More stories

  • in

    Biogeographical and seasonal dynamics of the marine Roseobacter community and ecological links to DMSP-producing phytoplankton

    Luo H, Moran MA. Evolutionary ecology of the marine Roseobacter clade. Microbiol Mol Biol Rev. 2014;78:573–87.PubMed 
    PubMed Central 

    Google Scholar 
    Wietz M, Gram L, Jørgensen B, Schramm A. Latitudinal patterns in the abundance of major marine bacterioplankton groups. Aquat Microbial Ecol. 2010;61:179–89.
    Google Scholar 
    Sunagawa S, Coelho LP, Chaffron S, Kultima JR, Labadie K, Salazar G, et al. Structure and function of the global ocean microbiome. Science. 2015;348:1261359.PubMed 

    Google Scholar 
    González JM, Simó R, Massana R, Covert JS, Casamayor EO, Pedrós-Alió C, et al. Bacterial community structure associated with a dimethylsulfoniopropionate-producing North Atlantic algal bloom. Appli Environ Microbiol. 2000;66:4237–46.
    Google Scholar 
    González JM, Moran MA. Numerical dominance of a group of marine bacteria in the alpha-subclass of the class Proteobacteria in coastal seawater. Appl Environ Microbiol. 1997;63:4237–42.PubMed 
    PubMed Central 

    Google Scholar 
    Grossart HP, Levold F, Allgaier M, Simon M, Brinkhoff T. Marine diatom species harbour distinct bacterial communities. Environ Microbiol. 2005;7:860–73.CAS 
    PubMed 

    Google Scholar 
    Amin SA, Parker MS, Armbrust EV. Interactions between diatoms and bacteria. Microbiol Mol Biol Rev. 2012;76:667–84.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Alavi M, Miller T, Erlandson K, Schneider R, Belas R. Bacterial community associated with Pfiesteria‐like dinoflagellate cultures. Environ Microbiol. 2001;3:380–96.CAS 
    PubMed 

    Google Scholar 
    Jasti S, Sieracki ME, Poulton NJ, Giewat MW, Rooney-Varga JN. Phylogenetic diversity and specificity of bacteria closely associated with Alexandrium spp. and other phytoplankton. Appl Environ Microbiol. 2005;71:3483–94.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Zubkov MV, Fuchs BM, Archer SD, Kiene RP, Amann R, Burkill PH. Rapid turnover of dissolved DMS and DMSP by defined bacterioplankton communities in the stratified euphotic zone of the North Sea. Deep Sea Res Top Stud Oceanogr. 2002;49:3017–38.CAS 

    Google Scholar 
    Zubkov MV, Fuchs BM, Archer SD, Kiene RP, Amann R, Burkill PH. Linking the composition of bacterioplankton to rapid turnover of dissolved dimethylsulphoniopropionate in an algal bloom in the North Sea. Environ Microbiol. 2001;3:304–11.CAS 
    PubMed 

    Google Scholar 
    Teeling H, Fuchs BM, Becher D, Klockow C, Gardebrecht A, Bennke CM, et al. Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science. 2012;336:608–11.CAS 
    PubMed 

    Google Scholar 
    Voget S, Wemheuer B, Brinkhoff T, Vollmers J, Dietrich S, Giebel H-A, et al. Adaptation of an abundant Roseobacter RCA organism to pelagic systems revealed by genomic and transcriptomic analyses. ISME J. 2015;9:371–84.CAS 
    PubMed 

    Google Scholar 
    Billerbeck S, Wemheuer B, Voget S, Poehlein A, Giebel H-A, Brinkhoff T, et al. Biogeography and environmental genomics of the Roseobacter-affiliated pelagic CHAB-I-5 lineage. Nat Microbiol. 2016;1:16063.CAS 
    PubMed 

    Google Scholar 
    Buchan A, LeCleir GR, Gulvik CA, González JM. Master recyclers: features and functions of bacteria associated with phytoplankton blooms. Nat Rev Microbiol. 2014;12:686–98.CAS 
    PubMed 

    Google Scholar 
    Amin S, Hmelo L, van Tol H, Durham B, Carlson L, Heal K, et al. Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature. 2015;522:98–101.CAS 
    PubMed 

    Google Scholar 
    Landa M, Burns AS, Durham BP, Esson K, Nowinski B, Sharma S, et al. Sulfur metabolites that facilitate oceanic phytoplankton–bacteria carbon flux. ISME J. 2019;13:2536–50.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Durham BP, Boysen AK, Carlson LT, Groussman RD, Heal KR, Cain KR, et al. Sulfonate-based networks between eukaryotic phytoplankton and heterotrophic bacteria in the surface ocean. Nat Microbiol. 2019;4:1706–15.CAS 
    PubMed 

    Google Scholar 
    Howard EC, Henriksen JR, Buchan A, Reisch CR, Bürgmann H, Welsh R, et al. Bacterial taxa that limit sulfur flux from the ocean. Science. 2006;314:649–52.CAS 
    PubMed 

    Google Scholar 
    Levine NM, Toole DA, Neeley A, Bates NR, Doney SC, Dacey JW. Revising upper-ocean sulfur dynamics near Bermuda: new lessons from 3 years of concentration and rate measurements. Environ Chem. 2016;13:302–13.CAS 

    Google Scholar 
    Kiene RP. Turnover of dissolved DMSP in estuarine and shelf waters of the northern Gulf of Mexico. In Biological and environmental chemistry of DMSP and related sulfonium compounds. Boston, MA: Springer; 1996. pp. 337–49.Kiene RP, Linn LJ. Distribution and turnover of dissolved DMSP and its relationship with bacterial production and dimethylsulfide in the Gulf of Mexico. Limnol Oceanogr. 2000;45:849–61.CAS 

    Google Scholar 
    Curson AR, Todd JD, Sullivan MJ, Johnston AW. Catabolism of dimethylsulphoniopropionate: microorganisms, enzymes and genes. Nat Rev Microbiol. 2011;9:849–59.CAS 
    PubMed 

    Google Scholar 
    Simó R. Production of atmospheric sulfur by oceanic plankton: biogeochemical, ecological and evolutionary links. Trends Ecol Evol. 2001;16:287–94.PubMed 

    Google Scholar 
    Charlson RJ, Lovelock JE, Andreae MO, Warren SG. Oceanic phytoplankton, atmospheric sulphur, cloud albedo and climate. Nature. 1987;326:655–61.CAS 

    Google Scholar 
    Reisch CR, Moran MA, Whitman WB. Bacterial catabolism of dimethylsulfoniopropionate (DMSP). Front Microbiol. 2011;2:172.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Varaljay VA, Howard EC, Sun S, Moran MA. Deep sequencing of a dimethylsulfoniopropionate-degrading gene (dmdA) by using PCR primer pairs designed on the basis of marine metagenomic data. Appl Environ Microbiol. 2010;76:609–17.CAS 
    PubMed 

    Google Scholar 
    Varaljay VA, Robidart J, Preston CM, Gifford SM, Durham BP, Burns AS, et al. Single-taxon field measurements of bacterial gene regulation controlling DMSP fate. ISME J. 2015;9:1677.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ledyard KM, DeLong EF, Dacey JW. Characterization of a DMSP-degrading bacterial isolate from the Sargasso Sea. Arch Microbiol. 1993;160:312–8.CAS 

    Google Scholar 
    Todd JD, Kirkwood M, Newton-Payne S, Johnston AW. DddW, a third DMSP lyase in a model Roseobacter marine bacterium, Ruegeria pomeroyi DSS-3. ISME J. 2012;6:223–6.CAS 
    PubMed 

    Google Scholar 
    Todd JD, Curson AR, Kirkwood M, Sullivan MJ, Green RT, Johnston AW. DddQ, a novel, cupin‐containing, dimethylsulfoniopropionate lyase in marine roseobacters and in uncultured marine bacteria. Environ Microbiol. 2011;13:427–38.CAS 
    PubMed 

    Google Scholar 
    Todd J, Curson A, Dupont C, Nicholson P, Johnston A. The dddP gene, encoding a novel enzyme that converts dimethylsulfoniopropionate into dimethyl sulfide, is widespread in ocean metagenomes and marine bacteria and also occurs in some Ascomycete fungi. Environ Microbiol. 2009;11:1376–85.CAS 
    PubMed 

    Google Scholar 
    Todd JD, Curson AR, Nikolaidou‐Katsaraidou N, Brearley CA, Watmough NJ, Chan Y, et al. Molecular dissection of bacterial acrylate catabolism–unexpected links with dimethylsulfoniopropionate catabolism and dimethyl sulfide production. Environ Microbiol. 2010;12:327–43.CAS 
    PubMed 

    Google Scholar 
    Curson A, Rogers R, Todd J, Brearley C, Johnston A. Molecular genetic analysis of a dimethylsulfoniopropionate lyase that liberates the climate‐changing gas dimethylsulfide in several marine α‐proteobacteria and Rhodobacter sphaeroides. Environ Microbiol. 2008;10:757–67.CAS 
    PubMed 

    Google Scholar 
    Delmont TO, Hammar KM, Ducklow HW, Yager PL, Post AF. Phaeocystis antarctica blooms strongly influence bacterial community structures in the Amundsen Sea polynya. Front Microbiol. 2014;5:646.PubMed 
    PubMed Central 

    Google Scholar 
    Stoica E, Herndl GJ. Bacterioplankton community composition in nearshore waters of the NW Black Sea during consecutive diatom and coccolithophorid blooms. Aquat Sci. 2007;69:413–8.CAS 

    Google Scholar 
    Giebel HA, Brinkhoff T, Zwisler W, Selje N, Simon M. Distribution of Roseobacter RCA and SAR11 lineages and distinct bacterial communities from the subtropics to the Southern Ocean. Environ Microbiol. 2009;11:2164–78.CAS 
    PubMed 

    Google Scholar 
    Landa M, Blain S, Christaki U, Monchy S, Obernosterer I. Shifts in bacterial community composition associated with increased carbon cycling in a mosaic of phytoplankton blooms. ISME J. 2016;10:39–50.CAS 
    PubMed 

    Google Scholar 
    Wemheuer B, Güllert S, Billerbeck S, Giebel H-A, Voget S, Simon M, et al. Impact of a phytoplankton bloom on the diversity of the active bacterial community in the southern North Sea as revealed by metatranscriptomic approaches. FEMS Microbiol Ecol. 2014;87:378–89.CAS 
    PubMed 

    Google Scholar 
    Alonso-Gutiérrez J, Lekunberri I, Teira E, Gasol JM, Figueras A, Novoa B. Bacterioplankton composition of the coastal upwelling system of ‘Ría de Vigo’, NW Spain. FEMS Microbiol Ecol. 2009;70:493–505.PubMed 

    Google Scholar 
    Brown MV, Van De Kamp J, Ostrowski M, Seymour JR, Ingleton T, Messer LF, et al. Systematic, continental scale temporal monitoring of marine pelagic microbiota by the Australian Marine Microbial Biodiversity Initiative. Sci Data. 2018;5:180130.PubMed 
    PubMed Central 

    Google Scholar 
    Ajani P, Hallegraeff G, Allen D, Coughlan A, Richardson A, Armand L, et al. Establishing baselines: a review of eighty years of phytoplankton diversity and biomass in southeastern Australia. Oceanogr Mar Biol. 2016;54:387–412.
    Google Scholar 
    Matear R, Chamberlain M, Sun C, Feng M. Climate change projection of the Tasman Sea from an eddy‐resolving ocean model. J Geophys Res Oceans. 2013;118:2961–76.
    Google Scholar 
    Ostrowski M, Seymour J, Messer L, Varkey D, Goosen K, Smith M, et al. Status of Australian marine microbial assemblages. In State and Trends of Australia’s Ocean Report, Integrated Marine Observing System (IMOS). 2020. https://doi.org/10.26198/5e16aa3e49e7f.Lynch TP, Morello EB, Evans K, Richardson AJ, Rochester W, Steinberg CR, et al. IMOS National Reference Stations: a continental-wide physical, chemical and biological coastal observing system. PloS ONE. 2014;9:e113652.PubMed 
    PubMed Central 

    Google Scholar 
    Lynch T, Roughan M, Mclaughlan D, Hughes D, Cherry D, Critchley G, et al. A national reference station infrastructure for Australia – Using telemetry and central processing to report multi-disciplinary data streams for monitoring marine ecosystem response to climate change. In: OCEANS 2008. 2008. https://doi.org/10.1109/OCEANS.2008.5151856.Appleyard SA, Abell G, Watson R. Tackling microbial related issues in cultured shellfish via integrated molecular and water chemistry approaches. Clayton: CSIRO Marine and Atmospheric Research; 2013.Parada AE, Needham DM, Fuhrman JA. Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ Microbiol. 2016;18:1403–14.CAS 
    PubMed 

    Google Scholar 
    Duarte CM. Seafaring in the 21st century: the Malaspina 2010 circumnavigation expedition. Limnol Oceanogr Bull. 2015;24:11–4.
    Google Scholar 
    Biller SJ, Berube PM, Dooley K, Williams M, Satinsky BM, Hackl T, et al. Marine microbial metagenomes sampled across space and time. Sci Data. 2018;5:1–7.
    Google Scholar 
    Logares R, Sunagawa S, Salazar G, Cornejo‐Castillo FM, Ferrera I, Sarmento H, et al. Metagenomic 16S rDNA Illumina tags are a powerful alternative to amplicon sequencing to explore diversity and structure of microbial communities. Environm Microbiol. 2014;16:2659–71.CAS 

    Google Scholar 
    Dadon-Pilosof A, Conley KR, Jacobi Y, Haber M, Lombard F, Sutherland KR, et al. Surface properties of SAR11 bacteria facilitate grazing avoidance. Nat Microbiol. 2017;2:1608–15.PubMed 

    Google Scholar 
    Lane D. 16S/23S rRNA sequencing. In: Nucleic acid techniques in bacterial systematics. New York: John Wiley & Sons; 1991, pp. 115–75.Lane DJ, Pace B, Olsen GJ, Stahl DA, Sogin ML, Pace NR. Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proc Natl Acad Sci. 1985;82:6955–9.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Piredda R, Tomasino M, D’erchia A, Manzari C, Pesole G, Montresor M, et al. Diversity and temporal patterns of planktonic protist assemblages at a Mediterranean Long Term Ecological Research site. FEMS Microbiol Ecol. 2017;93.Stoeck T, Bass D, Nebel M, Christen R, Jones MD, Breiner HW, et al. Multiple marker parallel tag environmental DNA sequencing reveals a highly complex eukaryotic community in marine anoxic water. Mol Ecol. 2010;19:21–31.CAS 
    PubMed 

    Google Scholar 
    Andrews S. FastQC: a quality control tool for high throughput sequence data. Cambridge, United Kingdom: Babraham Bioinformatics, Babraham Institute; 2010.Magoč T, Salzberg SL. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics. 2011;27:2957–63.PubMed 
    PubMed Central 

    Google Scholar 
    Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26:2460–1.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Gordon A, Hannon G. Fastx-toolkit. FASTQ/A short-reads preprocessing tools. 2010;5. http://hannonlab.cshl.edu/fastx_toolkit/.Yilmaz P, Parfrey LW, Yarza P, Gerken J, Pruesse E, Quast C, et al. The SILVA and “all-species living tree project (LTP)” taxonomic frameworks. Nucl Acids Res. 2014;42:D643–8.CAS 
    PubMed 

    Google Scholar 
    Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol. 2007;73:5261–7.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Guillou L, Bachar D, Audic S, Bass D, Berney C, Bittner L, et al. The Protist Ribosomal Reference database (PR2): a catalog of unicellular eukaryote small sub-unit rRNA sequences with curated taxonomy. Nucl Acids Res. 2012;41:D597–604.PubMed 
    PubMed Central 

    Google Scholar 
    Simon M, Scheuner C, Meier-Kolthoff JP, Brinkhoff T, Wagner-Döbler I, Ulbrich M, et al. Phylogenomics of Rhodobacteraceae reveals evolutionary adaptation to marine and non-marine habitats. ISME J. 2017;11:1483–99.PubMed 
    PubMed Central 

    Google Scholar 
    Brinkhoff T, Giebel H-A, Simon M. Diversity, ecology, and genomics of the Roseobacter clade: a short overview. Arch Microbiol. 2008;189:531–9.CAS 
    PubMed 

    Google Scholar 
    Rognes T, Flouri T, Nichols B, Quince C, Mahé F. VSEARCH: a versatile open source tool for metagenomics. PeerJ. 2016;4:e2584.PubMed 
    PubMed Central 

    Google Scholar 
    Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol. 2016;33:1870–4.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucl Acids Res. 2004;32:1792–7.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Felsenstein J. Evolutionary trees from gene frequencies and quantitative characters: finding maximum likelihood estimates. Evolution. 1981:1229–42.Tamura K, Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol. 1993;10:512–26.CAS 
    PubMed 

    Google Scholar 
    emcparland. emcparland/dmspOTUs: first release. 2021. https://doi.org/10.5281/zenodo.5090864.Keeling PJ, Burki F, Wilcox HM, Allam B, Allen EE, Amaral-Zettler LA, et al. The Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP): illuminating the functional diversity of eukaryotic life in the oceans through transcriptome sequencing. PLoS Biol. 2014;12:e1001889.PubMed 
    PubMed Central 

    Google Scholar 
    Nawrocki EP, Eddy SR. Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics. 2013;29:2933–5.CAS 
    PubMed 
    PubMed Central 

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

    Google Scholar 
    Matsen FA, Kodner RB, Armbrust EV. pplacer: linear time maximum-likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree. BMC Bioinform. 2010;11:538.
    Google Scholar 
    McParland EL, Levine NM. The role of differential DMSP production and community composition in predicting variability of global surface DMSP concentrations. Limnol Oceanogr. 2019;64:757–73.CAS 

    Google Scholar 
    Reshef DN, Reshef YA, Sabeti PC, Mitzenmacher M. An empirical study of the maximal and total information coefficients and leading measures of dependence. Ann Appl Stat. 2018;12:123–55.
    Google Scholar 
    Hammer Ø, Harper DA, Ryan PD. PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron. 2001;4:9.
    Google Scholar 
    Buchan A, González JM, Moran MA. Overview of the marine Roseobacter lineage. Appl Environ Microbiol. 2005;71:5665–77.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Moran MA, González JM, Kiene RP. Linking a bacterial taxon to sulfur cycling in the sea: studies of the marine Roseobacter group. Geomicrobiol J. 2003;20:375–88.CAS 

    Google Scholar 
    Harris G, Nilsson C, Clementson L, Thomas D. The water masses of the east coast of Tasmania: seasonal and interannual variability and the influence on phytoplankton biomass and productivity. Mar Freshw Res. 1987;38:569–90.CAS 

    Google Scholar 
    Kiene RP, Linn LJ, González J, Moran MA, Bruton JA. Dimethylsulfoniopropionate and methanethiol are important precursors of methionine and protein-sulfur in marine bacterioplankton. Appl Environ Microbiol. 1999;65:4549–58.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Raina J-B, Tapiolas D, Willis BL, Bourne DG. Coral-associated bacteria and their role in the biogeochemical cycling of sulfur. Appl Environ Microbiol. 2009;75:3492–501.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Brinkmeyer R, Rappé M, Gallacher S, Medlin L. Development of clade-(Roseobacter and Alteromonas) and taxon-specific oligonucleotide probes to study interactions between toxic dinoflagellates and their associated bacteria. Eur J Phycol. 2000;35:315–29.
    Google Scholar 
    Töpel M, Pinder MI, Johansson ON, Kourtchenko O, Clarke AK, Godhe A. Complete genome sequence of novel Sulfitobacter pseudonitzschiae Strain SMR1, isolated from a culture of the marine diatom Skeletonema marinoi. J Genomics. 2019;7:7.PubMed 
    PubMed Central 

    Google Scholar 
    Hong Z, Lai Q, Luo Q, Jiang S, Zhu R, Liang J, et al. Sulfitobacter pseudonitzschiae sp. nov., isolated from the toxic marine diatom Pseudo-nitzschia multiseries. Int J Syst Evol Microbiol. 2015;65:95–100.CAS 
    PubMed 

    Google Scholar 
    Yang Q, Ge Y-M, Iqbal NM, Yang X, Zhang X-l. Sulfitobacter alexandrii sp. nov., a new microalgae growth-promoting bacterium with exopolysaccharides bioflocculanting potential isolated from marine phycosphere. Antonie Van Leeuwenhoek. 2021;114:1091–106.CAS 
    PubMed 

    Google Scholar 
    Ankrah NY, Lane T, Budinoff CR, Hadden MK, Buchan A. Draft genome sequence of Sulfitobacter sp. CB2047, a member of the Roseobacter clade of marine bacteria, isolated from an emiliania huxleyi bloom. Genome Announc. 2014;2:e01125–14.PubMed 
    PubMed Central 

    Google Scholar 
    Kwak M-J, Lee J-S, Lee KC, Kim KK, Eom MK, Kim BK, et al. Sulfitobacter geojensis sp. nov., Sulfitobacter noctilucae sp. nov., and Sulfitobacternoctilucicola sp. nov., isolated from coastal seawater. Int J Syst Evol Microbiol. 2014;64:3760–7.PubMed 

    Google Scholar 
    Zhang F, Fan Y, Zhang D, Chen S, Bai X, Ma X, et al. Effect and mechanism of the algicidal bacterium Sulfitobacter porphyrae ZFX1 on the mitigation of harmful algal blooms caused by Prorocentrum donghaiense. Environ Pollut. 2020;263:114475.CAS 
    PubMed 

    Google Scholar 
    Keller MD. Dimethyl sulfide production and marine phytoplankton: the importance of species composition and cell size. Biol Oceanogr. 1989;6:375–82.
    Google Scholar 
    McParland EL, Lee MD, Webb EA, Alexander H, Levine NM. DMSP synthesis genes distinguish two types of DMSP producer phenotypes. Environ Microbiol. 2021;23:1656–69.CAS 
    PubMed 

    Google Scholar 
    Galí M, Simó R. A meta‐analysis of oceanic DMS and DMSP cycling processes: disentangling the summer paradox. Glob Biogeochem Cycles. 2015;29:496–515.
    Google Scholar 
    Carr A, Diener C, Baliga NS, Gibbons SM. Use and abuse of correlation analyses in microbial ecology. ISME J. 2019;13:2647–55.PubMed 
    PubMed Central 

    Google Scholar 
    Amin S, Hmelo L, Van Tol H, Durham B, Carlson L, Heal K, et al. Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature. 2015;522:98.CAS 
    PubMed 

    Google Scholar 
    Miller TR, Hnilicka K, Dziedzic A, Desplats P, Belas R. Chemotaxis of Silicibacter sp. strain TM1040 toward dinoflagellate products. Appl Environ Microbiol. 2004;70:4692–701.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Seymour JR, Simó R, Ahmed T, Stocker R. Chemoattraction to dimethylsulfoniopropionate throughout the marine microbial food web. Science. 2010;329:342–5.CAS 
    PubMed 

    Google Scholar  More

  • in

    Reply to: Conclusions of low extinction risk for most species of reef-building corals are premature

    Dietzel, A., Bode, M., Connolly, S. R. & Hughes, T. P. The population sizes and global extinction risk of reef-building coral species at biogeographic scales. Nat. Ecol. Evol. 5, 663–669 (2021).Article 

    Google Scholar 
    Hubbell, S. P. et al. How many tree species are there in the Amazon and how many of them will go extinct? Proc. Natl Acad. Sci. USA 105, 11498–11504 (2008).CAS 
    Article 

    Google Scholar 
    Carpenter, K. E. et al. One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 321, 560–563 (2008).CAS 
    Article 

    Google Scholar 
    Muir, P. R. et al. Conclusions of low extinction risk for most species of reef-building corals are premature. Nat. Ecol. Evol. https://doi.org/10.1038/s41559-022-01659-5 (2022).Richards, Z. T., Syms, C., Wallace, C. C., Muir, P. R. & Willis, B. L. Multiple occupancy–abundance patterns in staghorn coral communities. Divers. Distrib. 19, 884–895 (2013).Article 

    Google Scholar 
    Zvuloni, A., Artzy-Randrup, Y., Stone, L., van Woesik, R. & Loya, Y. Ecological size–frequency distributions: how to prevent and correct biases in spatial sampling. Limnol. Oceanogr. Methods 6, 144–153 (2008).Article 

    Google Scholar  More

  • in

    Conclusions of low extinction risk for most species of reef-building corals are premature

    Dietzel, A., Bode, M., Connolly, S. R. & Hughes, T. P. The population sizes and global extinction risk of reef-building coral species at biogeographic scales. Nat. Ecol. Evol. 5, 663–669 (2021).Article 

    Google Scholar 
    Richards, Z. T., van Oppen, M. J., Wallace, C. C., Willis, B. L. & Miller, D. J. Some rare Indo-Pacific coral species are probable hybrids. PLoS ONE 3, e3240 (2008).Article 

    Google Scholar 
    Carpenter, K. E. et al. One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 321, 560–563 (2008).CAS 
    Article 

    Google Scholar 
    Richards, Z. T., Syms, C., Wallace, C. C., Muir, P. R. & Willis, B. L. Multiple occupancy–abundance patterns in staghorn coral communities. Divers. Distrib. 19, 84–895 (2013).Article 

    Google Scholar 
    Hoeksema, B. W. & Cairns, S. World List of Scleractinia (accessed 6 May 2021); http://www.marinespecies.org/scleractiniaHughes, T. P. et al. Global warming transforms coral reef assemblages. Nature 556, 493–496 (2018).Article 

    Google Scholar 
    Thurba, R. V. et al. Deciphering coral disease dynamics: integrating host, microbiome, and the changing environment. Front. Ecol. Evol. 8, 575927 (2020).Article 

    Google Scholar 
    Muir, P. R., Marshall, P. A., Abdulla, A. & Aguirre, J. D. Species identity and depth predict bleaching severity in reef building corals: shall the deep inherit the reef? Proc. R. Soc. B 284, 20171551 (2017).Article 

    Google Scholar 
    van Woesik, R., Sakai, K., Ganase, A. & Loya, Y. Revisiting the winners and the losers a decade after coral bleaching. Mar. Ecol. Prog. Ser. 434, 67–76 (2011).Article 

    Google Scholar 
    Chen, Y.-H., Shertzer, K. W. & Viehman, T. S. Spatio-temporal dynamics of the threatened elkhorn coral Acropora palmata: implications for conservation. Divers. Distrib. 26, 1582–1597 (2020).Article 

    Google Scholar 
    Sheppard, C., Sheppard, A. & Fenner, D. Coral mass mortalities in the Chagos Archipelago over 40 years: regional species and assemblage extinctions and indications of positive feedbacks. Mar. Poll. Bull. 154, 111075 (2020).CAS 
    Article 

    Google Scholar 
    DeVantier, L. & Turak, E. Species richness and relative abundance of reef-building corals in the Indo-West Pacific. Diversity 9, 25 (2017).Article 

    Google Scholar 
    Wallace, C. C. Staghorn Corals of the World (CSIRO, 1999).Benzoni, F., Stefani, F., Pichon, M. & Galli, P. The name game: morpho-molecular species boundaries in the genus Psammocora (Cnidaria, Scleractinia). Zool. J. Linn. Soc. 160, 421–456 (2010).Article 

    Google Scholar 
    Richards, Z. T., Berry, O. & van Oppen, M. J. H. Cryptic genetic divergence within threatened species of Acropora coral from the Indian and Pacific Oceans. Conserv. Genet. 17, 577–591 (2016).Article 

    Google Scholar 
    Sheets, E. A., Warner, P. A. & Palumbi, S. R. Accurate population genetic measurements require cryptic species identification in corals. Coral Reefs 37, 549–563 (2018).Article 

    Google Scholar 
    Bongaerts, P. et al. Morphological stasis masks ecologically divergent coral species on tropical reefs. Curr. Biol. 31, 2286–2298 (2021).CAS 
    Article 

    Google Scholar 
    Frankham, R. Effective population size/adult population size ratios in wildlife: a review. Genet. Res. 89, 491–503 (2008).Article 

    Google Scholar  More

  • in

    Decreasing rainfall frequency contributes to earlier leaf onset in northern ecosystems

    Keenan, T. F. et al. Net carbon uptake has increased through warming-induced changes in temperate forest phenology. Nat. Clim. Change 4, 598–604 (2014).CAS 

    Google Scholar 
    Barichivich, J. et al. Large-scale variations in the vegetation growing season and annual cycle of atmospheric CO2 at high northern latitudes from 1950 to 2011. Glob. Change Biol. 19, 3167–3183 (2013).
    Google Scholar 
    Vitasse, Y. et al. Assessing the effects of climate change on the phenology of European temperate trees. Agr. Forest Meteorol. 151, 969–980 (2011).
    Google Scholar 
    Menzel, A. et al. European phenological response to climate change matches the warming pattern. Glob. Change Biol. 12, 1969–1976 (2006).
    Google Scholar 
    Fu, Y. H. et al. Declining global warming effects on the phenology of spring leaf unfolding. Nature 526, 104–107 (2015).CAS 

    Google Scholar 
    Wang, H. et al. Overestimation of the effect of climatic warming on spring phenology due to misrepresentation of chilling. Nat. Commun. 11, 4945 (2020).CAS 

    Google Scholar 
    Myneni, R. C. et al. Increased plant growth in the northern high latitudes from 1981 to 1991. Nature 386, 698–702 (1997).CAS 

    Google Scholar 
    Piao, S. et al. Leaf onset in the Northern Hemisphere triggered by daytime temperature. Nat. Commun. 6, 6911 (2015).CAS 

    Google Scholar 
    Richardson, A. D. et al. Influence of spring and autumn phenological transitions on forest ecosystem productivity. Phil. Trans. R. Soc. B 365, 3227–3246 (2010).
    Google Scholar 
    Piao, S. et al. Plant phenology and global climate change: current progresses and challenges. Glob. Change Biol. 25, 1922–1940 (2019).
    Google Scholar 
    White, A., Cannell, M. G. R. & Friend, A. D. The high-latitude terrestrial carbon sink: a model analysis. Glob. Change Biol. 6, 227–245 (2000).
    Google Scholar 
    Piao, S. et al. Net carbon dioxide losses of northern ecosystems in response to autumn warming. Nature 451, 49–53 (2008).CAS 

    Google Scholar 
    Fu, Y. H. et al. Unexpected role of winter precipitation in determining heat requirement for spring vegetation green-up at northern middle and high latitudes. Glob. Change Biol. 20, 3743–3755 (2014).
    Google Scholar 
    Yun, J. et al. Influence of winter precipitation on spring phenology in boreal forests. Glob. Change Biol. 11, 5176–5187 (2018).
    Google Scholar 
    Fu, Y. H. et al. Increased heat requirement for leaf flushing in temperate woody species over 1980–2012: effects of chilling, precipitation and insolation. Glob. Change Biol. 21, 2687–2697 (2015).
    Google Scholar 
    Wipf, S., Stoeckli, V. & Bebi, P. Winter climate change in alpine tundra: plant responses to changes in snow depth and snowmelt timing. Climatic Change 94, 105–121 (2009).
    Google Scholar 
    Peñuelas, J. et al. Complex spatiotemporal phenological shifts as a response to rainfall changes. New Phytol. 161, 837–846 (2004).
    Google Scholar 
    Paschalis, A. et al. Rainfall manipulation experiments as simulated by terrestrial biosphere models: where do we stand? Glob. Change Biol. 26, 3336–3355 (2020).
    Google Scholar 
    Green, J. K. et al. Regionally strong feedbacks between the atmosphere and terrestrial biosphere. Nat. Geosci. 10, 410–414 (2017).CAS 

    Google Scholar 
    Trenberth, K. E., Dai, A., Rasmussen, R. M. & Parsons, D. B. The changing character of precipitation. Bull. Am. Meteorol. Soc. 84, 1205–1217 (2003).
    Google Scholar 
    Qian, W., Fu, J. & Yan, Z. Decrease of light rain events in summer associated with a warming environment in China during 1961–2005. Geophys. Res. Lett. 34, L11705 (2007).
    Google Scholar 
    Sun, Y., Solomon, S., Dai, A. & Portmann, R. W. How often will it rain? J. Clim. 20, 4801–4818 (2007).
    Google Scholar 
    Chou, C. et al. Mechanisms for global warming impacts on precipitation frequency and intensity. J. Clim. 13, 3291–3306 (2012).
    Google Scholar 
    Held, I. M. & Soden, B. J. Robust responses of the hydrological cycle to global warming. J. Clim. 19, 5686–5699 (2006).
    Google Scholar 
    Fowler, M. D., Kooperman, G. J., Randerson, J. T. & Pritchard, M. S. The effect of plant physiological responses to rising CO2 on global streamflow. Nat. Clim. Change 9, 873–879 (2019).CAS 

    Google Scholar 
    Belnap, J., Phillips, S. L. & Miller, M. E. Response of desert biological soil crusts to alterations in precipitation frequency. Oecologia 141, 306–316 (2004).
    Google Scholar 
    Knapp, A. K. et al. Consequences of more extreme precipitation regimes for terrestrial ecosystems. Bioscience 58, 811–821 (2008).
    Google Scholar 
    Chen, L. et al. Leaf senescence exhibits stronger climatic responses during warm than during cold autumns. Nat. Clim. Change 10, 777–780 (2020).CAS 

    Google Scholar 
    De Boeck, H. J., Dreesen, F. E., Janssens, I. A. & Nijs, I. Climatic characteristics of heat waves and their simulation in plant experiments. Glob. Change Biol. 16, 1992–2000 (2010).
    Google Scholar 
    Shen, M. et al. Precipitation impacts on vegetation spring phenology on the Tibetan Plateau. Glob. Change Biol. 21, 3647–3656 (2015).
    Google Scholar 
    Peaucelle, M. et al. Spatial variance of spring phenology in temperate deciduous forests is constrained by background climatic conditions. Nat. Commun. 10, 5388 (2019).
    Google Scholar 
    Estiarte, M. & Peñuelas, J. Alteration of the phenology of leaf senescence and fall in winter deciduous species by climate change: effects on nutrient proficiency. Glob. Change Biol. 21, 1005–1017 (2015).
    Google Scholar 
    Austin, A. T. et al. Water pulses and biogeochemical cycles in arid and semiarid ecosystems. Oecologia 141, 221–235 (2004).
    Google Scholar 
    White, M. A., Thornton, P. E. & Running, S. W. A continental phenology model for monitoring vegetation responses to interannual climatic variability. Glob. Biogeochem. Cycles 11, 217–234 (1997).CAS 

    Google Scholar 
    Templ, B. et al. Pan European Phenological database (PEP725): a single point of access for European data. Int. J. Biometeorol. 62, 1109–1113 (2018).
    Google Scholar 
    Ge, Q., Wang, H., Rutishauser, T. & Dai, J. Phenological response to climate change in China: a meta-analysis. Glob. Change Biol. 21, 265–274 (2015).
    Google Scholar 
    Schwartz, M. D., Betancourt, J. L. & Weltzin, J. F. From Caprio’s lilacs to the USA National Phenology Network. Front. Ecol. Environ. 10, 324–327 (2012).
    Google Scholar 
    Wu, C. et al. Interannual variability of net ecosystem productivity in forests is explained by carbon flux phenology in autumn. Glob. Ecol. Biogeogr. 22, 994–1006 (2013).
    Google Scholar 
    Zhang, X. et al. Monitoring vegetation phenology using MODIS. Remote Sens. Environ. 84, 471–475 (2003).
    Google Scholar 
    Shen, M. et al. Can changes in autumn phenology facilitate earlier green-up date of northern vegetation? Agr. Forest Meteorol. 291, 108077 (2020).
    Google Scholar 
    Chen, J. et al. A simple method for reconstructing a high-quality NDVI time-series data set based on the Savitzky–Golay filter. Remote Sens. Environ. 91, 332–344 (2004).
    Google Scholar 
    Shen, M. et al. Increasing altitudinal gradient of spring vegetation phenology during the last decade on the Qinghai–Tibetan Plateau. Agr. Forest Meteorol. 189, 71–80 (2014).
    Google Scholar 
    Wu, C. et al. Widespread decline in winds delayed autumn foliar senescence over high latitudes. Proc. Natl Acad. Sci. USA 118, e2015821118 (2021).CAS 

    Google Scholar 
    Elmore, A. J. et al. Landscape controls on the timing of spring, autumn, and growing season length in mid-Atlantic forests. Glob. Change Biol. 18, 656–674 (2012).
    Google Scholar 
    Olson, D. M. et al. Terrestrial ecoregions of the world: a new map of life on Earth. Bioscience 51, 933–938 (2001).
    Google Scholar 
    Harris, I., Jones, P. D., Osborn, T. J. & Lister, D. H. Updated high-resolution grids of monthly climatic observations—the CRU TS3.10 dataset. Int. J. Climatol. 34, 623–642 (2014).
    Google Scholar 
    New, M., Hulme, M. & Jones, P. D. Representing twentieth‐century space–time climate variability. Part I: development of a 1961–90 mean monthly terrestrial climatology. J. Clim. 12, 829–856 (1999).
    Google Scholar 
    Hempel, S., Frieler, K., Warszawski, L., Schewe, J. & Piontek, F. A trend-preserving bias correction—the ISI-MIP approach. Earth Syst. Dynam. 4, 219–236 (2013).
    Google Scholar 
    Abatzoglou, J. T., Dobrowski, S. Z., Parks, S. A. & Hegewisch, K. C. TerraClimate, a high-resolution global dataset of monthly climate and climatic water balance from 1958–2015. Sci. Data 5, 170191 (2018).
    Google Scholar 
    Vicenteserrano, S. M., Beguería, S. & López-Moreno, J. I. A multiscalar drought index sensitive to global warming: the Standardized Precipitation Evapotranspiration Index. J. Clim. 23, 1696–1718 (2010).
    Google Scholar 
    Barr, A. G. et al. Inter‐annual variability in the leaf area index of a boreal aspen–hazelnut forest in relation to net ecosystem production. Agr. Forest Meteorol. 126, 237–255 (2004).
    Google Scholar 
    Chen, J., Chen, W., Liu, J., Cihlar, J. & Gray, S. Annual carbon balance of Canada’s forests during 1895–1996. Glob. Biogeochem. Cycles 14, 839–849 (2000).CAS 

    Google Scholar 
    Krinner, G. et al. A dynamic global vegetation model for studies of the coupled atmosphere–biosphere system. Glob. Biogeochem. Cycles 19, GB1015 (2005).
    Google Scholar  More

  • in

    Reconciling human health with the environment while struggling against the COVID-19 pandemic through improved face mask eco-design

    Inventory analysisBefore computing the environmental impacts, we analyzed inventory data and input them into the software program for simulations. With respect to reusable masks, on-site measurements of raw materials, energy requirements for processing (e.g., laying, cutting, sewing, etc.), packaging material configurations, reuse options, cleaning activities and transport distances were provided by the Italian Social District. In particular, requirements for washing the reusable face mask were adapted from Schmutz et al.9 in compliance with the information provided by the producer. Moreover, waste disposal scenario data for both types was collected from the preprint by Allison et al.23 Finally, inventory data for single-use masks were collected from independent producers via certified laboratories. The final set of background and foreground data are provided in “Supplementary Table S1”.Single-use face masks consist of three layers of polypropylene non-wovens. The inner and outer fabric layers are Spunbond and the middle layer is 99% filtering Meltblown24. Reusable face masks (Type IIR) are also composed of three layers: an internal layer of antibacterial quality cotton, a middle layer of Meltblown, and an external layer of Spunbond. Mask quality is determined by the quality of the component parts and is therefore traceable to the component suppliers. Information on the suppliers and product component types (including certifications and features) is provided in “Supplementary Table S2”. Meltblown (supplied by Ramina) makes up the central part of reusable masks. This component guarantees a filtering performance of more than 99%, which—combined with the high-quality water-repellent anti-drop C6 antibacterial cotton (supplied by Olmetex) of the inner layer—resists up to 10 washes per immersion. These materials, forged together using specialized machinery, enhance Type IIR surgical masks above all others, with respect to their superior performance in the overall trade-off between filtering quality, reusability, and environmental sustainability. Furthermore, the cotton inner fabric of these masks has the same effectiveness as single-use masks in reducing the transmission of respiratory viruses25.Regarding elastic bands, nose clip material (for single-use masks), and fabric layers, no direct datasets are available in the ecoinvent database. Thus, for the present study, non-allergenic latex-free elastic bands, produced using a “polyurethane, flexible foam” process, were assumed. Nose clip material, which is only used for single-use masks, was assumed to be modelled using a “polyvinyl chloride resin (B-PVC)” process. Finally, we assumed that a “polypropylene, granulate” process was used for the TnT Spunbond and Meltblown layers. Regarding packaging materials, reusable face masks are wrapped in biodegradable plastic bags, while single-use masks are packaged in plastic bags. Both types of masks are packaged in sets of 10 and delivered in recycled cardboard boxes. In the present study, packaging materials were introduced to the software as “polyester-complexed starch biopolymer”, “packaging film, low-density polyethylene”, and “corrugated board boxes: 16.6% primary fiber, 83.4% recycled fiber”. For transportation, a “transport, freight, lorry 16–32 metric ton, EURO6” process was assumed from the manufacturing facility and nationwide distribution by road, using Euro 6D vans.To calculate the number of face masks used in Italy in 2020, we estimated the Italian population at 60.6 million, based on Organisation for Economic Co-operation and Development (OECD) statistics26. We assumed one mask per person, per day, for both mask types, according to WHO recommendations27. As reusable face masks can be washed up to 10 times without losing their virus filtration performance (according to the manufacturer’s own specification), we assumed the maximum number of washes for the use phase. Accordingly, the total number of face masks used in Italy was calculated at 2.18 and 22.1 billion for reusable and single-use face masks, respectively. The total amount of waste was calculated in terms of the number of used masks, alongside their packaging materials (i.e., plastic wrap and cardboard boxes) (Table 2). Single-use face masks were found to generate almost 10 times more waste for each waste category, relative to reusable face masks.Table 2 Total waste generated from used face masks in Italy, 2020 (kton/year).Full size tableWith respect to mask use, our basic case scenario was based on WHO recommendations27, which stipulate that reusable face masks should be washed daily with soap/detergent and hot (60 °C) water. We assumed that the entire household (2.3 people for Italian case) masks are washed together with other clothes in a standard 7 kg washing machine, following both the literature9 and producer instructions. Schmutz et al.9 reported that the requirements for a half-full washing machine (a typical situation in Europe) are 84 g detergent, 52.3 L tap water and 1.1 kWh electricity per load. Accordingly, the average washing consumables required for each mask is calculated by normalizing the specified requirements with respect to one mask (i.e., via multiplying a half-full load requirement by 0.2%).It should be noted, however, that user behavior is not easy to predict and the washing machine might not be always considered as the preferred option. Hence, as a further step, we investigated different user behaviors as sensitivity cases. First of all, hand washing was introduced as the main sensitivity scenario9,23,28. In this case, we assumed that the entire household masks will be washed together every day after use, in a bowl of 5 L filled up to 3 L level with water at 60 °C and then rinsed with water without soap/detergent. Approximately 6.24 g of liquid detergent and 6 L of water is required in each manual washing session23. Similar to the machine wash case, the average washing consumables required for each mask is calculated by normalizing the specified requirements with respect to one mask (i.e., the requirements per mask per wash are 2.609 L tap water, 2.713 g detergent, 447.7 kJ energy provided by the gas boiler).Moreover, we also considered other possible user behavior scenarios, assuming that reusable face masks might be washed for more than the recommended lifespan (i.e., 10 washes). Accordingly, a second sensitivity case was modelled for reusable masks washed 15 times prior to disposal. Finally, with reference to single-use masks, we took into consideration a longer period of wearing. Although the recommended face mask use is one mask per day (or 4–8 h), many users wear single-use surgical masks for longer than this recommended period. Thus, in this sensitivity case, we assumed that users would wear the same mask for 2 subsequent days. It should be noted, however, that the latter two sensitivity cases, i.e., concerning longer wearing period of both types, might compromise the protection level of masks and thereby human health.Regarding the packaging and waste disposal activities, the Italian Social District provided some data from their ongoing studies regarding the biodegradability of packaging materials for reusable (Type IIR) face masks. However, the present study could not consider actual waste disposal activities (i.e., recycling, reuse) due to the lack of approved assessments. Thus, waste disposal was based mainly on previous studies indicating incineration and landfilling as viable options23,29. We assumed that contaminated masks and discarded packaging materials would go directly to waste disposal sites, and 43% of mixed waste would be landfilled while 57% of mixed waste would be incinerated23. Regarding alternative disposal activities, we considered two sensitivity cases: one that assumed that all masks from each type would be fully incinerated9,30 and another that assumed that all masks from each type would be fully landfilled31. More

  • in

    Range expansion decreases the reproductive fitness of Gentiana officinalis (Gentianaceae)

    Seed collectionMature seeds of G. officinalis were collected from the natural-growing plant community at the Hezuo alpine meadow and wetland ecosystem research station of Lanzhou University on the southeast Qinghai-Tibet Plateau (lat. 34°53′ N, long. 101°53′ E, alt. 2900 m) in 2014 and grown in a nursery. Robust seedlings were selected and transplanted to the Haibei Alpine Meadow Ecosystem Research Station of the Chinese Academy of Sciences on the northeast Qinghai-Tibet Plateau (lat. 37°37′N, long. 101°19′ E, alt. 3200 m) and Datong ecological agriculture experimental station of the Northwest Institute of Plateau Biology (lat. 34°53′ N, long. 101°53′ E, alt. 2900 m). Transplantation was also performed in a natural environment (the Hezuo alpine meadow and a wetland ecosystem research station of Lanzhou University).Study plots and transplantingThe naturally studied population is located at the Hezuo alpine meadow and wetland ecosystem research station of Lanzhou University on the southeast Qinghai-Tibet Plateau (henceforth referred to as the natural environment (NE)), China (lat. 34°53′ N, long. 101°53′ E, alt. 2900 m). The third transplantation site was created in a natural environment and was termed “natural transplant” (NT). The average annual air temperature is 2 °C, with extremes of 11.5 °C (maximum) and –8.9 °C (minimum). The annual precipitation is approximately 550 mm, 80% of which falls in the short summer growing season between May and September. Hezuo station is dominated by Kobresia humilis, Pedicularis kansuensis, Heteropappus altaicus, Stellera chamaejasme, Aconitum gymnandrum and Nepeta pratti, which bloom at the same time as G. officinalis.The higher-elevation transplanted plot was located at the Haibei Alpine Meadow Ecosystem Research Station of the Chinese Academy of Sciences on the northeast Qinghai-Tibet Plateau (henceforth referred to as the high-elevation environment (HE) (lat. 37°37′N, long. 101°19′ E, alt. 3200 m). The average annual air temperature was –1.7 °C, with extremes of 27.6 °C (maximum) and –37.1 °C (minimum). The annual precipitation ranged between 426 and 860 mm, mainly in July and August.The lower-elevation transplanted plot was located at the Datong ecological agriculture experimental station of the Northwest Institute of Plateau Biology on the transition zone between Qinghai-Tibet Plateau and loess plateau (henceforth referred to as the low-elevation environment (LE)) (lat. 34°53′ N, long. 101°53′ E, alt. 2900 m). The average annual air temperature was 7.6 °C, with extremes of 34.6 °C (maximum) and –18.9 °C (minimum). The annual precipitation was approximately 380 mm, mainly in July and August. The study area was dominated by cultivated crops.Robust seedlings with floral buds were selected for transplantation. The density of G. officinalis under the NE was approximately 1.5 plants/m2; therefore, we planted individuals at the same plant density in all transplanted plots. Moreover, more than 300 robust seedlings of G. officinalis were transplanted to each transplanted plot. The total planting area was greater than 200 m2 at each plot. The transplanted seedlings flowered in the summer, and we conducted our experiments during the following 2 years (2016–2017).Flowing phenology and flower durationTo observe flowering phenology, three 1 × 10-m areas were created within each experimental plot in 2016. In each plot, flower opening and duration were monitored and recorded every morning until all flowers withered.At the full anthesis phase of G. officinalis in 2016, 10 plants from each plot were randomly selected. On each plant, two buds at the middle position of the inflorescence were selected, and the floral duration of all the selected buds was monitored and recorded. The pollen (male phase) and stigma (female phase) presentations were monitored and recorded.Floral display and reproductive allocationAt the full-bloom stage, 50 single plants were selected from each plot to test the inflorescence traits. Stem length (the distance from the stem base to apex) was measured by a straightedge. The number of sprays on each plant and the average flower numbers (including buds and fruits) on each spray were counted.We selected 100–150 fully open flowers on different plants in each population to test the flower sizes at each plot. To avoid the position effect as much as possible, we did not choose terminal flowers. The length and width (diameter) of the flowers in each plot were measured by Vernier calipers. To test the sexual allocation changes in G. officinalis among the three plots, 30 buds on different plants in each plot were selected randomly. Then, the pollen numbers (PNs) and ovule numbers (ONs) were counted. The pollen/ovule ratios (P/O) were calculated as P/O = pollen numbers in all five anthers/ovule numbers21.Sampling dates corresponded to the height of the flowering season at each site (mid-August in the LE and early September in the NE and HE) before fruiting had occurred. While fresh, the aboveground parts of 30 fully flowering plants per site were dissected into inflorescences, peduncles, leaves, and stems. Plant material was oven-dried at 70 °C for 3 days, and the dry weights were obtained to the nearest 0.1 mg on an analytical balance (Ohaus). The inflorescence and peduncle fractions of each plant were summed to provide a measure of reproductive biomass (R), and the leaf and stem fractions of each plant were summed to provide a measure of vegetative biomass (V). The reproductive allocation (RA) was calculated as RA = R/(R + V).Observation of pollinatorsThe floral visitors to G. officinalis were recorded in the three plots. Ten neighbouring inflorescences on different individual plants were selected at random and labelled. Before observation, we counted all the open flowers on one inflorescence and then recorded the number of flowers visited by pollinators. We observed these flowers between 9:00 a.m. and 6:00 p.m. in each plot during 2016 and 2017. In total, observations were carried out for 65 h in each plot over the 2 years. While carrying out these observations, we stayed 2 m away from the focal flowers to observe all of the floral visitors without disturbing their foraging behaviours. The visitor species, behaviour in the flower, and visiting times of each species were recorded, and the visit frequencies of each visitor species were calculated. The visit frequency was calculated as visit frequency = visit times/visit flower numbers/hour.To identify whether flower visitors were legitimate pollinators of G. officinalis, collected visitors were observed and photographed with a stereomicroscope to identify whether G. officinalis pollen was attached to their bodies. Additionally, each visitor was observed to determine whether the reproductive structures of flowers had been touched. Visitors that were positive for all these factors were considered legitimate pollinators.Seed productionTo test the self-compatibility of G. officinalis, flowers subjected to self-pollination treatment (unopened flowers were isolated with paper bags) in 2017 on the three plots were subjected. To further analyse self-compatibility, we conducted outcrossing pollination. In addition, 30 individual inflorescences on different plants were bagged, and two buds at the same position on each inflorescence were selected. Both buds on each inflorescence were emasculated before the flowers opened. When the stigma opened, one flower was pollinated with fresh pollen from the same inflorescence or different inflorescences on the same plant (selfing), and the other was pollinated with fresh pollen from a plant 5 m away (outcrossing). To test whether facilitated selfing occurred, 30 individual plants in each plot were tagged. On each tagged plant, two individual buds were selected: one was assigned to natural pollination, and the other was assigned to emasculation (removal of all anthers before stigma lobe opening). To test whether agamospermy occurred, the flowers were subjected to emasculation treatment and isolated in three plots. Thirty buds on different plants were randomly selected, and all the anthers were removed before the flowers opened, and then all the buds were isolated with paper bags. At maturity, all fruits were collected, and all of the seeds (including mature and abortive seeds) were counted. Seed-set ratios were used to assess the reproductive success of each treatment, which were calculated by the number of mature seeds divided by the total ovules in each ovary. The facilitated selfing data were calculated as the natural seed-set ratio minus the emasculated seed-set ratio.Similarly, 30 inflorescences were tagged on different plants in each plot, and two buds were then tagged at the same position on each inflorescence; one bud was assigned to natural pollination, and the other was assigned to supplemental hand pollination when stigmas opened. For supplemental hand pollination, pollen was collected randomly from unmarked individuals at a minimum distance of 5 m from the recipient individual. Supplemental hand pollination events were conducted every day until the flower was permanently closed. When mature, all seeds were counted, and seed-set ratios were calculated. For each plot, we calculated an index of pollen limitation (IPL): IPL = 1 − (Po/Ps), where Po is the natural seed-set ratio and Ps is the supplemental hand-pollination seed-set ratio. As the seed-set ratios showed no significant difference between natural and supplemental hand pollination in the natural environment, we considered the IPL at this plot to be 0. The IPL data at the other two plots were compared using an independent-samples t test.Statistical analysisThe normality of the data was tested using one-sample Kolmogorov–Smirnov (1-K-S) tests, and then one-way ANOVAs (with Tukey’s multiple contrasts) were used to test differences in all traits among the three environments. More

  • in

    Predator interference and complexity–stability in food webs

    Paine, R. T. Food web complexity and species diversity. Am. Nat. 100, 65–75 (1966).
    Google Scholar 
    McGrady-Steed, J., Harris, P. M. & Morin, P. J. Biodiversity regulates ecosystem predictability. Nature 390, 162–165 (1997).CAS 
    ADS 

    Google Scholar 
    Naeem, S. & Li, S. Biodiversity enhances ecosystem reliability. Nature 390, 507–509 (1997).CAS 
    ADS 

    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 
    May, R. M. Will a large complex system be stable?. Nature 238, 413–414 (1972).CAS 
    PubMed 
    ADS 

    Google Scholar 
    Namba, T. Multi-faceted approaches toward unravelling complex ecological networks. Popul. Ecol. 57, 3–19 (2015).
    Google Scholar 
    McCann, K. S. The diversity–stability debate. Nature 405, 228–233 (2000).CAS 
    PubMed 

    Google Scholar 
    Pimm, S. L. & Pimm, S. L. The balance of nature?: Ecological issues in the conservation of species and communities (University of Chicago Press, 1991).MATH 

    Google Scholar 
    Landi, P., Minoarivelo, H. O., Brännström, Å., Hui, C. & Dieckmann, U. Complexity and stability of ecological networks: a review of the theory. Popul. Ecol. 60, 319–345 (2018).
    Google Scholar 
    Baiser, B., Gotelli, N. J., Buckley, H. L., Miller, T. E. & Ellison, A. M. Geographic variation in network structure of a nearctic aquatic food web. Glob. Ecol. Biogeogr. 21, 579–591 (2012).
    Google Scholar 
    Marczak, L. B. et al. Latitudinal variation in top-down and bottom-up control of a salt marsh food web. Ecology 92, 276–281 (2011).CAS 
    PubMed 

    Google Scholar 
    Takemoto, K., Kanamaru, S. & Feng, W. Climatic seasonality may affect ecological network structure: food webs and mutualistic networks. Biosystems 121, 29–37 (2014).PubMed 

    Google Scholar 
    De Angelis, D. L. Stability and connectance in food web models. Ecology 56, 238–243 (1975).
    Google Scholar 
    Borrvall, C., Ebenman, B. & Tomas Jonsson, T. J. Biodiversity lessens the risk of cascading extinction in model food webs. Ecol. Lett. 3, 131–136 (2000).
    Google Scholar 
    Stouffer, D. B. & Bascompte, J. Compartmentalization increases food-web persistence. Proc. Natl. Acad. Sci. 108, 3648–3652 (2011).CAS 
    PubMed 
    PubMed Central 
    ADS 

    Google Scholar 
    Dunne, J. A., Williams, R. J. & Martinez, N. D. Network structure and biodiversity loss in food webs: robustness increases with connectance. Ecol. Lett. 5, 558–567 (2002).
    Google Scholar 
    Dunne, J. A. & Williams, R. J. Cascading extinctions and community collapse in model food webs. Philos. Trans. R. Soc. B. Biol. Sci. 364, 1711–1723 (2009).
    Google Scholar 
    McCann, K., Hastings, A. & Huxel, G. R. Weak trophic interactions and the balance of nature. Nature 395, 794–798 (1998).CAS 
    ADS 

    Google Scholar 
    Barabás, G., Michalska-Smith, M. J. & Allesina, S. Self-regulation and the stability of large ecological networks. Nat. Ecol. Evol. 1, 1870–1875 (2017).PubMed 

    Google Scholar 
    Winemiller, K. O. Spatial and temporal variation in tropical fish trophic networks. Ecol. Monogr. 60, 331–367 (1990).
    Google Scholar 
    Paine, R. T. Food-web analysis through field measurement of per capita interaction strength. Nature 355, 73–75 (1992).ADS 

    Google Scholar 
    Wootton, J. T. Estimates and tests of per capita interaction strength: diet, abundance, and impact of intertidally foraging birds. Ecol. Monogr. 67, 45–64 (1997).
    Google Scholar 
    Gellner, G. & McCann, K. S. Consistent role of weak and strong interactions in high-and low-diversity trophic food webs. Nat. Commun. 7, 1–7 (2016).
    Google Scholar 
    Mougi, A. & Kondoh, M. Diversity of interaction types and ecological community stability. Science (80-.) 337, 349–351 (2012).MathSciNet 
    CAS 
    MATH 
    ADS 

    Google Scholar 
    Kondoh, M. & Mougi, A. Interaction-type diversity hypothesis and interaction strength: the condition for the positive complexity–stability effect to arise. Popul. Ecol. 57, 21–27 (2015).
    Google Scholar 
    Mougi, A. & Kondoh, M. Stability of competition–antagonism–mutualism hybrid community and the role of community network structure. J. Theor. Biol. 360, 54–58 (2014).PubMed 
    MATH 
    ADS 

    Google Scholar 
    Mougi, A. & Kondoh, M. Food-web complexity, meta-community complexity and community stability. Sci. Rep. 6, 1–5 (2016).
    Google Scholar 
    Brose, U., Williams, R. J. & Martinez, N. D. Allometric scaling enhances stability in complex food webs. Ecol. Lett. 9, 1228–1236 (2006).PubMed 

    Google Scholar 
    Kondoh, M. Foraging adaptation and the relationship between food-web complexity and stability. Science (80-.) 299, 1388–1391 (2003).CAS 

    Google Scholar 
    Kawatsu, K. & Kondoh, M. Density-dependent interspecific interactions and the complexity-stability relationship. Proc. R. Soc. B Biol. Sci. 285, 20180698 (2018).
    Google Scholar 
    Oaten, A. & Murdoch, W. W. Functional response and stability in predator-prey systems. Am. Nat. 109, 289–298 (1975).
    Google Scholar 
    Chesson, P. Mechanisms of maintenance of species diversity. Annu. Rev. Ecol. Syst. 31, 343–366 (2000).
    Google Scholar 
    Nunney, L. The stability of complex model ecosystems. Am. Nat. 115, 639–649 (1980).MathSciNet 

    Google Scholar 
    Kartascheff, B., Guill, C. & Drossel, B. Positive complexity–stability relations in food web models without foraging adaptation. J. Theor. Biol. 259, 12–23 (2009).MathSciNet 
    PubMed 
    MATH 
    ADS 

    Google Scholar 
    Sih, A., Englund, G. & Wooster, D. Emergent impacts of multiple predators on prey. Trends Ecol. Evol. 13, 350–355 (1998).CAS 
    PubMed 

    Google Scholar 
    Kéfi, S. et al. More than a meal… integrating non-feeding interactions into food webs. Ecol. Lett. 15, 291–300 (2012).PubMed 

    Google Scholar 
    Terry, J. C. D., Morris, R. J. & Bonsall, M. B. Trophic interaction modifications: an empirical and theoretical framework. Ecol. Lett. 20, 1219–1230 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    Wootton, J. T. The nature and consequences of indirect effects in ecological communities. Annu. Rev. Ecol. Syst. 25, 443–466 (1994).
    Google Scholar 
    Werner, E. E. & Peacor, S. D. A review of trait-mediated indirect interactions in ecological communities. Ecology 84, 1083–1100 (2003).
    Google Scholar 
    Bolker, B., Holyoak, M., Křivan, V., Rowe, L. & Schmitz, O. Connecting theoretical and empirical studies of trait-mediated interactions. Ecology 84, 1101–1114 (2003).
    Google Scholar 
    Schmitz, O. J. Predator diversity and trophic interactions. Ecology 88, 2415–2426 (2007).PubMed 

    Google Scholar 
    Feng, J., Dakos, V. & van Nes, E. H. Does predator interference cause alternative stable states in multispecies communities?. Theor. Popul. Biol. 82, 170–176 (2012).PubMed 
    MATH 

    Google Scholar 
    Arditi, R., Callois, J.-M., Tyutyunov, Y. & Jost, C. Does mutual interference always stabilize predator–prey dynamics? A comparison of models. C. R. Biol. 327, 1037–1057 (2004).PubMed 

    Google Scholar 
    DeAngelis, D. L., Goldstein, R. A. & O’Neill, R. V. A model for tropic interaction. Ecology 56, 881–892 (1975).
    Google Scholar 
    Rall, B. C., Guill, C. & Brose, U. Food-web connectance and predator interference dampen the paradox of enrichment. Oikos 117, 202–213 (2008).
    Google Scholar 
    Neutel, A.-M., Heesterbeek, J. A. P. & de Ruiter, P. C. Stability in real food webs: weak links in long loops. Science (80-.) 296, 1120–1123 (2002).CAS 
    ADS 

    Google Scholar 
    Havens, K. Scale and structure in natural food webs. Science (80-.) 257, 1107–1109 (1992).CAS 
    ADS 

    Google Scholar 
    Martinez, N. D. Constant connectance in community food webs. Am. Nat. 139, 1208–1218 (1992).
    Google Scholar 
    Dunne, J. A., Williams, R. J. & Martinez, N. D. Food-web structure and network theory: the role of connectance and size. Proc. Natl. Acad. Sci. 99, 12917–12922 (2002).CAS 
    PubMed 
    PubMed Central 
    ADS 

    Google Scholar 
    MacArthur, R. Species packing and competitive equilibrium for many species. Theor. Popul. Biol. 1, 1–11 (1970).CAS 
    PubMed 

    Google Scholar 
    Langkilde, T. & Shine, R. Competing for crevices: interspecific conflict influences retreat-site selection in montane lizards. Oecologia 140, 684–691 (2004).PubMed 
    ADS 

    Google Scholar 
    Elliott, J. M. Interspecific interference and the functional response of four species of carnivorous stoneflies. Freshw. Biol. 48, 1527–1539 (2003).
    Google Scholar 
    Franke, H. D. & Janke, M. Mechanisms and consequences of intra- and interspecific interference competition in Idotea baltica (Pallas) and Idotea emarginata (Fabricius) (Crustacea: Isopoda): a laboratory study of possible proximate causes of habitat segregation. J. Exp. Mar. Bio. Ecol. 227, 1–21 (1998).
    Google Scholar 
    Peckarsky, B. L. Mechanisms of intra-and interspecific interference between larval stoneflies. Oecologia 85, 521–529 (1991).PubMed 
    ADS 

    Google Scholar 
    Kimura, K. & Chiba, S. Interspecific interference competition alters habitat use patterns in two species of land snails. Evol. Ecol. 24, 815–825 (2010).
    Google Scholar 
    Franke, H.-D. & Janke, M. Mechanisms and consequences of intra-and interspecific interference competition in Idotea baltica (Pallas) and Idotea emarginata (Fabricius)(Crustacea: Isopoda): a laboratory study of possible proximate causes of habitat segregation. J. Exp. Mar. Bio. Ecol. 227, 1–21 (1998).
    Google Scholar 
    Pasch, B., Bolker, B. M. & Phelps, S. M. Interspecific dominance via vocal interactions mediates altitudinal zonation in neotropical singing mice. Am. Nat. 182, E161–E173 (2013).PubMed 

    Google Scholar 
    Bolger, D. T. & Case, T. J. Intra-and interspecific interference behaviour among sexual and asexual geckos. Anim. Behav. 44, 21–30 (1992).
    Google Scholar 
    Wolff, J. O. The effects of density, food, and interspecific interference on home range size in Peromyscus leucopus and Peromyscus maniculatus. Can. J. Zool. 63, 2657–2662 (1985).
    Google Scholar 
    Hasegawa, K. & Maekawa, K. Role of visual barriers on mitigation of interspecific interference competition between native and non-native salmonid species. Can. J. Zool. 87, 781–786 (2009).
    Google Scholar 
    Denno, R. F., McClure, M. S. & Ott, J. R. Interactions in resurrected. Annu. Rev. Entomol. 40, 297–331 (1995).CAS 

    Google Scholar 
    Grether, G. F., Losin, N., Anderson, C. N. & Okamoto, K. The role of interspecific interference competition in character displacement and the evolution of competitor recognition. Biol. Rev. 84, 617–635 (2009).PubMed 

    Google Scholar 
    Carothers, J. H., Jaksić, F. M. & Jaksic, F. M. Time as a Niche difference: the role of interference competition. Oikos 42, 403 (1984).
    Google Scholar 
    Grether, G. F., Peiman, K. S., Tobias, J. A. & Robinson, B. W. Causes and consequences of behavioral interference between species. Trends Ecol. Evol. 32, 760–772 (2017).PubMed 

    Google Scholar 
    Stouffer, D. B. & Novak, M. Hidden layers of density dependence in consumer feeding rates. Ecol. Lett. 24, 520–532 (2021).PubMed 

    Google Scholar 
    Beddington, J. R. Mutual interference between parasites or predators and its effect on searching efficiency. J. Anim. Ecol. 44, 331–340 (1975).
    Google Scholar 
    Cervantes-Loreto, A., Ayers, C. A., Dobbs, E. K., Brosi, B. J. & Stouffer, D. B. The context dependency of pollinator interference: how environmental conditions and co-foraging species impact floral visitation. Ecol. Lett. 24, 1443–1454 (2021).PubMed 

    Google Scholar 
    Chen, X. & Cohen, J. E. Transient dynamics and food–web complexity in the Lotka-Volterra cascade model. Proc. R. Soc. Lond. Ser. B Biol. Sci. 268, 869–877 (2001).CAS 

    Google Scholar 
    Thébault, E. & Fontaine, C. Stability of ecological communities and the architecture of mutualistic and trophic networks. Science (80-.) 329, 853–856 (2010).ADS 

    Google Scholar 
    Guill, C. & Drossel, B. Emergence of complexity in evolving niche-model food webs. J. Theor. Biol. 251, 108–120 (2008).MathSciNet 
    PubMed 
    MATH 
    ADS 

    Google Scholar  More

  • in

    Modelling the emergence dynamics of the western corn rootworm beetle (Diabrotica virgifera virgifera)

    Let (y_{itk}) denote the WCR count observed for trap i in week t in year k, and assume it to follow a Poisson distribution with parameter (mu _{itk})$$begin{aligned} y_{itk} | mu _{itk}, sim Poisson(mu _{itk}) end{aligned}$$
    (1)
    The intensity parameter (mu _{itk}) represents the rate of emergence for a given time period. Instead of allowing it to depend purely on time t, a phenological variable of growing degree days (GDD) is used, as warmer temperatures are required for WCR development25,26,27,28. GDDs reflect the heat accumulation and are defined as an integral of warmth above a base temperature after a given start date:$$begin{aligned} GDD = int (T(t)-T_{base})dt. end{aligned}$$
    (2)
    The above integral can be approximated by$$begin{aligned} GDD = max left( frac{T_{max} – T_{min}}{2} – T_{base}, 0 right) . end{aligned}$$
    (3)
    Here (T_{min}) is the minimum daily temperature, (T_{max}) is the maximum daily temperature, and (T_{base}) is a set base temperature. In this study, the base temperature was set to (10,^{circ })C, and the starting date was the beginning of April, which marks the start of the growing season in Austria.The rate of cumulative emergence of the WCR beetle can be described by a Gompertz function. The Gompertz function is a sigmoidal function which describes growth as being slowest at the beginning and the end of a given period and is defined as$$begin{aligned} f(z_t) = alpha exp (-beta exp (-gamma z_t)). end{aligned}$$
    (4)
    where (alpha) is the upper asymptote, (beta) is a relative starting value, (gamma) is a growth rate coefficient which affects the slope, and (z_t) are the cumulative growing degree days. In this study, one can consider the asymptote as proxy to the saturation level of WCR population growth. Lower values of (beta) suggest an earlier first emergence in the season, while lower values of (gamma) indicate a longer emergence period. To investigate whether there is an association between climate variables and the emergence dynamics, the Gompertz curve parameters were assumed to linearly depend on climate covariates. In this regression modelling framework, a spatially correlated residual structure can be added in either (alpha), (beta), and/or (gamma) if there is evidence to do so.To reflect the nature of the emergence dynamics and to preserve the shape of the increasing Gompertz curve, the parameters of the model were restricted to positive values such that (alpha >0), (beta >0), and (gamma >0). The time at inflection or period of highest growth can be obtained by solving Eq. (4) for the value of t at which the concavity of the function changes. The time at inflection is described as:$$begin{aligned} T_z^* = frac{log (beta )}{gamma } end{aligned}$$
    (5)
    The Gompertz function describes cumulative emergence. Thus to describe the marginal emergence rate, the derivative of the Gompertz function can be used instead. Consequently, as the WCR trapping data consisted of weekly counts, the rate of emergence (mu _{itk}) is better described by the log of the derivative of the Gompertz function$$begin{aligned} log (mu _{itk}) = log (alpha _{ik}) + log (gamma _{ik}) + log (beta _{ik}) + gamma _i z_{itk} – beta _{ik} exp (-gamma z_{itk}). end{aligned}$$
    (6)
    The parameters (alpha _{ik}), (beta _{ik}) and (gamma _{ik}) are site and year specific such that:$$begin{aligned}&alpha _{ik} sim N(mu _{alpha _{ik}}, tau _{alpha }) end{aligned}$$
    (7)
    $$begin{aligned}&gamma _{ik} sim N(mu _{gamma _{ik}}, tau _{gamma }) end{aligned}$$
    (8)
    $$begin{aligned}&beta _{ik} sim N(mu _{beta _{ik}}, tau _{beta }). end{aligned}$$
    (9)
    Here, (tau _{alpha }), (tau _{beta }), and (tau _{gamma }) are the precision (inverse variance) parameters of the prior distributions for (alpha), (beta) and (gamma) respectively. Moreover, the means of the distributions (mu _{alpha _{ik}}), (mu _{beta _{ik}}), and (mu _{gamma _{ik}}) can be expressed as functions of known covariates:$$begin{aligned} mu _{alpha _{ik}}= & {} a_{0} + {mathbf {w}}^T X_{alpha _{ik}}, end{aligned}$$
    (10)
    $$begin{aligned} mu _{beta _{ik}}= & {} b_{0}, end{aligned}$$
    (11)
    $$begin{aligned} mu _{gamma _{ik}}= & {} g_{0} + {mathbf {u}}^T X_{gamma _{ik}}. end{aligned}$$
    (12)
    Here (a_{0}) is the intercept, ({mathbf {w}}) is a vector of the regression coefficients, and (X_{alpha _{ik}}) are the location and year specific covariates. The predictors used in the regression of (mu _{alpha _{ik}}) are the average winter temperature, the precipitation sum during winter, the year, the percentage of the agricultural area per Austrian municipality used for cultivating maize crops (maize), and the corresponding centred coordinates of the trap locations; x, y, and their functions (x^2), (y^2), and xy. The parameter (g_{0}) is the intercept for the regression of (mu _{gamma _{ik}}), and u is the corresponding regression coefficient. The predictor used for (mu _{gamma _ik}) is the average yearly spring temperature.The intercepts and regression coefficients ((mathbf {w}) and (mathbf {u})) were given non-informative normal priors N(0, 0.01). The precision parameters (tau _{alpha }), (tau _{beta }) and (tau _{gamma }) were assigned prior distributions Gamma(0.01, 0.01).The model was fitted using WinBUGS through the R2WinBUGS package in R29,30,31. The model was run for 20000 iterations, with a burn-in of 10000 iterations, and a thinning rate of five. Convergence was determined by visual assessments of trace plots and marginal posterior densities. More