. Sci. Total Environ. 726, 137864 (2020).CAS 

    Google Scholar 
    Lafferty, D. C. et al. Statistically bias-corrected and downscaled climate models underestimate the adverse effects of extreme heat on U.S. maize yields. Commun. Earth Environ. 2, 196 (2021).
    Google Scholar 
    Davis, K. F., Downs, S. & Gephart, J. A. Towards food supply chain resilience to environmental shocks. Nat. Food. 2, 54–65 (2021).
    Google Scholar 
    Wang, X. et al. Emergent constraint on crop yield response to warmer temperature from field experiments. Nat. Sustain. 3, 908–916 (2020).
    Google Scholar 
    Sun, T. et al. Current rice models underestimate yield losses from short-term heat stresses. Glob. Chang. Biol. 27, 402–416 (2020).
    Google Scholar 
    Challinor, A. J. et al. A meta-analysis of crop yield under climate change and adaptation. Nat. Clim. Chang. 4, 287–291 (2014).
    Google Scholar 
    Iizumi, T. & Ramankutty, N. Changes in yield variability of major crops for 1981–2010 explained by climate change. Environ. Res. Lett. 11, 034003 (2016).
    Google Scholar 
    Ray, D. K., Ramankutty, N., Mueller, N. D., West, P. C. & Foley, J. A. Recent patterns of crop yield growth and stagnation. Nat. Commun. 3, 1293 (2012).
    Google Scholar 
    Amelung, W. et al. Towards a global-scale soil climate mitigation strategy. Nat. Commun. 11, 1–10 (2020).
    Google Scholar 
    Mueller, N. D. et al. Closing yield gaps through nutrient and water management. Nature 494, 390 (2013).CAS 

    Google Scholar 
    Chen, X. et al. Producing more grain with lower environmental costs. Nature 514, 486–489 (2014).CAS 

    Google Scholar 
    Zhang, X. et al. Managing nitrogen for sustainable development. Nature 528, 51–59 (2015).CAS 

    Google Scholar 
    Guo, J. et al. Significant acidification in major Chinese croplands. Science 327, 1008–1010 (2010).CAS 

    Google Scholar 
    Galloway, J. et al. Transformation of the nitrogen cycle: Recent trends, questions, and potential solutions. Science 320, 889–892 (2008).CAS 

    Google Scholar 
    Xia, L., Lam, S. K., Yan, X. & Chen, D. How does recycling of livestock manure in agroecosystems affect crop productivity, reactive nitrogen losses, and soil carbon balance? Environ. Sci. Technol. 51, 7450–7457 (2017).CAS 

    Google Scholar 
    Zhang, T. et al. Replacing synthetic fertilizer by manure requires adjusted technology and incentives: A farm survey across China. Resour. Conserv. Recycl. 168, 105301 (2021).
    Google Scholar 
    Bi, L. et al. Long-term effects of organic amendments on the rice yields for double rice cropping systems in subtropical China. Agric. Ecosyst. Environ. 129, 534–541 (2009).
    Google Scholar 
    Du, Y. et al. Effects of manure fertilizer on crop yield and soil properties in China: A meta-analysis. Catena 193, 104617 (2020).CAS 

    Google Scholar 
    Wang, K., Zhang, X. & Ervin, E. Antioxidative responses in roots and shoots of creeping bentgrass under high temperature: Effects of nitrogen and cytokinin. J. Plant Physiol. 169, 492–500 (2012).CAS 

    Google Scholar 
    Jespersen, D. & Huang, B. Proteins associated with heat‐induced leaf senescence in creeping bentgrass as affected by foliar application of nitrogen, cytokinins, and an ethylene inhibitor. Proteomics. 15, 798–812 (2015).CAS 

    Google Scholar 
    Xi, Y. et al. Exogenous phosphite application alleviates the adverse effects of heat stress and improves thermotolerance of potato (Solanum tuberosum L.) seedlings. Ecotoxicol. Environ. Saf. 190, 110048 (2020).CAS 

    Google Scholar 
    Waraich, E. A., Ahmad, R., Halim, A. & Aziz, T. Alleviation of temperature stress by nutrient management in crop plants: a review. J. Soil Sci. Plant Nut. 12, 221–244 (2012).
    Google Scholar 
    Yamori, W., Noguchi, K., Hikosaka, K. & Terashima, I. Phenotypic plasticity in photosynthetic temperature acclimation among crop species with different cold tolerances. Plant Physiol. 152, 388–399 (2010).CAS 

    Google Scholar 
    Mittler, R. Oxidative stress, antioxidants and stress tolerance. Trends. Plant Sci. 7, 405–410 (2002).CAS 

    Google Scholar 
    Wang, Q., Chen, J., He, N. & Guo, F. Metabolic reprogramming in chloroplasts under heat stress in plants. Int. J. Mol. Sci. 19, 849 (2018).
    Google Scholar 
    Cheng, Q. et al. An alternatively spliced heat shock transcription factor, OsHSFA2dI, functions in the heat stress-induced unfolded protein response in rice. Plant Biol. 17, 419–429 (2015).CAS 

    Google Scholar 
    Miura, K. et al. SIZ1-mediated sumoylation of ICE1 controls CBF3/DREB1A expression and freezing tolerance in Arabidopsis. Plant Cell 19, 1403–1414 (2007).CAS 

    Google Scholar 
    Xie, G., Kato, H., Sasaki, K. & Imai, R. A cold-induced thioredoxin h of rice, OsTrx23, negatively regulates kinase activities of OsMPK3 and OsMPK6 in vitro. FEBS Lett. 583, 2734–2738 (2009).CAS 

    Google Scholar 
    Hasanuzzaman, M., Hossain, M. A. & Fujita, M. Nitric oxide modulates antioxidant defense and the methylglyoxal detoxification system and reduces salinity-induced damage of wheat seedlings. Plant Biotechnol. Rep. 5, 353 (2011).
    Google Scholar 
    Uchida, A., Jagendorf, A. T., Hibino, T., Takabe, T. & Takabe, T. Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Sci. 163, 515–523 (2002).CAS 

    Google Scholar 
    Khan, S. et al. Plants mechanisms and adaptation strategies to improve heat tolerance in rice. A review. Plants 8, 508 (2019).CAS 

    Google Scholar 
    Li, Y., Gao, Y., Xu, X., Shen, Q. & Guo, S. Light-saturated photosynthetic rate in high-nitrogen rice (Oryza sativa L.) leaves is related to chloroplastic CO2 concentration. J. Exp. Bot. 60, 2351–2360 (2009).CAS 

    Google Scholar 
    Xiong, D. et al. Rapid responses of mesophyll conductance to changes of CO2 concentration, temperature, and irradiance are affected by N supplements in rice. Plant. Cell Environ. 38, 2541–2550 (2015).CAS 

    Google Scholar 
    Waraich, E. A., Ahmad, R., Ashraf, M. Y., Saifullah & Ahmad, M. Improving agricultural water use effciency by nutrient management in crop plants. Acta Agric. Scand. Sect.-B Soil. Plant Sci. 61, 291–304 (2011).CAS 

    Google Scholar 
    Dias, A. S. & Lidon, F. C. Bread and durum wheat tolerance under heat stress: A synoptical overview. Emir. J. Food Agric. 22, 412–436 (2010).
    Google Scholar 
    Meshah, E. A. E. Effect of irrigation regimes and foliar spraying of potassium on yield, yield components and water use efficiency of wheat in sandy soils. World J. Agric. Sci. 5, 662–669 (2009).
    Google Scholar 
    Huang, G., Zhang, Q., Wei, X., Peng, S. & Li, Y. Nitrogen can alleviate the inhibition of photosynthesis caused by high temperature stress under both steady-state and flecked irradiance. Front. Plant Sci. 8, 945 (2017).
    Google Scholar 
    Zhou, Y. et al. High nitrogen input reduces yield loss from low temperature during the seedling stage in early-season rice. Field Crop. Res. 228, 68–75 (2018).
    Google Scholar 
    Hou, L. et al. Effects of different phosphate fertilizer application on permeability of membrane and antioxidative enzymes in rice under low temperature stress. Acta Agriculturae. Boreali-Sinica 27, 118–123 (2012).
    Google Scholar 
    Dong, W. et al. Effect of different fertilizer application on the soil fertility of paddy soils in red soil region of southern China. PLoS One 7, e44504 (2012).CAS 

    Google Scholar 
    Bertollo, A. M. et al. Precrops alleviate soil physical limitations for soybean root growth in an Oxisol from southern Brazil. Soil Till. Res. 206, 104820 (2021).
    Google Scholar 
    Ren, Y. et al. Functional compensation dominates plant rhizosphere microbiota assembly of plant rhizospheric bacterial community. Soil Biol. Biochem. 150, 107968 (2020).CAS 

    Google Scholar 
    Oka, Y. Mechanisms of nematode suppression by organic soil amendments—a review. Appl. Soil Ecol. 44, 101–115 (2010).
    Google Scholar 
    Rose, M. T. et al. A meta-analysis and review of plant-growth response to humic substances: Practical implications for agriculture. Adv. Agron 124, 37–89 (2014).CAS 

    Google Scholar 
    García, A. C. et al. Vermicompost humic acids modulate the accumulation and metabolism of ROS in rice plants. J. Plant Physiol. 192, 56–63 (2016).
    Google Scholar 
    Dieleman, W. I. et al. Simple additive effects are rare: A quantitative review of plant biomass and soil process responses to combined manipulations of CO2 and temperature. Glob. Chang. Biol. 18, 2681–2693 (2012).
    Google Scholar 
    Muhammad, Q. et al. Yield sustainability, soil organic carbon sequestration, and nutrients balance under long-term combined application of manure and inorganic fertilizers in acidic paddy soil. Soil Till. Res. 198, 104509 (2020).
    Google Scholar 
    Zhang, X. et al. Benefits and trade-offs of replacing synthetic fertilizers by animal manures in crop production in China: A meta‐analysis. Glob. Chang. Biol. 26, 888–900 (2020).
    Google Scholar 
    Zhang, X. et al. Significant residual effects of wheat fertilization on greenhouse gas emissions in succeeding soybean growing season. Soil Till. Res. 169, 7–15 (2017).
    Google Scholar 
    Latare, A. M., Kumar, O., Singh, S. K. & Gupta, A. Direct and residual effect of sewage sludge on yield, heavy metals content and soil fertility under rice–wheat system. Ecol. Eng. 69, 17–24 (2014).
    Google Scholar 
    Zhang, J. et al. Long-term straw incorporation increases rice yield stability under high fertilization level conditions in the rice–wheat system. Crop J. 9, 1191–1197 (2021).
    Google Scholar 
    Pachauri, R. K. et al. Climate change 2014: Synthesis Report. Contribution of Working Groups I, II, and III to the fifth assessment report of the Intergovernmental Panel on Climate Change (IPCC, 2014).Choi, W. J., Lee, M. S., Choi, J. E., Yoon, S. & Kim, H. Y. How do weather extremes affect rice productivity in a changing climate? An answer to episodic lack of sunshine. Glob. Chang. Biol. 19, 1300–1310 (2013).
    Google Scholar 
    FAO. FAOSTAT Online Statistical Service. https://www.fao.org/faostat/en/#data/RFN, (FAO, 2016).Carlson, K. M. et al. Greenhouse gas emissions intensity of global croplands. Nat. Clim. Chang. 7, 63–68 (2017).CAS 

    Google Scholar 
    Sheldrick, W., Syers, J. K. & Lingard, J. Contribution of livestock excreta to nutrient balances. Nutr. Cycling Agroecosyst. 66, 119–131 (2003).
    Google Scholar 
    Thangarajan, R., Bolan, N. S., Tian, G., Naidu, R. & Kunhikrishnan, A. Role of organic amendment application on greenhouse gas emission from soil. Sci. Total Environ. 465, 72–96 (2013).CAS 

    Google Scholar 
    Aryal, J. P. et al. Factors affecting farmers’ use of organic and inorganic fertilizers in South Asia. Environ. Sci. Pollut. Res. 28, 51480–51496 (2021).CAS 

    Google Scholar 
    Zhang, Q. et al. Targeting hotspots to achieve sustainable nitrogen management in China’s smallholder-dominated cereal production. Agronomy 11, 557 (2021).
    Google Scholar 
    Tyagi, V. K. et al. Anaerobic co-digestion of organic fraction of municipal solid waste (OFMSW): Progress and challenges. Renewable Sustain. Energy Rev. 93, 380–399 (2018).
    Google Scholar 
    Schlesinger, W. H. Carbon sequestration in soils: Some cautions amidst optimism. Agric. Ecosyst. Environ. 82, 121–127 (2000).CAS 

    Google Scholar 
    Potter, P., Ramankutty, N., Bennett, E. M. & Donner, S. D. Characterizing the spatial patterns of global fertilizer application and manure production. Earth Interact. 14, 1–22 (2010).
    Google Scholar 
    Zhao, F., Yang, L., Chen, L., Li, S. & Sun, L. Bioaccumulation of antibiotics in crops under long-term manure application: Occurrence, biomass response, and human exposure. Chemosphere 219, 882–895 (2019).CAS 

    Google Scholar 
    Chadwick, D. R. et al. Strategies to reduce nutrient pollution from manure management in China. Front. Agr. Sci. Eng. 7, 45–55 (2020).
    Google Scholar 
    Jin, S. et al. Decoupling livestock and crop production at the household level in China. Nat. Sustain 4, 48–55 (2021).
    Google Scholar 
    Chen, D., Yuan, L., Liu, Y., Ji, J. & Hou, H. Long-term application of manures plus chemical fertilizers sustained high rice yield and improved soil chemical and bacterial properties. Eur. J. Agron. 90, 34–42 (2017).
    Google Scholar 
    Siddik, M. A. et al. Responses of indica rice yield and quality to extreme high and low temperatures during the reproductive period. Eur. J. Agron. 106, 30–38 (2019).
    Google Scholar 
    Bates, L. S., Waldren, R. P. & Teare, I. D. Rapid determination of free proline for water stress studies. Plant Soil 39, 205–207 (1973).CAS 

    Google Scholar 
    Page, A. L., Miller, R. H. & Dennis, R. K. Methods of Soil Analysis. Part 2 Chemical Methods (ed Page, A. L.) (Soil Science Society of America, 1982).Black, C. A. Methods of Soil Analysis Part II. Chemical and Microbiological Properties (ed Norman, A. G.) (American Society of Agriculture, 1965).Murphy, J. & Riley, J. P. A modified single solution method for the determination of phosphate in natural waters. Anal. Chim. Acta 27, 31–36 (1962).CAS 

    Google Scholar 
    Knudsen, D., Peterson, G. A. & Pratt, P. F. Methods of Soil Analysis. Part 2. Chemical and Microbiological Properties (ed Page, A. L.) (American Society of Agriculture, 1982).Olsen, S. R. Estimation of Available Phosphorus in Soils by Extraction with Sodium Bicarbonate (United States Department of Agriculture Circular, 1954).Lewis, S. L., Brando, P. M., Phillips, O. L., Van Der Heijden, G. M. F. & Nepstad, D. The 2010 amazon drought. Science 331, 554–554 (2011).CAS 

    Google Scholar 
    Hedges, L. V., Gurevitch, J. & Curtis, P. S. The meta‐analysis of response ratios in experimental ecology. Ecology 80, 1150–1156 (1999).
    Google Scholar 
    van Groenigen, K. J., Van Kessel, C. & Hungate, B. A. Increased greenhouse-gas intensity of rice production under future atmospheric conditions. Nat. Clim. Chang. 3, 288–291 (2013).
    Google Scholar 
    Monfreda, C., Ramankutty, N. & Foley, J. A. Farming the planet: 2. Geographic distribution of crop areas, yields, physiological types, and net primary production in the year 2000. Global Biogeochem. Cycles 22, GB1022 (2008).
    Google Scholar 
    Laborte, A. G. et al. RiceAtlas, a spatial database of global rice calendars and production. Sci. Data 4, 170074 (2017).
    Google Scholar  More

  • in

    Value wild animals’ carbon services to fill the biodiversity financing gap

    Pettorelli, N. et al. J. Appl. Ecol. 58, 2384–2393 (2021).Article 

    Google Scholar 
    CBD High-Level Panel Resourcing the Aichi Biodiversity Targets: An Assessment of Benefits, Investments and Resource Needs for Implementing the Strategic Plan for Biodiversity 2011–2020 (Secretariat of the Convention on Biological Diversity, 2014).Schmitz, O. J. et al. Science 362, eaar3213 (2018).Article 

    Google Scholar 
    Krause, T. & Nielsen, M. R. Forests 10, 344 (2019).Article 

    Google Scholar 
    Jørgensen, D. BioScience 63, 719–720 (2013).Article 

    Google Scholar 
    Berzaghi, F., Chami, R., Cosimano, T. & Fullenkamp, C. Proc. Natl Acad. Sci. USA 119, e2120426119 (2022).Article 

    Google Scholar 
    van Duuren, E., Plantinga, A. & Scholtens, B. J. Bus. Ethics 138, 525–533 (2016).Article 

    Google Scholar 
    Broadstock, D. C., Chan, K., Cheng, L. T. W. & Wang, X. Finance Res. Lett. 38, 101716 (2021).Article 

    Google Scholar 
    Joos, F., Meyer, R., Bruno, M. & Leuenberger, M. Geophys. Res. Lett. 26, 1437–1440 (1999).CAS 
    Article 

    Google Scholar 
    Wang, F. et al. Biol. Conserv. 253, 108913 (2021).Article 

    Google Scholar 
    Sullivan, S. Antipode 45, 198–217 (2013).Article 

    Google Scholar 
    Kamilaris, A., Cole, I. R. & Prenafeta-Boldú, F. X., in Food Technology Disruptions (ed. Galanakis, C. M.) 247–284 (Academic Press, 2021).O’Donnell, E. & Talbot-Jones, J. Ecol. Soc. 23, 7 (2018).Article 

    Google Scholar 
    Anderson, K. & Peters, G. Science 354, 182–183 (2016).CAS 
    Article 

    Google Scholar 
    Berzaghi, F. et al. Nat. Geosci. 12, 725–729 (2019).CAS 
    Article 

    Google Scholar 
    Mariani, G. et al. Sci. Adv. 6, eabb4848 (2020).CAS 
    Article 

    Google Scholar 
    Martin, A. H., Pearson, H. C., Saba, G. K. & Olsen, E. M. One Earth 4, 680–693 (2021).Article 

    Google Scholar 
    Durfort, A., Mariani, G., Troussellier, M., Tulloch, V. & Mouillot, D. Preprint at Research Square https://doi.org/10.21203/rs.3.rs-92037/v1 (2021).Norris, K., Terry, A., Hansford, J. P. & Turvey, S. T. Trends Ecol. Evol. 35, 919–926 (2020).Article 

    Google Scholar 
    Berzaghi, F. et al. Ecography 41, 1934–1954 (2018).Article 

    Google Scholar  More

  • in

    Regenerative living cities and the urban climate–biodiversity–wellbeing nexus

    CIAT Global Rural-Urban Mapping Project, v1 (GRUMPv1): Urban Extents Grid (NASA SEDAC, 2011).Global Status Report for Buildings and Construction: Towards a Zero-Emission, Efficient and Resilient Buildings and Construction Sector (UNEP, 2020).Harris, N. L. et al. Nat. Clim. Change 11, 234–240 (2021).Article 

    Google Scholar 
    Reid, W. V. et al. Ecosystems and Human Well-being: Biodiversity Synthesis (Millenium Ecosystem Assessment, World Resources Institute, 2005).Xu, C. et al. Resour. Conserv. Recycl. 151, 104478 (2019).Article 

    Google Scholar 
    Su, J., Friess, D. A. & Gasparatos, A. Nat. Commun. 12, 5050 (2021).CAS 
    Article 

    Google Scholar 
    van den Berg, M. et al. Urban For. Urban Green. 14, 806–816 (2015).Article 

    Google Scholar 
    Aerts, R., Honnay, O. & Van Nieuwenhuyse, A. Br. Med. Bull. 127, 5–22 (2018).Article 

    Google Scholar 
    Lindenmayer, D. et al. Ecol. Lett. 11, 78–91 (2008).
    Google Scholar 
    Knapp, S., Jaganmohan, M. & Schwarz, N. in Atlas of Ecosystem Services: Drivers, Risks, and Societal Responses (eds Schröter, M. et al.) 167–172 (Springer, 2019).Kim, H. Y. Geomat. Nat. Hazards Risk 12, 1181–1194 (2021).Article 

    Google Scholar 
    Vargas-Hernández, J. G., Pallagst, K. & Zdunek-Wielgołaska, J. in Handbook of Engaged Sustainability (ed. Marques, J.) 885–916 (Springer, 2018).Manso, M. et al. Renew. Sustain. Energy Rev. 135, 110111 (2021).Article 

    Google Scholar 
    Assimakopoulos, M.-N. et al. Sustainability 12, 3772 (2020).CAS 
    Article 

    Google Scholar 
    Mora-Melià, D. et al. Sustainability 10, 1130 (2018).Article 

    Google Scholar 
    IPBES. Curr. Opin. Environ. Sustain. 26, 7–16 (2017).
    Google Scholar 
    Schröpfer, T. & Menz, S. in Dense and Green Building Typologies: Research, Policy and Practice Perspectives (eds Schröpfer, T. & Menz, S.) 1–4 (Springer, 2019).Pedersen Zari, M. & Hecht, K. Biomimetics 5, 18 (2020).Article 

    Google Scholar  More

  • in

    Accounting for ecosystem service values in climate policy

    IPCC Climate Change 2007: Synthesis Report (eds Pachauri, R. K. & Reisinger, A.) (IPCC, 2007).Boyd, J. & Banzhaf, S. Ecol. Econ. 63, 616–626 (2007).Article 

    Google Scholar 
    Ruhl, J. B. et al. Front. Ecol. Environ. 19, 519–525 (2021).Article 

    Google Scholar 
    Carleton, T. & Greenstone, M. Updating the United States Government’s Social Cost of Carbon Working Paper 2021-04 (Univ. Chicago, Becker Friedman Institute for Economics, 2021).Mandle, L. et al. Nat. Sustain. 4, 161–169 (2021).Article 

    Google Scholar 
    Druckenmiller, H. Estimating an Economic and Social Value of Forests: Evidence from Tree Mortality in the American West (Univ. California Berkeley, 2021).Burkett, V. R. et al. Ecol. Complexity 2, 357–394 (2005).Article 

    Google Scholar 
    Hanley, N. & Czajkowski, M. Rev. Environ. Econ. Policy 13, 248–266 (2019).Article 

    Google Scholar 
    Mendelsohn, R. Rev. Environ. Econ. Policy 13, 267–282 (2019).Article 

    Google Scholar 
    Fenichel, E. P. et al. Proc. Natl Acad. Sci. USA 113, 2382–2387 (2016).CAS 
    Article 

    Google Scholar 
    Martin-Ortega, J. et al. Ecosyst. Serv. 50, 101327 (2021).Article 

    Google Scholar 
    Borrelli, P. et al. Proc. Natl Acad. Sci. USA 117, 21994–22001 (2020).CAS 
    Article 

    Google Scholar 
    Tropek, R. et al. Science 344, 981–981 (2014).CAS 
    Article 

    Google Scholar 
    Vardon, M., Burnett, P. & Dovers, S. Ecol. Econ. 124, 145–152 (2016).Article 

    Google Scholar 
    Bastien-Olvera, B. A. & Moore, F. C. Nat. Sustain. 4, 101–108 (2021).Article 

    Google Scholar 
    Beland, M. et al. For. Ecol. Manage. 450, 117484 (2019).Article 

    Google Scholar 
    Vargas, L., Willemen, L. & Hein, L. Environ. Manage. 63, 1–15 (2019).Article 

    Google Scholar 
    Hallgren, W. et al. Environ. Model. Softw. 76, 182–186 (2016).Article 

    Google Scholar 
    Rolf, E. et al. Nat. Commun. 12, 4392 (2021).CAS 
    Article 

    Google Scholar 
    Chernozhukov, V. et al. NBER Working Paper 24678 (National Bureau of Economic Research, 2018). More

  • in

    Network analysis suggests changes in food web stability produced by bottom trawl fishery in Patagonia

    Pauly, D. Anecdotes and the shifting baseline syndrome of fisheries. Trends Ecol. Evol. 10, 430 (1995).CAS 
    PubMed 

    Google Scholar 
    FAO. The State of World Fisheries and Aquaculture 2018—Meeting the Sustainable Development Goals. (2018).Teh, L. C. L. & Sumaila, U. R. Contribution of marine fisheries to worldwide employment. Fish Fish. 14, 77–88 (2013).
    Google Scholar 
    Halpern, B. S., Selkoe, K. A., Micheli, F. & Kappel, C. V. Evaluating and ranking the vulnerability of global marine ecosystems to anthropogenic threats. Conserv. Biol. 21, 1301–1315 (2007).PubMed 

    Google Scholar 
    Kaiser, M. J., Collie, J. S., Hall, S. J., Jennings, S. & Poiner, I. R. Modification of marine habitats by trawling activities: Prognosis and solutions. Fish Fish. 3, 114–136 (2002).
    Google Scholar 
    Hiddink, J. G. et al. Selection of indicators for assessing and managing the impacts of bottom trawling on seabed habitats. J. Appl. Ecol. 57, 1199–1209 (2020).
    Google Scholar 
    Funes, M., Marinao, C. & Galván, D. E. Does trawl fisheries affect the diet of fishes? A stable isotope analysis approach. Isotop. Environ. Health Stud. 10, 1–17 (2019).
    Google Scholar 
    Preciado, I. et al. Small-scale spatial variations of trawling impact on food web structure. Ecol. Ind. 98, 442–452 (2019).
    Google Scholar 
    Su, L. et al. Decadal-scale variation in mean trophic level in Beibu Gulf based on bottom-trawl survey data. Mar. Coast. Fish. 13, 174–182 (2021).
    Google Scholar 
    Jennings, S., van Hal, R., Hiddink, J. G. & Maxwell, T. A. D. Fishing effects on energy use by North Sea fishes. J. Sea Res. 60, 74–88 (2008).ADS 

    Google Scholar 
    de Ruiter, P. C., Neutel, A.-M. & Moore, J. C. Energetics, patterns of interaction strengths, and stability in real ecosystems. Science 269, 1257–1260 (1995).ADS 
    PubMed 

    Google Scholar 
    Bascompte, J. Disentangling the web of life. Science 325, 416–419 (2009).ADS 
    MathSciNet 
    CAS 
    PubMed 
    MATH 

    Google Scholar 
    Wootton, K. L. Omnivory and stability in freshwater habitats: Does theory match reality?. Freshw. Biol. 62, 821–832 (2017).
    Google Scholar 
    Borrelli, J. J. & Ginzburg, L. R. Why there are so few trophic levels: Selection against instability explains the pattern. Food Webs 1, 10–17 (2014).
    Google Scholar 
    Stouffer, D. B. & Bascompte, J. Compartmentalization increases food-web persistence. Proc. Natl. Acad. Sci. USA 108, 3648–52 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Márquez-Velásquez, V., Raimundo, R. L. G., de Souza Rosa, R. & Navia, A. F. The use of ecological networks as tools for understanding and conserving marine biodiversity. In Marine Coastal Ecosystems Modelling and Conservation: Latin American Experiences, pp 179–202 (eds Ortiz, M. & Jordán, F.) (Springer, 2021). https://doi.org/10.1007/978-3-030-58211-1_9.Chapter 

    Google Scholar 
    Neutel, A.-M. & Thorne, M. A. S. Interaction strengths in balanced carbon cycles and the absence of a relation between ecosystem complexity and stability. Ecol. Lett. 17, 651–661 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    Neutel, A.-M. & Thorne, M. A. S. Beyond connectedness: Why pairwise metrics cannot capture community stability. Ecol. Evol. 6, 7199–7206 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    Saravia, L. A., Marina, T. I., Kristensen, N. P., De Troch, M. & Momo, F. R. Ecological network assembly: How the regional metaweb influences local food webs. J. Anim. Ecol. 3, 25 (2021).
    Google Scholar 
    Góngora, M. E., GonzalezZevallos, D., Pettovello, A. & Mendia, L. Caracterizacion de las principales pesquerias del golfo San Jorge Patagonia, Argentina. Latin Am. J. Aquat. Res. 40, 1–11 (2012).
    Google Scholar 
    Yorio, P. Marine protected areas, spatial scales, and governance: Implications for the conservation of breeding seabirds. Conserv. Lett. 2, 171–178 (2009).
    Google Scholar 
    Rincón-Díaz, M. P., Bovcon, N. D., Cochia, P. D., Góngora, M. E. & Galván, D. E. Fish functional diversity as an indicator of resilience to industrial fishing in Patagonia Argentina. J. Fish Biol. 99, 1650–1667 (2021).PubMed 

    Google Scholar 
    González-Zevallos, D. & Yorio, P. Consumption of discards and interactions between Black-browed Albatrosses (Thalassarche melanophrys) and Kelp Gulls (Larus dominicanus) at trawl fisheries in Golfo San Jorge, Argentina. J. Ornithol. 152, 827–838 (2011).
    Google Scholar 
    Vinuesa, J. H. & Varisco, M. Trophic ecology of the lobster krill Munida gregaria in San Jorge Gulf, Argentina. Investig. Mar. 35, 25–34 (2007).
    Google Scholar 
    Belleggia, M. et al. Trophic ecology of yellownose skate Zearaja chilensis, a top predator in the south-western Atlantic Ocean. J. Fish Biol. 88, 1070–1087 (2016).CAS 
    PubMed 

    Google Scholar 
    Pasti, A. T. et al. The diet of Mustelus schmitti in areas with and without commercial bottom trawling (Central Patagonia, Southwestern Atlantic): Is it evidence of trophic interaction with the Patagonian shrimp fishery?. Food Webs 29, e00214 (2021).
    Google Scholar 
    Yorio, P., Bertellotti, M., Gandini, P. & Frere, E. Kelp gulls Larus dominicanus breeding on the argentine coast: Population status and relationship with coastal management and conservation. Mar. Ornithol. 26, 11–18 (1998).
    Google Scholar 
    Dans, S. et al. El golfo san jorge como área prioritaria de investigación, manejo y conservación en el marco de la iniciativa pampa azul. Rev. Cie. Investig. 71, 21–43 (2021).
    Google Scholar 
    de la Garza, J. M., Ferníndez, M. & Ravalli, C. Langostino patagónico (Pleoticus muelleri). Inf. Campa 20, 20 (2013).
    Google Scholar 
    Varisco, M. & La Vinuesa, J. H. Alimentación de Munida gregaria (Fabricius, 1793) (Crustacea:Anomura:Galatheidae) en fondos de pesca del Golfo San Jorge, Argentina. Rev. Biol. Mar. Oceanogr. 42, 221–229 (2007).
    Google Scholar 
    Tschopp, A., Cristiani, F., García, N. A., Crespo, E. A. & Coscarella, M. A. Trophic niche partitioning of five skate species of genus Bathyraja in northern and central Patagonia, Argentina. J. Fish. Biol. 97, 656–667 (2020).PubMed 

    Google Scholar 
    Kasinsky, T., Yorio, P., Dell’Arciprete, P., Marinao, C. & Suárez, N. Geographical differences in sex-specific foraging behaviour and diet during the breeding season in the opportunistic Kelp Gull (Larus dominicanus). Mar. Biol. 168, 14 (2021).CAS 

    Google Scholar 
    González-Zevallos, D. & Yorio, P. Seabird use of discards and incidental captures at the Argentine hake trawl fishery in the Golfo San Jorge, Argentina. Mar. Ecol. Progress Ser. 316, 175–183 (2006).ADS 

    Google Scholar 
    Crespo, E. A. et al. Direct and indirect effects of the Highseas fisheries on the marine mammal populations in the northern and central Patagonian coast. J. Northw. Atl. Fish. Sci. 22, 189–207 (1997).
    Google Scholar 
    Gandini, P. A., Frere, E., Pettovello, A. D. & Cedrola, P. V. Interaction between Magellanic Penguins and Shrimp Fisheries in Patagonia, Argentina. Condor 101, 783–789 (1999).
    Google Scholar 
    Fu, C. et al. Making ecological indicators management ready: Assessing the specificity, sensitivity, and threshold response of ecological indicators. Ecol. Ind. 105, 16–28 (2019).
    Google Scholar 
    Olivier, P. et al. Exploring the temporal variability of a food web using long-term biomonitoring data. Ecography 42, 2107–2121 (2019).
    Google Scholar 
    Bersier, L.-F., Banašek-Richter, C. & Cattin, M.-F. Quantitative descriptors of food-web matrices. Ecology 83, 2394–2407 (2002).MATH 

    Google Scholar 
    Gellner, G. & McCann, K. Reconciling the omnivory-stability debate. Am. Nat. 179, 22–37 (2012).PubMed 

    Google Scholar 
    Newman, M. E. J. & Girvan, M. Finding and evaluating community structure in networks. Phys. Rev. E 69, 26113 (2004).ADS 
    CAS 

    Google Scholar 
    Reichardt, J. & Bornholdt, S. Statistical mechanics of community detection. Phys. Rev. E 74, 16110 (2006).ADS 
    MathSciNet 

    Google Scholar 
    Allesina, S. & Pascual, M. Network structure, predator-prey modules, and stability in large food webs. Theor. Ecol. 1, 55–64 (2008).
    Google Scholar 
    Strona, G., Nappo, D., Boccacci, F., Fattorini, S. & San-Miguel-Ayanz, J. A fast and unbiased procedure to randomize ecological binary matrices with fixed row and column totals. Nat. Commun. 5, 4114 (2014).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Scholz, F. W. & Stephens, M. A. K-sample Anderson–Darling tests. J. Am. Stat. Assoc. 82, 918–924 (1987).MathSciNet 

    Google Scholar 
    Lakens, D. Calculating and reporting effect sizes to facilitate cumulative science: A practical primer for t-tests and ANOVAs. Front. Psychol. 4, 863 (2013).PubMed 
    PubMed Central 

    Google Scholar 
    Saravia, L. A. Multiweb: An R Package for Multiple Interaction Ecological Networks (Zenodo, 2019). https://doi.org/10.5281/zenodo.3370397.Book 

    Google Scholar 
    Kortsch, S. et al. Disentangling temporal food web dynamics facilitates understanding of ecosystem functioning. J. Anim. Ecol. 20, 20 (2021).
    Google Scholar 
    Marina, T. I. et al. Architecture of marine food webs: To be or not be a “small-world’’. PLoS One 13, 1–13 (2018).
    Google Scholar 
    Panel, E. P. A. Ecosystem-based Fishery Management: A Report to Congress by the Ecosystem Principles Advisory Panel. https://repository.library.noaa.gov/view/noaa/23730 (1998)Armoškaitė, A. et al. Establishing the links between marine ecosystem components, functions and services: An ecosystem service assessment tool. Ocean Coast. Manage. 193, 105229 (2020).
    Google Scholar 
    Navia, A. F., Cruz-Escalona, V. H., Giraldo, A. & Barausse, A. The structure of a marine tropical food web, and its implications for ecosystem-based fisheries management. Ecol. Model. 328, 23–33 (2016).
    Google Scholar 
    Agnetta, D. et al. Benthic-pelagic coupling mediates interactions in Mediterranean mixed fisheries: An ecosystem modeling approach. PLoS One 14, e0210659 (2019).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Baum, J. K. et al. Collapse and conservation of shark populations in the Northwest Atlantic. Sciencehttps://doi.org/10.1126/science.1079777 (2003).Article 
    PubMed 

    Google Scholar 
    Bearzi, G. et al. Overfishing and the disappearance of short-beaked common dolphins from western Greece. Endang. Species Res. 5, 1–12 (2008).
    Google Scholar 
    Lotze, H. K., Coll, M., Magera, A. M., Ward-Paige, C. & Airoldi, L. Recovery of marine animal populations and ecosystems. Trends Ecol. Evol. 26, 595–605 (2011).PubMed 

    Google Scholar 
    Reyes, L. M. Cetaceans of Central Patagonia, Argentina. Aquat. Mammals 32, 20–30 (2006).
    Google Scholar 
    Lisnizer, N., Garcia-Borboroglu, P. & Yorio, P. Spatial and temporal variation in population trends of Kelp Gulls in northern Patagonia, Argentina. Emu Austral Ornithol. 111, 259–267 (2011).
    Google Scholar 
    Yorio, P. et al. Population trends of Imperial Cormorants (Leucocarbo atriceps) in northern coastal Argentine Patagonia over 26 years. Emu Austral Ornithol. 120, 114–122 (2020).
    Google Scholar 
    Irigoyen, A. & Trobbiani, G. Depletion of trophy large-sized sharks populations of the Argentinean coast, south-western Atlantic: Insights from fishers’ knowledge. Neotrop. Ichthyol. 14, 20 (2016).
    Google Scholar 
    Vasas, V., Lancelot, C., Rousseau, V. & Jordán, F. Eutrophication and overfishing in temperate nearshore pelagic food webs: A network perspective. Mar. Ecol. Prog. Ser. 336, 1–14 (2007).ADS 
    CAS 

    Google Scholar 
    Gilarranz, L. J., Mora, C. & Bascompte, J. Anthropogenic effects are associated with a lower persistence of marine food webs. Nat. Commun. 7, 10737 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Bartley, T. J. et al. Food web rewiring in a changing world. Nat. Ecol. Evol. 3, 345–354 (2019).PubMed 

    Google Scholar 
    May, R. M. Stability and Complexity in Model Ecosystems Vol. 6 (Princeton University Press, 1974).
    Google Scholar 
    McCann, K. S. The diversity-stability debate. Nature 405, 228–233 (2000).CAS 
    PubMed 

    Google Scholar 
    van Altena, C., Hemerik, L. & de Ruiter, P. C. Food web stability and weighted connectance: The complexity-stability debate revisited. Theor. Ecol. 9, 49–58 (2016).
    Google Scholar 
    Dougoud, M., Vinckenbosch, L., Rohr, R. P., Bersier, L.-F. & Mazza, C. The feasibility of equilibria in large ecosystems: A primary but neglected concept in the complexity-stability debate. PLoS Comput. Biol. 14, e1005988 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    McCann, K. & Hastings, A. Re-evaluating the omnivory-stability relationship in food webs. Proc. R. Soc. Lond. B 264, 1249–1254 (1997).ADS 

    Google Scholar 
    Pimm, S. L. & Lawton, J. H. On feeding on more than one trophic level. Nature 275, 542–544 (1978).ADS 

    Google Scholar 
    Link, J. Does food web theory work for marine ecosystems?. Mar. Ecol. Prog. Ser. 230, 1–9 (2002).ADS 

    Google Scholar 
    Bieg, C. et al. Linking humans to food webs: A framework for the classification of global fisheries. Front. Ecol. Environ. 16, 412–420 (2018).
    Google Scholar 
    Shephard, S. et al. Scavenging on trawled seabeds can modify trophic size structure of bottom-dwelling fish. ICES J. Mar. Sci. 71, 398–405 (2014).
    Google Scholar 
    Gilarranz, L. J., Rayfield, B., Liñán-Cembrano, G., Bascompte, J. & Gonzalez, A. Effects of network modularity on the spread of perturbation impact in experimental metapopulations. Science 357, 199–201 (2017).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Danet, A., Mouchet, M., Bonnaffé, W., Thébault, E. & Fontaine, C. Species richness and food-web structure jointly drive community biomass and its temporal stability in fish communities. Ecol. Lett. 24, 2364–2377 (2021).PubMed 

    Google Scholar 
    Shanafelt, D. W. & Loreau, M. Stability trophic cascades in food chains. R. Soc. Open Sci. 5, 180995 (2018).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Barbier, M. & Loreau, M. Pyramids and cascades: A synthesis of food chain functioning and stability. Ecol. Lett. 22, 405–419 (2019).PubMed 

    Google Scholar 
    Sánchez, M. F. et al. Caracterización ecológica del Golfo San Jorge (Argentina) mediante modelación ecotrófica multiespecífica. 30 https://www.inidep.edu.ar/wordpress/?page_id=1959 (2009)Gaitán, E. N. Tramas Tróficas en Sistemas Frontales del Mar Argentino: Estructura, Dinámica y Complejidad Analizada Mediante Isótopos Estables (Universidad Nacional de Mar del Plata, Facultad de Ciencias Exactas y Naturales, 2012).
    Google Scholar 
    Pinnegar, J. K. & Polunin, N. V. C. Differential fractionation of 13C and 15N among fish tissues: Implications for the study of trophic interactions. Funct. Ecol. 13, 225–231 (1999).
    Google Scholar 
    Philippsen, J. S. & Benedito, E. Discrimination factor in the trophic ecology of fishes: A review about sources of variation and methods to obtain it. Oecol. Aust. 17, 205–2016 (2013).
    Google Scholar 
    Hussey, N. E. et al. Rescaling the trophic structure of marine food webs. Ecol. Lett. 17, 239–250 (2014).PubMed 

    Google Scholar 
    Lefebvre, S. & Dubois, S. The stony road to understand isotopic enrichment and turnover rates: Insight into the metabolic part. Vie Milieu-life Environ. 66, 305–314 (2016).
    Google Scholar 
    Funes, M., Irigoyen, A. J., Trobbiani, G. A. & Galván, D. E. Stable isotopes reveal different dependencies on benthic and pelagic pathways between Munida gregaria ecotypes. Food Webs 17, e00101 (2018).
    Google Scholar 
    Santos, B. & Villarino, M. F. Evaluación del Estado de Explotación del Efectivo sur de 41 S de la Merluza (Merluccius hubbsi) y Estimación de la Captura Biológicamente Aceptable Para 2014. Informe Técnico Oficial INIDEP. 1–30 (2013).Belleggia, M., Giberto, D. & Bremec, C. Adaptation of diet in a changed environment: Increased consumption of lobster krill Munida gregaria (Fabricius, 1793) by Argentine hake. Mar. Ecol. 38, e12445 (2017).ADS 

    Google Scholar 
    Diez, M. J., Cabreira, A. G., Madirolas, A. & Lovrich, G. A. Hydroacoustical evidence of the expansion of pelagic swarms of Munida gregaria (Decapoda, Munididae) in the Beagle Channel and the Argentine Patagonian Shelf, and its relationship with habitat features. J. Sea Res. 114, 1–12 (2016).ADS 

    Google Scholar 
    Ravalli, C., De La Garza, J. & Greco, L. L. Distribución de los morfotipos gregaria y subrugosa de la langostilla Munida gregaria (Decapoda, Galatheidae) en el Golfo San Jorge en la campaña de verano AE-01/2011. Integración de resultados con las campañas 2009 y 2010. Rev. Invest. Desarr. Pesq. 22, 29–41 (2013).
    Google Scholar 
    Belleggia, M. et al. Are hakes truly opportunistic feeders? A case of prey selection by the Argentine hake Merluccius hubbsi off southwestern Atlantic. Fish. Res. 214, 166–174 (2019).
    Google Scholar 
    Roux, A., Piñero, R., Moriondo, P. & Fernández, M. Diet of the red shrimp Pleoticus muelleri (Bate, 1888) in Patagonian fishing grounds, Argentine. Rev. Biol. Mar. Oceanogr. 44, 25 (2009).
    Google Scholar 
    de la Garza, J. et al. An Overview of the Argentine Red Shrimp (Pleoticus muelleri, Decapoda, Solenoceridae) Fishery in Argentina: Biology, Fishing, Management and Ecological Interactions (Instituto Nacional de Investigación y Desarrollo Pesquero (INIDEP), 2017).
    Google Scholar 
    Sánchez, M. F. & Prenski, L. B. Ecología trófica de peces demersales en el Golfo San Jorge. Trophic Ecol. Demersal Fish San Jorge Gulf 10, 57–71 (1996).
    Google Scholar 
    Copello, S., Quintana, F. & Pérez, F. Diet of the southern giant petrel in Patagonia: Fishery-related items and natural prey. Endang. Species Res. 6, 15–23 (2008).
    Google Scholar 
    Alonso, R. B. et al. The opportunistic sense: The diet of Argentine hake Merluccius hubbsi reflects changes in prey availability. Region. Stud. Mar. Sci. 27, 100540 (2019).
    Google Scholar 
    Marón, C. F. et al. Increased wounding of southern right whale (Eubalaena australis) calves by kelp gulls (Larus dominicanus) at Península Valdés, Argentina. PLoS One 10, e0139291 (2015).PubMed 
    PubMed Central 

    Google Scholar 
    Fazio, A., Argüelles, M. B. & Bertellotti, M. Change in southern right whale breathing behavior in response to gull attacks. Mar. Biol. 162, 267–273 (2015).
    Google Scholar 
    Pocock, M. J. O., Evans, D. M. & Memmott, J. The robustness and restoration of a network of ecological networks. Science 335, 973–977 (2012).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Kéfi, S. et al. Network structure beyond food webs: Mapping non-trophic and trophic interactions on Chilean rocky shores. Ecology 96, 291–303 (2015).
    Google Scholar 
    Mougi, A. The roles of amensalistic and commensalistic interactions in large ecological network stability. Sci. Rep. 6, 29929 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Mougi, A. & Kondoh, M. Diversity of interaction types and ecological community stability. Science 337, 349–351 (2012).ADS 
    MathSciNet 
    CAS 
    PubMed 
    MATH 

    Google Scholar 
    Kéfi, S., Miele, V., Wieters, E. A., Navarrete, S. A. & Berlow, E. L. How structured is the entangled bank? The surprisingly simple organization of multiplex ecological networks leads to increased persistence and resilience. PLoS Biol. 14, e1002527 (2016).PubMed 
    PubMed Central 

    Google Scholar  More