More stories

  • in

    Globally distributed mining-impacted environments are underexplored hotspots of multidrug resistance genes

    World Health Organization. Antimicrobial resistance: global report on surveillance. World Health Organization. 2014. https://www.who.int/publications/i/item/9789241564748.O’Neill J. Tackling drug-resistant infections globally: final report and recommendations. Government of the United Kingdom. 2016. https://apo.org.au/sites/default/files/resource-files/2016-05/apo-nid63983.pdf.UN Environment. Frontiers 2017: emerging Issues of environmental concern. United Nations Environment Programme. 2017. https://wedocs.unep.org/20.500.11822/22255.Davies J, Davies D. Origins and evolution of antibiotic resistance. Microbiol Mol Biol Rev. 2010;74:417–33.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    D’Costa VM, King CE, Kalan L, Morar M, Sung WW, Schwarz C, et al. Antibiotic resistance is ancient. Nature. 2011;477:457–61.PubMed 
    Article 
    CAS 

    Google Scholar 
    Baker-Austin C, Wright MS, Stepanauskas R, McArthur JV. Co-selection of antibiotic and metal resistance. Trends Microbiol. 2006;14:176–82.CAS 
    PubMed 
    Article 

    Google Scholar 
    Wang F, Fu Y-H, Sheng H-J, Topp E, Jiang X, Zhu Y-G, et al. Antibiotic resistance in the soil ecosystem: a one health perspective. Curr Opin Environ Sci Health. 2021;20:100230.Article 

    Google Scholar 
    Zhang F, Zhao X, Li Q, Liu J, Ding J, Wu H, et al. Bacterial community structure and abundances of antibiotic resistance genes in heavy metals contaminated agricultural soil. Environ Sci Pollut Res. 2018;25:9547–55.CAS 
    Article 

    Google Scholar 
    Seiler C, Berendonk T. Heavy metal driven co-selection of antibiotic resistance in soil and water bodies impacted by agriculture and aquaculture. Front Microbiol. 2012;3:399.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Ji X, Shen Q, Liu F, Ma J, Xu G, Wang Y, et al. Antibiotic resistance gene abundances associated with antibiotics and heavy metals in animal manures and agricultural soils adjacent to feedlots in Shanghai; China. J Hazard Mater. 2012;235-236:178–85.CAS 
    PubMed 
    Article 

    Google Scholar 
    Komijani M, Shamabadi NS, Shahin K, Eghbalpour F, Tahsili MR, Bahram M. Heavy metal pollution promotes antibiotic resistance potential in the aquatic environment. Environ Pollut. 2021;274:116569.CAS 
    PubMed 
    Article 

    Google Scholar 
    Zhao Y, Cocerva T, Cox S, Tardif S, Su J-Q, Zhu Y-G, et al. Evidence for co-selection of antibiotic resistance genes and mobile genetic elements in metal polluted urban soils. Sci Total Environ. 2019;656:512–20.CAS 
    PubMed 
    Article 

    Google Scholar 
    Bhattacharyya A, Haldar A, Bhattacharyya M, Ghosh A. Anthropogenic influence shapes the distribution of antibiotic resistant bacteria (ARB) in the sediment of Sundarban estuary in India. Sci Total Environ. 2019;647:1626–39.CAS 
    PubMed 
    Article 

    Google Scholar 
    Bridge G. Contested terrain: mining and the environment. Annu Rev Environ Resour. 2004;29:205–59.Article 

    Google Scholar 
    Liu J-L, Yao J, Zhu X, Zhou D-L, Duran R, Mihucz VG, et al. Metagenomic exploration of multi-resistance genes linked to microbial attributes in active nonferrous metal(loid) tailings. Environ Pollut. 2021;273:115667.CAS 
    Article 

    Google Scholar 
    Baker BJ, Banfield JF. Microbial communities in acid mine drainage. FEMS Microbiol Ecol. 2003;44:139–52.CAS 
    PubMed 
    Article 

    Google Scholar 
    Mendez MO, Maier RM. Phytostabilization of mine tailings in arid and semiarid environments—an emerging remediation technology. Environ Health Perspect. 2008;116:278–83.CAS 
    PubMed 
    Article 

    Google Scholar 
    Cycoń M, Mrozik A, Piotrowska-Seget Z. Antibiotics in the soil environment—degradation and their impact on microbial activity and diversity. Front Microbiol. 2019;10:338.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Hu H-W, Wang J-T, Li J, Li J-J, Ma Y-B, Chen D, et al. Field-based evidence for copper contamination induced changes of antibiotic resistance in agricultural soils. Environ Microbiol. 2016;18:3896–909.CAS 
    PubMed 
    Article 

    Google Scholar 
    Huang L-N, Zhou W-H, Hallberg Kevin B, Wan C-Y, Li J, Shu W-S. Spatial and temporal analysis of the microbial community in the tailings of a Pb-Zn mine generating acidic drainage. Appl Environ Microbiol. 2011;77:5540–44.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Milaković M, Vestergaard G, González-Plaza JJ, Petrić I, Šimatović A, Senta I, et al. Pollution from azithromycin-manufacturing promotes macrolide-resistance gene propagation and induces spatial and seasonal bacterial community shifts in receiving river sediments. Environ Int. 2019;123:501–11.PubMed 
    Article 
    CAS 

    Google Scholar 
    Tricco AC, Lillie E, Zarin W, O’Brien KK, Colquhoun H, Levac D, et al. PRISMA extension for scoping reviews (PRISMA-ScR): checklist and explanation. Ann Intern Med. 2018;169:467–73.PubMed 
    Article 

    Google Scholar 
    Yang T-T, Liu J, Chen W-C, Chen X, Shu H-Y, Jia P, et al. Changes in microbial community composition following phytostabilization of an extremely acidic Cu mine tailings. Soil Biol Biochem. 2017;114:52–58.CAS 
    Article 

    Google Scholar 
    Zhao L, Anderson CW, Qiu G, Meng B, Wang D, Feng X. Mercury methylation in paddy soil: source and distribution of mercury species at a Hg mining area, Guizhou Province, China. Biogeosciences. 2016;13:2429–40.CAS 
    Article 

    Google Scholar 
    Liang J-L, Liu J, Jia P, Yang T-T, Zeng Q-W, Zhang S-C, et al. Novel phosphate-solubilizing bacteria enhance soil phosphorus cycling following ecological restoration of land degraded by mining. ISME J. 2020;14:1600–13.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Nurk S, Meleshko D, Korobeynikov A, Pevzner PA. metaSPAdes: a new versatile metagenomic assembler. Genome Res. 2017;27:824–34.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Li D, Liu C-M, Luo R, Sadakane K, Lam T-W. MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics. 2015;31:1674–76.CAS 
    PubMed 
    Article 

    Google Scholar 
    Sieber CMK, Probst AJ, Sharrar A, Thomas BC, Hess M, Tringe SG, et al. Recovery of genomes from metagenomes via a dereplication, aggregation and scoring strategy. Nat Microbiol. 2018;3:836–43.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Lu YY, Chen T, Fuhrman JA, Sun F. COCACOLA: binning metagenomic contigs using sequence COmposition, read CoverAge, CO-alignment and paired-end read LinkAge. Bioinformatics. 2017;33:791–98.CAS 
    PubMed 

    Google Scholar 
    Wu Y-W, Simmons BA, Singer SW. MaxBin 2.0: an automated binning algorithm to recover genomes from multiple metagenomic datasets. Bioinformatics. 2016;32:605–7.CAS 
    PubMed 
    Article 

    Google Scholar 
    Kang DD, Froula J, Egan R, Wang Z. MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities. PeerJ. 2015;3:e1165.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Uritskiy GV, DiRuggiero J, Taylor J. MetaWRAP—a flexible pipeline for genome-resolved metagenomic data analysis. Microbiome. 2018;6:158.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Parks DH, Rinke C, Chuvochina M, Chaumeil P-A, Woodcroft BJ, Evans PN, et al. Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life. Nat Microbiol. 2017;2:1533–42.CAS 
    PubMed 
    Article 

    Google Scholar 
    Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 2015;25:1043–55.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Hyatt D, LoCascio PF, Hauser LJ, Uberbacher EC. Gene and translation initiation site prediction in metagenomic sequences. Bioinformatics. 2012;28:2223–30.CAS 
    PubMed 
    Article 

    Google Scholar 
    Li W, Godzik A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics. 2006;22:1658–59.CAS 
    PubMed 
    Article 

    Google Scholar 
    Arango-Argoty G, Garner E, Pruden A, Heath LS, Vikesland P, Zhang L. DeepARG: a deep learning approach for predicting antibiotic resistance genes from metagenomic data. Microbiome. 2018;6:23.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Doster E, Lakin SM, Dean CJ, Wolfe C, Young JG, Boucher C, et al. MEGARes 2.0: a database for classification of antimicrobial drug, biocide and metal resistance determinants in metagenomic sequence data. Nucleic Acids Res. 2020;48:D561–69.CAS 
    PubMed 
    Article 

    Google Scholar 
    Pal C, Bengtsson-Palme J, Rensing C, Kristiansson E, Larsson DJ. BacMet: antibacterial biocide and metal resistance genes database. Nucleic Acids Res. 2014;42:D737–43.CAS 
    PubMed 
    Article 

    Google Scholar 
    Martin C, Stebbins B, Ajmani A, Comendul A, Hamner S, Hasan NA, et al. Nanopore-based metagenomics analysis reveals prevalence of mobile antibiotic and heavy metal resistome in wastewater. Ecotoxicology. 2021;30:1572–85.CAS 
    PubMed 
    Article 

    Google Scholar 
    Siguier P, Pérochon J, Lestrade L, Mahillon J, Chandler M. ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res. 2006;34:D32–36.CAS 
    PubMed 
    Article 

    Google Scholar 
    Moura A, Soares M, Pereira C, Leitão N, Henriques I, Correia A. INTEGRALL: a database and search engine for integrons, integrases and gene cassettes. Bioinformatics. 2009;25:1096–98.CAS 
    PubMed 
    Article 

    Google Scholar 
    Tansirichaiya S, Rahman MA, Roberts AP. The transposon registry. Mob DNA. 2019;10:40.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods. 2015;12:59–60.CAS 
    PubMed 
    Article 

    Google Scholar 
    Chakraborty J, Sapkale V, Rajput V, Shah M, Kamble S, Dharne M. Shotgun metagenome guided exploration of anthropogenically driven resistomic hotspots within Lonar soda lake of India. Ecotoxicol Environ Saf. 2020;194:110443.CAS 
    PubMed 
    Article 

    Google Scholar 
    Krawczyk PS, Lipinski L, Dziembowski A. PlasFlow: predicting plasmid sequences in metagenomic data using genome signatures. Nucleic Acids Res. 2018;46:e35.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Bushnell B. BBMap: a fast, accurate, splice-aware aligner. 2014. The 9th Annual Genomics of Energy & Environment Meeting. US. https://www.osti.gov/servlets/purl/1241166.Ma L, Xia Y, Li B, Yang Y, Li L-G, Tiedje JM, et al. Metagenomic assembly reveals hosts of antibiotic resistance genes and the shared resistome in pig, chicken, and human feces. Environ Sci Technol. 2016;50:420–7.CAS 
    PubMed 
    Article 

    Google Scholar 
    Li L-G, Xia Y, Zhang T. Co-occurrence of antibiotic and metal resistance genes revealed in complete genome collection. ISME J. 2017;11:651–62.CAS 
    PubMed 
    Article 

    Google Scholar 
    Segata N, Börnigen D, Morgan XC, Huttenhower C. PhyloPhlAn is a new method for improved phylogenetic and taxonomic placement of microbes. Nat Commun. 2013;4:2304.PubMed 
    Article 
    CAS 

    Google Scholar 
    Letunic I, Bork P. Interactive tree of life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res. 2011;39:W475–78.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Parks DH, Chuvochina M, Waite DW, Rinke C, Skarshewski A, Chaumeil P-A, et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol. 2018;36:996–1004.CAS 
    PubMed 
    Article 

    Google Scholar 
    Littman RA, Fiorenza EA, Wenger AS, Berry KL, van de Water JA, Nguyen L, et al. Coastal urbanization influences human pathogens and microdebris contamination in seafood. Sci Total Environ. 2020;736:139081.CAS 
    PubMed 
    Article 

    Google Scholar 
    Zheng W, Huyan J, Tian Z, Zhang Y, Wen X. Clinical class 1 integron-integrase gene–a promising indicator to monitor the abundance and elimination of antibiotic resistance genes in an urban wastewater treatment plant. Environ Int. 2020;135:105372.CAS 
    PubMed 
    Article 

    Google Scholar 
    Tasker S, Caney SM, Day MJ, Dean RS, Helps CR, Knowles TG, et al. Effect of chronic FIV infection, and efficacy of marbofloxacin treatment, on Mycoplasma haemofelis infection. Vet Microbiol. 2006;117:169–79.CAS 
    PubMed 
    Article 

    Google Scholar 
    Holden MT, Seth-Smith HM, Crossman LC, Sebaihia M, Bentley SD, Cerdeño-Tárraga AM, et al. The genome of Burkholderia cenocepacia J2315, an epidemic pathogen of cystic fibrosis patients. J Bacteriol. 2009;191:261–77.CAS 
    PubMed 
    Article 

    Google Scholar 
    Moebius N, Ross C, Scherlach K, Rohm B, Roth M, Hertweck C. Biosynthesis of the respiratory toxin bongkrekic acid in the pathogenic bacterium Burkholderia gladioli. Chem Biol. 2012;19:1164–74.CAS 
    PubMed 
    Article 

    Google Scholar 
    Stryjewski ME, LiPuma JJ, Messier RH Jr, Reller LB, Alexander BD. Sepsis, multiple organ failure, and death due to Pandoraea pnomenusa infection after lung transplantation. J Clin Microbiol. 2003;41:2255–57.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Anaissie E, Fainstein V, Miller P, Kassamali H, Pitlik S, Bodey GP, et al. Pseudomonas putida: newly recognized pathogen in patients with cancer. Am J Med. 1987;82:1191–94.CAS 
    PubMed 
    Article 

    Google Scholar 
    Hinse D, Vollmer T, Rückert C, Blom J, Kalinowski J, Knabbe C, et al. Complete genome and comparative analysis of Streptococcus gallolyticus subsp. gallolyticus, an emerging pathogen of infective endocarditis. BMC Genom. 2011;12:400.CAS 
    Article 

    Google Scholar 
    Looney WJ, Narita M, Mühlemann K. Stenotrophomonas maltophilia: an emerging opportunist human pathogen. Lancet Infect Dis. 2009;9:312–23.CAS 
    PubMed 
    Article 

    Google Scholar 
    de Nies L, Lopes S, Busi SB, Galata V, Heintz-Buschart A, Laczny CC, et al. PathoFact: a pipeline for the prediction of virulence factors and antimicrobial resistance genes in metagenomic data. Microbiome. 2021;9:49.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Hendriksen RS, Munk P, Njage P, Van Bunnik B, McNally L, Lukjancenko O, et al. Global monitoring of antimicrobial resistance based on metagenomics analyses of urban sewage. Nat Commun. 2019;10:1124.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Rodriguez-R LM, Konstantinidis KT. Nonpareil: a redundancy-based approach to assess the level of coverage in metagenomic datasets. Bioinformatics. 2014;30:629–35.CAS 
    PubMed 
    Article 

    Google Scholar 
    Wood DE, Lu J, Langmead B. Improved metagenomic analysis with Kraken 2. Genome Biol. 2019;20:257.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’hara R, et al. Vegan: community ecology package. R package version 2.5-7. 2013. http://CRAN.R-project.org/package=vegan.Hijmans RJ. geosphere: spherical trigonometry. R package version 1.5-10. 2019. https://CRAN.R-project.org/package=geosphere.Wickham H. ggplot2: elegant graphics for data analysis. R package version 3.3.2. 2016. https://CRAN.R-project.org/package=ggplot2.Larsson J, Godfrey AJR, Gustafsson P, Eberly DH, Huber E, Slowikowski K, et al. Eulerr: area-proportional Euler and Venn diagrams with ellipses. R package version 6.1.0. 2018. https://CRAN.R-project.org/package=eulerr.Bivand R, Keitt T, Rowlingson B, Pebesma E, Sumner M, Hijmans R, et al. rgdal: Bindings for the ‘Geospatial’ data abstraction library. R package version 1.5.18. 2015. https://CRAN.R-project.org/package=rgdal.Brownrigg R, McIlroy D, Minka TP, Bivand R. mapproj: Map projections. R package version 1.2.7. 2020. https://CRAN.R-project.org/package=mapproj.Bivand R, Lewin-Koh N, Pebesma E, Archer E, Baddeley A, Bearman N, et al. maptools: Tools for handling spatial objects. R package version 0.9-9. 2020. https://CRAN.R-project.org/package=maptools.Rice EW, Wang P, Smith AL, Stadler LB. Determining hosts of antibiotic resistance genes: a review of methodological advances. Environ Sci Technol Lett. 2020;7:282–91.CAS 
    Article 

    Google Scholar 
    Forsberg KJ, Patel S, Gibson MK, Lauber CL, Knight R, Fierer N, et al. Bacterial phylogeny structures soil resistomes across habitats. Nature. 2014;509:612–16.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Hu H-W, Wang J-T, Singh BK, Liu Y-R, Chen Y-L, Zhang Y-J, et al. Diversity of herbaceous plants and bacterial communities regulates soil resistome across forest biomes. Environ Microbiol. 2018;20:3186–200.CAS 
    PubMed 
    Article 

    Google Scholar 
    Ju F, Beck K, Yin X, Maccagnan A, McArdell CS, Singer HP, et al. Wastewater treatment plant resistomes are shaped by bacterial composition, genetic exchange, and upregulated expression in the effluent microbiomes. ISME J. 2019;13:346–60.PubMed 
    Article 

    Google Scholar 
    Chen Q-L, An X-L, Zheng B-X, Gillings M, Peñuelas J, Cui L, et al. Loss of soil microbial diversity exacerbates spread of antibiotic resistance. Soil Ecol Lett. 2019;1:3–13.Article 

    Google Scholar 
    Martinez JL, Sánchez MB, Martínez-Solano L, Hernandez A, Garmendia L, Fajardo A, et al. Functional role of bacterial multidrug efflux pumps in microbial natural ecosystems. FEMS Microbiol Rev. 2009;33:430–49.CAS 
    PubMed 
    Article 

    Google Scholar 
    Karkman A, Pärnänen K, Larsson DJ. Fecal pollution can explain antibiotic resistance gene abundances in anthropogenically impacted environments. Nat Commun. 2019;10:80.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Cao J, Yang G, Mai Q, Zhuang Z, Zhuang L. Co-selection of antibiotic-resistant bacteria in a paddy soil exposed to as (III) contamination with an emphasis on potential pathogens. Sci Total Environ. 2020;725:138367.CAS 
    PubMed 
    Article 

    Google Scholar 
    Pal C, Bengtsson-Palme J, Kristiansson E, Larsson DJ. Co-occurrence of resistance genes to antibiotics, biocides and metals reveals novel insights into their co-selection potential. BMC Genom. 2015;16:964.Article 
    CAS 

    Google Scholar 
    Teare MD, Barrett JH. Genetic linkage studies. Lancet. 2005;366:1036–44.CAS 
    Article 

    Google Scholar 
    Learman DR, Ahmad Z, Brookshier A, Henson MW, Hewitt V, Lis A, et al. Comparative genomics of 16 Microbacterium spp. that tolerate multiple heavy metals and antibiotics. PeerJ. 2019;6:e6258.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Liu Z, Klümper U, Liu Y, Yang Y, Wei Q, Lin J-G, et al. Metagenomic and metatranscriptomic analyses reveal activity and hosts of antibiotic resistance genes in activated sludge. Environ Int. 2019;129:208–20.CAS 
    PubMed 
    Article 

    Google Scholar 
    Fresia P, Antelo V, Salazar C, Giménez M, D’Alessandro B, Afshinnekoo E, et al. Urban metagenomics uncover antibiotic resistance reservoirs in coastal beach and sewage waters. Microbiome. 2019;7:35.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Zhu Y-G, Johnson TA, Su J-Q, Qiao M, Guo G-X, Stedtfeld RD, et al. Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proc Natl Acad Sci USA. 2013;110:3435–40.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Zhu Y-G, Zhao Y, Li B, Huang C-L, Zhang S-Y, Yu S, et al. Continental-scale pollution of estuaries with antibiotic resistance genes. Nat Microbiol. 2017;2:16270.CAS 
    PubMed 
    Article 

    Google Scholar 
    Williams AB. In: Kovalchuk I, Kovalchuk O, editors. Genome stability. Boston: Academic Press; 2016. p. 69–85.Cury J, Touchon M, Rocha EP. Integrative and conjugative elements and their hosts: composition, distribution and organization. Nucleic Acids Res. 2017;45:8943–56.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Liu M, Li X, Xie Y, Bi D, Sun J, Li J, et al. ICEberg 2.0: an updated database of bacterial integrative and conjugative elements. Nucleic Acids Res. 2018;47:D660–65.PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Su J-Q, An X-L, Li B, Chen Q-L, Gillings MR, Chen H, et al. Metagenomics of urban sewage identifies an extensively shared antibiotic resistome in China. Microbiome. 2017;5:84.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Zhao R, Feng J, Yin X, Liu J, Fu W, Berendonk TU, et al. Antibiotic resistome in landfill leachate from different cities of China deciphered by metagenomic analysis. Water Res. 2018;134:126–39.CAS 
    PubMed 
    Article 

    Google Scholar 
    Alcock BP, Raphenya AR, Lau TT, Tsang KK, Bouchard M, Edalatmand A, et al. CARD 2020: antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucleic Acids Res. 2020;48:D517–25.CAS 
    PubMed 
    Article 

    Google Scholar 
    Li B, Yang Y, Ma L, Ju F, Guo F, Tiedje JM, et al. Metagenomic and network analysis reveal wide distribution and co-occurrence of environmental antibiotic resistance genes. ISME J. 2015;9:2490–502.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Zhao X, Li X, Li Y, Sun Y, Zhang X, Weng L, et al. Shifting interactions among bacteria, fungi and archaea enhance removal of antibiotics and antibiotic resistance genes in the soil bioelectrochemical remediation. Biotechnol Biofuels. 2019;12:160.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Khelaifia S, Drancourt M. Susceptibility of archaea to antimicrobial agents: applications to clinical microbiology. Clin Microbiol Infect. 2012;18:841–48.CAS 
    PubMed 
    Article 

    Google Scholar 
    Fuchsman CA, Collins RE, Rocap G, Brazelton WJ. Effect of the environment on horizontal gene transfer between bacteria and archaea. PeerJ. 2017;5:e3865.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Cangelosi GA, Freitag NE, Buckley M. From outside to inside: environmental microorganisms as human pathogens. 2005. https://www.asmscience.org/content/report/colloquia/colloquia.14Molina L, Ramos C, Duque E, Ronchel MC, Garcı́a JM, Wyke L, et al. Survival of Pseudomonas putida KT2440 in soil and in the rhizosphere of plants under greenhouse and environmental conditions. Soil Biol Biochem. 2000;32:315–21.CAS 
    Article 

    Google Scholar 
    Furlan JPR, Pitondo-Silva A, Stehling EG. Detection of blaNDM-1 in Stenotrophomonas maltophilia isolated from Brazilian soil. Mem Inst Oswaldo Cruz. 2018;113:e170558.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Gao J, Li B-Y, Wang H-H, Liu Z-Q. Pseudomonas hunanensis sp. nov., isolated from soil subjected to long-term manganese pollution. Curr Microbiol. 2014;69:19–24.CAS 
    PubMed 
    Article 

    Google Scholar 
    Green SK, Schroth MN, Cho JJ, Kominos SD, Vitanza-Jack VB. Agricultural plants and soil as a reservoir for Pseudomonas aeruginosa. Appl Microbiol. 1974;28:987–91.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar  More

  • in

    Group differences in feeding and diet composition of wild western gorillas

    Wallace, R. B. & Painter, R. L. Phenological patterns in a southern Amazonian tropical forest: Implications for sustainable management. For. Ecol. Manag. 160, 19–33 (2002).Article 

    Google Scholar 
    Malhi, Y. & Wright, J. Spatial patterns and recent trends in the climate of tropical rainforest regions. PTRBAE 359, 311–329 (2004).PubMed 
    PubMed Central 

    Google Scholar 
    Adamescu, G. S. et al. Annual cycles are the most common reproductive strategy in African tropical tree communities. Biotropica 50(3), 418–430 (2018).Article 

    Google Scholar 
    Brockman, D. K., Van Schaik, C. P., & Schaik, C. P. (Eds.) (2005) Seasonality in primates: Studies of living and extinct human and non-human primates (Vol. 44). Cambridge University Press.Morellato, L. P. C. et al. Phenology of Atlantic rain forest trees: A comparative study. Biotropica 32, 811–823 (2000).Article 

    Google Scholar 
    Brugiere, D., Gautier, J. P., Moungazi, A. & Gautier-Hion, A. Primate diet and biomass in relation to vegetation composition and fruiting phenology in a rain forest in Gabon. Int J Primatol 23, 999–1024 (2002).Article 

    Google Scholar 
    Bollen, A. & Donati, G. Phenology of the littoral forest of Sainte Luce, Southeastern Madagascar. Biotropica 37, 32–43 (2005).Article 

    Google Scholar 
    Chapman, C. A., Wrangham, R. W., Chapman, L. J., Kennard, D. K. & Zanne, A. E. Fruit and flower phenology at two sites in Kibale National Park, Uganda. J. Trop. Ecol. 15, 189–211 (1999).Article 

    Google Scholar 
    Van Schaik, C. P. & Pfannes, K. R. Tropical climates and phenology: A primate perspective. Camb. Stud. Biol. Evol. Anthropol. 44, 23–54 (2005).
    Google Scholar 
    Birkhofer, K. & Wolters, V. The global relationship between climate, net primary production and the diet of spiders. Glob. Ecol. Biogeogr. 21, 100–108 (2012).Article 

    Google Scholar 
    Creel, S. et al. Changes in African large carnivore diets over the past half-century reveal the loss of large prey. J. Appl. Ecol. 55, 2908–2916 (2018).Article 

    Google Scholar 
    Hemingway, C. A. & Bynum, N. The influence of seasonality on primate diet and ranging. Camb. Stud. Biol. Evol. Anthropol. 44, 57–104 (2005).
    Google Scholar 
    Trapanese, C., Meunier, H. & Masi, S. What, where and when: spatial foraging decisions in primates. Biol. Rev. 94, 483–502 (2019).PubMed 
    Article 

    Google Scholar 
    Jahn, A. E., Levey, D. J., Hostetler, J. A. & Mamani, A. M. Determinants of partial bird migration in the Amazon Basin. J. Anim. Ecol. 79, 983–992 (2010).PubMed 
    Article 

    Google Scholar 
    Catterall, C. P., Kingston, M. B., Park, K. & Sewell, S. Deforestation, urbanisation and seasonality: Interacting effects on a regional bird assemblage. Biol. Conserv. 84, 65–81 (1998).Article 

    Google Scholar 
    Pettorelli, N. et al. Using the satellite-derived NDVI to assess ecological responses to environmental change. Trends Ecol. Evol. 20, 503–510 (2005).PubMed 
    Article 

    Google Scholar 
    Monteith, K. L. et al. Timing of seasonal migration in mule deer: Effects of climate, plant phenology, and life-history characteristics. Ecosphere. 2, 1–34 (2011).Article 

    Google Scholar 
    Levey, D. J. & Karasov, W. H. Digestive modulation in a seasonal frugivore, the American robin (Turdus migratorius). Am. J. Physiol.-Gastr. L 262, 711–718 (1992).
    Google Scholar 
    Seri, H. et al. Effects of seasonal variation, group size and sex on the activity budget and diet composition of the addax antelope. Afr. J. Range Forage Sci. 35, 89–100 (2018).Article 

    Google Scholar 
    Pavelka, M. S. & Knopff, K. H. Diet and activity in black howler monkeys (Alouatta pigra) in southern Belize: Does degree of frugivory influence activity level?. Primates 45, 105–111 (2004).PubMed 
    Article 

    Google Scholar 
    Joshi, R. & Singh, R. Feeding behaviour of wild Asian elephants (Elephas maximus) in the Rajaji National Park. J. Am. Sci. 4, 34–48 (2008).
    Google Scholar 
    Remis, M. J., Dierenfeld, E. S., Mowry, C. B. & Carroll, R. W. Nutritional aspects of western lowland gorilla (Gorilla gorilla gorilla) diet during seasons of fruit scarcity at Bai Hokou, Central African Republic. Int. J. Primatol. 22, 807–836 (2001).Article 

    Google Scholar 
    Doran-Sheehy, D. M., Greer, D., Mongo, P. & Schwindt, D. Impact of ecological and social factors on ranging in western gorillas. Am. J. Primatol. 64, 207–222 (2004).PubMed 
    Article 

    Google Scholar 
    Masi, S., Cipolletta, C. & Robbins, M. M. Western Lowland Gorillas (Gorilla gorilla gorilla) change their activity patterns in response to Frugivory. Am. J. Primatol. 71, 91–100 (2009).PubMed 
    Article 

    Google Scholar 
    Masi, S. et al. The influence of seasonal frugivory on nutrient and energy intake in wild western gorillas. PLoS ONE 10(7), e0129254 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Kuntz, R., Kubalek, C., Ruf, T., Tataruch, F. & Arnold, W. Seasonal adjustments of energy budgets in free ranging Przewalski horses (Equus ferus przewalskii). I. Energy intake. J. Exp. Biol 209, 4557–4565 (2006).PubMed 
    Article 

    Google Scholar 
    Arnold, W., Ruf, T. & Kuntz, R. Seasonal adjustment of energy budget in a large wild mammal, the Przewalski horse (Equus ferus przewalskii). II Energy expenditure. J. Experim. Biol. 209, 4566–4573 (2006).Article 

    Google Scholar 
    Campera, M. et al. Effects of habitat quality and seasonality on ranging patterns of collared brown lemur (Eulemur collaris) in littoral forest fragments. Int. J. Primatol. 35, 957–975 (2014).Article 

    Google Scholar 
    Irwin, M. T. Diademed sifaka (Propithecus diadema) ranging and habitat use in continuous and fragmented forest: Higher density but lower viability in fragments?. Biotropica 40, 231–240 (2008).Article 

    Google Scholar 
    Volampeno, M. S., Masters, J. C. & Downs, C. T. Home range size in the blue-eyed black lemur (Eulemur flavifrons): A comparison between dry and wet seasons. Mamm. Biol. 76, 157–164 (2011).Article 

    Google Scholar 
    Boyle, S. A., Lourenço, W. A., da Silva, L. R. & Smith, A. T. Travel and spatial patterns change when Chiropotes satanas chiropotes inhabit forest fragments. Int. J. Primatol. 30, 515–531 (2009).Article 

    Google Scholar 
    Snaith, T. V. & Chapman, C. A. Red colobus monkeys display alternative behavioral responses to the costs of scramble competition. Behav. Ecol. 19, 1289–1296 (2008).Article 

    Google Scholar 
    Conklin-Brittain, N. L., Wrangham, R. W. & Hunt, K. D. Dietary response of chimpanzees and cercopithecines to seasonal variation in fruit abundance. II. Macronutrients. Int. J. Primatol. 19, 971–998 (1998).Article 

    Google Scholar 
    Wrangham, R. W., Conklin-Brittain, N. L. & Hunt, K. D. Dietary response of chimpanzees and cercopithecines to seasonal variation in fruit abundance. I. Antifeedants. Int. J. Primatol. 19, 949–970 (1998).Article 

    Google Scholar 
    Knott, C. D. Changes in orangutan caloric intake, energy balance, and ketones in response to fluctuating fruit availability. Int. J. Primatol. 19, 1061–1079 (1998).Article 

    Google Scholar 
    Campbell-Smith, G., Campbell-Smith, M., Singleton, I. & Linkie, M. Raiders of the lost bark: Orangutan foraging strategies in a degraded landscape. PLoS ONE 6, e20962. https://doi.org/10.1371/journal.pone.0020962 (2011).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    N’guessan, A. K., Ortmann, S. & Boesch C.,. Daily energy balance and protein gain among Pan troglodytes verus in the Taï National Park, Côte d’Ivoire. Int. J. Primatol. 30, 481 (2009).Article 

    Google Scholar 
    Yamakoshi, G. Food seasonality and socioecology in Pan: Are West African chimpanzees another bonobo?. Afr. Study Monogr. 25, 45–60 (2004).
    Google Scholar 
    Ganas, J. & Robbins, M. M. Ranging behavior of the mountain gorillas (Gorilla beringei beringei) in Bwindi Impenetrable National Park, Uganda: a test of the ecological constraints model. Behav. Ecol. Sociobiol. 58, 277–288 (2005).Article 

    Google Scholar 
    Rothman, J. M., Dierenfeld, E. S., Hintz, H. F. & Pell, A. N. Nutritional quality of gorilla diets: Consequences of age, sex, and season. Oecologia 155, 111–122. https://doi.org/10.1007/s00442-007-0901-1 (2008) (PMID: 17999090).ADS 
    Article 
    PubMed 

    Google Scholar 
    Grueter, C. C., Deschner, T., Behringer, V., Fawcett, K. & Robbins, M. M. Socioecological correlates of energy balance using urinary C-peptide measurements in wild female mountain gorillas. Physiol. Behav. 127, 13–19 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    Clutton-Brock, T. H. & Harvey, P. H. Species differences in feeding and ranging behaviour in Primates, Primate ecology: Studies on feeding and ranging behaviour in lemurs, monkeys and apes p l-631 (1977).Chapman, C. A. & Chapman, L. J. Constraints on group size in red colobus and red-tailed guenons: Examining the generality of the ecological constraints model. Int. J. Primatol. 21, 565–585 (2000).Article 

    Google Scholar 
    Markham, A. C., Gesquiere, L. R., Alberts, S. C. & Altmann, J. Optimal group size in a highly social mammal. PNAS 112, 14882–14887 (2015).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Janson, C. H. Food competition in brown capuchin monkey (Cebus apella)—Quantitative effects of group-size and tree productivity. Behaviour 105, 53–73 (1988).Article 

    Google Scholar 
    Aureli, F., Schaffner, C. M., Verpooten, J., Slater, K. & Ramos-Fernandez, G. Raiding parties of male spider monkeys: Insights into human warfare?. Am J Phys Anthropol 131, 486–497 (2006).PubMed 
    Article 

    Google Scholar 
    Donati, G. et al. Better few than hungry: flexible feeding ecology of collared lemurs Eulemur collaris in littoral forest fragments. PLoS ONE 6(5), e19807 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Milton, K. Habitat, diet, and activity patterns of free-ranging woolly spider monkeys (Brachyteles arachnoides E. Geoffroy 1806). Int. J. Primatol. 5, 491–514 (1984).Article 

    Google Scholar 
    Wrangham, R. W., Gittleman, J. & Chapman, C. A. Constraints on group size in primates and carnivores: Population density and day-range as assays of exploitation competition. Behav. Ecol. Sociobiol. 32, 199–209. https://doi.org/10.1007/BF00173778 (1993).Article 

    Google Scholar 
    Chapman, C. A., Wrangham, R. W. & Chapman, L. J. Ecological constraints on group-size—An analysis of spider monkey and chimpanzee subgroups. Behav. Ecol. Sociobiol. 36, 59–70 (1995).Article 

    Google Scholar 
    Janson, C. H. & Goldsmith, M. L. Predicting group size in primates: Foraging costs and predation risks. Behav. Ecol. 6, 326–336 (1995).Article 

    Google Scholar 
    Chapman, C. A. & Pavelka, M. S. Group size in folivorous primates: Ecological constraints and the possible influence of social factors. Primates 46, 1–9 (2005).PubMed 
    Article 

    Google Scholar 
    Clutton-Brock, T. H. & Harvey, P. H. Primate ecology and social organization. J. Zool. 183, 1–39 (1977).Article 

    Google Scholar 
    Isbell, L. A. Contest and scramble competition: Patterns of female aggression and ranging behavior among primates. Behav. Ecol. 2, 143–155 (1991).Article 

    Google Scholar 
    Fimbel, C., Vedder, A., Dierenfeld, E. & Mulindahabi, F. An ecological basis for large group size in Colobus angolensis in the Nyungwe Forest, Rwanda. Afric. J. Ecol. 39, 83–92 (2001).
    Google Scholar 
    Snaith, T. V. & Chapman, C. A. Primate group size and socioecological models: Do folivores really play by different rules?. Evol. Anthropol. 16(3), 94–106 (2007).Article 

    Google Scholar 
    Gogarten, J. F. et al. Increasing group size alters behavior of a folivorous primate. Int. J. Primatol. 35, 590–608 (2014).Article 

    Google Scholar 
    Grueter, C. C. & van Schaik, C. P. Evolutionary determinants of modular societies in colobines. Behav. Ecol. 21, 63–71 (2010).Article 

    Google Scholar 
    Zhang, K., Zhou, Q., Xu, H. & Huang, Z. Effect of group size on time budgets and ranging behavior of white-headed Langurs in Limestone Forest, Southwest China. Folia Primatol. 91, 188–201. https://doi.org/10.1159/000502812 (2020).Article 

    Google Scholar 
    Lukas, D. & Huchard, E. The evolution of infanticide by males in mammalian societies. Science 346, 841–844 (2014).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Treves, A. & Chapmam, C. A. Conspecific threat, predation avoidance, and resource defense: Implications for grouping in langurs. Behav. Ecol. Sociobiol. 39, 43–53 (1996).Article 

    Google Scholar 
    Crockett, C. M. & Janson, C. H. Infanticide in red howlers: female group size, male membership, and a possible link to folivory. In Infanticide by Males and Its Implications (eds van Schaik, C. P. & Janson, C. H.) 75–98 (Cambridge University Press, 2000).Chapter 

    Google Scholar 
    Gillespie, T. R. & Chapman, C. A. Determinants of group size in the red colobus monkey (Procolobus badius): An evaluation of the generality of the ecological-constraints model. Behav. Ecol. Sociobiol. 50, 329–338 (2001).Article 

    Google Scholar 
    Smith, R. J. & Jungers, W. L. Body mass in comparative primatology. J. Hum. Evol. 32, 523–559 (1997).CAS 
    PubMed 
    Article 

    Google Scholar 
    Harcourt, A. H. & Stewart, K. J. Gorilla Society: Conflict, Compromise, and Cooperation Between the Sexes (University of Chicago Press, 2007).Book 

    Google Scholar 
    Masi, S. & Bouret, S. Odor signals in wild western lowland gorillas: An involuntary and extra-group communication hypothesis. Physiol. Behav. 145, 123–126 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    Klailova, M. et al. Non-human predator interactions with wild great apes in Africa and the use of camera traps to study their dynamics. Folia Primatol. 83, 312–328 (2012).Article 

    Google Scholar 
    Remis, M. J. Ranging and grouping patterns of a western lowland gorilla group at Bai Hokou, Central African Republic. Am. J. Primatol. 43, 111–133 (1997).CAS 
    PubMed 
    Article 

    Google Scholar 
    Remis, M. J. Western lowland gorillas (Gorilla gorilla gorilla) as seasonal frugivores: Use of variable resources. Am. J. Primatol. 43, 87–109 (1997).CAS 
    PubMed 
    Article 

    Google Scholar 
    Tutin, C. E. G. Ranging and Social Structure of Lowland Gorillas in the Lope Reserve, Gabon. In McGrew WC 58–70 (Nishida TE Great ape societies. Cambridge University Press, 1996).
    Google Scholar 
    Goldsmith, M. L. Ecological constraints on the foraging effort of western gorillas (Gorilla gorilla gorilla) at Bai Hokou, Central African Republic. Int. J. Primatol. 20, 1–23 (1999).Article 

    Google Scholar 
    Cipolletta, C. Effects of group dynamics and diet on the ranging patterns of a western gorilla group (Gorilla gorilla gorilla) at Bai Hokou, Central African Republic. Am. J. Primatol. 64, 193–205 (2004).PubMed 
    Article 

    Google Scholar 
    Masi, S. et al. Unusual feeding behavior in wild great apes, a window to understand origins of self-medication in humans: Role of sociality and physiology on learning process. Physiol. Behav. 105, 337–349 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    Gomez, A. et al. Gut microbiome composition and metabolomic profiles of wild western lowland gorillas (Gorilla gorilla gorilla) reflect host ecology. Molecul. Ecol. 24, 2551–2565 (2015).CAS 
    Article 

    Google Scholar 
    Hicks, A. L. et al. Gut microbiomes of wild great apes fluctuate seasonally in response to diet. Nat. Commun. 9, 1–8 (2018).CAS 
    Article 

    Google Scholar 
    Doran, D. M. et al. Western lowland gorilla diet and resource availability: New evidence, cross-site comparisons, and reflections on indirect sampling methods. Am. J. Primatol. 58, 91–116 (2002).PubMed 
    Article 

    Google Scholar 
    Cipolletta, C. Ranging patterns of a western gorilla group during habituation to humans in the Dzanga-Ndoki National Park, Central African Republic. Int. J. Primatol. 24, 1207–1226 (2003).Article 

    Google Scholar 
    Rogers, M. E. et al. Western gorilla diet: A synthesis from six sites. Am. J. Primatol. 64, 173–192 (2004).PubMed 
    Article 

    Google Scholar 
    Doran-Sheehy, D., Mongo, P., Lodwick, J. & Conklin-Brittain, N. L. Male and Female Western Gorilla Diet: Preferred foods, use of fallback resources, and implications for ape versus Old World Monkey Foraging Strategies. Am. J. Phys. Anthropol. 140, 727–738 (2009).CAS 
    PubMed 
    Article 

    Google Scholar 
    Watts, D. P. Composition and variability of mountain gorilla diets in the central Virungas. Am. J. Primatol. 7, 323–356 (1984).PubMed 
    Article 

    Google Scholar 
    Fossey, D. Gorillas in the Mist (Houghton Mifflin Company, 1983).
    Google Scholar 
    Granjon, A. C. et al. Estimating abundance and growth rates in a wild mountain gorilla population. Anim. Conserv. 23, 455–465 (2020).Article 

    Google Scholar 
    Parnell, R. J. Group size and structure in western lowland gorillas (Gorilla gorilla gorilla) at Mbeli Bai, Republic of Congo. Am. J. Primatol. 56, 193–206 (2002).PubMed 
    Article 

    Google Scholar 
    Vecellio, V. Rapid decline in the largest group of mountain gorillas. Gorilla J. 37, 6–7 (2008).
    Google Scholar 
    Bermejo, M. Home-range use and intergroup encounters in western gorillas (Gorilla g. gorilla) at Lossi forest, North Congo. Am. J. Primatol. 64, 223–232 (2004).CAS 
    PubMed 
    Article 

    Google Scholar 
    Breuer, T., Hockemba, M. B. N., Olejniczak, C., Parnell, R. J. & Stokes, E. J. Physical maturation, life-history classes and age estimates of free-ranging Western Gorillas-Insights from Mbeli Bai, Republic of Congo. Am. J. Primatol. 71, 106–119 (2009).PubMed 
    Article 

    Google Scholar 
    Altmann, J. Observational study of behavior: Sampling methods. Behaviour 49, 227–266 (1974).CAS 
    PubMed 
    Article 

    Google Scholar 
    Watts, D. P. Environmental-influences on mountain gorilla time budgets. Am. J. Primatol. 15, 195–211 (1988).PubMed 
    Article 

    Google Scholar 
    Bolker, B. M. et al. Generalized linear mixed models: a practical guide for ecology and evolution. Trend. Ecol. Evol. 24(3), 127–135 (2009).Article 

    Google Scholar 
    Focardi, S. & Pecchioli, E. Social cohesion and foraging decrease with group size in fallow deer (Dama dama). Behav. Ecol. Sociobiol. 59, 84–91 (2005).Article 

    Google Scholar 
    Lagory, K. E. Habitat, group size, and the behaviour of white-tailed deer. Behaviour 98, 68–179 (1986).Article 

    Google Scholar 
    White, F. J. Seasonality and socioecology: The importance of variation in fruit abundance to bonobo sociality. Int. J. Primatol. 19, 1013–1027 (1998).Article 

    Google Scholar 
    Brockman, D. K. & Van Schaik, C. P. Seasonality in Primates: Studies of Living and Extinct Human and Non-human Primates (Cambridge University Press, 2005).Book 

    Google Scholar 
    Donati, G., Bollen, A., Borgognini-Tarli, S. M. & Ganzhorn, J. U. Feeding over the 24-h cycle: dietary flexibility of cathemeral collared lemurs (Eulemur collaris). Behav. Ecol. Sociobiol. 61, 1237–1251 (2007).Article 

    Google Scholar 
    Simmen, B. et al. Total energy expenditure and body composition in two free-living sympatric lemurs. PLoS ONE 5, e9860 (2010).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Harrison, M. E., Morrogh-Bernard, H. C. & Chivers, D. J. Orangutan energetics and the influence of fruit availability in the nonmasting peat-swamp forest of Sabangau, Indonesian Borneo. Int. J. Primatol. 31, 585–607 (2010).Article 

    Google Scholar 
    Seiler, N. & Robbins, M. M. Using long-term ranging patterns to assess within-group and between-group competition in wild mountain gorillas. BMC Ecol. 20(1), 1–13 (2020).Article 

    Google Scholar 
    Dias, P. A. D., Rangel-Negrín, A., Coyohua-Fuentes, A. & Canales-Espinosa, D. Variation in dietary breadth among groups of black howler monkeys is not associated with the vegetation attributes of forest fragments. Am. J. Primatol. 76, 1151–1162 (2014).PubMed 
    Article 

    Google Scholar 
    Parker, K. L., Barboza, P. S. & Stephenson, T. R. Protein conservation in female caribou (Rangifer tarandus): Effects of decreasing diet quality during winter. J. Mammal 86, 610–622. https://doi.org/10.1644/1545-1542 (2005).Article 

    Google Scholar 
    Bean, A. Ecology of sex differences in great ape foraging. Comparat. Primate Socioecol. 19, 22–339 (2001).
    Google Scholar 
    Grueter, C. C. et al. Fallback foods of temperate-living primates: A case study on snub-nosed monkeys. Am. J. Phys. Anthrop. 40(4), 700–715 (2009).Article 

    Google Scholar 
    Milton, K. Distribution patterns of tropical plant foods as an evolutionary stimulus to primate mental development. Am. Anthropol. 83, 534–548 (1981).Article 

    Google Scholar 
    Koenig, A., Beise, J., Chalise, M. K. & Ganzhorn, J. U. When females should contest for food—Testing hypotheses about resource density, distribution, size, and quality with Hanuman langurs (Presbytis entellus). Behav. Ecol. Sociobiol. 42, 225–237 (1998).Article 

    Google Scholar 
    Van Soest, P. J. Nutritional Ecology of the Ruminant (Cornell University Press, 2018).
    Google Scholar 
    Chivers, D. J. & Hladik, C. M. Morphology of the gastrointestinal tract in primates: Comparisons with other mammals in relation to diet. J. Morphol. 166, 337–386 (1980).CAS 
    PubMed 
    Article 

    Google Scholar 
    Remis, M. J. & Dierenfeld, E. S. Digesta passage, digestibility and behavior in captive gorillas under two dietary regimens. Int. J. Primatol. 25, 825–845 (2004).Article 

    Google Scholar 
    Redford, K. H. & Dorea, J. G. The nutritional value of invertebrates with emphasis on ants and termites as food for mammals. J. Zool. 203, 385–395 (1984).CAS 
    Article 

    Google Scholar 
    McGrew, W. C. The ‘other faunivory’revisited: insectivory in human and non-human primates and the evolution of human diet. J. Hum. Evol. 71, 4–11 (2014).PubMed 
    Article 

    Google Scholar 
    Isbell, L. A. & Young, T. P. Interspecific and temporal variation of ant species within Acacia drepanolobium ant domatia, a staple food of patas monkeys (Erythrocebus patas) in Laikipia, Kenya. Am. J. Primatol. 69, 1387–1398 (2007).PubMed 
    Article 

    Google Scholar 
    Deblauwe, I., Dupain, J., Nguenang, G. M., Werdenich, D. & Van Elsacker, L. Insectivory by Gorilla gorilla gorilla in Southeast Cameroon. Int. J. Primatol. 24, 493–502 (2003).Article 

    Google Scholar 
    Cipolletta, C. et al. Termite feeding by Gorilla gorilla gorilla at Bai Hokou, Central African Republic. Int. J. Primatol. 28, 457–476 (2007).Article 

    Google Scholar 
    Janson, C. H. Evolutionary ecology of primate social structure. Evol. Ecol. Hum. Behav. 95–130 (1992).Chapman, C. Ecological constraints on group size in three species of neotropical primates. Folia Primatol. 55, 1–9. https://doi.org/10.1159/000156492 (1990).CAS 
    Article 

    Google Scholar 
    Doran, D. M. & McNeilage, A. Subspecific Variation in Gorilla Behavior: The Influence of Ecological and Social Factors. In Mountain gorillas: three decades of research at Karisoke (eds Robbins, M. M. et al.) 123–149 (Cambridge University Press, 2001).Chapter 

    Google Scholar 
    Thouless, C. R. Feeding competition between grazing red deer hinds. Anim. Behav. 40, 105–111 (1990).Article 

    Google Scholar 
    Baudouin, A. et al. Disease avoidance, and breeding group age and size condition the dispersal patterns of western lowland gorilla females. Ecology 100, e02786. https://doi.org/10.1002/ecy.2786 (2019).Article 
    PubMed 

    Google Scholar 
    Breuer, T., Robbins, A. M., Boesch, C. & Robbins, M. M. Phenotypic correlates of male reproductive success in western gorillas. J. Hum. Evol. 62, 466–472 (2012).PubMed 
    Article 

    Google Scholar 
    Stokes, E. J., Parnell, R. J. & Olejniczak, C. Female dispersal and reproductive success in wild western lowland gorillas (Gorilla gorilla gorilla). Behav. Ecol. Sociobiol. 54, 329–339. https://doi.org/10.1007/s00265-003-0630- (2003).Article 

    Google Scholar 
    Manguette, M. L., Breuer, T., Robeyst, J., Kandza, V. H. & Robbins, M. M. Infant survival in western lowland gorillas after voluntary dispersal by pregnant females. Primates https://doi.org/10.1007/s10329-020-00844-z (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar  More

  • in

    Global assessment of coralline algae mineralogy points to high vulnerability of Southwestern Atlantic reefs and rhodolith beds to ocean acidification

    The data reported in this study expands upon the present knowledge concerning the mineralogy of coralline algae species worldwide, encompassing for the first time coralline algae species data from the Southwest Atlantic Ocean, where this group is the main frame-builders in coral reefs and the major inner component in rhodoliths16,26.Mineralogical analysis revealed that coralline algae species of the Brazilian Shelf were mainly formed of high-Mg calcite. Six coralline algae species in this study had the same range of high-Mg calcite, between 80 and 100%, than the same species from different regions of the world: Lithophyllum corallinae, Lithophyllum kaiseri (as Lithophyllum congestum), Lithophyllum stictaeforme, Lithothamnion crispatum, Melyvonnea erubecens (as Lithothamnion erubecens) and Sporolithon episporum (Table S2). This result confirms that species from different families, such as Corallinaceae, Hapalidiaceae and Sporolithaceae have a CaCO3 skeleton formed mainly of high-Mg calcite.In agreement with earlier studies, the average high-Mg calcite content in Corallinaceae was very similar to the results compiled by Smith et al.11 (96.7 wt.% and 96.2 wt.%, respectively). This pattern was also observed for Hapalidiaceae, which presented a mean value of 88.9 ± 3.6 wt.% in our study and 90.2 wt.%. However, Smith et al.11 registered a high-Mg calcite content of 98 wt.% for Sporolithaceae, while in our study this polymorph had a mean occurrence of 86.2 ± 6.5 wt.%. This percentage can be attributed mainly to the lower content of high-Mg calcite found in Sporolithon yoneshigueae, which is an endemic species of the Brazilian Shelf27.The high similarity between the mineralogy (% high-Mg calcite, % aragonite and % dolomite) of the species belonging to three encrusting algae families, revealed by the cluster analysis, emphasizes the lack of CaCO3 disparities over skeleton mineralogy of coralline algae at family level. This aspect was also evidenced by several studies concerning coralline algae mineralogy11,21,22,23,24,25. This fact was confirmed in the cluster analysis between the mineralogy of the studied coralline species, in which samples from different families were grouped. Considering these findings, the mineralogical pattern exhibited by the crustose algae may not be driven by taxonomic classification, as was first proposed by Chave28. Therefore, the skeletal mineralogy from Brazilian coralline algae species can not be used as a taxonomic character, not even for higher taxonomic levels.In this sense, the mineralogical analysis from L. crispatum, the most common rhodolith-forming species on the Brazilian Shelf16, revealed that samples from the Abrolhos Bank presented higher high-Mg calcite in their composition, and the highest % of Mg substitution in the calcite lattice than the species from the other four regions studied. One of the possible explanations is that the Abrolhos Bank has the highest seawater temperature compared to the other four sites, which influences CCA mineralogy. This result corroborates the hypothesis that coralline algae species do not have a strict control over Mg precipitation as stated by Stanley et al.29. In addition to seawater temperature, Mg/Ca ratio in seawater can also affect the incorporation of magnesium into coralline algae skeletons11,29.In relation to other CaCO3 polymorphs, previous studies have registered some species with up to 20% aragonite11,12. Meanwhile, in this study, S. yoneshigueae presented CaCO3 skeletons formed of more than 30% of aragonite, which expands the range found in coralline algae for this polymorph. The high percentage of aragonite found in S. yoneshigueae could be related to the fact that this species presents larger overgrown calcified empty tetrasporangial compartments, in comparison with other Sporolithaceae species27, which could be filled with aragonite. This feature has mainly been described in the overgrown conceptacles of Lithothamnion sp.30 and in cell infills of Porolithon onkodes31. The presence of aragonite could be also attributed to the use of aragonite granules in the sediment to repair any damage in the alga-substrate attachment32.Raman mapping showed the presence of high-Mg calcite in the bulk of the cell wall with little aragonite in its inner part, which seems to form an inner “shell”, closer to the cell membrane. To date, this is the first study that has utilized Raman maps to show the localization of aragonite in cell walls of coralline algae. The maps consisted of the cellular living layer from the coralline algae crust, right beneath the epithelial cells, which indicates that the mineralization of aragonite occurred in live cells and it was probably not a remineralization process.Aragonite inside cell bodies was first seen by Nash et al.12 using Backscattered Scanning Electron Microscopy. They also reported the presence of dolomite or protodolomite, which were not observed herein by Raman spectroscopy, probably because of the low amount of this polymorph.Previous studies considered that the inclusion of dolomite into carbonate skeletons is a microbial-mediated process after cell death upon the discovery of microbial-associated dolomite formation in anoxic marine33 and freshwater environments34. The presence of several calcium carbonate polymorphs found in coralline algae raises the question of whether all these polymorphs are in fact synthesized by the algae.Indeed, the role of coralline algae in the different forms of calcium carbonate crystal precipitation is a crucial issue that should be addressed. Nowadays, studies calculate the production of CaCO3 by coralline algae based on CCA coverage35, without considering that not all CaCO3 produced in that structure is related to coralline algae biomineralization processes (e.g. secondary calcification processes such as infilling of the older skeleton and skeletal dissolution vs newly deposited carbonate). Therefore, it would be misleading to presume the net CaCO3 accretion of coralline algae structures without knowing the origin of the CaCO3 processes. This is also valid in relation to studies on the influences of atmospheric [CO2] rise on coralline algae, based on weight changes36,37,38 and its impacts on the mineralogy of the existing crust21.Concerning Mg2+ substitution in the high-Mg calcite lattice, we found that Brazilian encrusting algae possess a higher Mg-substitution (46.3% more Mg2+ than the global average) in calcite than specimens collected worldwide. A possible explanation for the higher mean Mg2+ content might be related to the high seawater temperatures39, as this was also observed along the tropical Brazilian Continental Shelf. This can be exemplified by the high Mg2+ content found in fourteen species that occur in warmer waters of the Brazilian Shelf, where the mean surface seawater temperature (SST) ranged between 26.4 and 29.8 °C (from 2008 to 2016), between 17°S and 3°N. The lower Mg2+ amounts presented in L. margaritae and L. attlanticum could also be explained by the temperature, as these species were collected at the southernmost site (27°S) in the temperate zone, where the mean SST (from 2008 to 2016) varied between 22.5 and 25 °C (NOAA Comprehensive Large Array-Data Stewardship System-CLASS: SST50). A relationship between the Mg2+ content and temperature has already been proposed in previous works39 and is widely accepted. Nash and Adey40, when plotting the data collected using XRD, found a very strong correlation coefficient (R2 = 0.975) between mol% MgCO3 in coralline algae and temperature. Moreover, the Mg/Ca rate in coralline algae is used as a proxy archive41 and to generate multicentury-scale climate records from extratropical oceans42.Although seawater temperature is loosely associated with latitude, the New Zealand species, for example, are subjected to lower temperatures (2012 annual maximum and minimum surface seawater temperatures: 21 and 18.7 °C, respectively), while Caribbean and Cocos Island algae grow at higher temperatures (2008–2016 annual maximum and minimum surface seawater temperatures: 29.5 and 23.4 °C, respectively) (NOAA Comprehensive Large Array-Data Stewardship System – CLASS: SST50). If we consider the differences in temperature (≅ 6 °C) and Mg2+ content difference (7.67 wt.%) between the sampling sites along the Brazilian Shelf, we can infer that there is an average increase of 1.27 wt.% of Mg2+ per °C. This value is in the range from 0.4 to 2 wt.% Mg per °C reported previously, both in experimentally and in situ studies39.This relationship between Mg substitution and temperature is also critical in face of the temperature risen episodes that we are seeing all over the world43, including the Brazilian Shelf44. If coralline algae produces High Mg calcite with more Mg substitution in higher seawater temperatures, these thermal anomalies could force the production of a highly soluble polymorph, making coralline algae skeleton even more prone to dissolution.It is well known that high-Mg calcite is the most soluble CaCO3 crystalline polymorph under acidified conditions and that this dissolution is more evident when Mg substitution in the calcite lattice is higher45. In our study 70% of the coralline algae species presented a Mg substitution in the range of 12 to 24% and the mean Mg substitution was 21.1%, which reinforces the susceptibility of Southwestern Atlantic coralline algae to future high [CO2] scenarios.Even though previous experiments using synthetic calcium carbonate showed that the rise of seawater temperature increases Mg substitution, making high-Mg calcite more stable46 and other studies claiming that coralline algae with higher Mg substitution (more than 24% in average) presented less dissolution when exposed to high [CO2]13, Southwestern Ocean coralline algae are already living in a limit situation, where seawater can reach temperatures up to 28 ºC. Since we have a correlation between Mg substitution and temperature around 1.27% Mg per 1 ºC, it would take 2.4 to 6.2 ºC rise so the alga starts to produce a more stable calcite polymorph. Such a temperature rise could be lethal to these algae, also promoting a surface microbial shift that could be crucial to sucectional processes (e.g. settlement) involving other marine organisms, such as corals, which is critical for reef regeneration and recovery from climate-related mortality events47. The comparisons of results obtained through assays with synthetic calcium carbonate must be done with caution, because it should be take into account that the complex calcium carbonate biomineralization processes performed by marine organisms are highly dependent of a narrow range of environmental conditions.In face of the dependency of these environmental conditions, the broad range of Mg content in temperate coralline algae25, a high inter species variability in the % Mg in this study (Abrolhos Bank; 14.5 to 28.8% Mg), as well as an anatomical difference in Mg content in coralline algae40, suggest that other environmental parameters (e.g. Mg/Ca in seawater, light, salinity, etc.) could also drive Mg substitution in coralline algae. Furthemore, coralline algae biological processes might exert some kind of control over Mg-calcite calcification which make them more resilient under rising CO239.Long-term projections of ocean acidification and the CaCO3 saturation state indicated that high-latitude seawater will be undersaturated with respect to high-Mg calcite in the second half of this century45. Early results with coralline algae Sonderophycus capensis and Lithothamnion crispatum in a subtropical mesocosm in Brazil showed that an increase in seawater pCO2 (1000 ppm) enabled both species to continue photosynthesizing but did cause carbonate dissolution48.However, coralline algae from the North Atlantic Ocean, where the temperatures are lower, presented the lowest Mg substitution mean (11.91%), with some algae presenting only 8% of Mg substitution. This fact confers a more stable calcite skeleton to face ocean acidification then individuals from tropical environments. In addition, coralline algae from the Southwestern Atlantic Ocean are already living at temperatures that can be considered a limit for their survival. In fact, for cold water species, a subtle temperature increase could be beneficial in terms of their metabolism, photosynthesis and biomineralization.By the year 2100, surface seawater in all climatic zones could be undersaturated or at metastable equilibrium, with a high-Mg calcite phase containing ≥ 12 mol% Mg45. This could be catastrophic to coralline algae from the Southwest Atlantic Ocean, which produce CaCO3 crystals with more than 20% of Mg substitution in average as shown by the present study and for all the carbonate structures (e.g. rhodolith beds, coralline reefs, etc.) that depends on these skeletons to maintain and grow.It is worth to mention that coralline algae are present since the Mesozoic, in particular Sporolithaceans, which were already abundant in Cretaceous shallow waters49 and have already been submitted to bigger climate change events in the past, such as the Paleocene-Eocene Thermal Maximum (PETM), in which the deep-water temperature increased ∼5 ºC and a massive carbon cycle change took place with a large amount of CO2 absorbed by the oceans50. One of the possible explanations for the survival of coralline algae is that their biomineralogical control is limited to polymorph specification and would be ineffectual in the regulation of skeletal Mg incorporation51. In this sense, in past geological eras, such as the Cretaceous and Paleogene, the Mg/Ca ratio of the oceans favors the precitation of low Mg calcite29,52, which are more stable to dissolution. In a parallel to present day, other fundamental aspect we should take into account is the speed of progression of these changes. Actually, we know that the fast evolution of temperature and acidification present scenarios may result in significant impact on marine biodiversity and in marine calcium carbonate cycle players, as reef organisms and CCA.Carvalho et al.53 proposed that there would be a suitable area for rhodolith occurrence around 230,000 km2, providing a new magnitude to Brazilian Continental Shelf relevance as a major world biofactory of carbonate. In fact, this work confirms the estimation from previous studies, which indicated that this area would correspond to a 2 × 1011 tons of carbonate deposit of the Brazilian coast53. Among the most critical regions in the Brazilian coast, the Abrolhos Bank encompasses the largest continuous latitudinal rhodolith beds registered to date6, which is responsible for the production of approximately 0.025 Gt−1 year−1 of calcium carbonate, similar to those values reported for major tropical reef environments54,55. Another recently described important reef area on the Brazilian Shelf is an extensive carbonate system (≅ 9500 km2) off the Amazon River mouth56, which is composed of mesophotic carbonate reefs and rhodolith beds. These huge carbonate reservoirs and biodiversity hotspots may undergo a major decline if global ocean acidification and temperature rise take place in the near future. More

  • in

    Diversity and distribution of CO2-fixing microbial community along elevation gradients in meadow soils on the Tibetan Plateau

    Zhou, J. Z. et al. Microbial mediation of carbon-cycle feedbacks to climate warming. Nat. Clim. Change 2, 106–110. https://doi.org/10.1038/nclimate1331 (2012).Li, F. L., Liu, M., Li, Z. P., Jiang, C. Y., Han, F. X. & Che, Y. P.Changes in soil microbial biomass and functional diversity with a nitrogen gradient in soil columns. Appl. Soil Ecol. 64, 1–6. https://doi.org/10.1016/j.apsoil.2012.10.006 (2013).Gryta, A., Frąc, M. & Oszust, K. The application of the Biolog EcoPlate approach in ecotoxicological evaluation of dairy sewage sludge. Appl. Biochem. Biotechnol. 174, 1434–1443. https://doi.org/10.1007/s12010-014-1131-8 (2014).Djukic, I., Zehetner, F., Mentler, A. & Gerzabek, M. H. Microbial community composition and activity in different Alpine vegetation zones. Soil Boil Biochem. 42, 155–161. https://doi.org/10.1016/j.soilbio.2009.10.006 (2010)Bell, T., Newman, J. A., Silverman, B. W., Turner, S. L. & Lilley, A. K. The contribution of species richness and composition to bacterial services. Nature. 436 (7054), 1157–1160. https://doi.org/10.1038/nature03891 (2015).Zhang, X., Zhao, X. & Zhang, M. Functional diversity changes of microbial communities along a soil aquifer for reclaimed water recharge. FEMS Microbiol. Ecol. 80, 9–18. https://doi.org/10.1111/j.1574-6941.2011.01263.x (2012).Hügler, M. & Sievert, S. M. Beyond the Calvin cycle: Autotrophic carbon fixation in the ocean. Annu. Rev. Mar. Sci. 3, 261–289. https://doi.org/10.1146/annurev-marine-120709-142712 (2010)Falkowski, P. et al. The global carbon cycle: A test of our knowledge of earth as a system. Science 290, 291–296. https://doi.org/10.1126/science.290.5490.291 (2000).Tabita, F. R. Molecular and cellular regulation of autotrophic carbon dioxide fixation in microorganisms. Microbiol. Rev. 52, 155–189. https://doi.org/10.1128/mr.52.2.155-189.1988 (1988).Yuan, H., Ge, T., Chen, C., O’Donnell, A. G. & Wu, J. Significant role for microbial autotrophy in the sequestration of soil carbon. Appl. Environ. Microbiol. 78, 2328–2336. https://doi.org/10.1128/AEM.06881-11 (2012).Xu, H. H. & Tabita, F. R. Ribulose-1,5-bisphosphate carboxylase/oxygenase gene expression and diversity of Lake Erie planktonic microorganisms. Appl. Environ. Microbiol. 62, 1913–1921. https://doi.org/10.1128/aem.62.6.1913-1921.1996 (1996).Bräuer, S. L. et al. Dark carbon fixation in the Columbia River’s Estuarine Turbidity Maxima: Molecular characterization of red-type cbbL genes and measurement of DIC uptake rates in response to added electron donors. Estuaries Coast. 36(5), 1073–1083. https://doi.org/10.1007/s12237-013-9603-6 (2013).Hanson, T. E. & Tabita, F. R. A ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO)-like protein from chlorobium tepidum that is involved with sulfur metabolism and the response to oxidative stress. Proc. Natl. Acad. Sci. USA 98, 4397–4402. https://doi.org/10.1073/pnas.081610398 (2001).Selesi, D., Pattis, I., Schmid, M., Kandeler, Ellen. & Hartmann, A. Quantification of bacterial RubisCO genes in soils by cbbL targeted real-time PCR. J. Microbiol. Meth. 69, 497–503. https://doi.org/10.1016/j.mimet.2007.03.002 (2007).Shanmugam, S. G.et al. Bacterial diversity patterns differ in soils developing in sub-tropical and cool-temperate ecosystems. Microb. Ecol. 73, 556–569. https://doi.org/10.1007/s00248-016-0884-8 (2017).Guo, G., Kong, W., Liu, J., Zhao, J. & Du H. Diversity and distribution of autotrophic microbial community along environmental gradients in grassland soils on the Tibetan Plateau. Appl. Microbiol. Biotechnol. 99, 8765–8776. https://doi.org/10.1093/femsec/fiw160 (2015).Bryant, J. A., Lamanna, C., Morlon, H., Kerkhoff, A. J., Enquist, B. J. & Green, J. L. Microbes on mountainsides: Contrasting elevational patterns of bacterial and plant diversity. Proc Natl Acad Sci U S A. 105, 11505–11511. https://doi.org/10.1073/pnas.0801920105 (2008)Shen, C., Ni, Y., Liang, W. & Chu, H. Distinct soil bacterial communities along a small-scale elevational gradient in alpine tundra. Front. Microbiol. 6, 582. https://doi.org/10.3389/fmicb.2015.00582 (2015).Lugo, M. A., Ferrero, M., Menoyo, E., Estévez, M.C., Sieriz, F. & Anton, A. Arbuscular mycorrhizal fungi and rhizospheric bacteria diversity along an altitudinal gradient in South American Puna grassland. Microb. Ecol. 55, 705–713. https://doi.org/10.1007/s00248-007-9313-3 (2008).Singh, D., Takahashi, K., & Adams, J. M. Elevational patterns in archaeal diversity on Mt. Fuji. Plos One. 7, e44494. https://doi.org/10.1371/journal.pone.0044494 (2012)Miyamoto, Y., Nakano, T., Hattori, M. & Nara, K. The mid-domain effect in ectomycorrhizal fungi: Range overlap along an elevation gradient on Mount Fuji Japan. ISME J. 8(8), 1739–1746. https://doi.org/10.1038/ismej.2014.34 (2014).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Singh, D., Lee-Cruz, L., Kim, W. S. & Kerfahi D. Strong elevational trends in soil bacterial community composition on Mt. Halla, South Korea. Soil. Boil. Biochem. 68, 140–149. https://doi.org/10.1016/j.soilbio.2013.09.027 (2014).Qiu, J. China: The third pole. Nature 454, 393–396. https://doi.org/10.1038/454393a (2008)Singh, D., Takahashi, K., Kim, M., Chun, J. & Adams, J. M. A hump-backed trend in bacterial diversity with elevation on mount Fuji, Japan. Microb. Ecol. 63, 429–437. https://doi.org/10.1007/s00248-011-9900-1 (2012).Shen, C. et al. Soil pH drives the spatial distribution of bacterial communities along elevation on Changbai Mountain. Soil Boil. Biochem. 57, 204–211. https://doi.org/10.1016/j.soilbio.2012.07.013 (2013).Zhang, B., Chen, S. Y., Zhang, J. F. & Tian, C. Depth-related responses of soil microbial communities toexperimental warming in an alpine meadow on the Qinghai-Tibet Plateau. Eur. J. Soil Sci. 66, 496–504. https://doi.org/10.1111/ejss.12240 (2015).Liu, J.et al. High throughput sequencing analysis of biogeographical distribution of bacterial communities in the black soils of northeast China. Soil Boil. Biochem. 70, 113–122. https://doi.org/10.1016/j.soilbio.2013.12.014 (2014)Wu, X. D., Xu, H. Y., Liu, G. M., Ma, X., Mu, C. & Zhao L. Bacterial communities in the upper soil layers in the permafrost regions on the Qinghai-Tibetan Plateau. Appl. Soil Ecol. 120, 81–88. https://doi.org/10.1016/j.apsoil.2017.08.001 (2017).Horner-Devine, M. C., Lage, M., Hughes, J. B. & Bohannan, B. J. M.A taxa-area relationship for bacteria. Nature 432, 750–753. https://doi.org/10.1038/nature03073 (2004).Fuks, D. et al. Relationships between heterotrophic bacteria and cyanobacteria in the northern Adriatic in relation to the mucilage phenomenon. Sci. Total Environ. 353, 178–188. https://doi.org/10.1016/j.scitotenv.2005.09.015 (2005).Dziallas, C. & Grossart, H. P. Microbial interactions with the cyanobacterium Microcystis aeruginosa and their dependence on temperature. Mar Biol. 159, 2389–2398. https://doi.org/10.1007/s00227-012-1927-4 (2012).Shen, H., Niu, Y., Xie, P., Tao, M. & Yang, X. Morphological and physiological changes in Microcystis aeruginosa as a result of interactions with heterotrophic bacteria. Freshw. Biol. 56, 1065–1080. https://doi.org/10.1111/j.1365-2427.2010.02551.x (2011).Xun, L., Sun, M. L., Zhang, H. H., Xu, N. & Sun, G. Y. Use of mulberry-soybean intercropping in salt-alkali soil impacts the diversity of the soil bacterial community. Microb. Biotechnol. 9, 293–304. https://doi.org/10.1111/1751-7915.12342 (2016).Mohamed, H., Miloud, B., Zohra, F., García-Arenzana, J. M. & Rodríguez-Couto, S. Isolation and characterization of actinobacteria from Algerian Sahara soils with antimicrobial activities. Int. J. Mol. Cell Med. 6, 109–120. https://doi.org/10.22088/acadpub.BUMS.6.2.5 (2017).Wang, J. T. et al. Altitudinal distribution patterns of soil bacterial and archaeal communities along Mt. Shegyla on the Tibetan Plateau. Microb. Ecol. 69, 135–145. https://doi.org/10.1007/s00248-014-0465-7 (2015).Zhang, Y. G. et al. Soil bacterial diversity patterns and drivers along an elevational gradient on Shennongjia Mountain, China. Microb. Biotechnol. 8, 739–746. https://doi.org/10.1111/1751-7915.12288 (2015).Li, G., Xu, G., Shen, C., Yong, T., Zhang, Y., Ma, K.Contrasting elevational diversity patterns for soil bacteria between two ecosystems divided by the treeline. Sci. China Life Sci. 59, 1177–1186. https://doi.org/10.1007/s11427-016-0072-6 (2016).Liu, L., Hart M. M., Zhang, J., Cai, X. & Gai, J. Altitudinal distribution patterns of AM fungal assemblages in a Tibeta.n alpine grassland. FEMS Microbiol. Ecol. 91, fiv078. https://doi.org/10.1093/femsec/fiv078 (2015).Xiao, K. Q. et al. Quantitative analyses of ribulose-1, 5-bisphosphate carboxylase/oxygenase (RubisCO) large-subunit genes (cbb L) in typical paddy soils. FEMS Microbiol. Ecol. 87, 89–101. https://doi.org/10.1111/1574-6941.12193 (2014).Sardans, J., Peñuelas, J. & Estiarte, M. Changes in soil enzymes related to C and N cycle and in soil C and N content under prolonged warming and drought in a Mediterranean shrubland. Appl. Soil Ecol. 39, 223–235. https://doi.org/10.1016/j.apsoil.2007.12.011 (2008).Article 

    Google Scholar 
    Sidari, M., Ronzello, G., Vecchio, G. & Muscolo, A. Influence of slope aspects on soil chemical and biochemical properties in a Pinus Iaricio forest ecosystem of Aspromonte (Southern Italy). Eur. J. Soil Biol. 44, 364–372. https://doi.org/10.1016/j.ejsobi.2008.05.001(2008) (2008).CAS 
    Article 

    Google Scholar 
    La, D., Zhang, Y. J., Pang, Y. Z., Cui, L. L., Liu J. & Suo, N. C.Numerical analysis on plant community and species richness patterns along an altitudinal gradient in the Mila Hill, Tibet. J. Tibet Univ. 12–20 (in Chinese) (2015). More

  • in

    The complete chloroplast genome of critically endangered Chimonobambusa hirtinoda (Poaceae: Chimonobambusa) and phylogenetic analysis

    Assembly and annotation of the chloroplast genomesAssembly resulted in a whole cp genome sequence of C. hirtinoda with a length of 139, 561 bp (Fig. 1), consisting of 83, 166 bp large single-copy region, 20, 811 bp small single-copy regions, and two 21,792 bp IR regions, comprising the typical quadripartite structure of terrestrial plants. The cp genome of C. hirtinoda was annotated with 130 genes, including 85 protein-coding genes, 37 tRNA genes, and 8 rRNA genes (Table 1). Most of the 15 genes in the C. hirtinoda cp genome contain introns. Of these, 13 genes contain one intron (atpF, ndhA, ndhB, petB, petD, rpl2, rpl16, rps16, trnA-UGC, trnI-GAU, trnK-UUU, trnL-UAA, trnV-UAC) and only the gene cyf3 includes two introns, and the gene clpP intron was deleted (Supplementary Table S1). The rps12 gene contained two copies, and the three exons were spliced into a trans-splicing gene18.Figure 1Chloroplast genome map of C. hirtinoda. Different colors represent different functional genes groups. Genes outside the circle indicate counterclockwise transcription, and genes inside the clockwise transcription. The thick black line on the outer circle represents the two IR regions. The GC content is the dark gray area within the ring.Full size imageTable 1 Summary of the chloroplast genome of C. hirtinoda.Full size tableThe accD, ycf1, and ycf2 genes were missing in the cp genome of C. hirtinoda, and the introns in the genes clpP and rpoC1 were lost. This phenomenon is consistent with previous systematic evolutionary studies on the genome structure of plants in the Poaceae family19. The phenomenon of missing genes is reported in other plants20,21,22,23.The total GC content in the C. hirtinoda cp genome was 38.90%, and the content for each of the four bases, A, T, G, and C, was 30.63%, 30.46%, 19.57%, and 19.33%, respectively (Table 2). The LSC region (36.98%) and SSC region (33.21%) exhibited much lower values than the IR region (44.23%), indicating a non-uniform distribution of the base contents in the cp genome, probably because of four rRNAs in the IR region, which in turn makes the GC content higher in the IR region. These values were similar to cp genome results previously reported for some Poaceae plants24,25.Table 2 Base composition in the C. hirtinoda choloroplast genome.Full size tableRepeat sequences and codon analysisSSR consists of 10-bp-long base repeats and is widely used for exploring phylogenetic evolution and genetic diversity analysis26,27,28,29.In total, 48 SSRs were detected in C. hirtinoda, including 27 mononucleotide versions, accounting for 56.25% of the total SSRs, primarily consisting of A or T. Additionally, four dinucleotide repeats consisting of AT/TA and TC/CT repeats, and 3 tri, 13 tetra, and 1penta-repeats (Fig. 2A). From the SSRs distribution perspective, the majority (79%) of SSRs (38) were observed in the LSC area, whereas 6 SSRs in the IR region (13%) and 4 SSRs in the SSC region (8%) were discovered (Fig. 2B). Previous research suggests that the distribution of SSRs numbers in each region and the differences among locations in GC content are related to the expansion or contraction of the IR boundary30.Figure 2Analysis of simple sequence repeats in C. hirtinoda cp genome. (A) The percentage distribution of 45 SSRs in LSC, SSC, and IR regions. (B).Full size imageThe REPuter program revealed that the cp genome of C. hirtinoda was identified with 61 repeats, consisting of 15 palindromic, 19 forward and no reverse and complement repeats (Fig. 3). We noticed that repeat analyses of three Chimonobambusa genus species exhibited 61–65 repeats, with only one reverse in C. hejiangensis. Most of the repeat lengths were between 30 and 100 bp, and the repeat sequences were located in either IR or LSC region31 (Supplementary Table S2).Figure 3Information of chloroplast genome repeats of Chimonobambusa genus species.Full size imageWe identified 20,180 codons in the coding region of C. hirtinoda (Fig. 4, Supplementary Table S3). The codon AUU of Ile was the most used, and the TER of UAG was the least used codon (817 and 19), excluding the termination codons. Leu was the most encoded amino acid (2,170), and TER was the lowest (85). The Relative Synonymous Codon Usage (RSCU) value greater than 1.0 means a codon is used more frequently32. The RSCU values for 31 codons exceeded 1 in the C. hirtinoda cp genome, and of these, the third most frequent codon was A/U with 29 (93.55%), and the frequency of start codons AUG and UGG used demonstrated no bias (RSCU = 1).Figure 4Amino acid frequencies in C. hirtinoda cp genome protein coding sequences. The column diagrams indicate the number of amino acid codes, and the broken line indicates the proportion of amino acid codes.Full size imageComparative analysis of genome structureThe nucleotide variability (Pi) values of the three cp genomes discovered in the Chimonobambusa genus species ranged from 0 to 0.021 with an average value of 0.000544, as demonstrated from DnaSP 5.10 software analysis. Five peaks were observed in the two single-copy regions, and the highest peak was present in the trnT-trnE-trnY region of the LSC region (Fig. 5). The Pi value for LSC and SSC is significantly higher than that of the IR region. In the IR region, highly different sequences were not observed, a highly conserved region. The sequences of these highly variable regions are reported in other plants during examinations for species identification, phylogenetic analysis, and population genetics research33,34,35.Figure 5Sliding window analysis of Chimonobambusa genus complete chloroplast genome sequences. X-axis: position of the midpoint of a window, Y-axis: nucleotide diversity of each window.Full size imageThe structural information for the complete cp genomes among three Chimonobambusa genus species revealed that the sequences in most regions were conserved (Fig. 6). The LSC and SSC regions exhibit a remarkable degree of variation, higher than the IR region, and the non-coding region demonstrates higher variability than the coding region. In the non-coding areas, 7–9 k, 28–30 k, 36 k and other gene loci differed significantly. Genes rpoC2, rps19, ndhJ and other regions differ in the protein-coding region. However, the agreement between the tRNA and rRNA regions is 100%. A similar phenomenon has also been reported by others36.Figure 6Visualization of genome alignment of three species chloroplast genome sequences using Chimonobambusa hejiangensis as reference. The vertical scale shows the percent of identity, ranging from 50 to 100%. The horizontal axis shows the coordinates within the cp genome. Those are some colors represents protein coding, intron, mRNA and conserved non-coding sequence, respectively.Full size imageIR contraction and expansion in the chloroplast genomeDue to the unique circular structure of the cp genome, there are four junctions between the LSC/IRB/SSC/IRA regions. During species evolution, the stability of the two IR regions sequences was ensured by the IR region of the chloroplast genome expanding and contracting to some degree, and this adjustment is the primary reason for chloroplast genome length variation37,38.The variations at IR/SC boundary regions in the three Chimonobambusa genus chloroplast genomes were highly similar in the organization, gene content, and gene order. The size of IR ranges from 21,797 bp (C. tumidissinoda) to 21,835 bp (C. hejiangensis). The ndhH gene spans the SSC/IRa boundary, and this gene extended 181–224 bp into the IRa region for all three Chimonobambusa genus. The gene rps19 was extended from the IRb to the LSC region with a 31–35 bp gap. The rpl12 gene was located in the LSC region of all genomes, varied from 35–36 bp apart from the LSC/IRb (Fig. 7).Figure 7Comparison of LSC, SSC and IR boundaries of chloroplast genomes among the three Chimonobambusa species. The LSC, SSC and IRs regions are represented with different colors. JLB, JSB, JSA and JLA represent the connecting sites between the corresponding regions of the genome, respectively. Genes are showed by boxes.Full size imageThree chloroplast genomes of the Chimonobambusa genus were compared using the Mauve alignment. The results showed that all sequences show perfect synteny conservation with no inversion or rearrangements (Fig. 8).Figure 8The chloroplast genomes of three Chimonobambusa species rearranged by the software MAUVE. Locally collinear blocks (LCBs) are represented by the same color blocks connected by lines. The vertical line indicates the degree of conservatism among position. The small red bar represents rRNA.Full size imagePhylogenetic analysisWe performed a phylogenetic analysis using the complete chloroplast genomes and matK gene reflecting the phylogenetic position of C. hirtinoda. The maximum likelihood (ML) analysis based on the complete chloroplast genomes indicated seven nodes with entirely branch support (100% bootstrap value). However, the three Chimonobambusa genera exhibited a moderate relationship due to fewer samples used, supporting that C. hirtinoda is closely related to C. tumidissinoda with a 62% bootstrap value more than C. hejiangensis. A phylogenetic tree based on the matK gene revealed that Chimonobambusa species clustered in one branch was consistent with the phylogenetic tree constructed by the complete cp genome tree (Fig. 9). The results show that the whole chloroplast genome identified related species better than the former, consistent with the previous study39.Figure 9Maximum likelihood phylogenetic tree based on the complete chloroplast genomes (A) and matK gene (B).Full size image More

  • in

    Deep ocean drivers better explain habitat preferences of sperm whales Physeter macrocephalus than beaked whales in the Bay of Biscay

    Elith, J. & Leathwick, J. R. Species distribution models: Ecological explanation and prediction across space and time. Annu. Rev. Ecol. Evol. Syst. 40, 677–697 (2009).Article 

    Google Scholar 
    Esselman, P. C. & Allan, J. D. Application of species distribution models and conservation planning software to the design of a reserve network for the riverine fishes of northeastern Mesoamerica. Freshw. Biol. 56, 71–88 (2011).Article 

    Google Scholar 
    Valle, M. et al. Comparing the performance of species distribution models of Zostera marina: Implications for conservation. J. Sea Res. 83, 56–64 (2013).ADS 
    Article 

    Google Scholar 
    Robinson, N. M., Nelson, W. A., Costello, M. J., Sutherland, J. E. & Lundquist, C. J. A systematic review of marine-based species distribution models (SDMs) with recommendations for best practice. Front. Mar. Sci. 4:421, (2017).Roberts, J. J. et al. Habitat-based cetacean density models for the US Atlantic and Gulf of Mexico. Sci. Rep. 6, 22615 (2016).Lambert, C. et al. How does ocean seasonality drive habitat preferences of highly mobile top predators? Part I: The north-western Mediterranean Sea. Deep Sea. Res. Part II Top. Stud. Oceanogr. 141, 115–132 (2017).ADS 
    Article 

    Google Scholar 
    Lan, K.-W., Shimada, T., Lee, M.-A., Su, N.-J. & Chang, Y. Using remote-sensing environmental and fishery data to map potential Yellowfin Tuna habitats in the tropical pacific Ocean. Remote Sens. 9, 444 (2017).ADS 
    Article 

    Google Scholar 
    Austin, R. A. et al. Predicting habitat suitability for basking sharks (Cetorhinus maximus) in UK waters using ensemble ecological niche modelling. J. Sea Res. 153, 101767 (2019).Article 

    Google Scholar 
    Hobday, A. J. et al. Impacts of climate change on marine top predators: Advances and future challenges. Deep Sea Res. Part II Top. Stud. Oceanogr. 113, 1–8 (2015).ADS 
    Article 

    Google Scholar 
    Avila, I. C., Kaschner, K. & Dormann, C. F. Current global risks to marine mammals: Taking stock of the threats. Biol. Conserv. 221, 44–58 (2018).Article 

    Google Scholar 
    Panti, C. et al. Marine litter: One of the major threats for marine mammals. Outcomes from the European Cetacean Society workshop. Environ. Pollut. 247, 72–79 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Grémillet, D. et al. Spatial match-mismatch in the Benguela upwelling zone: should we expect chlorophyll and sea-surface temperature to predict marine predator distributions?. J. Appl. Ecol. 45, 610–621 (2008).Article 
    CAS 

    Google Scholar 
    Österblom, H., Olsson, O., Blenckner, T. & Furness, R. W. Junk-food in marine ecosystems. Oikos 117, 967–977 (2008).Article 

    Google Scholar 
    Hazen, E. L., Nowacek, D. P., Laurent, L. S., Halpin, P. N. & Moretti, D. J. The relationship among oceanography, prey fields, and beaked whale foraging habitat in the tongue of the ocean. PLoS ONE 6, e19269 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Louzao, M. et al. Marine megafauna niche coexistence and hotspot areas in a temperate ecosystem. Cont. Shelf Res. 186, 77–87 (2019).ADS 
    Article 

    Google Scholar 
    Rogan, E. et al. Distribution, abundance and habitat use of deep diving cetaceans in the North-East Atlantic. Deep Sea Res. Part II Top. Stud. Oceanogr. 141, 8–19 (2017).ADS 
    Article 

    Google Scholar 
    Bangley, C. W., Curtis, T. H., Secor, D. H., Latour, R. J. & Ogburn, M. B. Identifying important juvenile dusky shark habitat in the northwest atlantic ocean using acoustic telemetry and spatial modeling. Mar. Coast. Fish. 12, 348–363 (2020).Article 

    Google Scholar 
    Yen, P. P. W., Sydeman, W. J. & Hyrenbach, K. D. Marine bird and cetacean associations with bathymetric habitats and shallow-water topographies: implications for trophic transfer and conservation. J. Mar. Syst. 50, 79–99 (2004).Article 

    Google Scholar 
    Redfern, J. V et al. Techniques for cetacean–habitat modeling. Mar. Ecol. Prog. Ser. 310, 271-295 (2006).Robison, B. H. Deep pelagic biology. J. Exp. Mar. Bio. Ecol. 300, 253–272 (2004).Article 

    Google Scholar 
    Reijnders, P. J. H., Aguilar, A. & Borrell, A. Pollution and marine mammals. In Encyclopedia of Marine Mammal (eds Perrin, W. F. et al.) 890–898 (Academic Press, New York, 2009).Chapter 

    Google Scholar 
    Spitz, J. et al. Prey preferences among the community of deep-diving odontocetes from the Bay of Biscay, Northeast Atlantic. Deep Sea Res. Part I Oceanogr. Res. Pap. 58, 273–282 (2011).ADS 
    Article 

    Google Scholar 
    Cañadas, A. et al. The challenge of habitat modelling for threatened low density species using heterogeneous data: The case of Cuvier’s beaked whales in the Mediterranean. Ecol. Indic. 85, 128–136 (2018).Article 

    Google Scholar 
    Pirotta, E., Brotons, J. M., Cerdà, M., Bakkers, S. & Rendell, L. E. Multi-scale analysis reveals changing distribution patterns and the influence of social structure on the habitat use of an endangered marine predator, the sperm whale Physeter macrocephalus in the Western Mediterranean Sea. Deep Sea Res. Part I Oceanogr. Res. Pap. 155, 103169 (2020).Article 

    Google Scholar 
    Watwood, S. L., Miller, P. J. O., Johnson, M., Madsen, P. T. & Tyack, P. L. Deep-diving foraging behaviour of sperm whales (Physeter macrocephalus). J. Anim. Ecol. 75, 814–825 (2006).PubMed 
    Article 

    Google Scholar 
    Warren, V. E. et al. Spatio-temporal variation in click production rates of beaked whales: Implications for passive acoustic density estimation. J. Acoust. Soc. Am. 141, 1962–1974 (2017).ADS 
    PubMed 
    Article 

    Google Scholar 
    Shearer, J. M. et al. Diving behaviour of Cuvier’s beaked whales (Ziphius cavirostris) off Cape Hatteras, North Carolina. R. Soc. Open Sci. 6: 181728 (2019).Brodie, S. et al. Integrating dynamic subsurface habitat metrics into species distribution models. Front. Mar. Sci. 5:219 (2018).Becker, E. et al. Moving towards dynamic ocean management: How well do modeled ocean products predict species distributions?. Remote Sens. 8, 149 (2016).ADS 
    Article 

    Google Scholar 
    Wood, S. N. On confidence intervals for generalized additive models based on penalized regression splines. Aust. N. Z. J. Stat. 48, 445–464 (2006).MathSciNet 
    MATH 
    Article 

    Google Scholar 
    Virgili, A. et al. Combining multiple visual surveys to model the habitat of deep-diving cetaceans at the basin scale. Glob. Ecol. Biogeogr. 28, 300–314 (2019).Article 

    Google Scholar 
    Burnham, K. P. & Anderson, D. R. Model Selection and Multimodel Inference (Springer, New York, 2004).MATH 
    Book 

    Google Scholar 
    Voss, N. A., Vecchione, M., Toll, R. B. & Sweeney, M. J. Systematics and Biogeography of Cephalopods (Smithsonian Institution Press, New York, 1998).
    Google Scholar 
    Kostylev, V. E., Erlandsson, J., Ming, M. Y. & Williams, G. A. The relative importance of habitat complexity and surface area in assessing biodiversity: Fractal application on rocky shores. Ecol. Complex. 2, 272–286 (2005).Article 

    Google Scholar 
    Pingree, R. D. & Cann, B. L. Three anticyclonic slope water oceanic eDDIES (SWODDIES) in the Southern Bay of Biscay in 1990. Deep Sea Res. Part A Oceanogr. Res. Pap. 39, 1147–1175 (1991).ADS 
    Article 

    Google Scholar 
    Koutsikopoulos, C. & Cann, B. L. Physical processes and hydrological structures related to the Bay of Biscay anchovy. Sci. Mar. 60, 9–19 (1996).
    Google Scholar 
    Bost, C. A. et al. The importance of oceanographic fronts to marine birds and mammals of the southern oceans. J. Mar. Syst. 78, 363–376 (2009).Article 

    Google Scholar 
    Woodson, C. B. & Litvin, S. Y. Ocean fronts drive marine fishery production and biogeochemical cycling. Proc. Natl. Acad. Sci. 112, 1710–1715 (2015).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Kiszka, J., Macleod, K., Van Canneyt, O., Walker, D. & Ridoux, V. Distribution, encounter rates, and habitat characteristics of toothed cetaceans in the Bay of Biscay and adjacent waters from platform-of-opportunity Data. ICES J. Mar. Sci. 64, 1033–1043 (2007).Article 

    Google Scholar 
    Waring, G. T., Hamazaki, T., Sheehan, D., Wood, G. & Baker, S. Characterization of beaked whale (Ziphiidae) and sperm whale (Physeter macrocephalus) summer habitat in shelf-edge and deeper waters off the Northeast U.S.. Mar. Mammal Sci. 17, 703–717 (2001).Article 

    Google Scholar 
    Moulins, A., Rosso, M., Nani, B. & Würtz, M. Aspects of the distribution of Cuvier’s beaked whale (Ziphius cavirostris) in relation to topographic features in the Pelagos Sanctuary (north-western Mediterranean Sea). J. Mar. Biol. Assoc. U. K. 87, 177–186 (2007).Article 

    Google Scholar 
    Mussi, B., Miragliuolo, A., Zucchini, A. & Pace, D. S. Occurrence and spatio-temporal distribution of sperm whale (Physeter macrocephalus) in the submarine canyon of Cuma (Tyrrhenian Sea, Italy). Aquat. Conserv. Mar. Freshw. Ecosyst. 24, 59–70 (2014).Article 

    Google Scholar 
    Moors-Murphy, H. B. Submarine canyons as important habitat for cetaceans, with special reference to the Gully: A review. Deep Res. Part II Top. Stud. Oceanogr. 104, 6–19 (2014).ADS 
    Article 

    Google Scholar 
    Millot, C. & Taupier-Letage, I. Circulation in the Mediterranean Sea. In: Saliot, A. (eds) The Mediterranean Sea. Handbook of Environmental Chemistry, vol 5K. Springer, Berlin, Heidelberg. (2005). https://doi.org/10.1007/b107143Robbins, J. R., Bell, E., Potts, J., Babey, L. & Marley, S. A. Likely year-round presence of beaked whales in the Bay of Biscay. Hydrobiologia https://doi.org/10.1007/s10750-022-04822-y (2022).Article 

    Google Scholar 
    McSweeney, D. J., Baird, R. W. & Mahaffy, S. D. Site fidelity, associations, and movements of Cuvier’s (Ziphius cavirostris) and Blainville’s (Mesoplodon densirostris) beaked whales off the island of Hawai’i. Mar. Mammal Sci. 23, 666–687 (2007).Article 

    Google Scholar 
    Wimmer, T. & Whitehead, H. Movements and distribution of northern bottlenose whales, Hyperoodon ampullatus, on the Scotian Slope and in adjacent waters. Can. J. Zool. 82, 1782–1794 (2004).Article 

    Google Scholar 
    Mannocci, L., Monestiez, P., Spitz, J. & Ridoux, V. Extrapolating cetacean densities beyond surveyed regions: Habitat-based predictions in the circumtropical belt. J. Biogeogr. 42, 1267–1280 (2015).Article 

    Google Scholar 
    Symonds, M. R. E. & Moussalli, A. A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike’s information criterion. Behav. Ecol. Sociobiol. 65, 13–21 (2011).Article 

    Google Scholar 
    Lambert, C., Mannocci, L., Lehodey, P. & Ridoux, V. Predicting cetacean habitats from their energetic needs and the distribution of their prey in two contrasted tropical regions. PLoS ONE 9, e105958 (2014).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Virgili, A. et al. Towards a better characterisation of deep-diving whales’ distributions by using prey distribution model outputs?. PLoS ONE 16, e0255667 (2021).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Scales, K. L. et al. Fit to predict? Eco-informatics for predicting the catchability of a pelagic fish in near real time. Ecol. Appl. 27, 2313–2329 (2017).PubMed 
    Article 

    Google Scholar 
    Amano, M. & Yoshioka, M. Sperm whale diving behavior monitored using a suction-cup-attached TDR tag. Mar. Ecol. Prog. Ser. 258, 291–295 (2003).ADS 
    Article 

    Google Scholar 
    Irvine, L., Palacios, D. M., Urbán, J. & Mate, B. Sperm whale dive behavior characteristics derived from intermediate-duration archival tag data. Ecol. Evol. 7, 7822–7837 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Shearer, J. M. et al. Diving behaviour of Cuvier’s beaked whales (Ziphius cavirostris) off Cape Hatteras, North Carolina. R. Soc. Open Sci. 6, 181728 (2019).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Towers, J. R. et al. Movements and dive behaviour of a toothfish-depredating killer and sperm whale. ICES J. Mar. Sci. 76, 298–311 (2019).Article 

    Google Scholar 
    ESRI. ArcGIS Desktop: Release 10.3. Redlands, CA: Environmental Systems Research Institute (2016).Roberts, J. J., Best, B. D., Dunn, D. C., Treml, E. A. & Halpin, P. N. Marine geospatial ecology tools: An integrated framework for ecological geoprocessing with ArcGIS, Python, R, MATLAB, and C++. Environ. Model. Softw. 25, 1197–1207 (2010).Article 

    Google Scholar 
    Buckland, S. T., Rexstad, E. A., Marques, T. A. & Oedekoven, C. S. Distance Sampling: Methods and Applications (Springer International Publishing, New York, 2015).MATH 
    Book 

    Google Scholar 
    Bivand, R. S. & Wong, D. W. S. Comparing implementations of global and local indicators of spatial association. TEST 27, 716–748 (2018).MathSciNet 
    MATH 
    Article 

    Google Scholar 
    Baird, R. W. et al. Diving behaviour of Cuvier’s (Ziphius cavirostris) and Blainville’s (Mesoplodon densirostris) beaked whales in Hawai‘i. Can. J. Zool. 84, 1120–1128 (2006).Article 

    Google Scholar 
    Harris, P. T., Macmillan-Lawler, M., Rupp, J. & Baker, E. K. Geomorphology of the oceans. Mar. Geol. 352, 4–24 (2014).ADS 
    Article 

    Google Scholar 
    Hijmans, R. J. raster: Geographic data analysis and modeling. R package version 3. 4–5. https://CRAN.R-project.org/package=raster (2020).Lau-Medrano, W. grec: Gradient-based recognition of spatial patterns in environmental data. R package version 1.4.1. (2020).Foster, S. D. & Bravington, M. V. A Poisson-Gamma model for analysis of ecological non-negative continuous data. Environ. Ecol. Stat. 20, 533–552 (2013).MathSciNet 
    Article 

    Google Scholar 
    Wood, S. Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. J. R. Stat. Soc (B), 73(1), 3-36 (2011).Hedley, S. L. & Buckland, S. T. Spatial models for line transect sampling. J. Agric. Biol. Environ. Stat. 9, 181–199 (2004).Article 

    Google Scholar 
    Mannocci, L. et al. Predicting cetacean and seabird habitats across a productivity gradient in the South Pacific gyre. Prog. Oceanogr. 120, 383–398 (2014).ADS 
    Article 

    Google Scholar 
    Wei, T. & Simko, V. R package ‘corrplot’: Visualization of a correlation matrix (Version 0.84). https://github.com/taiyun/corrplot (2017).Spiess, A. qpcR: Modelling and analysis of real‐time PCR data. R package version 1.4‐1. https://CRAN.R-project.org/package=qpcR (2018).Fabozzi, F. J., Focardi, S. M., Rachev, S. T. & Arshanapalli, B. G. The basics of financial econometrics: Tools, concepts, and asset management applications. John Wiley & Sons (2014).Becker, E. A. et al. Habitat-based density models for three cetacean species off southern california illustrate pronounced seasonal differences. Front. Mar. Sci. 4:121 (2017).Neill, S. P. & Hashemi, M. R. Fundamentals of ocean renewable energy: Generating electricity from the sea. Academic Press (2018).Becker, E. A. et al. Performance evaluation of cetacean species distribution models developed using generalized additive models and boosted regression trees. Ecol. Evol. 10, 5759–5784 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar  More

  • in

    Deciphering waste bound nitrogen by employing psychrophillic Aporrectodea caliginosa and priming of coprolites by associated heterotrophic nitrifiers under high altitude Himalayas

    Blume-Werry, G. et al. Invasive earthworms unlock arctic plant nitrogen limitation. Nat. Commun. 11, 1–10 (2020).Article 
    CAS 

    Google Scholar 
    Marhan, S. & Scheu, S. Mixing of different mineral soil layers by endogeic earthworms affects carbon and nitrogen mineralization. Biol. Fertil. Soils 42, 308 (2006).Article 

    Google Scholar 
    Sanchez-Hernandez, J. C. Vermiremediation of Pharmaceutical-Contaminated Soils and Organic Amendments (Springer, Berlin, 2020).Book 

    Google Scholar 
    Gómez-Brandón, M., Aira, M., Lores, M. & Domínguez, J. Changes in microbial community structure and function during vermicomposting of pig slurry. Bioresour. Technol. 102, 4171–4178. https://doi.org/10.1016/j.biortech.2010.12.057 (2011).CAS 
    Article 
    PubMed 

    Google Scholar 
    Aira, M. & Domínguez, J. Earthworm effects without earthworms: Inoculation of raw organic matter with worm-worked substrates alters microbial community functioning. PLoS ONE 6, e16354. https://doi.org/10.1371/journal.pone.0016354 (2011).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Blair, J., Parmelee, R. W., Allen, M. F., McCartney, D. & Stinner, B. R. Changes in soil N pools in response to earthworm population manipulations in agroecosystem with different N sources. Soil Biol. Biochem. 29, 361–367. https://doi.org/10.1016/S0038-0717(96)00098-3 (1997).CAS 
    Article 

    Google Scholar 
    Abail, Z. & Whalen, J. K. Earthworm contributions to soil nitrogen supply in corn-soybean agroecosystems in Quebec. Canada. Pedosphere 31, 405–412. https://doi.org/10.1016/S1002-0160(20)60086-8 (2021).Article 

    Google Scholar 
    Frelich, L. E. et al. Earthworm invasion into previously earthworm-free temperate and boreal forests. Biol. Invasions 8, 1235–1245. https://doi.org/10.1007/s10530-006-9019-3 (2006).Article 

    Google Scholar 
    Ding, W. et al. Effect thresholds for the earthworm Eisenia fetida: Toxicity comparison between conventional and biodegradable microplastics. Sci. Total Environ. 781, 146884 (2021).ADS 
    CAS 
    Article 

    Google Scholar 
    Treder, K., Jastrzębska, M., Kostrzewska, M. K. & Makowski, P. Do long-term continuous cropping and pesticides affect earthworm communities?. Agronomy 10, 586 (2020).CAS 
    Article 

    Google Scholar 
    Fonte, S. J., Kong, A. Y. Y., van Kessel, C., Hendrix, P. F. & Six, J. Influence of earthworm activity on aggregate-associated carbon and nitrogen dynamics differs with agroecosystem management. Soil Biol. Biochem. 39, 1014–1022. https://doi.org/10.1016/j.soilbio.2006.11.011 (2007).CAS 
    Article 

    Google Scholar 
    Scheu, S., Schlitt, N., Tiunov, A. V., Newington, J. E. & Jones, H. T. Effects of the presence and community composition of earthworms on microbial community functioning. Oecologia 133, 254–260. https://doi.org/10.1007/s00442-002-1023-4 (2002).ADS 
    Article 
    PubMed 

    Google Scholar 
    Sheikh, T. et al. Unveiling the efficiency of psychrophillic aporrectodea caliginosa in deciphering the nutrients from dalweed and cow manure with bio-optimization of coprolites. Sustainability 13, 5338 (2021).CAS 
    Article 

    Google Scholar 
    Lavelle, P. & Spain, A. V. Soil Ecology (Springer, Dordrecht, 2001).Book 

    Google Scholar 
    Aubert, L., Konradova, D., Barris, S. & Quinet, M. Different drought resistance mechanisms between two buckwheat species Fagopyrum esculentum and Fagopyrum tataricum. Physiol. Plant. https://doi.org/10.1111/ppl.13248 (2020).Article 
    PubMed 

    Google Scholar 
    Sistla, S. A., Asao, S. & Schimel, J. P. Detecting microbial N-limitation in tussock tundra soil: Implications for Arctic soil organic carbon cycling. Soil Biol. Biochem. 55, 78–84. https://doi.org/10.1016/j.soilbio.2012.06.010 (2012).CAS 
    Article 

    Google Scholar 
    Chkrebtii, O. A., Cameron, E. K., Campbell, D. A. & Bayne, E. M. Transdimensional approximate Bayesian computation for inference on invasive species models with latent variables of unknown dimension. Comput. Stat. Data Anal. 86, 97–110. https://doi.org/10.1016/j.csda.2015.01.002 (2015).MathSciNet 
    Article 
    MATH 

    Google Scholar 
    Szlavecz, K. et al. Invasive earthworm species and nitrogen cycling in remnant forest patches. Appl. Soil. Ecol. 32, 54–62. https://doi.org/10.1016/j.apsoil.2005.01.006 (2006).Article 

    Google Scholar 
    Liu, M., Cao, J. & Wang, C. Bioremediation by earthworms on soil microbial diversity and partial nitrification processes in oxytetracycline-contaminated soil. Ecotoxicol. Environ. Saf. 189, 109996 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Lubbers, I. M. et al. Greenhouse-gas emissions from soils increased by earthworms. Nat. Clim. Change 3, 187–194. https://doi.org/10.1038/nclimate1692 (2013).ADS 
    CAS 
    Article 

    Google Scholar 
    Wang, Z., Chen, Z., Niu, Y., Ren, P. & Hao, M. Feasibility of vermicomposting for spent drilling fluid from a nature-gas industry employing earthworms Eisenia fetida. Ecotoxicol. Environ. Saf. 214, 111994 (2021).CAS 
    PubMed 
    Article 

    Google Scholar 
    Elyamine, A. M. & Hu, C. Earthworms and rice straw enhanced soil bacterial diversity and promoted the degradation of phenanthrene. Environ. Sci. Eur. 32, 124. https://doi.org/10.1186/s12302-020-00400-y (2020).CAS 
    Article 

    Google Scholar 
    Sun, M. et al. Ecological role of earthworm intestinal bacteria in terrestrial environments: A review. Sci. Total Environ. https://doi.org/10.1016/j.scitotenv.2020.140008 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Turp, G. A., Turp, S. M., Ozdemir, S. & Yetilmezsoy, K. Vermicomposting of biomass ash with bio-waste for solubilizing nutrients and its effect on nitrogen fixation in common beans. Environ. Technol. Innov. https://doi.org/10.1016/j.eti.2021.101691 (2021).Article 

    Google Scholar 
    Lv, B., Zhang, D., Chen, Q. & Cui, Y. Effects of earthworms on nitrogen transformation and the correspond genes (amoA and nirS) in vermicomposting of sewage sludge and rice straw. Bioresour. Technol. 287, 121428. https://doi.org/10.1016/j.biortech.2019.121428 (2019).CAS 
    Article 
    PubMed 

    Google Scholar 
    Sharma, K. & Garg, V. K. Comparative analysis of vermicompost quality produced from rice straw and paper waste employing earthworm Eisenia fetida (Sav.). Bioresour. Technol. 250, 708–715. https://doi.org/10.1016/j.biortech.2017.11.101 (2018).CAS 
    Article 
    PubMed 

    Google Scholar 
    Castillo Diaz, J. M., Martin-Laurent, F., Beguet, J., Nogales, R. & Romero, E. Fate and effect of imidacloprid on vermicompost-amended soils under dissimilar conditions: Risk for soil functions, structure, and bacterial abundance. Sci. Total Environ. 579, 1111–1119. https://doi.org/10.1016/j.scitotenv.2016.11.082 (2017).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Samal, K., Raj Mohan, A., Chaudhary, N. & Moulick, S. Application of vermitechnology in waste management: A review on mechanism and performance. J. Environ. Chem. Eng. 7, 103392. https://doi.org/10.1016/j.jece.2019.103392 (2019).CAS 
    Article 

    Google Scholar 
    Katakula, A. A. N., Handura, B., Gawanab, W., Itanna, F. & Mupambwa, H. A. Optimized vermicomposting of a goat manure-vegetable food waste mixture for enhanced nutrient release. Sci. Afr. 12, e00727 (2021).
    Google Scholar 
    Cáceres, R., Malińska, K. & Marfà, O. Nitrification within composting: A review. Waste Manag. 72, 119–137. https://doi.org/10.1016/j.wasman.2017.10.049 (2018).CAS 
    Article 
    PubMed 

    Google Scholar 
    Lv, B., Cui, Y., Wei, H., Chen, Q. & Zhang, D. Elucidating the role of earthworms in N2O emission and production pathway during vermicomposting of sewage sludge and rice straw. J. Hazard. Mater. 400, 123215 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Zhang, L. et al. The non-negligibility of greenhouse gas emission from a combined pre-composting and vermicomposting system with maize stover and cow dung. Environ. Sci. Pollut. Res. 28, 19412–19423 (2021).CAS 
    Article 

    Google Scholar 
    Chen, C., Whalen, J. K. & Guo, X. Earthworms reduce soil nitrous oxide emissions during drying and rewetting cycles. Soil Biol. Biochem. 68, 117–124. https://doi.org/10.1016/j.soilbio.2013.09.020 (2014).CAS 
    Article 

    Google Scholar 
    Wang, X. et al. Treating low carbon/nitrogen (C/N) wastewater in simultaneous nitrification-endogenous denitrification and phosphorous removal (SNDPR) systems by strengthening anaerobic intracellular carbon storage. Water Res. 77, 191–200. https://doi.org/10.1016/j.watres.2015.03.019 (2015).CAS 
    Article 
    PubMed 

    Google Scholar 
    Yang, Z., Sun, H. & Wu, W. Intensified simultaneous nitrification and denitrification performance in integrated packed bed bioreactors using PHBV with different dosing methods. Environ. Sci. Pollut. Res. 27, 21560–21569. https://doi.org/10.1007/s11356-020-08290-6 (2020).CAS 
    Article 

    Google Scholar 
    Pan, Z. et al. Effects of COD/TN ratio on nitrogen removal efficiency, microbial community for high saline wastewater treatment based on heterotrophic nitrification-aerobic denitrification process. Bioresour. Technol. 301, 122726. https://doi.org/10.1016/j.biortech.2019.122726 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    Xia, L., Li, X., Fan, W. & Wang, J. Heterotrophic nitrification and aerobic denitrification by a novel Acinetobacter sp .ND7 isolated from municipal activated sludge. Bioresour. Technol. 301, 122749. https://doi.org/10.1016/j.biortech.2020.122749 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    Dad, J. M. & Khan, A. B. Threatened medicinal plants of Gurez Valley, Kashmir Himalayas. Int. J. Biodivers. Sci. Ecosyst. Serv. Manag. 7, 20–26. https://doi.org/10.1080/21513732.2011.602646 (2011).Article 

    Google Scholar 
    Cameira, M. D. & Mota, M. Nitrogen related diffuse pollution from horticulture production—mitigation practices and assessment strategies. Horticulturae https://doi.org/10.3390/horticulturae3010025 (2017).Article 

    Google Scholar 
    Yuvaraj, A., Thangaraj, R., Ravindran, B., Chang, S. W. & Karmegam, N. Centrality of cattle solid wastes in vermicomposting technology—A cleaner resource recovery and biowaste recycling option for agricultural and environmental sustainability. Environ. Pollut. 268, 115688. https://doi.org/10.1016/j.envpol.2020.115688 (2021).CAS 
    Article 
    PubMed 

    Google Scholar 
    Kuzyakov, Y., Friedel, J. K. & Stahr, K. Review of mechanisms and quantification of priming effects. Soil Biol. Biochem. 32, 1485–1498. https://doi.org/10.1016/S0038-0717(00)00084-5 (2000).CAS 
    Article 

    Google Scholar 
    Bertrand, M. et al. Earthworm services for cropping systems. A review. Agron. Sustain. Dev. 35, 553–567 (2015).CAS 
    Article 

    Google Scholar 
    Makoto, K., Bryanin, S. V. & Takagi, K. The effect of snow reduction and Eisenia japonica earthworm traits on soil nitrogen dynamics in spring in a cool-temperate forest. Appl. Soil. Ecol. 144, 1–7. https://doi.org/10.1016/j.apsoil.2019.06.019 (2019).Article 

    Google Scholar 
    Huang, K. et al. Optimal growth condition of earthworms and their vermicompost features during recycling of five different fresh fruit and vegetable wastes. Environ. Sci. Pollut. Res. Int. 23, 13569–13575. https://doi.org/10.1007/s11356-016-6848-1 (2016).CAS 
    Article 
    PubMed 

    Google Scholar 
    Makoto, K., Minamiya, Y. & Kaneko, N. Differences in soil type drive the intraspecific variation in the responses of an earthworm species and consequently, tree growth to warming. Plant Soil 404, 209–218. https://doi.org/10.1007/s11104-016-2827-z (2016).CAS 
    Article 

    Google Scholar 
    Grenon, F., Bradley, R. L. & Titus, B. D. Temperature sensitivity of mineral N transformation rates, and heterotrophic nitrification: possible factors controlling the post-disturbance mineral N flush in forest floors. Soil Biol. Biochem. 36, 1465–1474. https://doi.org/10.1016/j.soilbio.2004.04.021 (2004).CAS 
    Article 

    Google Scholar 
    Zhang, H., Li, J., Zhang, Y. & Huang, K. Quality of vermicompost and microbial community diversity affected by the contrasting temperature during vermicomposting of dewatered sludge. Int. J. Env. Res. Public Health 17, 1748 (2020).CAS 
    Article 

    Google Scholar 
    Velasco-Velasco, J., Parkinson, R. & Kuri, V. Ammonia emissions during vermicomposting of sheep manure. Bioresour. Technol. 102, 10959–10964 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    Dan, X. et al. Effects of changing temperature on gross N transformation rates in acidic subtropical forest soils. Forests 10, 894 (2019).Article 

    Google Scholar 
    Gusain, R. & Suthar, S. Vermicomposting of invasive weed Ageratum conyzoids: Assessment of nutrient mineralization, enzymatic activities, and microbial properties. Bioresour. Technol. 312, 123537 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Klaasen, H. L., Koopman, J. P., Poelma, F. G. & Beynen, A. C. Intestinal, segmented, filamentous bacteria. FEMS Microbiol. Rev. 8, 165–180. https://doi.org/10.1111/j.1574-6968.1992.tb04986.x (1992).CAS 
    Article 
    PubMed 

    Google Scholar 
    Fischer, K., Hahn, D., Daniel, O., Zeyer, J. & Amann, R. I. In situ analysis of the bacterial community in the gut of the earthworm Lumbricus terrestris L. by whole-cell hybridization. Can. J. Microbiol. 41, 666–673. https://doi.org/10.1139/m95-092 (1995).CAS 
    Article 

    Google Scholar 
    Karsten, G. R. & Drake, H. L. Comparative assessment of the aerobic and anaerobic microfloras of earthworm guts and forest soils. Appl. Environ. Microbiol. 61, 1039–1044. https://doi.org/10.1128/AEM.61.3.1039-1044.1995 (1995).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Hobson, A. M., Frederickson, J. & Dise, N. B. CH4 and N2O from mechanically turned windrow and vermicomposting systems following in-vessel pre-treatment. Waste Manag. 25, 345–352. https://doi.org/10.1016/j.wasman.2005.02.015 (2005).CAS 
    Article 
    PubMed 

    Google Scholar 
    Singh, A. et al. Earthworms and vermicompost: An eco-friendly approach for repaying nature’s debt. Environ. Geochem. Health 42, 1617–1642 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Zedelius, J. et al. Alkane degradation under anoxic conditions by a nitrate-reducing bacterium with possible involvement of the electron acceptor in substrate activation. Environ Microbiol. Rep. 3, 125–135. https://doi.org/10.1111/j.1758-2229.2010.00198.x (2011).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Liu, R., Suter, H. C., He, J.-Z., Hayden, H. & Chen, D. Influence of temperature and moisture on the relative contributions of heterotrophic and autotrophic nitrification to gross nitrification in an acid cropping soil. J. Soils Sed. https://doi.org/10.1007/s11368-015-1170-y (2015).Article 

    Google Scholar 
    Zhang, Y. et al. Composition of soil recalcitrant C regulates nitrification rates in acidic soils. Geoderma 337, 965–972. https://doi.org/10.1016/j.geoderma.2018.11.014 (2019).ADS 
    CAS 
    Article 

    Google Scholar 
    Zhang, J., Sun, W., Zhong, W. & Cai, Z. The substrate is an important factor in controlling the significance of heterotrophic nitrification in acidic forest soils. Soil Biol. Biochem. 76, 143–148. https://doi.org/10.1016/j.soilbio.2014.05.001 (2014).CAS 
    Article 

    Google Scholar 
    Abail, Z., Sampedro, L. & Whalen, J. K. Short-term carbon mineralization from endogeic earthworm casts as influenced by properties of the ingested soil material. Appl. Soil. Ecol. 116, 79–86 (2017).Article 

    Google Scholar 
    Coq, S., Barthès, B. G., Oliver, R., Rabary, B. & Blanchart, E. Earthworm activity affects soil aggregation and organic matter dynamics according to the quality and localization of crop residues—an experimental study (Madagascar). Soil Biol. Biochem. 39, 2119–2128 (2007).CAS 
    Article 

    Google Scholar 
    Medina-Sauza, R. M. et al. Earthworms building up soil microbiota, a review. Front. Environ. Sci. https://doi.org/10.3389/fenvs.2019.00081 (2019).Article 

    Google Scholar 
    Aira, M., Monroy, F. & Domínguez, J. Ageing effects on nitrogen dynamics and enzyme activities in casts of Aporrectodea caliginosa (Lumbricidae). Pedobiologia 49, 467–473 (2005).CAS 
    Article 

    Google Scholar 
    Clause, J., Barot, S., Richard, B., Decaëns, T. & Forey, E. The interactions between soil type and earthworm species determine the properties of earthworm casts. Appl. Soil. Ecol. 83, 149–158 (2014).Article 

    Google Scholar 
    McDaniel, J. P., Stromberger, M. E., Barbarick, K. A. & Cranshaw, W. Survival of Aporrectodea caliginosa and its effects on nutrient availability in biosolids amended soil. Appl. Soil. Ecol. 71, 1–6 (2013).Article 

    Google Scholar 
    Ravishankara, A., Daniel, J. S. & Portmann, R. W. Nitrous oxide (N2O): The dominant ozone-depleting substance emitted in the 21st century. Science 326, 123–125 (2009).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Lubbers, I., Brussaard, L., Otten, W. & Van Groenigen, J. Earthworm-induced N mineralization in fertilized grassland increases both N2O emission and crop-N uptake. Eur. J. Soil Sci. 62, 152–161 (2011).CAS 
    Article 

    Google Scholar 
    Peter, S. D. J., George, G. B., Siu, M. T., Marcus, A. H. & Harold, L. D. Emission of nitrous oxide and dinitrogen by diverse earthworm families from Brazil and resolution of associated denitrifying and nitrate-dissimilating taxa. FEMS Microbiol. Ecol. 83, 375–391. https://doi.org/10.1111/j.1574-6941.2012.01476.x (2013).CAS 
    Article 

    Google Scholar 
    Firestone, M. K. & Davidson, E. A. Microbiological basis of NO and N2O production and consumption in soil. Exch. Trace Gases terr. Ecosyst. Atmos. 47, 7–21 (1989).CAS 

    Google Scholar 
    Zhu, X. et al. Exploring the relationships between soil fauna, different tillage regimes and CO2 and N2O emissions from black soil in China. Soil Biol. Biochem. 103, 106–116 (2016).CAS 
    Article 

    Google Scholar 
    Yu, D.-S. et al. Simultaneous nitrogen and phosphorus removal characteristics of an anaerobic/aerobic operated spndpr system treating low C/N urban sewage. Huan Jing ke Xue Huanjing Kexue 39, 5065–5073 (2018).PubMed 

    Google Scholar 
    Wang, F., Zhao, Y., Xie, S. & Li, J. Implication of nitrifying and denitrifying bacteria for nitrogen removal in a shallow lake. Clean: Soil, Air, Water 45, 1500319 (2017).
    Google Scholar 
    Wang, J. et al. Emissions of ammonia and greenhouse gases during combined pre-composting and vermicomposting of duck manure. Waste Manag. 34, 1546–1552. https://doi.org/10.1016/j.wasman.2014.04.010 (2014).CAS 
    Article 
    PubMed 

    Google Scholar 
    Nigussie, A., Kuyper, T. W., Bruun, S. & de Neergaard, A. Vermicomposting as a technology for reducing nitrogen losses and greenhouse gas emissions from small-scale composting. J. Clean. Prod. 139, 429–439. https://doi.org/10.1016/j.jclepro.2016.08.058 (2016).CAS 
    Article 

    Google Scholar 
    Yang, F., Li, G., Zang, B. & Zhang, Z. The maturity and CH4, N2O, NH3 emissions from vermicomposting with agricultural waste. Compost Sci. Util. 25, 262–271. https://doi.org/10.1080/1065657X.2017.1329037 (2017).CAS 
    Article 

    Google Scholar 
    Ma, L. et al. Soil properties alter plant and microbial communities to modulate denitrification rates in subtropical riparian wetlands. Land Degrad. Dev. 31, 1792–1802 (2020).Article 

    Google Scholar 
    Xu, X. et al. Effective nitrogen removal in a granule-based partial-denitrification/anammox reactor treating low C/N sewage. Bioresour. Technol. 297, 122467 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Ma, X., Xing, M., Wang, Y., Xu, Z. & Yang, J. Microbial enzyme and biomass responses: Deciphering the effects of earthworms and seasonal variation on treating excess sludge. J. Environ. Manag. 170, 207–214. https://doi.org/10.1016/j.jenvman.2016.01.022 (2016).CAS 
    Article 

    Google Scholar 
    Kremen, A., Bear, J., Shavit, U. & Shaviv, A. Model demonstrating the potential for coupled nitrification denitrification in soil aggregates. Environ. Sci. Technol. 39, 4180–4188. https://doi.org/10.1021/es048304z (2005).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Zhang, Y., Song, C., Zhou, Z., Cao, X. & Zhou, Y. Coupling between nitrification and denitrification as well as its effect on phosphorus release in sediments of Chinese Shallow Lakes. Water 11, 1809 (2019).ADS 
    CAS 
    Article 

    Google Scholar 
    Das, D. & Deka, H. Vermicomposting of harvested waste biomass of potato crop employing Eisenia fetida: Changes in nutrient profile and assessment of the maturity of the end products. Environ. Sci. Pollut. Res. 28, 35717–35727 (2021).CAS 
    Article 

    Google Scholar 
    Fernández-Gómez, M. J., Romero, E. & Nogales, R. Feasibility of vermicomposting for vegetable greenhouse waste recycling. Bioresour. Technol. 101, 9654–9660. https://doi.org/10.1016/j.biortech.2010.07.109 (2010).CAS 
    Article 
    PubMed 

    Google Scholar 
    Biruntha, M. et al. Vermiconversion of biowastes with low-to-high C/N ratio into value added vermicompost. Bioresour. Technol. 297, 122398 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Devi, C. & Khwairakpam, M. Feasibility of vermicomposting for the management of terrestrial weed Ageratum conyzoides using earthworm species Eisenia fetida. Environ. Technol. Innov. 18, 100696. https://doi.org/10.1016/j.eti.2020.100696 (2020).Article 

    Google Scholar 
    Garg, P., Gupta, A. & Satya, S. Vermicomposting of different types of waste using Eisenia foetida: A comparative study. Bioresour. Technol. 97, 391–395. https://doi.org/10.1016/j.biortech.2005.03.009 (2006).CAS 
    Article 
    PubMed 

    Google Scholar 
    Huang, K., Li, F., Wei, Y., Fu, X. & Chen, X. Effects of earthworms on physicochemical properties and microbial profiles during vermicomposting of fresh fruit and vegetable wastes. Bioresour. Technol. 170, 45–52. https://doi.org/10.1016/j.biortech.2014.07.058 (2014).CAS 
    Article 
    PubMed 

    Google Scholar 
    Gusain, R. & Suthar, S. Vermicomposting of duckweed (Spirodela polyrhiza) by employing Eisenia fetida: Changes in nutrient contents, microbial enzyme activities and earthworm biodynamics. Bioresour. Technol. 311, 123585 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Karmegam, N. et al. Precomposting and green manure amendment for effective vermitransformation of hazardous coir industrial waste into enriched vermicompost. Bioresour. Technol. 319, 124136. https://doi.org/10.1016/j.biortech.2020.124136 (2021).CAS 
    Article 
    PubMed 

    Google Scholar 
    Bhattacharya, S. S. & Chattopadhyay, G. N. Transformation of nitrogen during vermicomposting of fly ash. Waste Manag. Res. 22, 488–491. https://doi.org/10.1177/0734242X04048625 (2004).CAS 
    Article 
    PubMed 

    Google Scholar 
    Hussain, N., Abbasi, T. & Abbasi, S. Transformation of the pernicious and toxic weed parthenium into an organic fertilizer by vermicomposting. Int. J. Environ. Stud. 73, 731–745 (2016).CAS 
    Article 

    Google Scholar 
    Rai, R. & Suthar, S. Composting of toxic weed Parthenium hysterophorus: Nutrient changes, the fate of faecal coliforms, and biopesticide property assessment. Bioresour. Technol. 311, 123523 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Whalen, J. K., Parmelee, R. W. & Subler, S. Quantification of nitrogen excretion rates for three lumbricid earthworms using 15N. Biol. Fertil. Soils 32, 347–352. https://doi.org/10.1007/s003740000259 (2000).CAS 
    Article 

    Google Scholar 
    Esmaeili, A., Khoram, M. R., Gholami, M. & Eslami, H. Pistachio waste management using combined composting-vermicomposting technique: Physico-chemical changes and worm growth analysis. J. Clean. Prod. 242, 118523 (2020).CAS 
    Article 

    Google Scholar 
    Karmegam, N., Vijayan, P., Prakash, M. & Paul, J. A. J. Vermicomposting of paper industry sludge with cowdung and green manure plants using Eisenia fetida: A viable option for cleaner and enriched vermicompost production. J. Clean. Prod. 228, 718–728 (2019).CAS 
    Article 

    Google Scholar 
    Paul, J. A., Karmegam, N. & Daniel, T. Municipal solid waste (MSW) vermicomposting with an epigeic earthworm Perionyx ceylanensis Mich. Bioresour. Technol. 102, 6769–6773. https://doi.org/10.1016/j.biortech.2011.03.089 (2011).CAS 
    Article 
    PubMed 

    Google Scholar 
    Huang, K., Xia, H., Cui, G. & Li, F. Effects of earthworms on nitrification and ammonia oxidizers in vermicomposting systems for recycling of fruit and vegetable wastes. Sci. Total Environ. 578, 337–345. https://doi.org/10.1016/j.scitotenv.2016.10.172 (2017).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Mokgophi, M. M., Manyevere, A., Ayisi, K. K. & Munjonji, L. Characterisation of chamaecytisus tagasaste, moringa oleifera and vachellia karroo vermicomposts and their potential to improve soil fertility. Sustainability 12, 9305 (2020).CAS 
    Article 

    Google Scholar 
    Pathma, J. & Sakthivel, N. Microbial diversity of vermicompost bacteria that exhibit useful agricultural traits and waste management potential. Springerplus 1, 26–26. https://doi.org/10.1186/2193-1801-1-26 (2012).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Villar, I., Alves, D., Pérez-Díaz, D. & Mato, S. Changes in microbial dynamics during vermicomposting of fresh and composted sewage sludge. Waste Manag. 48, 409–417 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    Wang, Y. et al. Speciation of heavy metals and bacteria in cow dung after vermicomposting by the earthworm, Eisenia fetida. Bioresour. Technol. 245, 411–418 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    Svensson, B. H., Boström, U. & Klemedtson, L. Potential for higher rates of denitrification in earthworm casts than in the surrounding soil. Biol. Fertil. Soils 2, 147–149. https://doi.org/10.1007/BF00257593 (1986).Article 

    Google Scholar 
    Syers, J. K. & Springett, J. A. Earthworms and Soil Fertility. In Biological Processes and Soil Fertility (eds Tinsley, J. & Darbyshire, J. F.) 93–104 (Springer Netherlands, Dordrecht, 1984).Chapter 

    Google Scholar 
    Mohanty, S. R. et al. nitrification rates are affected by biogenic nitrate and volatile organic compounds in agricultural soils. Front. Microbiol. https://doi.org/10.3389/fmicb.2019.00772 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Cui, G. et al. Changes of quinolone resistance genes and their relations with microbial profiles during vermicomposting of municipal excess sludge. Sci. Total Environ. 644, 494–502 (2018).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Paliwal, R. & Julka, J. Checklist of earthworms of western Himalaya, India. Zoos’ Print J. 20, 1972–1976 (2005).Article 

    Google Scholar 
    Gal, C., Frenzel, W. & Möller, J. Re-examination of the cadmium reduction method and optimisation of conditions for the determination of nitrate by flow injection analysis. Microchim. Acta 146, 155–164. https://doi.org/10.1007/s00604-004-0193-7 (2004).CAS 
    Article 

    Google Scholar 
    Schmidt, L. W. in Methods of Soil Analysis: Part 2 Chemical and Microbiological Properties (ed A.L. Page) 1027–1042 (1982).Yoshinari, T., Hynes, R. & Knowles, R. Acetylene inhibition of nitrous oxide reduction and measurement of denitrification and nitrogen fixation in soil. Soil Biol. Biochem. 9, 177–183. https://doi.org/10.1016/0038-0717(77)90072-4 (1977).CAS 
    Article 

    Google Scholar 
    Parkin, T. B. Automated analysis of nitrous oxide. Soil Sci. Soc. Am. J. 49, 273 (1985).ADS 
    CAS 
    Article 

    Google Scholar 
    Hussain, M. et al. Bacteria in combination with fertilizers improve growth, productivity and net returns of wheat (Triticum aestivum L.). Pak. J. Agric. Sci. https://doi.org/10.21162/PAKJAS/16.4901 (2016).Article 

    Google Scholar 
    Gislin, D., Sudarsanam, D., Antony Raj, G. & Baskar, K. Antibacterial activity of soil bacteria isolated from Kochi, India and their molecular identification. J Genet. Eng. Biotechnol. 16, 287–294. https://doi.org/10.1016/j.jgeb.2018.05.010 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Rashid, K. M. H., Mohiuddin, M. & Rahman, M. Enumeration, isolation and identification of nitrogen-fixing bacterial strains at seedling stage in rhizosphere of rice grown in non-calcareous grey flood plain soil of Bangladesh. J. Fac. Environ. Sci. Technol. 13, 97 (2008).
    Google Scholar 
    Williams, S. & Association of Official Analytical, C. Official methods of analysis of the Association of official analytical chemists. (Association of official analytical chemists, 1984). More

  • in

    Comparative screening the life-time composition and crystallinity variation in gilthead seabream otoliths Sparus aurata from different marine environments

    Elsdon, T. S. et al. Otolith chemistry to describe movements and life-history parameters of fishes: Hypotheses, assumptions, limitations and inferences. Oceanogr. Mar. Biol. An Ann. Rev. 46, 297–330 (2008).
    Google Scholar 
    Franco, A., Elliott, M., Franzoi, P. & Torricelli, P. Life strategies of fishes in European estuaries: The functional guild approach. Mar. Ecol. Prog. Ser. 354, 219–228 (2008).ADS 
    Article 

    Google Scholar 
    Campana, S. E. Chemistry and composition of fish otoliths: Pathways, mechanisms and applications. Mar. Ecol. Prog. Ser. 188, 263–297 (1999).ADS 
    CAS 
    Article 

    Google Scholar 
    Campana, S. E. & Thorrold, S. R. Otoliths, increments, and elements: Keys to a comprehensive understanding of fish populations?. Can. J. Fish. Aquat. Sci. 58, 30–38 (2001).Article 

    Google Scholar 
    Campana, S. E. Calcium deposition and otolith check formation during periods of stress in Coho Salmon, Oncorhynchus Kisutch. Comp. Biochem. Physiol. 75A, 215–220 (1983).CAS 
    Article 

    Google Scholar 
    Gauldie, R. W. Vaterite otoliths from chinook salmon (Oncorhynchus tshawytscha). N. Z. J. Mar. Fish. Res. 20, 209–217 (1986).CAS 
    Article 

    Google Scholar 
    Casselman, J. M. & Gunn, J. M. Dynamics in year-class strength, growth, and calcified-structure size of native lake trout (Salvelinus namaycush) exposed to moderate acidification and whole-lake neutralization. Can. J. Fish. Aquat. Sci. 49, 102–111 (1992).CAS 
    Article 

    Google Scholar 
    Tomás, J. & Geffen, A. J. Morphometry and composition of aragonite and vaterite otoliths of deformed laboratory reared juvenile herring from two populations. J. Fish Biol. 63, 1383–1401 (2003).Article 

    Google Scholar 
    Brown, R. & Severin, K. P. Elemental distribution within polymorphic inconnu (Stenodus leucichthys) otoliths is affected by crystal structure. Can. J. Fish. Aquat. Sci. 56, 1898–1903 (1999).CAS 
    Article 

    Google Scholar 
    Melancon, S., Fryer, B. J., Gagnon, J. E., Ludsin, S. A. & Yang, Z. Effects of crystal structure on the uptake of metals by lake trout (Salvelinus namaycush) otoliths. Can. J. Fish. Aquat. Sci. 62, 2609–2619 (2005).CAS 
    Article 

    Google Scholar 
    Tzeng, W. N. et al. Misidentification of the migratory history of anguillid eels by Sr/Ca ratios of vaterite otoliths. Mar. Ecol. Prog. Ser. 348, 285–295 (2007).ADS 
    CAS 
    Article 

    Google Scholar 
    Jolivet, A., Bardeau, J.-F., Fablet, R., Paulet, Y. M. & de Pontual, H. Understanding otolith biomineralization processes: new insights into microscale spatial distribution of organic and mineral fractions from Raman micro-spectrometry. Anal. Bioanal. Chem. 392, 551–560 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    Barnes, T. C. & Gillanders, B. M. Combined effects of extrinsic and intrinsic factors on otolith chemistry: implications for environmental reconstructions. Can. J. Fish. Aquat. Sci. 70, 1159–1166 (2013).CAS 
    Article 

    Google Scholar 
    Javor, B. & Dorval, E. Stability of trace elements in otoliths of juvenile Pacific sardine Sardinops sagax. Calif. Coop. Oceanic Fish. Invest. Rep. 57, 109–123 (2016).
    Google Scholar 
    Hobbs, J. A., Yin, Q., Burton, J. & Bennett, W. A. Retrospective determination of natal habitats for an estuarine fish with otolith strontium isotope ratios. Mar. Fresh. Res. 56, 655–660 (2005).CAS 
    Article 

    Google Scholar 
    Nehrke, G., Poigner, H., Wilhelms-Dick, D., Brey, T. & Abele, D. Coexistence of three cal-30 cium carbonate polymorphs in the shell of the Antarctic clam Laternula elliptica. Geochem. Geophys. Geosyst. 13, Q05014 (2012).ADS 
    Article 
    CAS 

    Google Scholar 
    Montagna, P., McCulloch, M., Mazzoli, C., Silenzi, S. & Odorico, R. The non-tropical coral Cladocora caespitosa as the new climate archive for the Mediterranean: High-resolution (∼ weekly) trace element systematics. Quat. Sci. Rev. 26, 441–462 (2007).ADS 
    Article 

    Google Scholar 
    Sadekov, A. et al. Surface and subsurface seawater temperature reconstruction using Mg/Ca microanalysis of planktonic foraminifera Globigerinoides ruber, Globigerinoides sacculifer, and Pulleniatina obliquiloculata. Paleoce. Paleoclim. 24, 3201 (2009).ADS 

    Google Scholar 
    Fowler, A. M., Smith, S. M., Booth, D. J. & Stewart, J. Partial migration of grey mullet (Mugil cephalus) on Australia’s east coast revealed by otolith chemistry. Mar. Environ. Res. 119, 238–244 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    Gillanders, B. M. Using elemental chemistry of fish otoliths to determine connectivity between estuarine and coastal habitats. Estuar. Coast. Shelf. Sci. 64, 47–57 (2005).ADS 
    Article 

    Google Scholar 
    Secor, D. H. & Rooker, J. R. Is otolith strontium a useful scalar of life-cycles in estuarine fishes?. Fish. Res. 46, 359–371 (2000).Article 

    Google Scholar 
    Tabouret, H. et al. Otolith microchemistry in Sicydium punctatum: Indices of environmental condition changes after recruitment. Aquat. Liv. Res. 24, 369–378 (2011).Article 

    Google Scholar 
    Neves, V., Guedes, A., Valentim, B., Campos, J. & Freitas, V. High incidence of otolith abnormality in juvenile European flounder Platichthys flesus from a tidal freshwater area. Mar. Biol. Res. 13(9), 933–941 (2017).Article 

    Google Scholar 
    Coll-Lladó, C., Giebichenstein, J., Webb, P. B., Bridges, C. R. & de la Serrana, D. G. Ocean acidification promotes otolith growth and calcite deposition in gilthead sea bream (Sparus aurata) larvae. Sci. Rep. 8, 8384 (2018).ADS 
    PubMed 
    Article 
    CAS 

    Google Scholar 
    Kern, Z. et al. Fusiform vateritic inclusions observed in European eel (Anguilla anguilla L.) sagittae. Acta Biol. Hungar. 68, 267–278 (2017).CAS 
    Article 

    Google Scholar 
    Behrens, G., Kuhn, L. T., Ubic, R. & Heuer, A. H. Raman spectra of vateritic calcium carbonate. Spectrosc. Lett. 28, 983–995 (1995).ADS 
    CAS 
    Article 

    Google Scholar 
    Lazar, G. et al. Tracking the growing rings in biogenic aragonite from fish otolith using confocal Raman microspectroscopy and imaging. Stud. UBB Chem. 65(1), 125–136 (2020).CAS 
    Article 

    Google Scholar 
    Farrugio, H., Le Corre, G. & Vaudo, G. Population dynamics of sea bass, sea-bream and sole exploited by the French multigears demersal fishery in the Gulf of Lions (Northwestern Mediterranean). In Study for Assessment and Management of Fisheries in the Western Mediterranean EEC-FAR programme report MA (eds Farrugio, H. & Lleonart, J.) 3–621 (EEC-IFREMER, 1994).
    Google Scholar 
    Šegvić-Bubić, T. et al. Population genetic structure of reared and wild gilthead sea bream (Sparus aurata) in the Adriatic Sea inferred with microsatellite loci. Aquaculture 318, 309–315 (2011).Article 
    CAS 

    Google Scholar 
    Šegvić-Bubić, T., Talijančić, I., Grubišić, L., Izquierdo-Gomez, D. & Katavić, I. Morphological and molecular differentiation of wild and farmed gilthead sea bream Sparus aurata: Implications for management. Aquac. Environ. Interact. 6, 43–54 (2014).Article 

    Google Scholar 
    Šegvić-Bubić, T. et al. Site fidelity of farmed gilthead seabream Sparus aurata escapees in a coastal environment of the Adriatic Sea. Aquac. Environ. Interact. 10, 21–34 (2018).Article 

    Google Scholar 
    Somarakis, S., Pavlidis, M., Saapoglou, C., Tsigenopoulos, C. S. & Dempster, T. Evidence for ‘escape through spawning’ in large gilthead seabream Sparus aurata reared in commercial sea-cages. Aquac. Environ. Interact. 3, 135–152 (2013).Article 

    Google Scholar 
    Glamuzina, B. Neretva river fishery: History and perspectives. In Proceedings of Ribe I ribarstvo rijeke Neretve: Stanje i perspektive (eds Glamuzina, B. & Dulčić, J.) 20–30 (Sveučilište u Dubrovniku i Dubrovačko-Neretvanska Županija, 2010).
    Google Scholar 
    Glamuzina, B. et al. Observations on the increase of wild gilthead seabream, Sparus aurata abundance, in the eastern Adriatic Sea: Problems and opportunities. Int. Aquat. Res. 6, 127–134 (2014).Article 

    Google Scholar 
    Žužul, I. et al. Spatial connectivity pattern of expanding gilthead seabream populations and its interactions with aquaculture sites: a combined population genetic and physical modelling approach. Sci. Rep. 9, 1–14 (2019).Article 
    CAS 

    Google Scholar 
    Cowen, R. K., Lwiza, K. M. M., Sponaugle, S., Paris, C. B. & Olson, D. B. Connectivity of marine populations: Open or closed?. Science 287, 857–857 (2000).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Cowen, R. K. & Sponaugle, S. Larval dispersal and marine population connectivity. Ann. Rev. Mar. Sci. 1, 443–466 (2009).PubMed 
    Article 

    Google Scholar 
    Mercier, L., Mouillot, D., Bruguier, O., Vigliola, L. & Darnaude, A. M. Multi-element otolith fingerprints unravel sea-lagoon lifetime migrations of gilthead sea bream Sparus aurata. Mar. Ecol. Prog. Ser. 444, 175–194 (2012).ADS 
    Article 

    Google Scholar 
    Isnard, E. et al. Getting a good start in life? A comparative analysis of the quality of lagoons as juvenile habitats for the gilthead seabream Sparus aurata in the gulf of Lions. Estuaries Coasts 38, 1937–1950 (2015).CAS 
    Article 

    Google Scholar 
    Morais, P. et al. Response of Gilthead Seabream (Sparus aurata L., 1758) Larvae to Nursery Odor Cues as Described by a New Set of Behavioral Indexes. Front. Mar. Sci. 4, 318 (2017).Article 

    Google Scholar 
    Audouin, J. La daurade de l’étang de Thau Chrysophrys Aurata (LINNÉ) (1962)Lasserre, P. Osmoregulatory responses to estuarine conditions: chronic osmotic stress and competition. In Estuarine Processes (ed. Wiley, M.) 395–413 (Academic Press, 1976).Chapter 

    Google Scholar 
    Bauchot, M. L. & Hureau, J. C. In Fishes of the North-Eastern Atlantic and the Mediterranean. II (eds Whitehead, P. J. et al.) 883–907 (UNESCO, 1986).
    Google Scholar 
    Loeppky, A. R. et al. Influence of ontogenetic development, temperature, and pCO2 on otolith calcium carbonate polymorph composition in sturgeons. Sci. Rep. 11, 13878 (2021).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Barnett-Johnson, R., Ramos, F. C., Grimes, C. B. & MacFarlane, R. B. Validation of Sr isotopes in otoliths by laser ablation multicollector inductively coupled plasma mass spectrometry (LA-MC-ICPMS): Opening avenues in fisheries science applications. Can. J. Fish. Aquat. Sci. 62, 2425–2430 (2005).CAS 
    Article 

    Google Scholar 
    Beckman, D. W. & Wilson, C. A. Seasonal timing of opaque zone formation in fish otoliths. In Recent Developments in Fish otolith Research (eds Secor, D. H. et al.) 27–43 (University of South Carolina Press, 1995).
    Google Scholar 
    Hüssy, K. & Mosegaard, H. Atlantic cod (Gadus morhua) growth and otolith accretion characteristics modelled in a bioenergetics context. Can. J. Fish. Aquat. Sci. 61, 1021–1031 (2004).Article 

    Google Scholar 
    Hoff, G. R. & Fuiman, L. A. Morphometry and composition of red drum otoliths: Changes associated with temperature, somatic growth rate, and age. Comp. Biochem. Physiol. 106A, 209–219 (1993).CAS 
    Article 

    Google Scholar 
    Høie, H. & Folkvord, A. Estimating the timing of growth rings in Atlantic cod otoliths using stable oxygen isotopes. J. Fish Biol. 68(3), 826–837 (2006).Article 

    Google Scholar 
    Buljan, M. & Zore-Armanda, M. Oceanographical properities of the Adriatic Sea. Oceanogr. Mar. Biol. Ann. Rev. 14, 11–98 (1976).CAS 

    Google Scholar 
    Russo, T., Costa, C. & Cataudella, S. Correspondence between shape and feeding habit changes throughout ontogeny of gilthead sea bream Sparus aurata L., 1758. J. Fish Biol. 71, 629–656 (2007).Article 

    Google Scholar 
    Ellis, J. E., Wiens, J. A. & Rodell, C. F. A conceptual model of diet selection as an ecosystem process. J. Theor. Biol. 60, 93–108 (1976).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Grbec, B. & Morović, M. Seasonal thermohaline fluctuations in the middle Adriatic Sea. Il Nuovo Cimento C 2, 561–576 (1997).ADS 

    Google Scholar 
    Izzo, C., Reis-Santos, P. & Gillanders, B. M. Otolith chemistry does not just reflect environmental conditions: A meta-analytic evaluation. Fish Fish. 19, 441–454 (2018).Article 

    Google Scholar 
    Gillikin, D. P., Wanamaker, A. D. & Andrus, C. F. T. Chemical sclerochronology. Chem. Geol. 526, 1–6 (2019).ADS 
    CAS 
    Article 

    Google Scholar 
    Rea, D. G. Study of the experimental factors affecting raman band intensities in liquids. J. Opt. Soc. Am. 49, 90–101 (1959).ADS 
    CAS 
    Article 

    Google Scholar 
    Tuschel, D. Practical group theory and Raman spectroscopy, part II: Application of polarization. Spectroscopy 29(9), 14–21 (2014).
    Google Scholar 
    Sherwood, P. M. A. Vibrational Spectroscopy of Solids 4 (Cambridge University Press, 1972).
    Google Scholar 
    Dick, S. et al. Surface-enhanced raman spectroscopy as a probe of the surface chemistry of nanostructured materials. Adv. Mater. 28(27), 5705–5711. https://doi.org/10.1002/adma.201505355 (2016).CAS 
    Article 
    PubMed 

    Google Scholar 
    Neilson, J. D. & Geen, G. H. Effects of feeding regimes and diel temperature cycles on otolith increment formation in juvenile chinook salmon, Oncorhynchus tshawytscha. Fish. Bull. 83, 91–101 (1985).
    Google Scholar 
    Sturrock, A. M. et al. Quantifying physiological influences on otolith microchemistry. Method Ecol. Evol. 6, 806–816 (2018).Article 

    Google Scholar 
    DHMZ. Meteorological and Hydrological Service. Meteo. Hydro. Bull. 6. www.meteo.hr (2019).Jochum, K. P. et al. GeoReM: A new geochemical database for reference materials and isotopic standards. Geostand. Geoanalyt. Res. 29, 333–338 (2005).CAS 
    Article 

    Google Scholar 
    Jochum, K. P. et al. Determination of reference values for NIST SRM 610–617 glasses following ISO guidelines. Geostand. Geoanal. Res. 36, 397–429 (2011).Article 
    CAS 

    Google Scholar 
    Jochum, K. P. et al. Accurate trace element analysis of speleothems and biogenic calcium carbonates by LA-ICP-MS. Chem. Geol. 318–319, 31–44 (2012).ADS 
    Article 
    CAS 

    Google Scholar 
    Jochum, K. P., Stoll, B., Herwig, K. & Willbold, M. Validation of LA-ICP-MS trace element analysis of geological glasses using a new solid-state 193 nm Nd:YAG laser and matrix-matched calibration. J. Anal. Atmos. Spectrom. 22, 112–121 (2007).CAS 
    Article 

    Google Scholar 
    Mischel, S. A., Mertz-Kraus, R., Jochum, K. P. & Scholz, D. TERMITE: An R script for fast reduction of laser ablation inductively coupled plasma mass spectrometry data and its application to trace element measurements. Rapid Commun. Mass Spectrom. 131, 1079–1087 (2017).ADS 
    Article 
    CAS 

    Google Scholar 
    Yoshinaga, J., Nakama, A., Morita, M. & Edmonds, J. S. Fish otolith reference material for quality assurance of chemical analyses. Mar. Chem. 69, 91–97 (2000).CAS 
    Article 

    Google Scholar 
    Vrdoljak, D. et al. Otolith fingerprints reveals potential pollution exposure of newly settled juvenile Sparus aurata. Mar. Pollut. Bull. 160, 111695 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Anderson, M. J. & Willis, T. J. Canonical analysis of principal coordinates: A useful method of constrained ordination for ecology. Ecol. 84, 511–552 (2003).Article 

    Google Scholar  More