More stories

  • in

    Building a truly diverse biodiversity science

    npj Biodiversity aims to be a common forum where discoveries in all areas of biodiversity science can be discussed, so that the research in specific topics with broad implications for other disciplines permeates the whole community. This requires that scientific debates are made in egalitarian terms between people with different backgrounds and points of view. We will strive to provide safe spaces where all biodiversity research can be showcased without bias, and theoretical and practical advances can be subject to calm and civil debate. As journal editors we will implement measures to work towards a fairer and more inclusive science, such as giving proper recognition to all researchers involved in the research published13, or ensuring in revisions that former research made by different identity groups and local scientists is adequately acknowledged14. We will also acknowledge diversity by maintaining a diverse editorial board15 and engaging external peer-reviewers16 that represent local specialists, the diversity of approaches in each field, as well as early-career researchers across demographic groups. We will also encourage access to research and engage in the FAIR principles for data management and sharing17. Here, good practice includes making data available for reanalysis or compilation in larger databases by researchers anywhere in the world, promoting open software, and sharing reproducible code18,19. Our hope is that this extends the capacity of developing meta-analyses and macroecological and macroevolutionary research beyond the borders of high-income countries.npj Biodiversity seeks to promote scientific discussion and synthesis. As editors, we will act as guides and moderators rather than as gatekeepers that merely decide which papers are above the threshold of publication20. Thus, we encourage debate as a central part of the editorial process, allowing well-grounded and clearly-identified speculation and policy-related statements in published papers when appropriate. This may include publishing non-conventional papers that foster discussion in established topics or open new research avenues21, if and only if they are well supported by data or published evidence. In this sense, we welcome Comments on areas currently under discussion, as well as Reviews and Perspectives that allow synthesis in theoretical and practical topics that are not necessarily general, but can help advance specific subdisciplines or topics. Last but not least, we want to facilitate communication between basic research and applied practitioners through Perspectives that translate the implications of recent research for management, conservation and adaptation to global change, or that identify which theoretical advances or additional empirical evidence would be needed to tackle specific problems.Creating the appropriate publishing environment for journals to be true forums for debate and provide value to the scientific community is a challenging enterprise. Above all, it requires escaping from the haste imposed by the “publish or perish model”, and making an explicit effort to raise the quality of the editorial process. In npj Biodiversity we will seek to follow ‘slow publishing’ principles, putting emphasis on meaningful debate between authors, editors and reviewers22. Current research environments can prevent researchers from having time to think, but true advance stems from digesting ideas and discussing them with the detail, depth and time they may need (http://slow-science.org/)23,24,25. Therefore, to contribute to a healthier, gentler and more thoughtful approach to biodiversity science, we will provide thorough and thoughtful reviews. We will make editorial decisions that, when paired with equally thorough and thoughtful work by authors, can reduce the number of times a paper bounces back and forth in successive rounds of peer review and revision. Note that this does not necessarily mean longer editorial times! Paradoxically, when authors, reviewers and editors commit to these “slow” publishing principles, the publication process can speed up. And most importantly, it will promote the spirit of productive debate that we aim for in npj Biodiversity. More

  • in

    Biogenic climate change could have driven the demise of life on early Mars

    Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.This is a summary of: Sauterey, B. et al. Early Mars habitability and global cooling by H2-based methanogens. Nat. Astron. https://doi.org/10.1038/s41550-022-01786-w (2022). More

  • in

    Temporal and functional interrelationships between bacterioplankton communities and the development of a toxigenic Microcystis bloom in a lowland European reservoir

    Paerl, H. W. Mitigating toxic planktonic cyanobacterial blooms in aquatic ecosystems facing increasing anthropogenic and climatic pressures. Toxins. 10, 1–16 (2018).
    Google Scholar 
    Harke, M. J. et al. A review of the global ecology, genomics, and biogeography of the toxic cyanobacterium Microcystis spp. Harmful Algae 54, 4–20. https://doi.org/10.1016/j.hal.2015.12.007 (2016).Article 
    PubMed 

    Google Scholar 
    Paerl, H. W. & Barnard, M. A. Mitigating the global expansion of harmful cyanobacterial blooms: Moving targets in a human- and climatically-altered world. Harmful Algae 96, 101845. https://doi.org/10.1016/j.hal.2020.101845 (2020).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Paerl, H. W. Mitigating harmful cyanobacterial blooms in a human- and climatically-impacted world. Life. 4, 988–1012 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    Burford, M. A. et al. Perspective: Advancing the research agenda for improving understanding of cyanobacteria in a future of global change. Harmful Algae 91, 101601. https://doi.org/10.1016/j.hal.2019.04.004 (2020).Article 
    CAS 
    PubMed 

    Google Scholar 
    Havens, K. E., James, R. T., East, T. L. & Smith, V. H. N: P ratios, light limitation, and cyanobacterial dominance in a subtropical lake impacted by non-point source nutrient pollution. Environ. Pollut. 122, 379–390 (2003).CAS 
    PubMed 

    Google Scholar 
    Bernard, C. Cyanobacteria and cyanotoxins. Rev. Franç. Lab. 2014, 53–68 (2014).
    Google Scholar 
    Paerl, H. W. & Otten, T. G. Harmful cyanobacterial blooms: Causes, consequences, and controls. Microb. Ecol. 65, 995–1010 (2013).CAS 
    PubMed 

    Google Scholar 
    Dolman, A. M. et al. Cyanobacteria and cyanotoxins: The influence of nitrogen versus phosphorus. PLoS ONE 7, 38575 (2012).
    Google Scholar 
    Svirčev, Z. et al. Global geographical and historical overview of cyanotoxin distribution and cyanobacterial poisonings. Arch. Toxicol. https://doi.org/10.1007/s00204-019-02524-4 (2019).Article 
    PubMed 

    Google Scholar 
    Massey, I. Y. & Yang, F. A mini review on microcystins and bacterial degradation. Toxins 12, 268 (2020).CAS 
    PubMed Central 

    Google Scholar 
    Paerl, H. W. et al. Mitigating eutrophication and toxic cyanobacterial blooms in large lakes: The evolution of a dual nutrient (N and P) reduction paradigm. Hydrobiologia 847, 4359–4375. https://doi.org/10.1007/s10750-019-04087-y (2020).Article 
    CAS 

    Google Scholar 
    Sapp, M. et al. Species-specific bacterial communities in the phycosphere of microalgae?. Microb. Ecol. 53, 683–699 (2007).PubMed 

    Google Scholar 
    Cai, H., Jiang, H., Krumholz, L. R. & Yang, Z. Bacterial community composition of size-fractioned aggregates within the phycosphere of cyanobacterial blooms in a eutrophic freshwater lake. PLoS ONE 9, 102879 (2014).ADS 

    Google Scholar 
    Grant, M. A. A., Kazamia, E., Cicuta, P. & Smith, A. G. Direct exchange of vitamin B 12 is demonstrated by modelling the growth dynamics of algal-bacterial cocultures. ISME J. Nat. Publ. Group 8, 1418–1427 (2014).CAS 

    Google Scholar 
    Shi, L., Cai, Y., Kong, F. & Yu, Y. Specific association between bacteria and buoyant Microcystis colonies compared with other bulk bacterial communities in the eutrophic Lake Taihu, China. Environ. Microbiol. Rep. 4, 669–678 (2012).CAS 
    PubMed 

    Google Scholar 
    Brunberg, A. K. Contribution of bacteria in the mucilage of Microcystis spp (Cyanobacteria) to benthic and pelagic bacterial production in a hypereutrophic lake. FEMS Microbiol. Ecol. 29, 13–22 (1999).CAS 

    Google Scholar 
    Shao, K. et al. The responses of the taxa composition of particle-attached bacterial community to the decomposition of Microcystis blooms. Sci. Total. Environ. 488–489, 236–242. https://doi.org/10.1016/j.scitotenv.2014.04.101 (2014).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Jankowiak, J. G. & Gobler, C. J. The composition and function of microbiomes within microcystis colonies are significantly different than native bacterial assemblages in two North American lakes. Front. Microbiol. 11, 1–26 (2020).
    Google Scholar 
    Bauer, A. & Forchhammer, K. Bacterial predation on cyanobacteria. Microb. Physiol. 99, 108 (2021).
    Google Scholar 
    Ndlela, L. L., Oberholster, P. J., Van Wyk, J. H. & Cheng, P. H. Bacteria as biological control agents of freshwater cyanobacteria: Is it feasible beyond the laboratory?. Appl. Microbiol. Biotechnol. 102, 9911–9923 (2018).CAS 
    PubMed 

    Google Scholar 
    Yang, C. et al. Distinct network interactions in particle-associated and free-living bacterial communities during a Microcystis aeruginosa bloom in a plateau lake. Front. Microbiol. 8, 1–15 (2017).
    Google Scholar 
    Xu, H. et al. Contrasting network features between free-living and particle-attached bacterial communities in Taihu Lake. Microb. Ecol. 76, 303–313 (2018).PubMed 

    Google Scholar 
    Liu, M. et al. Community dynamics of free-living and particle-attached bacteria following a reservoir Microcystis bloom. Sci. Total Environ. 660, 501–511. https://doi.org/10.1016/j.scitotenv.2018.12.414 (2019).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Parveen, B. et al. Bacterial communities associated with Microcystis colonies differ from free-living communities living in the same ecosystem. Environ. Microbiol. Rep. 5, 716–724 (2013).CAS 
    PubMed 

    Google Scholar 
    Louati, I. et al. Structural diversity of bacterial communities associated with bloom-forming freshwater cyanobacteria differs according to the cyanobacterial genus. PLoS ONE 10, 0140614 (2015).
    Google Scholar 
    Zwirglmaier, K., Keiz, K., Engel, M., Geist, J. & Raeder, U. Seasonal and spatial patterns of microbial diversity along a trophic gradient in the interconnected lakes of the Osterseen Lake District, Bavaria. Front. Microbiol. 6, 1–18 (2015).
    Google Scholar 
    Scherer, P. I. et al. Temporal dynamics of the microbial community composition with a focus on toxic cyanobacteria and toxin presence during harmful algal blooms in two South German lakes. Front. Microbiol. 8, 1–17 (2017).
    Google Scholar 
    Kokocinski, M., Dziga, D., Antosiak, A. & Soininen, J. Are bacterio- and phytoplankton community compositions related in lakes differing in their cyanobacteria contribution and physico-chemical properties?. Genes 12, 855 (2021).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Dziga, D. et al. Correlation between specific groups of heterotrophic bacteria and microcystin biodegradation in freshwater bodies of central Europe. FEMS Microbiol. Ecol. https://doi.org/10.1111/j.1574-6941.1999.tb00594.x (2019).Article 
    PubMed 

    Google Scholar 
    Jurczak, T. et al. Elimination of microcystins by water treatment processes: Examples from Sulejow Reservoir, Poland. Water Res. 39, 2394–2406 (2005).CAS 
    PubMed 

    Google Scholar 
    Mankiewicz-Boczek, J. et al. Detection and monitoring toxigenicity of cyanobacteria by application of molecular methods. Environ Toxicol. 21, 380–387 (2006).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Rajaniemi-Wacklin, P. et al. Correspondence between phylogeny and morphology of Snowella spp. and Woronichinia naegeliana, cyanobacteria commonly occurring in lakes. J. Phycol. 42, 226–232 (2006).
    Google Scholar 
    DrobacBacković, D. et al. Cyanobacteria, cyanotoxins, and their histopathological effects on fish tissues in Fehérvárcsurgó reservoir Hungary. Environ. Monit. Assess. https://doi.org/10.1007/s10661-021-09324-3 (2021).Article 

    Google Scholar 
    Kallscheuer, N. et al. Analysis of bacterial communities in a municipal duck pond during a phytoplankton bloom and isolation of Anatilimnocola aggregata gen. nov., sp. Nov., Lacipirellula limnantheis sp. Nov. and Urbifossiella limnaea gen. nov. sp. nov. belonging to the phylum. Environ. Microbiol. 23, 1379–1396 (2021).CAS 
    PubMed 

    Google Scholar 
    Davis, T. W. et al. Effects of nitrogenous compounds and phosphorus on the growth of toxic and non-toxic strains of Microcystis during cyanobacterial blooms. Aquat. Microb. Ecol. 61, 149–162 (2010).
    Google Scholar 
    Gobler, C. J., Davis, T. W., Coyne, K. J. & Boyer, G. L. Interactive influences of nutrient loading, zooplankton grazing, and microcystin synthetase gene expression on cyanobacterial bloom dynamics in a eutrophic New York lake. Harmful Algae 6, 119–133 (2007).CAS 

    Google Scholar 
    Mankiewicz-Boczek, J. et al. Cyanophages infection of microcystis bloom in lowland dam reservoir of Sulejów, Poland. Microb. Ecol. 71, 315–325 (2016).CAS 
    PubMed 

    Google Scholar 
    Davis, T. W., Berry, D. L., Boyer, G. L. & Gobler, C. J. The effects of temperature and nutrients on the growth and dynamics of toxic and non-toxic strains of Microcystis during cyanobacteria blooms. Harmful Algae 8, 715–725 (2009).CAS 

    Google Scholar 
    Yoshida, M., Yoshida, T., Takashima, Y., Hosoda, N. & Hiroishi, S. Dynamics of microcystin-producing and non-microcystin-producing Microcystis populations is correlated with nitrate concentration in a Japanese lake. FEMS Microbiol. Lett. 266, 49–53 (2007).CAS 
    PubMed 

    Google Scholar 
    Sezenna, M. L. Proteobacteria: Phylogeny, Metabolic Diversity and Ecological Effects (Nova Science Publishers, Inc., 2011).
    Google Scholar 
    Rilling, J. I., Acuña, J. J., Sadowsky, M. J. & Jorquera, M. A. Putative nitrogen-fixing bacteria associated with the rhizosphere and root endosphere of wheat plants grown in an andisol from southern Chile. Front. Microbiol. 9, 1–13 (2018).
    Google Scholar 
    Lukumbuzya, M. et al. A refined set of rRNA-targeted oligonucleotide probes for in situ detection and quantification of ammonia-oxidizing bacteria. Water Res. 186, 116375 (2020).
    Google Scholar 
    Prosser, J. I., Head, I. M. & Stein, L. Y. The family Nitrosomonadaceae. In The Prokaryotes: Alphaproteobacteria and Betaproteobacteria (eds Rosenberg, E. et al.) 901–918 (Springer, 2014). https://doi.org/10.1007/978-3-642-30197-1_372.Chapter 

    Google Scholar 
    Jia, L., Jiang, B., Huang, F. & Hu, X. Nitrogen removal mechanism and microbial community changes of bioaugmentation subsurface wastewater infiltration system. Bioresour. Technol. 294, 122140. https://doi.org/10.1016/j.biortech.2019.122140 (2019).Article 
    CAS 
    PubMed 

    Google Scholar 
    Daft, M. J. & Stewart, W. D. P. Bacterial pathogens of freshwater blue-green algae. New Phytol. 70, 819–829 (1971).
    Google Scholar 
    Chun, S. J. et al. Network analysis reveals succession of Microcystis genotypes accompanying distinctive microbial modules with recurrent patterns. Water Res. 170, 115326. https://doi.org/10.1016/j.watres.2019.115326 (2020).Article 
    CAS 
    PubMed 

    Google Scholar 
    Parulekar, N. N. et al. Characterization of bacterial community associated with phytoplankton bloom in a eutrophic lake in South Norway using 16S rRNA gene amplicon sequence analysis. PLoS ONE 12, 1–22 (2017).
    Google Scholar 
    Guedes, I. A. et al. Close link between harmful cyanobacterial dominance and associated bacterioplankton in a tropical eutrophic reservoir. Front. Microbiol. 9, 424 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    Allgaier, M. & Grossart, H. P. Seasonal dynamics and phylogenetic diversity of free-living and particle-associated bacterial communities in four lakes in northeastern Germany. Aquat. Microb. Ecol. 45, 115–128 (2006).
    Google Scholar 
    Chen, S. et al. Disentangling the drivers of Microcystis decomposition: Metabolic profile and co-occurrence of bacterial community. Sci. Total Environ. 739, 140062. https://doi.org/10.1016/j.scitotenv.2020.140062 (2020).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Leflaive, J. & Ten-Hage, L. Algal and cyanobacterial secondary metabolites in freshwaters: A comparison of allelopathic compounds and toxins. Freshw. Biol. 52, 199–214 (2007).CAS 

    Google Scholar 
    Song, H. et al. Biological and chemical factors driving the temporal distribution of cyanobacteria and heterotrophic bacteria in a eutrophic lake (West Lake, China). Appl. Microbiol. Biotechnol. 101, 1685–1696. https://doi.org/10.1007/s00253-016-7968-8 (2017).Article 
    CAS 
    PubMed 

    Google Scholar 
    Bagatini, I. L. et al. Host-specificity and dynamics in bacterial communities associated with bloom-forming freshwater phytoplankton. PLoS ONE 9, 85957 (2014).ADS 

    Google Scholar 
    Kohler, E. et al. Biodegradation of microcystins during gravity-driven membrane (GDM) ultrafiltration. PLoS ONE 9, 111794 (2014).ADS 

    Google Scholar 
    Wu, X. et al. Culturing of “unculturable” subsurface microbes: Natural organic carbon source fuels the growth of diverse and distinct bacteria from groundwater. Front. Microbiol. 11, 1–10 (2020).CAS 

    Google Scholar 
    Morotomi, M., Nagai, F. & Watanabe, Y. Parasutterella secunda sp. no., isolated from human faeces and proposal of Sutterellaceae fam. nov. in the order Burkholderiales. Int. J. Syst. Evol. Microbiol. 61, 637–643 (2011).CAS 
    PubMed 

    Google Scholar 
    Kiedrzyńska, E. et al. Point sources of nutrient pollution in the lowland river catchment in the context of the baltic Sea eutrophication. Ecol. Eng. 70, 337–348 (2014).
    Google Scholar 
    Hwang, W. M., Ko, Y., Kim, J. H. & Kang, K. Ahniella affigens gen Nov, sp. nov., a gammaproteobacterium isolated from sandy soil near a stream. Int. J. Syst. Evol. Microbiol. 68, 2478–2484 (2018).CAS 
    PubMed 

    Google Scholar 
    Qian, H. et al. Spatial variability of cyanobacteria and heterotrophic bacteria in Lake Taihu (China). Bull. Environ. Contam. Toxicol. 99, 380–384 (2017).CAS 
    PubMed 

    Google Scholar 
    Humbert, J. F. et al. Comparison of the structure and composition of bacterial communities from temperate and tropical freshwater ecosystems. Environ. Microbiol. 11, 2339–2350 (2009).CAS 
    PubMed 

    Google Scholar 
    Newton, R. J., Jones, S. E., Eiler, A., McMahon, K. D. & Bertilsson, S. A guide to the natural history of freshwater lake Bacteria. Microbiol. Mol. Biol. Rev. 1, 1–10 (2011).
    Google Scholar 
    Parveen, B., Mary, I., Vellet, A., Ravet, V. & Debroas, D. Temporal dynamics and phylogenetic diversity of free-living and particle-associated Verrucomicrobia communities in relation to environmental variables in a mesotrophic lake. FEMS Microbiol. Ecol. 83, 189–201 (2013).CAS 
    PubMed 

    Google Scholar 
    Henson, M. W., Lanclos, V. C., Faircloth, B. C. & Thrash, J. C. Cultivation and genomics of the first freshwater SAR11 (LD12) isolate. ISME J. 12, 1846–1860 (2018).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Yang, C. et al. The characteristics and algicidal mechanisms of cyanobactericidal bacteria, a review. World J. Microbiol. Biotechnol. 36, 1–10. https://doi.org/10.1007/s11274-020-02965-5 (2020).Article 

    Google Scholar 
    Izydorczyk, K. et al. Influence of abiotic and biotic factors on microcystin content in Microcystis aeruginosa cells in a eutrophic temperate reservoir. J. Plankton Res. 30, 393–400 (2008).CAS 

    Google Scholar 
    Mankiewicz-Boczek, J. et al. Bacteria homologus to Aeromonas capable of microcystin degradation. Open Life Sci. 10, 106–116 (2015).CAS 

    Google Scholar 
    Jaskulska, A., Font Nájera, A., Czarny, P., Serwecińska, L. & Mankiewicz-boczek, J. Daily dynamic of transcripts abundance of Ma-LMM01-like cyanophages in two lowland European reservoirs. Ecohydrol. Hydrobiol. 21, 543–548 (2021).
    Google Scholar 
    Gągała, I. et al. Role of environmental factors and toxic genotypes in the regulation of microcystins-producing cyanobacterial blooms. Microb. Ecol. 67, 465–479 (2014).PubMed 

    Google Scholar 
    Klindworth, A. et al. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. 41, 1–11 (2013).
    Google Scholar 
    Illumina. 16S Metagenomic Sequencing Library Preparation. (2013). http://support.illumina.com/content/dam/illumina-support/documents/documentation/chemistry_documentation/16s/16s-metagenomic-library-prep-guide-15044223-b.pdf.Frangeul, L. et al. Highly plastic genome of Microcystis aeruginosa PCC 7806, a ubiquitous toxic freshwater cyanobacterium. BMC Genomics 9, 1–20 (2008).
    Google Scholar 
    Hammer, Ø., Harper, D. A. T. & Ryan, P. D. Past: Paleontological statistics software package for education and data analysis even a cursory glance at the recent paleontological literature should convince anyone tha. Palaeontol. Electron. 4, 1–9 (2001).
    Google Scholar 
    Suzuki, M. T., Taylor, L. T. & DeLong, E. F. Quantitative analysis of small-subunit rRNA genes in mixed microbial populations via 5’-nuclease assays. Appl. Environ. Microbiol. 66, 4605–4614. https://doi.org/10.1128/AEM.66.11.4605-4614.2000 (2000).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Neilan B. A et al. rRNA sequences and evolutionary relationships among toxic and nontoxic cyanobacteria of the genus Microcystis Int J Syst Bacteriol 47(3), 693–697, https://doi.org/10.1099/00207713-47-3-693 (1997).
    Google Scholar  More

  • in

    Mixtures of genotypes increase disease resistance in a coral nursery

    Vega Thurber, R. et al. Deciphering coral disease dynamics: Integrating host, microbiome, and the changing environment. Front. Ecol. Evol. 2020, 8 (2020).
    Google Scholar 
    Groner, M. L. et al. Managing marine disease emergencies in an era of rapid change. Philos. Trans. R. Soc. Lond. B Biol. Sci. 371, 1689 (2016).
    Google Scholar 
    Richardson, L. L. Coral diseases: What is really known?. Trends Ecol. Evol. 13, 438–443 (1998).CAS 
    PubMed 

    Google Scholar 
    Miller, M. W., Lohr, K. E., Cameron, C. M., Williams, D. E. & Peters, E. C. Disease dynamics and potential mitigation among restored and wild staghorn coral, Acropora cervicornis. PeerJ https://doi.org/10.7287/peerj.preprints.328 (2014).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Teplitski, M. & Ritchie, K. How feasible is the biological control of coral diseases?. Trends Ecol. Evol. 24, 378–385 (2009).PubMed 

    Google Scholar 
    Zhu, Y. et al. Genetic diversity and disease control in rice. Nature 406, 718–722 (2000).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Altermatt, F. & Ebert, D. Genetic diversity of Daphnia magna populations enhances resistance to parasites. Ecol. Lett. 11, 918–928 (2008).PubMed 

    Google Scholar 
    Aronson, R. B. & Precht, W. F. White-band disease and the changing face of Caribbean coral reefs. In (ed Porter, J. W.) The Ecology and Etiology of Newly Emerging Marine Diseases 25–38 (Springer Netherlands, 2001).Ruiz-Moreno, D. et al. Global coral disease prevalence associated with sea temperature anomalies and local factors. Dis. Aquat. Organ. 100, 249–261 (2012).PubMed 

    Google Scholar 
    Precht, W. F., Gintert, B. E., Robbart, M. L., Fura, R. & van Woesik, R. Unprecedented disease-related coral mortality in Southeastern Florida. Sci. Rep. 6, 31374 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Gignoux-Wolfsohn, S. A., Marks, C. J. & Vollmer, S. V. White Band Disease transmission in the threatened coral, Acropora cervicornis. Sci. Rep. 2, 804 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Aronson, R., Bruckner, A., Moore, J., Precht, B. & Weil, E. Acropora cervicornis. IUCN Red List of Threatened Species https://doi.org/10.2305/iucn.uk.2008.rlts.t133381a3716457.en (2008).Alvarez-Filip, L., González-Barrios, F. J., Pérez-Cervantes, E., Molina-Hernández, A. & Estrada-Saldívar, N. Stony coral tissue loss disease decimated Caribbean coral populations and reshaped reef functionality. Commun. Biol. 5, 440 (2022).PubMed 
    PubMed Central 

    Google Scholar 
    Heres, M. M., Farmer, B. H., Elmer, F. & Hertler, H. Ecological consequences of Stony Coral Tissue Loss Disease in the Turks and Caicos Islands. Coral Reefs 40, 609–624 (2021).
    Google Scholar 
    Neely, K. L., Shea, C. P., Macaulay, K. A., Hower, E. K. & Dobler, M. A. Short- and long-term effectiveness of coral disease treatments. Front. Mar. Sci. 2021, 8 (2021).
    Google Scholar 
    Neely, K. L., Macaulay, K. A., Hower, E. K. & Dobler, M. A. Effectiveness of topical antibiotics in treating corals affected by stony coral tissue loss disease. PeerJ 8, e9289 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    Shilling, E. N., Combs, I. R. & Voss, J. D. Assessing the effectiveness of two intervention methods for stony coral tissue loss disease on Montastraea cavernosa. Sci. Rep. 11, 8566 (2021).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Walker, B. K., Turner, N. R., Noren, H. K. G., Buckley, S. F. & Pitts, K. A. Optimizing stony coral tissue loss disease (SCTLD) intervention treatments on Montastraea cavernosa in an Endemic Zone. Front. Mar. Sci. 8, 666224 (2021).
    Google Scholar 
    Forrester, G. E., Arton, L., Horton, A., Nickles, K. & Forrester, L. M. Antibiotic treatment ameliorates the impact of stony coral tissue loss disease (SCTLD) on coral communities. Front. Mar. Sci. 2022, 9 (2022).
    Google Scholar 
    Lee-Hing, C. et al. Management responses in Belize and Honduras, as stony coral tissue loss disease expands its prevalence in the Mesoamerican reef. Front. Mar. Sci. 9, 1 (2022).ADS 

    Google Scholar 
    Young, C. N., Schopmeyer, S. A. & Lirman, D. A review of reef restoration and coral propagation using the threatened genus Acropora in the Caribbean and Western Atlantic. Bull. Mar. Sci. 88, 1075–1098 (2012).
    Google Scholar 
    Lirman, D. & Schopmeyer, S. Ecological solutions to reef degradation: Optimizing coral reef restoration in the Caribbean and Western Atlantic. PeerJ 4, e2597 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    Baums, I. B. et al. Considerations for maximizing the adaptive potential of restored coral populations in the western Atlantic. Ecol. Appl. 29, e01978 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    Rosales, S. M. et al. Microbiome differences in disease-resistant vs susceptible Acropora corals subjected to disease challenge assays. Sci. Rep. 9, 18279 (2019).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Pinzón, C. J. H., Beach-Letendre, J., Weil, E. & Mydlarz, L. D. Relationship between phylogeny and immunity suggests older caribbean coral lineages are more resistant to disease. PLoS ONE 9, e104787. https://doi.org/10.1371/journal.pone.0104787 (2014).Article 
    ADS 
    CAS 

    Google Scholar 
    Drury, C. et al. Genomic patterns in Acropora cervicornis show extensive population structure and variable genetic diversity. Ecol. Evol. 7, 6188–6200 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    Maneval, P., Jacoby, C. A., Harris, H. E. & Frazer, T. K. Genotype, nursery design, and depth influence the growth of Acropora cervicornis fragments. Front. Mar. Sci. 8, 1 (2021).
    Google Scholar 
    Wright, R. M. et al. Intraspecific differences in molecular stress responses and coral pathobiome contribute to mortality under bacterial challenge in Acropora millepora. Sci. Rep. 7, 2609 (2017).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Vollmer, S. V. & Kline, D. I. Natural disease resistance in threatened staghorn corals. PLoS ONE 3, e3718 (2008).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Miller, N., Maneval, P., Manfrino, C., Frazer, T. K. & Meyer, J. L. Spatial distribution of microbial communities among colonies and genotypes in nursery-reared Acropora cervicornis. PeerJ 8, e9635 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    Klinges, G., Maher, R. L., Vega-Thurber, R. L. & Muller, E. M. Parasitic, “Candidatus Aquarickettsia rohweri” is a marker of disease susceptibility in Acropora cervicornis but is lost during thermal stress. Environ. Microbiol. 22, 5341–5355 (2020).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Miller, M. W. et al. Genotypic variation in disease susceptibility among cultured stocks of elkhorn and staghorn corals. PeerJ 7, e6751 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    Rohr, J. R. et al. Towards common ground in the biodiversity-disease debate. Nat. Ecol. Evol. 4, 24–33 (2020).PubMed 

    Google Scholar 
    Shearer, T. L., Porto, I. & Zubillaga, A. L. Restoration of coral populations in light of genetic diversity estimates. Coral Reefs 28, 727–733 (2009).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ostfeld, R. S. & Keesing, F. Biodiversity and disease risk: The case of lyme disease. Conserv. Biol. 14, 722–728 (2000).
    Google Scholar 
    Lively, C. M. The effect of host genetic diversity on disease spread. Am. Nat. 175, E149–E152 (2010).PubMed 

    Google Scholar 
    Ostfeld, R. S. & Keesing, F. Effects of host diversity on infectious disease. Annu. Rev. Ecol. Evol. Syst. 43, 157–182 (2012).
    Google Scholar 
    King, K. C. & Lively, C. M. Does genetic diversity limit disease spread in natural host populations?. Heredity 109, 199–203 (2012).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Acevedo-Whitehouse, K., Gulland, F., Greig, D. & Amos, W. Inbreeding: Disease susceptibility in California sea lions. Nature 422, 35 (2003).ADS 
    CAS 
    PubMed 

    Google Scholar 
    O’Brien, S. J. et al. Genetic basis for species vulnerability in the cheetah. Science 227, 1428–1434 (1985).ADS 
    PubMed 

    Google Scholar 
    Pearman, P. B. & Garner, T. W. J. Susceptibility of Italian agile frog populations to an emerging strain of Ranavirus parallels population genetic diversity. Ecol. Lett. 8, 401–408 (2005).
    Google Scholar 
    Reber, A., Castella, G., Christe, P. & Chapuisat, M. Experimentally increased group diversity improves disease resistance in an ant species. Ecol. Lett. 11, 682–689 (2008).PubMed 

    Google Scholar 
    Mundt, C. C. Use of multiline cultivars and cultivar mixtures for disease management. Annu. Rev. Phytopathol. 40, 381–410 (2002).CAS 
    PubMed 

    Google Scholar 
    Elton, C. S. The Ecology of Invasions by Animals and Plants (University of Chicago Press, 2000).
    Google Scholar 
    Schopmeyer, S. A. et al. Regional restoration benchmarks for Acropora cervicornis. Coral Reefs 36, 1047–1057 (2017).ADS 

    Google Scholar 
    Baums, I. B., Miller, M. W. & Hellberg, M. E. Geographic variation in clonal structure in a reef-building Caribbean coral, Acropora palmata. Ecol. Monogr. 76, 503–519 (2006).
    Google Scholar 
    Gignoux-Wolfsohn, S. A., Precht, W. F., Peters, E. C., Gintert, B. E. & Kaufman, L. S. Ecology, histopathology, and microbial ecology of a white-band disease outbreak in the threatened staghorn coral Acropora cervicornis. Dis. Aquat. Organ. 137, 217–237 (2020).PubMed 

    Google Scholar 
    Gignoux-Wolfsohn, S. A. & Vollmer, S. V. Identification of candidate coral pathogens on white band disease-infected staghorn coral. PLoS ONE 10, e0134416 (2015).PubMed 
    PubMed Central 

    Google Scholar 
    Brooks, M. et al. GlmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J. 9, 378–400 (2017).
    Google Scholar 
    Fox, J. & Weisburg, S. An R Companion to Applied Regression 3rd edn. (Sage, 2019).
    Google Scholar  More

  • in

    Transmission of stony coral tissue loss disease (SCTLD) in simulated ballast water confirms the potential for ship-born spread

    Precht, W. F., Gintert, B. E., Robbart, M. L., Fura, R. & van Woesik, R. Unprecedented disease-related coral mortality in Southeastern Florida. Sci. Rep. 6, 31374 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    NOAA. Stony Coral Tissue Loss Disease Case Definition. NOAA, Silver Spring, MD 10 (2018).Aeby, G. S. et al. Pathogenesis of a tissue loss disease affecting multiple species of corals along the Florida Reef Tract. Front Mar. Sci. 6, 00678 (2019).
    Google Scholar 
    Landsberg, J. H. et al. Stony coral tissue loss disease in Florida is associated with disruption of host–zooxanthellae physiology. Front Mar. Sci. 7, 576013 (2020).
    Google Scholar 
    Neely, K. L., Macaulay, K. A., Hower, E. K. & Dobler, M. A. Effectiveness of topical antibiotics in treating corals affected by Stony Coral Tissue Loss Disease. PeerJ 8, 9289 (2020).
    Google Scholar 
    Shilling, E. N., Combs, I. R. & Voss, J. D. Assessing the effectiveness of two intervention methods for stony coral tissue loss disease on Montastraea cavernosa. Sci. Rep. 11, 8566 (2021).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Walker, B. K., Turner, N. R., Noren, H. K. G., Buckley, S. F. & Pitts, K. A. Optimizing stony coral tissue loss disease (SCTLD) intervention treatments on Montastraea cavernosa in an endemic zone. Front Mar. Sci. 8, 666224 (2021).
    Google Scholar 
    Work, T. M. et al. Viral-like particles are associated with endosymbiont pathology in Florida corals affected by stony coral tissue loss disease. Front Mar. Sci. 8, 750658 (2021).
    Google Scholar 
    Veglia, A. J. et al. Alphaflexivirus genomes in stony coral tissue loss disease-affected, disease-exposed, and disease-unexposed coral colonies in the U.S. Virgin Islands. Microbiol. Resource Announc. 11, e01199-e1221 (2022).CAS 

    Google Scholar 
    Rosales, S. M. et al. Bacterial metabolic potential and micro-eukaryotes enriched in stony coral tissue loss disease lesions. Front Mar. Sci. 8, 776859 (2022).
    Google Scholar 
    Rosales, S. M., Clark, A. S., Huebner, L. K., Ruzicka, R. R. & Muller, E. M. Rhodobacterales and Rhizobiales are associated with stony coral tissue loss disease and its suspected sources of transmission. Front. Microbiol. 11, 681 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    Studivan, M. S. et al. Reef sediments can act as a stony coral tissue loss disease vector. Front Mar. Sci. 8, 815698 (2022).
    Google Scholar 
    Meyer, J. L. et al. Microbial community shifts associated with the ongoing stony coral tissue loss disease outbreak on the Florida Reef Tract. Front. Microbiol. 10, 2244 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    Ushijima, B. et al. Disease diagnostics and potential coinfections by Vibrio coralliilyticus during an ongoing coral disease outbreak in Florida. Front. Microbiol. 11, 2682 (2020).
    Google Scholar 
    Meiling, S. S. et al. Variable species responses to experimental stony coral tissue loss disease (SCTLD) exposure. Front Mar. Sci. 8, 670829 (2021).
    Google Scholar 
    Becker, C. C., Brandt, M., Miller, C. A. & Apprill, A. Microbial bioindicators of stony coral tissue loss disease identified in corals and overlying waters using a rapid field-based sequencing approach. Environ. Microbiol. 24, 1166–1182 (2021).PubMed 

    Google Scholar 
    Dobbelaere, T., Muller, E. M., Gramer, L. J., Holstein, D. M. & Hanert, E. Coupled epidemio-hydrodynamic modeling to understand the spread of a deadly coral disease in Florida. Front Mar. Sci. 7, 591881 (2020).
    Google Scholar 
    Dobbelaere, T. et al. Connecting the dots: Transmission of stony coral tissue loss disease from the Marquesas to the Dry Tortugas. Front Mar. Sci. 9, 778938 (2022).
    Google Scholar 
    Muller, E. M., Sartor, C., Alcaraz, N. I. & van Woesik, R. Spatial epidemiology of the stony-coral-tissue-loss disease in Florida. Front Mar. Sci. 7, 00163 (2020).
    Google Scholar 
    Sharp, W. C., Shea, C. P., Maxwell, K. E., Muller, E. M. & Hunt, J. H. Evaluating the small-scale epidemiology of the stony-coral-tissue-loss-disease in the middle Florida Keys. PLoS ONE 15, e0241871 (2020).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Williamson, O. M., Dennison, C. E., O’Neil, K. L. & Baker, A. C. Susceptibility of Caribbean brain coral recruits to stony coral tissue loss disease (SCTLD). Front Mar. Sci. 9, 821165 (2022).
    Google Scholar 
    Noonan, K. R. & Childress, M. J. Association of butterflyfishes and stony coral tissue loss disease in the Florida Keys. Coral Reefs 39, 1581–1590 (2020).
    Google Scholar 
    Dahlgren, C., Pizarro, V., Sherman, K., Greene, W. & Oliver, J. Spatial and temporal patterns of stony coral tissue loss disease outbreaks in the Bahamas. Front Mar. Sci. 8, 682114 (2021).
    Google Scholar 
    Rosenau, N. A. et al. Considering commercial vessels as potential vectors of stony coral tissue loss disease. Front Mar. Sci. 8, 709764 (2021).
    Google Scholar 
    Roth, L., Kramer, P., Doyle, E. & O’Sullivan, C. Caribbean SCTLD Dashboard. Available www.agrra.org. Accessed 06 Mar 2021. (2020).Brandt, M. E. et al. The emergence and initial impact of stony coral tissue loss disease (SCTLD) in the United States Virgin Islands. Front Mar. Sci. 8, 715329 (2021).
    Google Scholar 
    Bailey, S. A. et al. Trends in the detection of aquatic non-indigenous species across global marine, estuarine and freshwater ecosystems: A 50-year perspective. Divers. Distrib. 26, 1780–1797 (2020).MathSciNet 

    Google Scholar 
    Hewitt, C. L., Gollasch, S. & Minchin, D. The vessel as a vector: Biofouling, ballast water and sediments. In Biological Invasions in Marine Ecosystems Vol. 204 (eds Rilov, G. & Crooks, J. A.) 117–131 (Springer, 2009).
    Google Scholar 
    Zabin, C. J. et al. Small boats provide connectivity for nonindigenous marine species between a highly invaded international port and nearby coastal harbors. Manag. Biol. Invas. 5, 97–112 (2014).
    Google Scholar 
    Ashton, G. V., Zabin, C. J., Davidson, I. C. & Ruiz, G. M. Recreational boats routinely transfer organisms and promote marine bioinvasions. Biol. Invas. 24, 1083–1096 (2022).
    Google Scholar 
    Drake, L. A., Doblin, M. A. & Dobbs, F. C. Potential microbial bioinvasions via ships’ ballast water, sediment, and biofilm. Mar. Pollut. Bull. 55, 333–341 (2007).CAS 
    PubMed 

    Google Scholar 
    Pagenkopp Lohan, K. M., Fleischer, R. C., Carney, K. J., Holzer, K. K. & Ruiz, G. M. Amplicon-based pyrosequencing reveals high diversity of protistan parasites in ships’ ballast water: Implications for biogeography and infectious diseases. Microb. Ecol. 71, 530–542 (2015).PubMed 

    Google Scholar 
    Ruiz, G. M. et al. Global spread of microorganisms by ships. Nature 408, 49–50 (2000).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Hwang, J., Park, S. Y., Lee, S. & Lee, T. K. High diversity and potential translocation of DNA viruses in ballast water. Mar. Pollut. Bull. 137, 449–455 (2018).CAS 
    PubMed 

    Google Scholar 
    Shikuma, N. J. & Hadfield, M. G. Marine biofilms on submerged surfaces are a reservoir for Escherichia coli and Vibrio cholerae. Biofouling 26, 39–46 (2009).
    Google Scholar 
    Aguirre-Macedo, M. L. et al. Ballast water as a vector of coral pathogens in the Gulf of Mexico: The case of the Cayo Arcas coral reef. Mar. Pollut. Bull. 56, 1570–1577 (2008).CAS 
    PubMed 

    Google Scholar 
    Bruno, J. F. The coral disease triangle. Nat. Clim. Chang. 5, 302–303 (2015).ADS 

    Google Scholar 
    Lakshmi, E., Priya, M. & Achari, V. S. An overview on the treatment of ballast water in ships. Ocean Coast. Manag. 199, 105296 (2021).
    Google Scholar 
    Petersen, N. B., Madsen, T., Glaring, M. A., Dobbs, F. C. & Jørgensen, N. O. G. Ballast water treatment and bacteria: Analysis of bacterial activity and diversity after treatment of simulated ballast water by electrochlorination and UV exposure. Sci. Total Environ. 648, 408–421 (2019).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Romero-Martínez, L., Moreno-Andrés, J., Acevedo-Merino, A. & Nebot, E. Evaluation of ultraviolet disinfection of microalgae by growth modeling: Application to ballast water treatment. J. Appl. Phycol. 28, 2831–2842 (2016).
    Google Scholar 
    First, M. R. et al. Stratification of living organisms in ballast tanks: How do organism concentrations vary as ballast water is discharged?. Environ. Sci. Technol. 47, 4442–4448 (2013).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Drake, L. A. et al. Microbial ecology of ballast water during a transoceanic voyage and the effects of open-ocean exchange. Mar. Ecol. Prog. Ser. 233, 13–20 (2002).ADS 

    Google Scholar 
    Khandeparker, L., Kuchi, N., Desai, D. V. & Anil, A. C. Changes in the ballast water tank bacterial community during a trans-sea voyage: Elucidation through next generation DNA sequencing. J. Environ. Manag. 273, 111018 (2020).
    Google Scholar 
    Ruiz, G. M., Lorda, J., Arnwine, A. & Lion, K. Shipping patterns associated with the Panama Canal: Effects on biotic exchange? In Bridging Divides Vol. 83 (eds Gollasch, S. et al.) 113–126 (Springer, 2006).
    Google Scholar 
    Pagano, A., Wang, G., Sánchez, O., Ungo, R. & Tapiero, E. The impact of the Panama Canal expansion on Panama’s maritime cluster. Marit. Policy Manag. 43, 164–178 (2016).
    Google Scholar 
    Muirhead, J. R., Minton, M. S., Miller, W. A. & Ruiz, G. M. Projected effects of the Panama Canal expansion on shipping traffic and biological invasions. Divers. Distrib. 21, 75–87 (2015).
    Google Scholar 
    Ros, M. et al. The Panama Canal and the transoceanic dispersal of marine invertebrates: Evaluation of the introduced amphipod Paracaprella pusilla Mayer, 1890 in the Pacific Ocean. Mar. Environ. Res. 99, 204–211 (2014).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Stehouwer, P. P., Buma, A. & Peperzak, L. A comparison of six different ballast water treatment systems based on UV radiation, electrochlorination and chlorine dioxide. Environ. Technol. 36, 2094–2104 (2015).CAS 
    PubMed 

    Google Scholar 
    Wu, Y., Li, Z., Du, W. & Gao, K. Physiological response of marine centric diatoms to ultraviolet radiation, with special reference to cell size. J. Photochem. Photobiol., B 153, 1–6 (2015).CAS 

    Google Scholar 
    Aguirre, L. E. et al. Diatom frustules protect DNA from ultraviolet light. Sci. Rep. 8, 5138 (2018).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    First, M. R. & Drake, L. A. Life after treatment: Detecting living microorganisms following exposure to UV light and chlorine dioxide. J. Appl. Phycol. 26, 227–235 (2014).CAS 

    Google Scholar 
    Liebich, V., Stehouwer, P. P. & Veldhuis, M. Re-growth of potential invasive phytoplankton following UV-based ballast water treatment. Aquat. Invas. 7, 29–36 (2012).
    Google Scholar 
    Hess-Erga, O. K., Moreno-Andrés, J., Enger, Ø. & Vadstein, O. Microorganisms in ballast water: Disinfection, community dynamics, and implications for management. Sci. Total Environ. 657, 704–716 (2019).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Endresen, Ø., Lee Behrens, H., Brynestad, S., Bjørn Andersen, A. & Skjong, R. Challenges in global ballast water management. Mar. Pollut. Bull. 48, 615–623 (2004).CAS 
    PubMed 

    Google Scholar 
    Vorkapić, A., Radonja, R. & Zec, D. Cost efficiency of ballast water treatment systems based on ultraviolet irradiation and electrochlorination. Promet Traffic Transp. 30, 343–348 (2018).
    Google Scholar 
    King, D., Hagan, P., Riggio, M. & Wright, D. Preview of global ballast water treatment markets. J. Mar. Eng. Technol. 11, 3–15 (2012).
    Google Scholar 
    Wang, Z., Saebi, M., Corbett, J. J., Grey, E. K. & Curasi, S. R. Integrated biological risk and cost model analysis supports a geopolitical shift in ballast water management. Environ. Sci. Technol. 55, 12791–12800 (2021).CAS 
    PubMed 

    Google Scholar 
    Moreno-Andrés, J. & Peperzak, L. Operational and environmental factors affecting disinfection byproducts formation in ballast water treatment systems. Chemosphere 232, 496–505 (2019).ADS 
    PubMed 

    Google Scholar 
    David, M., Linders, J., Gollasch, S. & David, J. Is the aquatic environment sufficiently protected from chemicals discharged with treated ballast water from vessels worldwide? A decadal environmental perspective and risk assessment. Chemosphere 207, 590–600 (2018).ADS 
    CAS 
    PubMed 

    Google Scholar 
    U.S. Environmental Protection Agency. Generic protocol for the verification of ballast water treatment technology, version 5.1. Report number EPA/600/R-10/146. Washington, D.C. 157 (2010).Evans, J. S., Paul, V. J., Ushijima, B. & Kellogg, C. A. Combining tangential flow filtration and size fractionation of mesocosm water as a method for the investigation of waterborne coral diseases. Biol. Methods Protocols 7, bpac007 (2022).
    Google Scholar 
    Fujimoto, M. et al. Application of Ion Torrent sequencing to the assessment of the effect of alkali ballast water treatment on microbial community diversity. PLoS ONE 9, e107534 (2014).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    United States Coast Guard. Ballast Water Best Management Practices to Reduce the Likelihood of Transporting Pathogens That May Spread Stony Coral Tissue Loss Disease. Marine Safety Information Bulletin 07–19. Washington, D.C. 2 (2019).Bolton, J. R. & Linden, K. G. Standardization of methods for fluence (UV dose) determination in bench-scale UV experiments. J. Environ. Eng. 129, 209–215 (2003).CAS 

    Google Scholar 
    Enochs, I. C. et al. The influence of diel carbonate chemistry fluctuations on the calcification rate of Acropora cervicornis under present day and future acidification conditions. J. Exp. Mar. Biol. Ecol. 506, 135–143 (2018).CAS 

    Google Scholar 
    R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/. Preprint at https://www.r-project.org/ (2019).Therneau, T. M. survival: A package for survival analysis in R. R package version 3.2–13. (2021).Kassambara, A., Kosinski, M. & Biecek, P. survminer: Drawing survival curves using “ggplot2”. R package version 0.4.9. (2021).Bakalar, G. Review of interdisciplinary devices for detecting the quality of ship ballast water. Springerplus 3, 468 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    Water Environmental Federation & American Public Health Association. Standard methods for the examination of water and wastewater. Washington, D.C. 21 (2005).Steinberg, M. K., Lemieux, E. J. & Drake, L. A. Determining the viability of marine protists using a combination of vital, fluorescent stains. Mar. Biol. 158, 1431–1437 (2011).
    Google Scholar 
    Oksanen, J. et al. vegan: Community ecology package. R package version 2.0–10. (2015).Martinez Arbizu, P. pairwiseAdonis: Pairwise multilevel comparison using adonis. R package version 0.4. (2020).Studivan, MS. Mstudiva/SCTLD-ballast-transmission: Stony coral tissue loss disease ballast transmission and treatment (Version 1.0), Zenodo, https://doi.org/10.5281/zenodo.6561517 (2022). More

  • in

    Plant-associated Bacillus mobilizes its secondary metabolites upon perception of the siderophore pyochelin produced by a Pseudomonas competitor

    Nayfach S, Roux S, Seshadri R, Udwary D, Varghese N, Schulz F, et al. A genomic catalog of Earth’s microbiomes. Nat Biotechnol. 2021;39:499–509.CAS 
    PubMed 

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

    Google Scholar 
    Cordovez V, Dini-Andreote F, Carrión VJ, Raaijmakers JM. Ecology and evolution of plant microbiomes. Annu Rev Microbiol. 2019;73:69–88.CAS 
    PubMed 

    Google Scholar 
    Trivedi P, Leach JE, Tringe SG, Sa T, Singh BK. Plant–microbiome interactions: from community assembly to plant health. Nat Rev Microbiol. 2020;18:607–21.CAS 
    PubMed 

    Google Scholar 
    Fitzpatrick CR, Salas-González I, Conway JM, Finkel OM, Gilbert S, Russ D, et al. The plant microbiome: From ecology to reductionism and beyond. Annu Rev Microbiol. 2020;74:81–100.CAS 
    PubMed 

    Google Scholar 
    Schmidt R, Ulanova D, Wick LY, Bode HB, Garbeva P. Microbe-driven chemical ecology: past, present and future. ISME J. 2019;13:2656–63.PubMed 
    PubMed Central 

    Google Scholar 
    Tyc O, Song C, Dickschat JS, Vos M, Garbeva P. The ecological role of volatile and soluble secondary metabolites produced by soil bacteria. Trends Microbiol. 2017;25:280–92.CAS 
    PubMed 

    Google Scholar 
    Romero D, Traxler MF, López D, Kolter R. Antibiotics as signal molecules. Chem Rev. 2011;111:5492–505.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Traxler MF, Seyedsayamdost MR, Clardy J, Kolter R. Interspecies modulation of bacterial development through iron competition and siderophore piracy. Mol Microbiol. 2012;86:628–44.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Bernal P, Llamas MA, Filloux A. Type VI secretion systems in plant-associated bacteria. Environ Microbiol. 2018;20:1–15.PubMed 

    Google Scholar 
    Okada BK, Seyedsayamdost MR. Antibiotic dialogues: induction of silent biosynthetic gene clusters by exogenous small molecules. FEMS Microbiol Rev. 2017;41:19–33.CAS 
    PubMed 

    Google Scholar 
    Zhang C, Straight PD. Antibiotic discovery through microbial interactions. Curr Opin Microbiol. 2019;51:64–71.CAS 
    PubMed 

    Google Scholar 
    Traxler MF, Kolter R. Natural products in soil microbe interactions and evolution. Nat Prod Rep. 2015;32:956–70.CAS 
    PubMed 

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

    Google Scholar 
    Anckaert A, Arias AA, Hoff G, Calonne-Salmon M, Declerck S, Ongena M. The use of Bacillus spp. as bacterial biocontrol agents to control plant diseases. In: Köhl J, Ravensberg W, editors. Microbial bioprotectants for plant disease management. Cambridge, UK: Burleigh Dodds Science Publishing; 2022. p. 1–54.Dunlap CA. Taxonomy of registered Bacillus spp. strains used as plant pathogen antagonists. Biol Control. 2019;134:82–86.
    Google Scholar 
    Ye M, Tang X, Yang R, Zhang H, Li F, Tao F, et al. Characteristics and application of a novel species of Bacillus: Bacillus velezensis. ACS Chem Biol. 2018;13:500–5.CAS 
    PubMed 

    Google Scholar 
    Grubbs KJ, Bleich RM, Santa Maria KC, Allen SE, Farag S, Shank EA, et al. Large-scale bioinformatics analysis of Bacillus genomes uncovers conserved roles of natural products in bacterial physiology. mSystems 2017;2:e00040–17.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Harwood CR, Mouillon J-MM, Pohl S, Arnau J. Secondary metabolite production and the safety of industrially important members of the Bacillus subtilis group. FEMS Microbiol Rev. 2018;42:721–38.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Köhl J, Kolnaar R, Ravensberg WJ. Mode of action of microbial biological control agents against plant diseases: Relevance beyond efficacy. Front Plant Sci. 2019;10:1–19.
    Google Scholar 
    Li Y, Rebuffat S. The manifold roles of microbial ribosomal peptide-based natural products in physiology and ecology. J Biol Chem. 2020;295:34–54.Andrić S, Meyer T, Ongena M. Bacillus responses to plant-associated fungal and bacterial communities. Front Microbiol. 2020;11:1350.PubMed 
    PubMed Central 

    Google Scholar 
    Zhang L, Sun C. Fengycins, cyclic lipopeptides from marine Bacillus subtilis strains, kill the plant-pathogenic fungus Magnaporthe grisea by inducing reactive oxygen species production and chromatin condensation. Appl Environ Microbiol. 2018;84:e00445–18.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Molina-Santiago C, Vela-Corcía D, Petras D, Díaz-Martínez L, Pérez-Lorente AI, Sopeña-Torres S, et al. Chemical interplay and complementary adaptative strategies toggle bacterial antagonism and co-existence. Cell Rep. 2021;36:109449.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Molina-Santiago C, Pearson JR, Navarro Y, Berlanga-Clavero MV, Caraballo-Rodriguez AM, Petras D, et al. The extracellular matrix protects Bacillus subtilis colonies from Pseudomonas invasion and modulates plant co-colonization. Nat Commun. 2019;10:1919.PubMed 
    PubMed Central 

    Google Scholar 
    Almoneafy AA, Kakar KU, Nawaz Z, Li B, Saand MA, Chun-lan Y, et al. Tomato plant growth promotion and antibacterial related-mechanisms of four rhizobacterial Bacillus strains against Ralstonia solanacearum. Symbiosis 2014;63:59–70.CAS 

    Google Scholar 
    Kakar KU, Duan Y-P, Nawaz Z, Sun G, Almoneafy AA, Hassan MA, et al. A novel rhizobacterium Bk7 for biological control of brown sheath rot of rice caused by Pseudomonas fuscovaginae and its mode of action. Eur J Plant Pathol. 2014;138:819–34.
    Google Scholar 
    Raynaud X, Nunan N. Spatial ecology of bacteria at the microscale in soil. PLoS ONE. 2014;9:e87217.PubMed 
    PubMed Central 

    Google Scholar 
    Girard L, Lood C, Höfte M, Vandamme P, Rokni-Zadeh H, van Noort V, et al. The ever-expanding Pseudomonas genus: description of 43 new species and partition of the Pseudomonas putida group. Microorganisms. 2021;9:1–24.
    Google Scholar 
    Hua GKH, Höfte M. The involvement of phenazines and cyclic lipopeptide sessilin in biocontrol of Rhizoctonia root rot on bean (Phaseolus vulgaris) by Pseudomonas sp. CMR12a is influenced by substrate composition. Plant Soil. 2015;388:243–53.CAS 

    Google Scholar 
    Ma Z, Hoang Hua GKH, Ongena M, Höfte M. Role of phenazines and cyclic lipopeptides produced by Pseudomonas sp. CMR12a in induced systemic resistance on rice and bean. Environ Microbiol Rep. 2016;8:896–904.PubMed 

    Google Scholar 
    Olorunleke FE, Hua GKH, Kieu NP, Ma Z, Höfte M. Interplay between orfamides, sessilins and phenazines in the control of Rhizoctonia diseases by Pseudomonas sp. CMR12a. Environ Microbiol Rep. 2015;7:774–81.CAS 
    PubMed 

    Google Scholar 
    van Gestel J, Vlamakis H, Kolter R. From cell differentiation to cell collectives: Bacillus subtilis uses division of labor to migrate. PLoS Biol. 2015;13:1–29.
    Google Scholar 
    Nihorimbere V, Cawoy H, Seyer A, Brunelle A, Thonart P, Ongena M. Impact of rhizosphere factors on cyclic lipopeptide signature from the plant beneficial strain Bacillus amyloliquefaciens S499. FEMS Microbiol Ecol. 2012;79:176–91.CAS 
    PubMed 

    Google Scholar 
    Hoff G, Arias AA, Boubsi F, Pršić J, Meyer T, Ibrahim HMM, et al. Surfactin stimulated by pectin molecular patterns and root exudates acts as a key driver of the Bacillus-plant mutualistic interaction. MBio 2021;12:e01774–21.CAS 
    PubMed Central 

    Google Scholar 
    Andrić S, Meyer T, Rigolet A, Prigent-Combaret C, Höfte M, Balleux G, et al. Lipopeptide interplay mediates molecular interactions between soil bacilli and pseudomonads. Microbiol Spectr. 2021;9:e0203821.PubMed 

    Google Scholar 
    Pluskal T, Castillo S, Villar-Briones A, Orešič M. MZmine 2: modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data. BMC Bioinform. 2010;11:395.
    Google Scholar 
    Li W, Godzik A. Cd-hit: A fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics. 2006;22:1658–9.CAS 
    PubMed 

    Google Scholar 
    Bodenhofer U, Bonatesta E, Horejš-Kainrath C, Hochreiter S. msa: an R package for multiple sequence alignment. Bioinformatics. 2015;31:3997–9.CAS 
    PubMed 

    Google Scholar 
    Paradis E, Claude J, Strimmer K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 2004;20:289–90.CAS 
    PubMed 

    Google Scholar 
    Ivica Letunic PB. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 2021;49:W293–W296.PubMed 
    PubMed Central 

    Google Scholar 
    R Core Team (2020). R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2020.Steinke K, Mohite OS, Weber T, Kovács ÁT. Phylogenetic distribution of secondary metabolites in the Bacillus subtilis species complex. mSystems. 2021;6:2–10.
    Google Scholar 
    Molinatto G, Puopolo G, Sonego P, Moretto M, Engelen K, Viti C, et al. Complete genome sequence of Bacillus amyloliquefaciens subsp. plantarum S499, a rhizobacterium that triggers plant defences and inhibits fungal phytopathogens. J Biotechnol. 2016;238:56–59.CAS 
    PubMed 

    Google Scholar 
    Fan B, Wang C, Song X, Ding X, Wu L, Wu H, et al. Bacillus velezensis FZB42 in 2018: The gram-positive model strain for plant growth promotion and biocontrol. Front Microbiol. 2018;9:3389.
    Google Scholar 
    Mansfield J, Genin S, Magori S, Citovsky V, Sriariyanum M, Ronald P, et al. Top 10 plant pathogenic bacteria in molecular plant pathology. Mol Plant Pathol. 2012;13:614–29.PubMed 
    PubMed Central 

    Google Scholar 
    Scholz R, Vater J, Budiharjo A, Wang Z, He Y, Dietel K, et al. Amylocyclicin, a novel circular bacteriocin produced by Bacillus amyloliquefaciens FZB42. J Bacteriol. 2014;196:1842–52.PubMed 
    PubMed Central 

    Google Scholar 
    Lembrechts JJ, van den Hoogen J, Aalto J, Ashcroft MB, De Frenne P, Kemppinen J, et al. Global maps of soil temperature. Glob Chang Biol. 2022;28:3110–44.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Blake C, Christensen MN, Kovacs AT. Molecular aspects of plant growth promotion and protection by Bacillus subtilis. Mol Plant-Microbe Interact. 2021;34:15–25.CAS 
    PubMed 

    Google Scholar 
    Arnaouteli S, Bamford NC, Stanley-Wall NR, Kovács ÁT. Bacillus subtilis biofilm formation and social interactions. Nat Rev Microbiol. 2021;19:600–14.CAS 
    PubMed 

    Google Scholar 
    D’aes J, Hua GKH, De Maeyer K, Pannecoucque J, Forrez I, Ongena M, et al. Biological control of Rhizoctonia root rot on bean by phenazine- and cyclic lipopeptide-producing Pseudomonas CMR12a. Phytopathology. 2011;101:996–1004.PubMed 

    Google Scholar 
    Grandchamp GM, Caro L, Shank EA. Pirated siderophores promote sporulation in Bacillus subtilis. Appl Environ Microbiol. 2017;83:e03293–16.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Miethke M, Klotz O, Linne U, May JJ, Beckering CL, Marahiel MA. Ferri-bacillibactin uptake and hydrolysis in Bacillus subtilis. Mol Microbiol. 2006;61:1413–27.CAS 
    PubMed 

    Google Scholar 
    Pi H, Helmann JD. Genome-wide characterization of the fur regulatory network reveals a link between catechol degradation and bacillibactin metabolism in Bacillus subtilis. MBio. 2018;9:1–15.
    Google Scholar 
    Adler C, Corbalán NS, Seyedsayamdost MR, Pomares MF, de Cristóbal RE, Clardy J, et al. Catecholate siderophores protect bacteria from pyochelin toxicity. PLoS ONE. 2012;7:e46754.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Trottmann F, Franke J, Ishida K, García-Altares M, Hertweck C. A pair of bacterial siderophores releases and traps an intercellular signal molecule: an unusual case of natural nitrone bioconjugation. Angew Chem. 2019;58:200–4.CAS 

    Google Scholar 
    Mongkolsuk S, Helmann JD. Regulation of inducible peroxide stress responses. Mol Microbiol. 2002;45:9–15.CAS 
    PubMed 

    Google Scholar 
    Cox CD, Rinehart KL, Moore ML, Cook JC. Pyochelin: novel structure of an iron-chelating growth promoter for Pseudomonas aeruginosa. Proc Natl Acad Sci USA. 1981;78:4256–60.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Youard ZA, Mislin GLA, Majcherczyk PA, Schalk IJ, Reimmann C. Pseudomonas fluorescens CHA0 produces enantio-pyochelin, the optical antipode of the Pseudomonas aeruginosa siderophore pyochelin. J Biol Chem. 2007;282:35546–53.CAS 
    PubMed 

    Google Scholar 
    Ronnebaum TA, Lamb AL. Nonribosomal peptides for iron acquisition: pyochelin biosynthesis as a case study. Curr Opini Struct Biol. 2018;53:1–11.CAS 

    Google Scholar 
    Seipke RF, Song L, Bicz J, Laskaris P, Yaxley AM, Challis GL, et al. The plant pathogen Streptomyces scabies 87-22 has a functional pyochelin biosynthetic pathway that is regulated by TetR- and AfsR-family proteins. Microbiology. 2011;157:2681–93.CAS 
    PubMed 

    Google Scholar 
    Gu S, Wei Z, Shao Z, Friman VP, Cao K, Yang T, et al. Competition for iron drives phytopathogen control by natural rhizosphere microbiomes. Nat Microbiol. 2020;5:1002–10.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Komaki H, Ichikawa N, Hosoyama A, Hamada M, Igarashi Y. In silico analysis of PKS and NRPS gene clusters in arisostatin-and kosinostatin-producers and description of Micromonospora okii sp. nov. Antibiotics. 2021;10:1447.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Engelbrecht A, Saad H, Gross H, Kaysser L. Natural products from Nocardia and their role in pathogenicity. Micro Physiol. 2021;31:217–32.
    Google Scholar 
    Inahashi Y, Zhou S, Bibb MJ, Song L, Al-Bassam MM, Bibb MJ, et al. Watasemycin biosynthesis in Streptomyces venezuelae: thiazoline C-methylation by a type B radical-SAM methylase homologue. Chem Sci. 2017;8:2823–31.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Song J, Qiu S, Zhao J, Han C, Wang Y, Sun X, et al. Pseudonocardia tritici sp. nov., a novel actinomycete isolated from rhizosphere soil of wheat (Triticum aestivum L.). Nat Microbiol. 2019;12:470–80.
    Google Scholar 
    Sayed AM, Abdel-Wahab NM, Hassan HM, Abdelmohsen UR. Saccharopolyspora: an underexplored source for bioactive natural products. J Appl Microbiol. 2020;128:314–29.CAS 
    PubMed 

    Google Scholar 
    Nordstedt NP, Jones ML. Genomic analysis of Serratia plymuthica MBSA-MJ1: A plant growth promoting rhizobacteria that improves water stress tolerance in greenhouse ornamentals. Front Microbiol. 2021;12:653556.PubMed 
    PubMed Central 

    Google Scholar 
    Zhalnina K, Louie KB, Hao Z, Mansoori N, Da Rocha UN, Shi S, et al. Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly. Nat Microbiol. 2018;3:470–80.CAS 
    PubMed 

    Google Scholar 
    Takahashi Y, Malisorn K, Kanchanasin P, Phongsopitanun W, Tanasupawat S, Spain AM, et al. Actinomadura rhizosphaerae sp. nov., isolated from rhizosphere soil of the plant Azadirachta indica. ISME J 2018;68:3012–6.
    Google Scholar 
    Takahashi Y. Genus Kitasatospora, taxonomic features and diversity of secondary metabolites. J Antibiot. 2017;70:506–13.CAS 

    Google Scholar 
    Bennur T, Kumar AR, Zinjarde S, Javdekar V. Nocardiopsis species: Incidence, ecological roles and adaptations. Microbiol Res. 2015;174:33–47.PubMed 

    Google Scholar 
    Walterson AM, Stavrinides J. Pantoea: Insights into a highly versatile and diverse genus within the Enterobacteriaceae. J Basic Microbiol. 2015;39:33–47.
    Google Scholar 
    Sungthong R, Nakaew N. The genus Nonomuraea: a review of a rare actinomycete taxon for novel metabolites. J Basic Microbiol. 2015;55:554–65.PubMed 

    Google Scholar 
    Müller S, Strack SN, Ryan SE, Kearns DB, Kirby JR. Predation by Myxococcus xanthus induces Bacillus subtilis to form spore-filled megastructures. Appl Environ Microbiol. 2015;81:203–10.PubMed 

    Google Scholar 
    Straight PD, Fischbach MA, Walsh CT, Rudner DZ, Kolter R. A singular enzymatic megacomplex from Bacillus subtilis. Proc Natl Acad Sci USA. 2007;104:305–10.CAS 
    PubMed 

    Google Scholar 
    Barger SR, Hoefler BC, Cubillos-Ruiz A, Russell WK, Russell DH, Straight PD. Imaging secondary metabolism of Streptomyces sp. Mg1 during cellular lysis and colony degradation of competing Bacillus subtilis. Antonie van Leeuwenhoek. 2012;102:435–45.CAS 
    PubMed 

    Google Scholar 
    Ogran A, Yardeni EH, Keren-Paz A, Bucher T, Jain R, Gilhar O, et al. The plant host induces antibiotic production to select the most-beneficial colonizers. Appl Environ Microbiol. 2019;85:1–15.
    Google Scholar 
    Rosenberg G, Steinberg N, Oppenheimer-Shaanan Y, Olender T, Doron S, Ben-Ari J, et al. Not so simple, not so subtle: The interspecies competition between Bacillus simplex and Bacillus subtilis and its impact on the evolution of biofilms. npj Biofilms Microbiomes. 2016;2:15027.PubMed 
    PubMed Central 

    Google Scholar 
    Straight PD, Willey JM, Kolter R. Interactions between Streptomyces coelicolor and Bacillus subtilis: Role of surfactants in raising aerial structures. J Bacteriol. 2006;188:4918–25.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Hoefler BC, Gorzelnik KV, Yang JY, Hendricks N, Dorrestein PC, Straight PD. Enzymatic resistance to the lipopeptide surfactin as identified through imaging mass spectrometry of bacterial competition. Proc Natl Acad Sci USA. 2012;109:13082–7.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Liu Y, Kyle S, Straight PD. Antibiotic stimulation of a Bacillus subtilis migratory response. mSphere 2018;3:e00586–17.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Qi G, Zhu F, Du P, Yang X, Qiu D, Yu Z, et al. Lipopeptide induces apoptosis in fungal cells by a mitochondria-dependent pathway. Peptides. 2010;31:1978–86.CAS 
    PubMed 

    Google Scholar 
    McCully LM, Bitzer AS, Seaton SC, Smith LM, Silby MW. Interspecies social spreading: interaction between two sessile soil bacteria leads to emergence of surface motility. mSphere. 2019;4:e00696–18.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Flemming HC, Wingender J, Szewzyk U, Steinberg P, Rice SA, Kjelleberg S. Biofilms: an emergent form of bacterial life. Nat Rev Microbiol. 2016;14:563–75.CAS 
    PubMed 

    Google Scholar 
    Townsley L, Shank EA. Natural-product antibiotics: cues for modulating bacterial biofilm formation. Trends Microbiol. 2017;25:1016–26.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Sun X, Xu Z, Xie J, Hesselberg-Thomsen V, Tan T, Zheng D, et al. Bacillus velezensis stimulates resident rhizosphere Pseudomonas stutzeri for plant health through metabolic interactions. ISME J. 2022;16:774–87.CAS 
    PubMed 

    Google Scholar 
    Dumas Z, Ross-Gillespie A, Kümmerli R. Switching between apparently redundant iron-uptake mechanisms benefits bacteria in changeable environments. Proc R Soc B Biol Sci. 2013;280:20131055.
    Google Scholar 
    Lee N, Kim W, Chung J, Lee Y, Cho S, Jang KS, et al. Iron competition triggers antibiotic biosynthesis in Streptomyces coelicolor during coculture with Myxococcus xanthus. ISME J. 2020;14:1111–24.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Kramer J, Özkaya Ö, Kümmerli R. Bacterial siderophores in community and host interactions. Nat Rev Microbiol. 2020;18:152–63.CAS 
    PubMed 

    Google Scholar 
    Niehus R, Picot A, Oliveira NM, Mitri S, Foster KR. The evolution of siderophore production as a competitive trait. Evolution. 2017;71:1443–55.CAS 
    PubMed 

    Google Scholar 
    Ho YN, Lee HJ, Hsieh CT, Peng CC, Yang YL. Chemistry and biology of salicyl-capped siderophores. Stud Nat Prod Chem. 2018;59:431–90.Schalk IJ, Rigouin C, Godet J. An overview of siderophore biosynthesis among fluorescent Pseudomonads and new insights into their complex cellular organization. Environ Microbiol. 2020;22:1447–66.PubMed 

    Google Scholar 
    Deveau A, Gross H, Palin B, Mehnaz S, Schnepf M, Leblond P, et al. Role of secondary metabolites in the interaction between Pseudomonas fluorescens and soil microorganisms under iron-limited conditions. FEMS Microbiol Ecol. 2016;92:1–11.
    Google Scholar 
    Jenul C, Keim K, Jens J, Zeiler MJ, Schilcher K, Schurr M, et al. Pyochelin biotransformation shapes bacterial competition. bioRxiv. 2022. https://doi.org/10.1101/2022.04.18.486787.Ho YN, Hoo SY, Wang BW, Hsieh CT, Lin CC, Sun CH, et al. Specific inactivation of an antifungal bacterial siderophore by a fungal plant pathogen. ISME J. 2021;15:1858–61.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Lopez-Medina E, Fan D, Coughlin LA, Ho EX, Lamont IL, Reimmann C, et al. Candida albicans inhibits Pseudomonas aeruginosa virulence through suppression of pyochelin and pyoverdine biosynthesis. PLoS Pathog. 2015;11:1–34.
    Google Scholar 
    Meisel JD, Panda O, Mahanti P, Schroeder FC, Kim DH. Chemosensation of bacterial secondary metabolites modulates neuroendocrine signaling and behavior of C. elegans. Cell. 2014;159:267–80.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Finkel OM, Castrillo G, Herrera Paredes S, Salas González I, Dangl JL. Understanding and exploiting plant beneficial microbes. Curr Opin Plant Biol. 2017;38:155–63.PubMed 
    PubMed Central 

    Google Scholar 
    Saad MM, Eida AA, Hirt H, Doerner P. Tailoring plant-associated microbial inoculants in agriculture: a roadmap for successful application. J Exp Bot. 2020;71:3878–901.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ansari FA, Ahmad I. Fluorescent Pseudomonas -FAP2 and Bacillus licheniformis interact positively in biofilm mode enhancing plant growth and photosynthetic attributes. Sci Rep. 2019;9:4547.PubMed 
    PubMed Central 

    Google Scholar 
    Domenech J, Reddy MS, Kloepper JW, Ramos B, Gutierrez-Mañero J. Combined application of the biological product LS213 with Bacillus, Pseudomonas or Chryseobacterium for growth promotion and biological control of soil-borne diseases in pepper and tomato. BioControl. 2006;51:245–58.CAS 

    Google Scholar 
    Powers MJ, Sanabria-Valentín E, Bowers AA, Shank EA. Inhibition of cell differentiation in Bacillus subtilis by Pseudomonas protegens. J Bacteriol. 2015;197:2129–38.CAS 
    PubMed 
    PubMed Central 

    Google Scholar  More

  • in

    Sensing whales, storms, ships and earthquakes using an Arctic fibre optic cable

    Howe, B. M. et al. Observing the oceans acoustically. Front. Mar. Sci. 6, 426. https://doi.org/10.3389/fmars.2019.00426 (2019).Article 

    Google Scholar 
    Molenaar, M. M., Hill, D., Webster, P., Fidan, E. & Birch, B. First downhole application of distributed acoustic sensing for hydraulic-fracturing monitoring and diagnostics. SPE Drill. Complet. 27, 32–38. https://doi.org/10.2118/140561-PA (2012).Article 

    Google Scholar 
    Lindsey, N. J. et al. Fiber-optic network observations of earthquake wavefields. Geophys. Res. Lett. 44, 11792–11799. https://doi.org/10.1002/2017GLO75722 (2017).Article 
    ADS 

    Google Scholar 
    Jousset, P. et al. Dynamic strain determination using fibre-optic cables allows imaging of seismological and structural features. Nat. Commun. 9, 1–11. https://doi.org/10.1038/s41467-018-04860-y (2018).Article 
    CAS 

    Google Scholar 
    Ajo-Franklin, J. B. et al. Distributed acoustic sensing using dark fiber for near-surface characterization and broadband seismic event detection. Sci. Rep. 9, 1–14. https://doi.org/10.1038/s41598-018-36675-8 (2019).Article 
    CAS 

    Google Scholar 
    Williams, E. F. et al. Distributed sensing of microseisms and teleseisms with submarine dark fibers. Nat. Commun. 10, 1–11. https://doi.org/10.1038/s41467-019-13262-7 (2019).Article 
    CAS 

    Google Scholar 
    Lindsey, N. J., Dawe, T. C. & Ajo-Franklin, J. B. Illuminating seafloor faults and ocean dynamics with dark fiber distributed acoustic sensing. Science 366, 1103–1107. https://doi.org/10.1126/science.aay5881 (2019).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Sladen, A. et al. Distributed sensing of earthquakes and ocean-solid Earth interactions on seafloor telecom cables. Nat. Commun. 10, 5777. https://doi.org/10.1038/s41467-019-13793-z (2019).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Williams, E. F. et al. Surface gravity wave interferometry and ocean current monitoring with ocean-bottom DAS. J. Geophys. Res. Oceans 127, e2021JC018375. https://doi.org/10.1029/2021JC018375 (2022).Article 
    ADS 

    Google Scholar 
    Zhan, Z. et al. Optical polarization-based seismic and water wave sensing on transoceanic cables. Science 371, 931–936. https://doi.org/10.1126/science.abe6648 (2021).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Waagaard, O. H. et al. Real-time low noise distributed acoustic sensing in 171 km low loss fiber. OSA Contin. 4, 688–701. https://doi.org/10.1364/OSAC.408761 (2021).Article 
    CAS 

    Google Scholar 
    Rivet, D., de Cacqueray, B., Sladen, A., Roques, A. & Calbris, G. Preliminary assessment of ship detection and trajectory evaluation using distributed acoustic sensing on an optical fiber telecom cable. J. Acoust. Soc. Am. 149, 2615–2627. https://doi.org/10.1121/10.0004129 (2021).Article 
    ADS 
    PubMed 

    Google Scholar 
    Taweesintananon, K., Landrø, M., Brenne, J. K. & Haukanes, A. Distributed acoustic sensing for near-surface imaging using submarine telecommunication cable: a case study in the Trondheimsfjord, Norway. Geophysics 86, B303–B320. https://doi.org/10.1190/geo2020-0834.1 (2021).Article 

    Google Scholar 
    Matsumoto, H. et al. Detection of hydroacoustic signals on a fiber-optic submarine cable. Sci. Rep. 11, 2797. https://doi.org/10.1038/s41598-021-82093-8 (2021).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Bouffaut, L. et al. Eavesdropping at the speed of light: Distributed acoustic sensing of baleen whales in the Arctic. Front. Mar. Sci. 9, 901348. https://doi.org/10.3389/fmars.2022.901348 (2022).Article 

    Google Scholar 
    Jones, N. The quest for quieter seas. Nature 568, 158–161. https://doi.org/10.1038/d41586-019-01098-6 (2019).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Williams, R. et al. Chronic ocean noise and cetacean population models. J. Cetacean Res. Manag. 21, 85–94. https://doi.org/10.47536/jcrm.v21i1.202 (2020).Article 

    Google Scholar 
    Roman, J. et al. Whales as marine ecosystem engineers. Front. Ecol. Environ. 12, 377–385. https://doi.org/10.1890/130220 (2014).Article 

    Google Scholar 
    Pershing, A. J., Christensen, L. B., Record, N. R., Sherwood, G. D. & Stetson, P. B. The impact of whaling on the ocean carbon cycle: Why bigger was better. PLoS ONE 5, 1–9. https://doi.org/10.1371/journal.pone.0012444 (2010).Article 
    CAS 

    Google Scholar 
    IUCN – SSC Cetacean Specialist Group. Status of the World’s cetaceans (2021). https://iucn-csg.org/status-of-the-worlds-cetaceans/.Bailey, H. et al. Behavioural estimation of blue whale movements in the Northeast Pacific from state-space model analysis of satellite tracks. Endanger. Species Res. 10, 93–106. https://doi.org/10.3354/esr00239 (2010).Article 

    Google Scholar 
    Thomas, P. O., Reeves, R. R. & Brownell, R. L. Jr. Status of the world’s baleen whales. Mar. Mamm. Sci. 32, 682–734. https://doi.org/10.1111/mms.12281 (2016).Article 

    Google Scholar 
    Grigoli, F. et al. Current challenges in monitoring, discrimination, and management of induced seismicity related to underground industrial activities: A European perspective. Rev. Geophys. 55, 310–340. https://doi.org/10.1002/2016RG000542 (2017).Article 
    ADS 

    Google Scholar 
    Bigg, G. R. & Hanna, E. Impacts and effects of ocean warming on the weather. In: Laffoley, D. & Baxter, J. M. (eds.) Explaining ocean warming: Causes, scale, effects and consequences, 359–372, https://doi.org/10.2305/IUCN.CH.2016.08.en (International Union for Conservation of Nature and Natural Resources (IUCN), Gland, Switzerland, 2016).Hartog, A. H. An Introduction to Distributed Optical Fibre Sensors 1st edn. (CRC Press, 2017). https://doi.org/10.1201/9781315119014.Book 

    Google Scholar 
    Lin, J., Fang, S., Li, X., Wu, R. & Zheng, H. Seismological observations of ocean swells induced by Typhoon Megi using dispersive microseisms recorded in coastal areas. Remote Sens.https://doi.org/10.3390/rs10091437 (2018).Article 

    Google Scholar 
    Munk, W. H., Miller, G. R., Snodgrass, F. E., Barber, N. F. & Deacon, G. E. R. Directional recording of swell from distant storms. Philos. Trans. R. Soc. Lond. Ser. A Math. Phys. Sci. 255, 505–584. https://doi.org/10.1098/rsta.1963.0011 (1963).Article 
    ADS 

    Google Scholar 
    Mellinger, D. K. & Clark, C. W. Blue whale (balaenoptera musculus) sounds from the North Atlantic. J. Acoust. Soc. Am. 114, 1108–1119. https://doi.org/10.1121/1.1593066 (2003).Article 
    ADS 
    PubMed 

    Google Scholar 
    Ou, H., Au, W. W., Van Parijs, S., Oleson, E. M. & Rankin, S. Discrimination of frequency-modulated baleen whale downsweep calls with overlapping frequencies. J. Acoust. Soc. Am. 137, 3024–3032. https://doi.org/10.1121/1.4919304 (2015).Article 
    ADS 
    PubMed 

    Google Scholar 
    Saito, T. & Tsushima, H. Synthesizing ocean bottom pressure records including seismic wave and tsunami contributions: Toward realistic tests of monitoring systems. J. Geophys. Res. Solid Earth 121, 8175–8195. https://doi.org/10.1002/2016JB013195 (2016).Article 
    ADS 

    Google Scholar 
    Rørstadbotnen, R. A. et al. Analysis of a local earthquake in the Arctic using a 120 km long fibre-optic cable. In 83rd EAGE Annual Conference & Exhibition, vol. 2022 of Conference Proceedings, 1–5, https://doi.org/10.3997/2214-4609.202210404 (European Association of Geoscientists & Engineers, 2022).Bromirski, P. D. & Duennebier, F. K. The near-coastal microseism spectrum: Spatial and temporal wave climate relationships. J. Geophys. Res. Solid Earth 107, ESE 5-1-20. https://doi.org/10.1029/2001JB000265 (2002).Article 

    Google Scholar 
    Pasch, R. J. National hurricane center tropical cyclone report: Tropical storm Edouard (AL052020). Technical report, National Oceanic and Atmospheric Administration (2021). https://www.nhc.noaa.gov/data/tcr/AL052020_Edouard.pdf.Gobato, R. & Heidari, A. Cyclone Bomb hits Southern Brazil in 2020. J. Atmos. Sci. Res. 3, 8–12. https://doi.org/10.30564/jasr.v3i3.2163 (2020).Article 

    Google Scholar 
    Khalid, A., de Lima, Ad. S., Cassalho, F., Miesse, T. & Ferreira, C. Hydrodynamic and wave responses during storm surges on the Southern Brazilian Coast: A real-time forecast system. Water 12, 3397. https://doi.org/10.3390/w12123397 (2020).Article 

    Google Scholar 
    Ćirić, J. Weather warning for Central Highland, Northwest Iceland (2020). https://www.icelandreview.com/travel/weather-warning-for-central-highland-northwest-iceland/.Schoeman, R. P., Patterson-Abrolat, C. & Plön, S. A global review of vessel collisions with marine animals. Front. Mar. Sci. 7, 292. https://doi.org/10.3389/fmars.2020.00292 (2020).Article 

    Google Scholar 
    Ringrose, P. S. et al. Storage of carbon dioxide in saline aquifers: Physicochemical processes, key constraints, and scale-up potential. Annu. Rev. Chem. Biomol. Eng. 12, 471–494. https://doi.org/10.1146/annurev-chembioeng-093020-091447 (2021).Article 
    CAS 
    PubMed 

    Google Scholar 
    Nishimura, T. et al. Source location of volcanic earthquakes and subsurface characterization using fiber-optic cable and distributed acoustic sensing system. Sci. Rep. 11, 6319. https://doi.org/10.1038/s41598-021-85621-8 (2021).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ardhuin, F. & Herbers, T. H. C. Noise generation in the solid Earth, oceans and atmosphere, from nonlinear interacting surface gravity waves in finite depth. J. Fluid Mech. 716, 316–348. https://doi.org/10.1017/jfm.2012.548 (2013).Article 
    ADS 
    MATH 

    Google Scholar 
    Airy, G. B. Encyclopaedia Metropolitana (1817–1845), vol. 3 of Mixed Sciences, chap. Tides and waves (London, 1841).Craik, A. D. The origins of water wave theory. Annu. Rev. Fluid Mech. 36, 1–28. https://doi.org/10.1146/annurev.fluid.36.050802.122118 (2004).Article 
    ADS 
    MathSciNet 
    MATH 

    Google Scholar 
    Matsumoto, H., Inoue, S. & Ohmachi, T. Dynamic response of bottom water pressure due to the 2011 Tohoku earthquake. J. Disaster Res. 7, 468–475. https://doi.org/10.20965/jdr.2012.p0468 (2012).Article 

    Google Scholar 
    Landrø, M. & Hatchell, P. Normal modes in seismic data: Revisited. Geophysics 77, W27–W40. https://doi.org/10.1190/geo2011-0094.1 (2012).Article 
    ADS 

    Google Scholar  More

  • in

    Site-specific temporal variation of population dynamics in subalpine endemic plant species

    Theurillat, J.-P. & Guisan, A. Potential impact of climate change on vegetation in the European Alps: A review. Clim. Change 50, 77–109 (2001).CAS 

    Google Scholar 
    Diaz, H. F. & Eischeid, J. K. Disappearing “alpine tundra” Köppen climatic type in the western United States. Geophys. Res. Lett. 34, L18707 (2007).ADS 

    Google Scholar 
    Dirnböck, T., Essl, F. & Rabitsch, W. Disproportional risk for habitat loss of high-altitude endemic species under climate change. Glob. Change Biol. 17, 990–996 (2011).ADS 

    Google Scholar 
    Myers, N., Mittermeier, R. A., Mittermeier, C. G., Da Fonseca, G. A. & Kent, J. Biodiversity hotspots for conservation priorities. Nature 403, 853–858 (2000).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Pauli, H., Gottfried, M., Dirnböck, T., Dullinger, S. & Grabherr, G. Assessing the long-term dynamics of endemic plants at summit habitats. In Alpine Biodiversity in Europe (eds. Nagy, L., Grabherr, G., Körner, C., & Thompson, D. B.) 195–207 (Springer, 2003).Cogoni, D., Sulis, E., Bacchetta, G. & Fenu, G. The unpredictable fate of the single population of a threatened narrow endemic Mediterranean plant. Biodivers. Conserv. 28, 1799–1813 (2019).
    Google Scholar 
    Cursach, J., Besnard, A., Rita, J. & Fréville, H. Demographic variation and conservation of the narrow endemic plant Ranunculus weyleri. Acta Oecol. 53, 102–109 (2013).ADS 

    Google Scholar 
    Dibner, R. R., DeMarche, M. L., Louthan, A. M. & Doak, D. F. Multiple mechanisms confer stability to isolated populations of a rare endemic plant. Ecol. Monogr. 89, e01360 (2019).
    Google Scholar 
    Boyce, M. S., Haridas, C. V., Lee, C. T., NCEAS Stochastic Demography Working Group. Demography in an increasingly variable world. Trends Ecol. Evol. 21, 141–148 (2006).PubMed 

    Google Scholar 
    Buckley, Y. M. et al. Causes and consequences of variation in plant population growth rate: A synthesis of matrix population models in a phylogenetic context. Ecol. Lett. 13, 1182–1197 (2010).PubMed 

    Google Scholar 
    Abbott, R. E., Doak, D. F. & DeMarche, M. L. Portfolio effects, climate change, and the persistence of small populations: Analyses on the rare plant Saussurea weberi. Ecology 98, 1071–1081 (2017).PubMed 

    Google Scholar 
    Villellas, J., Doak, D. F., García, M. B. & Morris, W. F. Demographic compensation among populations: What is it, how does it arise and what are its implications?. Ecol. Lett. 18, 1139–1152 (2015).PubMed 

    Google Scholar 
    Doak, D. F. & Morris, W. F. Demographic compensation and tipping points in climate-induced range shifts. Nature 467, 959–962 (2010).ADS 
    CAS 
    PubMed 

    Google Scholar 
    García-Camacho, R., Albert, M. J. & Escudero, A. Small-scale demographic compensation in a high-mountain endemic: The low edge stands still. Plant Ecol. Divers. 5, 37–44 (2012).
    Google Scholar 
    Andrello, M. et al. Accounting for stochasticity in demographic compensation along the elevational range of an alpine plant. Ecol. Lett. 23, 870–880 (2020).PubMed 

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

    Google Scholar 
    Ægisdóttir, H. H., Kuss, P. & Stöcklin, J. Isolated populations of a rare alpine plant show high genetic diversity and considerable population differentiation. Ann. Bot. 104, 1313–1322 (2009).PubMed 
    PubMed Central 

    Google Scholar 
    Morente-López, J. et al. Geography and environment shape landscape genetics of Mediterranean alpine species Silene ciliata Poiret. (Caryophyllaceae). Front. Plant Sci. 9, 1698 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    Franks, S. J., Weber, J. J. & Aitken, S. N. Evolutionary and plastic responses to climate change in terrestrial plant populations. Evol. Appl. 7, 123–139 (2014).PubMed 

    Google Scholar 
    Jeong, H., Cho, Y.-C. & Kim, E. Differential plastic responses to temperature and nitrogen deposition in the subalpine plant species, Primula farinosa subsp. modesta. AoB Plants 13, plab061 (2021).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Sulis, E., Bacchetta, G., Cogoni, D. & Fenu, G. From global to local scale: Where is the best for conservation purpose?. Biodivers. Conserv. 30, 183–200 (2021).
    Google Scholar 
    Hambler, D. & Dixon, J. Primula farinosa L. J. Ecol. 91, 694–705 (2003).
    Google Scholar 
    Arnold, E. & Richards, A. On the occurrence of unilateral incompatibility in Primula section Aleuritia Duby and the origin of Primula scotica Hook. Bot. J. Linn. Soc. 128, 359–368 (1998).
    Google Scholar 
    Tribsch, A. Areas of endemism of vascular plants in the eastern Alps in relation to Pleistocene glaciation. J. Biogeogr. 31, 747–760 (2004).
    Google Scholar 
    Chung, J.-M., Son, S.-W., Kim, S.-Y., Park, G.-W. & Kim, S.-S. Genetic diversity and geographic differentiation in the endangered Primula farinosa subsp. modesta, a subalpine endemic to Korea. Korean J. Plant. Taxon. 43, 236–243 (2013).
    Google Scholar 
    Lindborg, R. & Ehrlén, J. Evaluating the extinction risk of a perennial herb: Demographic data versus historical records. Conserv. Biol. 16, 683–690 (2002).
    Google Scholar 
    Caswell, H. Matrix Population Models, 2nd ed (Sinauer Associates Inc, 2000).Salguero-Gómez, R. & De Kroon, H. Matrix projection models meet variation in the real world. J. Ecol. 98, 250–254 (2010).
    Google Scholar 
    Jongejans, E. et al. Region versus site variation in the population dynamics of three short-lived perennials. J. Ecol. 98, 279–289 (2010).
    Google Scholar 
    Jongejans, E. & De Kroon, H. Space versus time variation in the population dynamics of three co-occurring perennial herbs. J. Ecol. 93, 681–692 (2005).
    Google Scholar 
    Suggitt, A. J. et al. Habitat microclimates drive fine-scale variation in extreme temperatures. Oikos 120, 1–8 (2011).
    Google Scholar 
    Tomimatsu, H. & Ohara, M. Demographic response of plant populations to habitat fragmentation and temporal environmental variability. Oecologia 162, 903–911 (2010).ADS 
    PubMed 

    Google Scholar 
    Kudernatsch, T., Fischer, A., Bernhardt-Römermann, M. & Abs, C. Short-term effects of temperature enhancement on growth and reproduction of alpine grassland species. Basic Appl. Ecol. 9, 263–274 (2008).
    Google Scholar 
    Kim, E. & Donohue, K. Local adaptation and plasticity of Erysimum capitatum to altitude: Its implications for responses to climate change. J. Ecol. 101, 796–805 (2013).
    Google Scholar 
    Forbis, T. A. Seedling demography in an alpine ecosystem. Am. J. Bot. 90, 1197–1206 (2003).PubMed 

    Google Scholar 
    Yenni, G., Adler, P. B. & Ernest, S. M. Strong self-limitation promotes the persistence of rare species. Ecology 93, 456–461 (2012).PubMed 

    Google Scholar 
    Doak, D. F. Source-sink models and the problem of habitat degradation: General models and applications to the Yellowstone grizzly. Conserv. Biol. 9, 1370–1379 (1995).
    Google Scholar 
    Lesica, P. & Crone, E. E. Arctic and boreal plant species decline at their southern range limits in the Rocky Mountains. Ecol. Lett. 20, 166–174 (2017).PubMed 

    Google Scholar 
    Oldfather, M. F. & Ackerly, D. D. Microclimate and demography interact to shape stable population dynamics across the range of an alpine plant. New Phytol. 222, 193–205 (2019).PubMed 

    Google Scholar 
    Ågren, J., Fortunel, C. & Ehrlén, J. Selection on floral display in insect-pollinated Primula farinosa: Effects of vegetation height and litter accumulation. Oecologia 150, 225–232 (2006).ADS 
    PubMed 

    Google Scholar 
    Ehrlén, J., Syrjänen, K., Leimu, R., Begona Garcia, M. & Lehtilä, K. Land use and population growth of Primula veris: An experimental demographic approach. J. Appl. Ecol. 42, 317–326 (2005).
    Google Scholar 
    Ehrlén, J. & Morris, W. F. Predicting changes in the distribution and abundance of species under environmental change. Ecol. Lett. 18, 303–314 (2015).PubMed 
    PubMed Central 

    Google Scholar 
    Stubben, C. & Milligan, B. Estimating and analyzing demographic models using the popbio package in R. J. Stat. Softw. 22, 1–23 (2007).
    Google Scholar 
    Weiss, N. Package ‘wPerm’. https://cran.r-project.org/web/packages/wPerm/wPerm.pdf. (2015).Frossard, J. & Renaud, O. Permutation tests for regression, ANOVA, and comparison of signals: The permuco package. J. Stat. Softw. 99, 1–32 (2021).
    Google Scholar  More