More stories

  • in

    Rethinking river water temperature in a changing, human-dominated world

    Ouellet, V. et al. Sci. Total Environ. 736, 139679 (2020).Article 
    CAS 
    PubMed 

    Google Scholar 
    Sutadian, A. D., Muttil, N., Yilmaz, A. G. & Perera, B. J. C. Environ. Monit. Assess. 188, 58 (2016).Article 
    PubMed 

    Google Scholar 
    Murdoch, P. S., Baron, J. S. & Miller, T. L. J. Am. Water Resour. Assoc. 36, 347–366 (2000).Article 
    CAS 

    Google Scholar 
    Hannah, D. M. & Garner, G. Prog Phys Geogr. 39, 68–92 (2015).Article 

    Google Scholar 
    Abbott, B. W. et al. Nat. Geosci. 12, 533–540 (2019).Article 
    CAS 

    Google Scholar 
    Grill, G. et al. Nature 569, 215–221 (2019).Article 
    CAS 
    PubMed 

    Google Scholar 
    Hermanson, L. et al. Bull. Am. Meteorol. Soc. 103, E1117–E1129 (2022).Article 

    Google Scholar 
    Webb, B. W., Hannah, D. M., Moore, R. D., Brown, L. E. & Nobilis, F. Hydrol. Process. 22, 902–918 (2008).Article 

    Google Scholar 
    Hester, E. T. & Doyle, M. W. J. Am. Water Resour. Assoc. 47, 571–587 (2011).Article 

    Google Scholar 
    Schliemann, S. A., Grevstad, N. & Brazeau, R. H. Hydrol. Process 35, e14001 (2021).Article 

    Google Scholar 
    Jackson, F. L., Fryer, R. J., Hannah, D. M., Millar, C. P. & Malcolm, I. A. Sci. Total Environ. 612, 1543–1558 (2018).Article 
    CAS 
    PubMed 

    Google Scholar 
    O’Sullivan, A. M., Devito, K. J. & Curry, R. A. Catena 177, 70–83 (2019).Article 

    Google Scholar 
    Chang, H. & Psaris, M. Sci. Total Environ. 461, 587–600 (2013).Article 
    PubMed 

    Google Scholar 
    Hester, E. T. & Bauman, K. S. J. Am. Water Resour. Assoc. 49, 328–342 (2013).Article 

    Google Scholar 
    Croghan, D., Van Loon, A. F., Sadler, J. P., Bradley, C. & Hannah, D. M. Hydrol. Process. 33, 144–159 (2018).Article 

    Google Scholar 
    Levia, D. F. et al. Nat. Geosci. 13, 656–658 (2020).Article 
    CAS 

    Google Scholar 
    Nelson, K. C. & Palmer, M. A. J. Am. Water Resour. Assoc 43, 440–452 (2007).Article 

    Google Scholar 
    Heggenes, J. et al. River Res. Appl. 37, 743–765 (2021).Article 

    Google Scholar 
    Menberg, K., Blum, P., Kurylyk, B. L. & Bayer, P. Hydrol. Earth Syst. Sci. 18, 4453–4466 (2014).Article 

    Google Scholar 
    Tissen, C., Benz, S. A., Menberg, K., Bayer, P. & Blum, P. Environ. Res. Lett. 14, 104012 (2019).Article 
    CAS 

    Google Scholar 
    Hannah, D. M. et al. Hydrol. Process. 36, e14525 (2022).Article 

    Google Scholar 
    Carothers, C. et al. Ecol. Soc. https://doi.org/10.5751/ES-11972-260116 (2021).Dugdale, S. J., Hannah, D. M. & Malcolm, I. A. Earth Sci. Rev. 175, 97–113 (2017).Article 

    Google Scholar 
    Wanders, N., van Vliet, M. T. H., Wada, Y., Bierkens, M. F. P. & van Beek, L. P. H. Water Resour. Res. 55, 2760–2778 (2019).Article 

    Google Scholar 
    Tavares, M. H. et al. Remote Sens. Environ. 241, 11172 (2020).Article 

    Google Scholar 
    Dugdale, S. J., Klaus, J. & Hannah, D. M. Water Resour. Res. 58, e2021WR031168 (2022).Article 

    Google Scholar 
    Mao, F. et al. Environ. Sci. Technol. 54, 9145–9158 (2020).Article 
    CAS 
    PubMed 

    Google Scholar 
    Hannah, D. M. et al. Hydrol. Process. 25, 1191–1200 (2011).Article 

    Google Scholar 
    Do, H. X., Gudmundsson, L., Leonard, M. & Westra, S. Earth Syst. Sci. Data 10, 765–785 (2018).Article 

    Google Scholar  More

  • in

    Non-synonymous variation and protein structure of candidate genes associated with selection in farm and wild populations of turbot (Scophthalmus maximus)

    Ilker, E. & Hinczewski, M. Modeling the growth of organisms validates a general relation between metabolic costs and natural selection. Phys. Rev. Lett. 122, 238101 (2019).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Boltaña, S. et al. Influences of thermal environment on fish growth. Ecol. Evol. 7, 6814–6825 (2017).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Rosenfeld, J., Richards, J., Allen, D., Van Leeuwen, T. & Monnet, G. Adaptive trade-offs in fish energetics and physiology: Insights from adaptive differentiation among juvenile salmonids. Can. J. Fish. Aquat. Sci. 77, 1243–1255 (2020).Article 

    Google Scholar 
    Robertson, D. R. & Collin, R. Inter- and intra-specific variation in egg size among reef fishes across the isthmus of Panama. Front. Ecol. Evol. 2, 84 (2015).Article 

    Google Scholar 
    Zueva, K. J., Lumme, J., Veselov, A. E., Kent, M. P. & Primmer, C. R. Genomic signatures of parasite-driven natural selection in north European Atlantic salmon (Salmo salar). Mar. Genom. 39, 26–38 (2018).Article 

    Google Scholar 
    Rajkov, J., El Taher, A., Böhne, A., Salzburger, W. & Egger, B. Gene expression remodelling and immune response during adaptive divergence in an African cichlid fish. Mol. Ecol. 30, 274–296 (2021).Article 
    CAS 
    PubMed 

    Google Scholar 
    Verhille, C. E. et al. Inter-population differences in salinity tolerance and osmoregulation of juvenile wild and hatchery-born Sacramento splittail. Conserv. Physiol. 4, 1–12 (2016).Article 

    Google Scholar 
    Froese, R. & Pauly, D. FishBase (version Feb 2018). In: Species 2000 & ITIS Catalogue of Life, 2019 Annual Checklist (Roskov Y. et al.). (2018). www.catalogueoflife.org/annual-checklist/2019. ISSN 2405–884X.Karås, P. & Klingsheim, V. Effects of temperature and salinity on embryonic development of turbot (Scophthalmus maximus L.) from the North Sea, and comparisons with Baltic populations. Helgolander Meeresuntersuchungen 51, 241–247 (1997).Article 
    ADS 

    Google Scholar 
    Barbut, L. et al. How larval traits of six flatfish species impact connectivity. Limnol. Oceanogr. 64, 1150–1171 (2019).Article 
    ADS 

    Google Scholar 
    Bouza, C., Presa, P., Castro, J., Sánchez, L. & Martínez, P. Allozyme and microsatellite diversity in natural and domestic populations of turbot (Scophthalmus maximus) in comparison with other Pleuronectiformes. Can. J. Fish. Aquat. Sci. 59, 1460–1473 (2002).Article 
    CAS 

    Google Scholar 
    Nielsen, E. E., Nielsen, P. H., Meldrup, D. & Hansen, M. M. Genetic population structure of turbot (Scophthalmus maximus L.) supports the presence of multiple hybrid zones for marine fishes in the transition zone between the Baltic Sea and the North Sea. Mol. Ecol. 13, 585–595 (2004).Article 
    PubMed 

    Google Scholar 
    Vandamme, S. G. et al. Regional environmental pressure influences population differentiation in turbot (Scophthalmus maximus). Mol. Ecol. 23, 618–636 (2014).Article 
    CAS 
    PubMed 

    Google Scholar 
    Vilas, R. et al. A genome scan for candidate genes involved in the adaptation of turbot (Scophthalmus maximus). Mar. Genom. 23, 77–86 (2015).Article 

    Google Scholar 
    Turan, C. et al. Genetics structure analysis of turbot (Scophthalmus maximus, Linnaeus, 1758) in the Black and Mediterranean Seas for application of innovative Management Strategies. Front. Mar. Sci. 6, 740 (2019).Article 

    Google Scholar 
    Ivanova, P. et al. Genetic diversity and morphological characterisation of three turbot (Scophthalmus maximus L., 1758) populations along the Bulgarian Black Sea coast. Nat. Conserv. 43, 123–146 (2021).Article 

    Google Scholar 
    do Prado, F. D. et al. Parallel evolution and adaptation to environmental factors in a marine flatfish: Implications for fisheries and aquaculture management of the turbot (Scophthalmus maximus). Evol. Appl. 11, 1322–1341 (2018).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    do Prado, F. D. et al. Tracing the genetic impact of farmed turbot Scophthalmus maximus on wild populations. Aquac. Environ. Interact. 10, 447–463 (2018).Article 

    Google Scholar 
    Robledo, D. et al. Integrating genomic resources of flatfish (Pleuronectiformes) to boost aquaculture production. Comp. Biochem. Physiol. Part D Genom. Proteom. 21, 41–55 (2017).CAS 

    Google Scholar 
    Sánchez-Molano, E. et al. Detection of growth-related QTL in turbot (Scophthalmus maximus). BMC Genomics 12, 473 (2011).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Rodríguez-Ramilo, S. T. et al. QTL detection for Aeromonas salmonicida resistance related traits in turbot (Scophthalmus maximus). BMC Genom. 12, 541 (2011).Article 

    Google Scholar 
    Robledo, D. et al. Integrative transcriptome, genome and quantitative trait loci resources identify single nucleotide polymorphisms in candidate genes for growth traits in turbot. Int. J. Mol. Sci. 17, 243 (2016).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Sciara, A. A. et al. Validation of growth-related quantitative trait loci markers in turbot (Scophthalmus maximus) families as a step toward marker assisted selection. Aquaculture 495, 602–610 (2018).Article 

    Google Scholar 
    Ma, A., Huang, Z., Wang, X. & Xu, Y. & Guo, X.,. Identification of quantitative trait loci associated with upper temperature tolerance in turbot, Scophthalmus maximus. Sci. Rep. 11, 1–12 (2021).Article 

    Google Scholar 
    Cui, W. et al. Comparative transcriptomic analysis reveals mechanisms of divergence in osmotic regulation of the turbot Scophthalmus maximus. Fish Physiol. Biochem. 46, 1519–1536 (2020).Article 
    CAS 
    PubMed 

    Google Scholar 
    Martínez, P. et al. Identification of the major sex-determining region of turbot (Scophthalmus maximus). Genetics 183, 1443–1452 (2009).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Martínez, P. et al. A genome-wide association study, supported by a new chromosome-level genome assembly, suggests sox2 as a main driver of the undifferentiatiated ZZ/ZW sex determination of turbot (Scophthalmus maximus). Genomics 113, 1705–1718 (2021).Article 
    PubMed 

    Google Scholar 
    Martínez, P. et al. Turbot (Scophthalmus maximus) genomic resources:application for boosting aquaculture production. Genomics in Aquaculture (Elsevier Inc., 2016). https://doi.org/10.1016/B978-0-12-801418-9.00006-8.Saura, M. et al. Disentangling genetic variation for resistance and endurance to scuticociliatosis in turbot using pedigree and genomic information. Front. Genet. 10, 539 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Aramburu, O. et al. Genomic signatures after five generations of intensive selective breeding: Runs of homozygosity and genetic diversity in representative domestic and wild populations of turbot (Scophthalmus maximus). Front. Genet. 11, 1–14 (2020).Article 

    Google Scholar 
    Aramburu, O., Blanco, A., Bouza, C. & Martínez, P. Integration of host-pathogen functional genomics data into the chromosome-level genome assembly of turbot (Scophthalmus maximus). Aquaculture 564, 739067 (2023).Article 
    CAS 

    Google Scholar 
    Saul, M. C., Philip, V. M., Reinholdt, L. G. & Chesler, E. J. High-diversity mouse populations for complex traits. Trends Genet. 35, 501–514 (2019).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Moen, T. et al. Epithelial cadherin determines resistance to infectious pancreatic necrosis virus in Atlantic salmon. Genetics 200, 1313–1326 (2015).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Pavelin, J. et al. The nedd-8 activating enzyme gene underlies genetic resistance to infectious pancreatic necrosis virus in Atlantic salmon. Genomics 113, 3842–3850 (2021).Article 
    CAS 
    PubMed 

    Google Scholar 
    Barson, N. J. et al. Sex-dependent dominance at a single locus maintains variation in age at maturity in salmon. Nature 528, 405–408 (2015).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Chen, J. et al. Functional differences between TSHR alleles associate with variation in spawning season in Atlantic herring. Commun. Biol. 4, 795 (2021).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Imsland, A. K., Brix, O., Nævdal, G. & Samuelsen, E. N. Hemoglobin genotypes in turbot (Scophthalmus maximus Rafinesque), their oxygen affinity properties and relation with growth. Comp. Biochem. Physiol. A Physiol. 116, 157–165 (1997).Article 

    Google Scholar 
    Imsland, A. K., Foss, A., Stefansson, S. O. & Nævdal, G. Hemoglobin genotypes of turbot (Scophthalmus maximus): Consequences for growth and variations in optimal temperature for growth. Fish Physiol. Biochem. 23, 75–81 (2000).Article 
    CAS 

    Google Scholar 
    Andersen, Ø., Rubiolo, J. A., De Rosa, M. C. & Martinez, P. The hemoglobin Gly16β1Asp polymorphism in turbot (Scophthalmus maximus) is differentially distributed across European populations. Fish Physiol. Biochem. 46, 2367–2376 (2020).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Torrisi, M., Pollastri, G. & Le, Q. Deep learning methods in protein structure prediction. Comput. Struct. Biotechnol. J. 18, 1301–1310 (2020).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Jumper, J. et al. Highly accurate protein structure prediction with AlphaFold. Nature 596, 583–589 (2021).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    AlQuraishi, M. Machine learning in protein structure prediction. Curr. Opin. Chem. Biol. 65, 1–8 (2021).Article 
    CAS 
    PubMed 

    Google Scholar 
    Powder, K. E., Cousin, H., McLinden, G. P. & Craig Albertson, R. A nonsynonymous mutation in the transcriptional regulator lbh is associated with cichlid craniofacial adaptation and neural crest cell development. Mol. Biol. Evol. 31, 3113–3124 (2014).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Lamichhaney, S. et al. Evolution of Darwin’s finches and their beaks revealed by genome sequencing. Nature 518, 371–375 (2015).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Gupta, A. M., Chakrabarti, J. & Mandal, S. Non-synonymous mutations of SARS-CoV-2 leads epitope loss and segregates its variants. Microbes Infect. 22, 598–607 (2020).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Verde, C. et al. Structure, function and molecular adaptations of haemoglobins of the polar cartilaginous fish Bathyraja eatonii and Raja hyperborea. Biochem. J. 389, 297–306 (2005).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Pearce, R. & Zhang, Y. Toward the solution of the protein structure prediction problem. J. Biol. Chem. 297, 100870 (2021).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Zhang, Y. I-TASSER server for protein 3D structure prediction. BMC Bioinf. 9, 40 (2008).Article 

    Google Scholar 
    Pirolli, D. et al. Insights from molecular dynamics simulations: Structural basis for the V567D mutation-induced instability of zebrafish alpha-dystroglycan and comparison with the murine model. PLoS ONE 9, e103866 (2014).Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Lee, J., Freddolino, P. L. & Zhang, Y. From Protein Structure to Function with Bioinformatics. In From Protein Structure to Function with Bioinformatics: Second Edition (ed. Rigden, D. J.) (2017). https://doi.org/10.1007/978-94-024-1069-3Baek, M. et al. Accurate prediction of protein structures and interactions using a 3-track neural network. Science 373, 871–876 (2021).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Castro, J. et al. Potential sources of error in parentage assessment of turbot (Scophthalmus maximus) using microsatellite loci. Aquaculture 242, 119–135 (2004).Article 
    CAS 

    Google Scholar 
    Chen, S., Zhou, Y., Chen, Y. & Gu, J. Fastp: An ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34, i884–i890 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Li, H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. ArXiv ID 1303.3997v2 00, 1–3 (2013).Li, H. A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics 27, 2987–2993 (2011).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Cingolani, P. et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly (Austin) 6, 80–92 (2012).Article 
    CAS 
    PubMed 

    Google Scholar 
    Vera, M. et al. Development and validation of single nucleotide polymorphisms (SNPs) markers from two transcriptome 454-runs of turbot (Scophthalmus maximus) using high-throughput genotyping. Int. J. Mol. Sci. 14, 5694–5711 (2013).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ellis, J. A. & Ong, B. The MassARRAY® system for targeted SNP genotyping. Methods in molecular biology vol. 1492 (2017).Choi, Y. & Chan, A. P. PROVEAN web server: A tool to predict the functional effect of amino acid substitutions and indels. Bioinformatics 31, 2745–2747 (2015).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Costello, M. J. Ecology of sea lice parasitic on farmed and wild fish. Trends Parasitol. 22, 475–483 (2006).Article 
    PubMed 

    Google Scholar 
    Blanchet, S., Rey, O. & Loot, G. Evidence for host variation in parasite tolerance in a wild fish population. Evol. Ecol. 24, 1129–1139 (2010).Article 

    Google Scholar 
    Rousset, F. GENEPOP’007: A complete re-implementation of the GENEPOP software for Windows and Linux. Mol. Ecol. Resour. 8, 103–106 (2008).Article 
    PubMed 

    Google Scholar 
    Foll, M. & Gaggiotti, O. A Genome-scan method to identify selected loci appropriate for both dominant and codominant markers: A bayesian perspective. Genetics 993, 977–993 (2008).Article 

    Google Scholar 
    Excoffier, L. & Lischer, H. E. L. Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 10, 564–567 (2010).Article 
    PubMed 

    Google Scholar 
    Narum, S. R. & Hess, J. E. Comparison of FST outlier tests for SNP loci under selection. Mol. Ecol. Resour. 11, 184–194 (2011).Article 
    PubMed 

    Google Scholar 
    Altschul, S. F. et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl. Acids Res. 25, 3389–3402 (1997).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Romero, P. et al. Sequence complexity of disordered protein. Prot. Struct. Funct. Genet. 42, 38–48 (2001).Article 
    CAS 

    Google Scholar 
    Jones, D. T. & Cozzetto, D. DISOPRED3: Precise disordered region predictions with annotated protein-binding activity. Bioinformatics 31, 857–863 (2015).Article 
    CAS 
    PubMed 

    Google Scholar 
    Mészáros, B., Erdös, G. & Dosztányi, Z. IUPred2A: Context-dependent prediction of protein disorder as a function of redox state and protein binding. Nucl. Acids Res. 46, W329–W337 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ishida, T. & Kinoshita, K. PrDOS: Prediction of disordered protein regions from amino acid sequence. Nucl. Acids Res. 35, W460-464 (2007).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ito, N., Komiyama, N. H. & Fermi, G. Structure of deoxyhaemoglobin of the Anctartic fish Pagothenia bernacchi and structural basis of the root effect. J. Mol. Biol. https://doi.org/10.2210/pdb1hbh/pdb (1995).Article 
    PubMed 

    Google Scholar 
    Šali, A. & Blundell, T. L. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234, 779–815 (1993).Article 
    PubMed 

    Google Scholar 
    Gou, X. et al. Whole-genome sequencing of six dog breeds from continuous altitudes reveals adaptation to high-altitude hypoxia. Genome Res. 24, 1308–1315 (2014).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Grossman, S. R. et al. Identifying recent adaptations in large-scale genomic data. Cell 152, 703–713 (2013).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Macpherson, J. M., Sella, G., Davis, J. C. & Petrov, D. A. Genomewide spatial correspondence between nonsynonymous divergence and neutral polymorphism reveals extensive adaptation in Drosophila. Genetics 177, 2083–2099 (2007).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Howe, D. G. et al. ZFIN, the Zebrafish model organism database: Increased support for mutants and transgenics. Nucl. Acids Res. 41, 854–860 (2013).Article 

    Google Scholar 
    Huber, C. D., Kim, B. Y., Marsden, C. D. & Lohmueller, K. E. Determining the factors driving selective effects of new nonsynonymous mutations. Proc. Natl. Acad. Sci. USA 114, 4465–4470 (2017).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Stenson, P. D. et al. The Human Gene Mutation Database (HGMD®): Optimizing its use in a clinical diagnostic or research setting. Hum. Genet. 139, 1197–1207 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Naruse, K., Hori, H., Shimizu, N., Kohara, Y. & Takeda, H. Medaka genomics: A bridge between mutant phenotype and gene function. Mech. Dev. 121, 619–628 (2004).Article 
    CAS 
    PubMed 

    Google Scholar 
    Chintalapati, M. & Moorjani, P. Evolution of the mutation rate across primates. Curr. Opin. Genet. Dev. 62, 58–64 (2020).Article 
    CAS 
    PubMed 

    Google Scholar 
    Rodin, R. E. et al. The landscape of somatic mutation in cerebral cortex of autistic and neurotypical individuals revealed by ultra-deep whole-genome sequencing. Nat. Neurosci. 24, 176–185 (2021).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Cayuela, H. et al. Thermal adaptation rather than demographic history drives genetic structure inferred by copy number variants in a marine fish. Mol. Ecol. 30, 1624–1641 (2021).Article 
    CAS 
    PubMed 

    Google Scholar 
    Kess, T. et al. A putative structural variant and environmental variation associated with genomic divergence across the Northwest Atlantic in Atlantic Halibut. ICES J. Mar. Sci. 78, 2371–2384 (2021).Article 

    Google Scholar 
    Le Moan, A., Bekkevold, D. & Hemmer-Hansen, J. Evolution at two time frames: ancient structural variants involved in post-glacial divergence of the European plaice (Pleuronectes platessa). Heredity (Edinb). 126, 668–683 (2021).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ruigrok, M. et al. The relative power of structural genomic variation versus SNPs in explaining the quantitative trait growth in the marine teleost Chrysophrys auratus. Genes (Basel). 13, 1129 (2022).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    De la Herran, R. et al. A chromosome-level genome assembly enables the identification of the follicle stimulating hormone receptor as the master sex determining gene in Solea senegalensis. Mol. Ecol. Resour. 00, 1–19 (2023).
    Google Scholar 
    Harrison, P. W. et al. The FAANG data portal: Global, open-access, “FAIR”, and richly validated genotype to phenotype data for high-quality functional annotation of animal genomes. Front. Genet. 12, 639238 (2021).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Figueras, A. et al. Whole genome sequencing of turbot (Scophthalmus maximus; Pleuronectiformes): A fish adapted to demersal life. DNA Res. 23, 181–192 (2016).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Moore, J. S. et al. Conservation genomics of anadromous Atlantic salmon across its North American range: Outlier loci identify the same patterns of population structure as neutral loci. Mol. Ecol. 23, 5680–5697 (2014).Article 
    CAS 
    PubMed 

    Google Scholar 
    Barrio, A. M. et al. The genetic basis for ecological adaptation of the Atlantic herring revealed by genome sequencing. Elife 5, e12081 (2016).Article 

    Google Scholar 
    Pettersson, M. E. et al. A chromosome-level assembly of the Atlantic herring genome-detection of a supergene and other signals of selection. Genome Res. 29, 1919–1928 (2019).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Bo, J. et al. Opah (Lampris megalopsis) genome sheds light on the evolution of aquatic endothermy. Zool. Res. 43, 26–29 (2022).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Wang, S. et al. Resequencing and SNP discovery of Amur ide (Leuciscus waleckii) provides insights into local adaptations to extreme environments. Sci. Rep. 11, 5064 (2021).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Meng, Z., Hu, P., Lei, J. & Jia, Y. Expression of insulin-like growth factors at mRNA levels during the metamorphic development of turbot (Scophthalmus maximus). Gen. Comp. Endocrinol. 235, 11–17 (2016).Article 
    CAS 
    PubMed 

    Google Scholar 
    Duan, C., Ren, H. & Gao, S. Insulin-like growth factors (IGFs), IGF receptors, and IGF-binding proteins: Roles in skeletal muscle growth and differentiation. Gen. Comp. Endocrinol. 167, 344–351 (2010).Article 
    CAS 
    PubMed 

    Google Scholar 
    Duan, C., Ding, J., Li, Q., Tsai, W. & Pozios, K. Insulin-like growth factor binding protein 2 is a growth inhibitory protein conserved in zebrafish. Proc. Natl. Acad. Sci. USA 96, 15274–15279 (1999).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Furqon, A., Gunawan, A., Ulupi, N., Suryati, T. & Sumantri, C. A Polymorphism of Insulin-like growth factor binding protein 2 gene associated with growth and body composition traits in Kampong Chickens. J. Vet. 19, 183 (2018).
    Google Scholar 
    Kibbey, M. M., Jameson, M. J., Eaton, E. M. & Rosenzweig, S. A. Insulin-like growth factor binding protein-2: Contributions of the C-terminal domain to insulin-like growth factor-1 binding. Mol. Pharmacol. 69, 833–845 (2006).Article 
    CAS 
    PubMed 

    Google Scholar 
    Coughlan, J. P. et al. Microsatellite DNA variation in wild populations and farmed strains of turbot from Ireland and Norway: A preliminary study. J. Fish Biol. 52, 916–922 (1998).Article 
    CAS 

    Google Scholar 
    Zhang, H. et al. Characterization and Identification of Single Nucleotide Polymorphism within the IGF-1R gene associated with growth traits of Odontobutis potamophila. J. World Aquac. Soc. 49, 366–379 (2018).Article 
    CAS 

    Google Scholar 
    Guo, L., Yang, S., Li, M. M., Meng, Z. N. & Lin, H. R. 2016) Divergence and polymorphism analysis of IGF1Ra and IGF1Rb from orange-spotted grouper, Epinephelus coioides (Hamilton). Genet. Mol. Res. 15, 1. https://doi.org/10.4238/gmr15048768 (2016).Article 
    CAS 

    Google Scholar 
    Yu, X. et al. Genome-wide association analysis of adaptation to oxygen stress in Nile tilapia (Oreochromis niloticus). BMC Genomics 22, 426 (2021).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Harano, T. et al. Hemoglobin Kawachi [α44 (CE2) Pro → Arg]: A new hemoglobin variant of high oxygen affinity with amino acid substitution at α1β2 contact. Hemoglobin 6, 43–49 (1982).Article 
    CAS 
    PubMed 

    Google Scholar 
    Alharby, E. et al. A homozygous potentially pathogenic variant in the PAXBP1 gene in a large family with global developmental delay and myopathic hypotonia. Clin. Genet. 92, 579–586 (2017).Article 
    CAS 
    PubMed 

    Google Scholar 
    Ceinos, R. M. et al. Differential circadian and light-driven rhythmicity of clock gene expression and behaviour in the turbot, Scophthalmus maximus. PLoS ONE 14, e0219153 (2019).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Nishiwaki-Ohkawa, T. & Yoshimura, T. Molecular basis for regulating seasonal reproduction in vertebrates. J. Endocrinol. 229, R117–R127 (2016).Article 
    CAS 
    PubMed 

    Google Scholar 
    Wood, S. H. et al. Circadian clock mechanism driving mammalian photoperiodism. Nat. Commun. 11, 4291 (2020).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Piovesan, D. et al. DisProt 7.0: A major update of the database of disordered proteins. Nucl. Acids Res. 45, 219–227 (2017).Article 

    Google Scholar 
    Pajkos, M. & Dosztányi, Z. Chapter Two – Functions of intrinsically disordered proteins through evolutionary lenses. in Dancing Protein Clouds: Intrinsically Disordered Proteins in the Norm and Pathology, Part C (ed. Uversky, V. N. B. T.-P. in M. B. and T. S.) vol. 183 45–74 (Academic Press, 2021).Malagrinò, F. et al. Understanding the binding induced folding of intrinsically disordered proteins by protein engineering: Caveats and pitfalls. Int. J. Mol. Sci. 21, 3484 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Doyle, A., Cowan, M. E., Migaud, H., Wright, P. J. & Davie, A. Neuroendocrine regulation of reproduction in Atlantic cod (Gadus morhua): Evidence of Eya3 as an integrator of photoperiodic cues and nutritional regulation to initiate sexual maturation. Comput. Biochem. Physiol. -Part A Mol. Integr. Physiol. 260, 111000 (2021).Silver, S. J., Davies, E. L., Doyon, L. & Rebay, I. Functional dissection of eyes absent reveals new modes of regulation within the retinal determination gene network. Mol. Cell. Biol. 23, 5989–5999 (2003).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Jin, M. & Mardon, G. Distinct biochemical activities of eyes absent during drosophila eye development. Sci. Rep. 6, 23228 (2016).Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    McGowan, K. L., Passow, C. N., Arias-Rodriguez, L., Tobler, M. & Kelley, J. L. Expression analyses of cave mollies (Poecilia mexicana) reveal key genes involved in the early evolution of eye regression. Biol. Lett. 15, 20190554 (2019).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Cui, W. et al. Transcriptomic analysis reveals putative osmoregulation mechanisms in the kidney of euryhaline turbot Scophthalmus maximus responded to hypo-saline seawater. J. Oceanol. Limnol. 38, 467–479 (2020).Article 
    CAS 

    Google Scholar 
    Mármol-Sánchez, E., Quintanilla, R., Cardoso, T. F., Jordana Vidal, J. & Amills, M. Polymorphisms of the cryptochrome 2 and mitoguardin 2 genes are associated with the variation of lipid-related traits in Duroc pigs. Sci. Rep. 9, 9025 (2019).Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Takvam, M., Wood, C. M., Kryvi, H. & Nilsen, T. O. Ion transporters and osmoregulation in the didney of teleost fishes as a function of salinity. Front. Physiol. 12, 664588 (2021).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Engelund, M. B. & Madsen, S. S. The role of aquaporins in the kidney of euryhaline teleosts. Front. Physiol. 2, 51 (2011).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Nam, B. H. et al. Identification and characterization of the prepro-vasoactive intestinal peptide gene from the teleost Paralichthys olivaceus. Vet. Immunol. Immunopathol. 127, 249–258 (2009).Article 
    CAS 
    PubMed 

    Google Scholar 
    Paladini, F. et al. Age-dependent association of idiopathic achalasia with vasoactive intestinal peptide receptor 1 gene. Neurogastroenterol. Motil. 21, 597–602 (2009).Article 
    CAS 
    PubMed 

    Google Scholar 
    Hosseinpour, L., Nikbin, S., Hedayat-Evrigh, N. & Elyasi-Zarringhabaie, G. Association of polymorphisms of vasoactive intestinal peptide and its receptor with reproductive traits of turkey hens. South Afr. J. Anim. Sci. 50, 345–352 (2020).Article 
    CAS 

    Google Scholar 
    Pereiro, P., Figueras, A. & Novoa, B. A novel hepcidin-like in turbot (Scophthalmus maximus L.) highly expressed after pathogen challenge but not after iron overload. Fish Shellfish Immunol. 32, 879–889 (2012).Article 
    CAS 
    PubMed 

    Google Scholar 
    Zhang, J., Yu, L., Ping, L., Fei, M. & Sun, L. Turbot (Scophthalmus maximus) hepcidin-1 and hepcidin-2 possess antimicrobial activity and promote resistance against bacterial and viral infection. Fish Shellfish Immunol. 38, 127–134 (2014).Article 
    PubMed 

    Google Scholar  More

  • in

    Upside down sulphate dynamics in a saline inland lake

    Canfield, D. E.; Kristensen, E.; Thamdrup, B. The Sulfur Cycle. In Advances in Marine Biology; Aquatic Geomicrobiology; Academic Press, 2005; Vol. 48, pp 313–381. https://doi.org/10.1016/S0065-2881(05)48009-8.Jørgensen, B. B., Findlay, A. J. & Pellerin, A. The biogeochemical sulfur cycle of marine sediments. Front. Microbiol. https://doi.org/10.3389/fmicb.2019.00849 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Thamdrup, B., Fossing, H. & Jørgensen, B. B. Manganese, iron and sulfur cycling in a coastal marine sediment, Aarhus Bay. Denmark. Geochim. Cosmochim. Acta 58(23), 5115–5129. https://doi.org/10.1016/0016-7037(94)90298-4 (1994).Article 
    ADS 
    CAS 

    Google Scholar 
    Holmer, M. & Storkholm, P. Sulphate reduction and sulphur cycling in lake sediments: A review. Freshw. Biol. 46(4), 431–451. https://doi.org/10.1046/j.1365-2427.2001.00687.x (2001).Article 
    CAS 

    Google Scholar 
    Koschorreck, M. Microbial sulphate reduction at a low PH. FEMS Microbiol. Ecol. 64(3), 329–342. https://doi.org/10.1111/j.1574-6941.2008.00482.x (2008).Article 
    CAS 
    PubMed 

    Google Scholar 
    Kwon, M. J. et al. Impact of organic carbon electron donors on microbial community development under iron- and sulfate-reducing conditions. PLoS ONE 11(1), e0146689. https://doi.org/10.1371/journal.pone.0146689 (2016).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Fründ, C. & Cohen, Y. Diurnal cycles of sulfate reduction under oxic conditions in cyanobacterial mats. Appl. Environ. Microbiol. 58(1), 70–77. https://doi.org/10.1128/aem.58.1.70-77.1992 (1992).
    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Marschall, C., Frenzel, P. & Cypionka, H. Influence of oxygen on sulfate reduction and growth of sulfate-reducing bacteria. Arch. Microbiol. 159(2), 168–173. https://doi.org/10.1007/BF00250278 (1993).Article 
    CAS 

    Google Scholar 
    Borzenko, S. V., Kolpakova, M. N., Shvartsev, S. L. & Isupov, V. P. Biogeochemical conversion of sulfur species in saline lakes of steppe Altai. J. Oceanol. Limnol. 36(3), 676–686. https://doi.org/10.1007/s00343-018-6293-8 (2018).Article 
    ADS 
    CAS 

    Google Scholar 
    Häusler, S. et al. Sulfate reduction and sulfide oxidation in extremely steep salinity gradients formed by freshwater springs emerging into the dead sea. FEMS Microbiol Ecol 90(3), 956–969. https://doi.org/10.1111/1574-6941.12449 (2014).Article 
    CAS 
    PubMed 

    Google Scholar 
    Komor, S. C. Bidirectional sulfate diffusion in saline-lake sediments: Evidence from Devils Lake, Northeast North Dakota. Geology 20(4), 319–322. https://doi.org/10.1130/0091-7613(1992)020%3c0319:BSDISL%3e2.3.CO;2 (1992).Article 
    ADS 
    CAS 

    Google Scholar 
    Valiente, N. et al. Tracing sulfate recycling in the hypersaline Pétrola Lake (SE Spain): A combined isotopic and microbiological approach. Chem. Geol. 473, 74–89. https://doi.org/10.1016/j.chemgeo.2017.10.024 (2017).Article 
    ADS 
    CAS 

    Google Scholar 
    Moreira, N., Walter, L., Vasconcelos, C., McKenzie, J. & McCall, P. Role of sulfide oxidation in dolomitization: Sediment and pore-water geochemistry of a modern hypersaline lagoon system. Geology 32(8), 701–704. https://doi.org/10.1130/G20353.1 (2004).Article 
    ADS 
    CAS 

    Google Scholar 
    Jolly, I. D., McEwan, K. L. & Holland, K. L. A review of groundwater-surface water interactions in arid/semi-arid wetlands and the consequences of salinity for wetland ecology. Ecohydrology https://doi.org/10.1002/eco.6 (2008).Article 

    Google Scholar 
    Williams, W. D. Environmental threats to salt lakes and the likely status of inland saline ecosystems in 2025. Environ. Conserv. 29(2), 154–167. https://doi.org/10.1017/S0376892902000103 (2002).Article 

    Google Scholar 
    CHE. Confederación Hidrográfica del Ebro. https://www.chebro.es/ (Accessed 1 June 2022).Comín, F. A., Rodó, X. & Comín, P. Lake Gallocanta (Aragon, NE Spain), a paradigm of fluctuations at different scales of time. Limnetica 8(1), 79–86 (1992).Article 

    Google Scholar 
    Luna, E.; Latorre, B.; Castañeda, C. Rainfall and the Presence of Water in Gallocanta Lake. http://digital.csic.es/handle/10261/117417. (2014).San Roman Saldaña, J.; García Vera, M. Á.; Blasco Herguedas, Ó.; Coloma López, P. Toma de Datos, Modelación y Gestión Del Agua Subterránea En La Cuenca Endorréica de La Laguna de Gallocanta (España); Alicante, Spain, 2005; pp 551–557.Orellana-Macías, J. M., Merchán, D. & Causapé, J. Evolution and assessment of a nitrate vulnerable zone over 20 years: Gallocanta groundwater body (Spain). Hydrogeol. J. https://doi.org/10.1007/s10040-020-02184-0 (2020).Article 

    Google Scholar 
    Gracia, F. J., Gutierrez, F. & Gutierrez, M. Origin and evolution of the Gallocanta Polije (Iberian range, NE Spain). Z. Geomorph. N. F. 46(2), 245–262 (2002).Article 

    Google Scholar 
    García-Vera, M.A.; San Román Saldaña, J.; Blasco Herguedas, O.; Coloma López, P. Hidrogeología de La Laguna de GalIocanta e Implicaciones Ambientales. In M.A. Casterad and C. Castañeda (Eds.). La Laguna de Gallocanta: Medio Natural, Conservación y Teledetección. Memorias de la Real Sociedad Española de Historia Natural. 2009, 7, 79–104.Comín, F. A., Juli, R., Comín, P. & Plana, F. Hydrogeochemistry of Lake Gallocanta (Aragón, NE Spain). Hydrobiologia 197, 51–66. https://doi.org/10.1007/bf00026938 (1990).Article 

    Google Scholar 
    Mayayo, M. J. et al. Sedimentological evolution of the holocene Gallocanta Lake, NE Spain. Limnol. Spain Tribute Kerry Kelts 14, 359–384 (2003).
    Google Scholar 
    Pérez, A. et al. Sedimentary facies distribution and genesis of a recent carbonate-rich Saline Lake: Gallocanta Lake, Iberian Chain, NE Spain. Sediment. Geol. 148(1–2), 185–202. https://doi.org/10.1016/S0037-0738(01)00217-2 (2002).Article 
    ADS 

    Google Scholar 
    Corzo, A. et al. Carbonate mineralogy along a biogeochemical gradient in recent lacustrine sediments of Gallocanta Lake (Spain). Geomicrobiol. J. 22(6), 283–298. https://doi.org/10.1080/01490450500183654 (2005).Article 
    CAS 

    Google Scholar 
    Castañeda, C., Gracia, F. J., Luna, E. & Rodríguez-Ochoa, R. Edaphic and geomorphic evidences of water level fluctuations in Gallocanta Lake, NE Spain. Geoderma 239–240, 265–279. https://doi.org/10.1016/j.geoderma.2014.11.005 (2015).Article 
    ADS 
    CAS 

    Google Scholar 
    Luzón, A. et al. Holocene environmental changes in the Gallocanta lacustrine basin, Iberian range, NE Spain. Holocene 17(5), 649–663. https://doi.org/10.1177/0959683607078994 (2007).Article 
    ADS 

    Google Scholar 
    Schütt, B. Reconstruction of holocene paleoenvironments in the endorheic basin of laguna de Gallocanta, Central Spain by investigation of mineralogical and geochemical characters from lacustrine sediments. J. Paleolimnol. 20, 217. https://doi.org/10.1023/A:1007924000636 (1998).Article 
    ADS 

    Google Scholar 
    Castañeda, C., Luna, E. & Rabenhorst, M. Reducing conditions in soil of Gallocanta Lake. Northeast Spain. Eur. J. Soil Sci. 68(2), 249–258. https://doi.org/10.1111/ejss.12407 (2017).Article 
    CAS 

    Google Scholar 
    Castañeda, C., Gracia, F. J., Conesa, J. A. & Latorre, B. Geomorphological control of habitat distribution in an intermittent shallow Saline Lake, Gallocanta Lake. NE Spain. Sci. Total Environ. 726, 138601. https://doi.org/10.1016/j.scitotenv.2020.138601 (2020).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Comín, F. A., Rodó, X. & Menéndez, M. Spatial heterogeneity of macrophytes in lake Gallocanta (Aragón, NE Spain). Hydrobiologia 267(1–3), 169–178. https://doi.org/10.1007/BF00018799 (1993).Article 

    Google Scholar 
    Castro, O. D. et al. A Contribution to the characterization of ruppia drepanensis (ruppiaceae), a key species of threatened mediterranean Wetlands. Ann. Mo. Bot. Gard. 106, 1–9. https://doi.org/10.3417/2020520 (2021).Article 

    Google Scholar 
    Alonso López, J. A., Alonso López, J. C., Cantos, F. J. & Bautista, L. M. Spring crane grus grus migration through Gallocanta, Spain. II. Timing and pattern of daily departures. Ardea 78, 379–388 (1990).
    Google Scholar 
    Alonso López, J. C., Alonso López, J. A., Cantos, F. J. & Bautista, L. M. Spring crane grus grus migration through Gallocanta, Spain. I. Daily Variations in Migration Volume. Ardea 78, 365–378 (1990).
    Google Scholar 
    Orellana-Macías, J. M., Bautista, L. M., Merchán, D., Causapé, J. & Alonso, J. C. Shifts in crane migration phenology associated with climate change in southwestern Europe. Avian Conserv. Ecol. 15(1), 1–13. https://doi.org/10.5751/ACE-01565-150116 (2020).Article 

    Google Scholar 
    Luzón, A., Mayayo, M. J. & Pérez, A. Stable isotope characterisation of co-existing carbonates from the holocene Gallocanta Lake (NE Spain): Palaeolimnological implications. Int. J. Earth Sci. 98(5), 1129–1150. https://doi.org/10.1007/s00531-008-0308-1 (2009).Article 
    CAS 

    Google Scholar 
    Accoe, F. et al. Evolution of the Δ13C signature related to total carbon contents and carbon decomposition rate constants in a soil profile under grassland. Rapid Commun. Mass Spectrom. 16(23), 2184–2189. https://doi.org/10.1002/rcm.767 (2002).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Menéndez-Serra, M., Triadó-Margarit, X., Castañeda, C., Herrero, J. & Casamayor, E. O. Microbial composition, potential functional roles and genetic novelty in gypsum-rich and hypersaline soils of Monegros and Gallocanta (Spain). Sci. Total Environ. 650(September), 343–353. https://doi.org/10.1016/j.scitotenv.2018.09.050 (2019).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Kendall, C. & McDonnell, J. J. Isotope Tracers in Catchment Hydrology 1st edn. (Elsevier, 1999).

    Google Scholar 
    Mayer, B., Fritz, P., Prietzel, J. & Krouse, H. R. The use of stable sulfur and oxygen isotope ratios for interpreting the mobility of sulfate in aerobic forest soils. Appl. Geochem. 10(2), 161–173. https://doi.org/10.1016/0883-2927(94)00054-A (1995).Article 
    ADS 
    CAS 

    Google Scholar 
    Otero, N., Canals, À. & Soler, A. Using dual-isotope data to trace the origin and processes of dissolved sulphate: A case study in calders stream (Llobregat Basin, Spain). Aquat. Geochem. 13(2), 109–126. https://doi.org/10.1007/s10498-007-9010-3 (2007).Article 
    CAS 

    Google Scholar 
    Canfield, D. E. Isotope fractionation by natural populations of sulfate-reducing bacteria. Geochim. Cosmochim. Acta 65(7), 1117–1124. https://doi.org/10.1016/S0016-7037(00)00584-6 (2001).Article 
    ADS 
    CAS 

    Google Scholar 
    Canfield, D. E. Biogeochemistry of sulfur isotopes. Rev. Mineral. Geochem. 43(1), 607–636. https://doi.org/10.2138/gsrmg.43.1.607 (2001).Article 
    CAS 

    Google Scholar 
    Antler, G., Turchyn, A. V., Ono, S., Sivan, O. & Bosak, T. Combined 34S, 33S and 18O isotope fractionations record different intracellular steps of microbial sulfate reduction. Geochim. Cosmochim. Acta 203, 364–380. https://doi.org/10.1016/j.gca.2017.01.015 (2017).Article 
    ADS 
    CAS 

    Google Scholar 
    Kaplan, I. R. & Rittenberg, S. C. Microbiological fractionation of sulphur isotopes. J. Gen. Microbiol. 34(2), 195–212. https://doi.org/10.1099/00221287-34-2-195 (1964).Article 
    CAS 
    PubMed 

    Google Scholar 
    Mangalo, M., Meckenstock, R. U., Stichler, W. & Einsiedl, F. Stable isotope fractionation during bacterial sulfate reduction is controlled by reoxidation of intermediates. Geochim. Cosmochim. Acta 71(17), 4161–4171. https://doi.org/10.1016/j.gca.2007.06.058 (2007).Article 
    ADS 
    CAS 

    Google Scholar 
    Strebel, O., Böttcher, J. & Fritz, P. Use of isotope fractionation of sulfate-sulfur and sulfate-oxygen to assess bacterial desulfurication in a sandy aquifer. J. Hydrol. 121(1–4), 155–172. https://doi.org/10.1016/0022-1694(90)90230-U (1990).Article 
    ADS 
    CAS 

    Google Scholar 
    Sim, M. S., Bosak, T. & Ono, S. Large sulfur isotope fractionation does not require disproportionation. Science 333(6038), 74–77. https://doi.org/10.1126/science.1205103 (2011).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Leavitt, W. D., Halevy, I., Bradley, A. S. & Johnston, D. T. Influence of sulfate reduction rates on the phanerozoic sulfur isotope record. Proc. Natl. Acad. Sci. 110(28), 11244–11249. https://doi.org/10.1073/pnas.1218874110 (2013).Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Utrilla, R., Pierre, C., Orti, F. & Pueyo, J. J. Oxygen and sulphur isotope compositions as indicators of the origin of mesozoic and cenozoic evaporites from Spain. Chem. Geol. 102(1), 229–244. https://doi.org/10.1016/0009-2541(92)90158-2 (1992).Article 
    ADS 
    CAS 

    Google Scholar 
    Driessche, A. E. S. V., Canals, A., Ossorio, M., Reyes, R. C. & García-Ruiz, J. M. Unraveling the sulfate sources of (Giant) gypsum crystals using gypsum isotope fractionation factors. J. Geol. https://doi.org/10.1086/684832 (2016).Article 

    Google Scholar 
    Wardlaw, G. D. & Valentine, D. L. Evidence for salt diffusion from sediments contributing to increasing salinity in the Salton sea, California. Hydrobiologia 533(1), 77–85. https://doi.org/10.1007/s10750-004-2395-8 (2005).Article 
    CAS 

    Google Scholar 
    Bak, F. & Pfennig, N. Microbial sulfate reduction in littoral sediment of lake constance. FEMS Microbiol. Lett. 85(1), 31–42. https://doi.org/10.1111/j.1574-6968.1991.tb04695.x (1991).Article 
    CAS 

    Google Scholar 
    Dogramaci, S. S., Herczeg, A. L., Schiff, S. L. & Bone, Y. Controls on Δ34S and Δ18O of dissolved sulfate in aquifers of the murray basin, Australia and their use as indicators of flow processes. Appl. Geochem. 16(4), 475–488. https://doi.org/10.1016/S0883-2927(00)00052-4 (2001).Article 
    ADS 
    CAS 

    Google Scholar 
    Rodier. L’analyse de l’eau, eaux naturelles, eaux résiduaires, eau de mer; Dunod, 1976.Romain, T. Tester Les Isotopes Stables de l’azote Des Matières Organiques Fossiles Terrestres Comme Marqueur Paléoclimatique Sur Des Séries Pré-Quaternaires, Université Pierre et Marie Curie – Paris VI, 2015. https://tel.archives-ouvertes.fr/tel-01408071. More

  • in

    Legally protect marine food web’s lower echelons

    Plankton are microscopic organisms at the base of aquatic food webs and therefore essential to all life on Earth. In our view, international legal protection of plankton is urgently needed because of their high susceptibility to the effects of climate change, including ocean warming and acidification.
    Competing Interests
    The authors declare no competing interests. More

  • in

    Fungal parasitism on diatoms alters formation and bio–physical properties of sinking aggregates

    Falkowski, P. The power of plankton. Nature 483, 17–20 (2012).Article 

    Google Scholar 
    Field, C. B., Behrenfeld, M. J., Randerson, J. T. & Falkowski, P. Primary production of the biosphere: Integrating terrestrial and oceanic components. Science 281, 237 (1998).Article 
    CAS 
    PubMed 

    Google Scholar 
    Grossart, H. P. & Simon, M. Significance of limnetic organic aggregates (lake snow) for the sinking flux of particulate organic matter in a large lake. Aquat. Microb. Ecol. 15, 115–125 (1998).Article 

    Google Scholar 
    Weyhenmeyer, G. A. & Bloesch, J. The pattern of particle flux variability in Swedish and Swiss lakes. Sci. Total Environ. 266, 69–78 (2001).Article 
    CAS 
    PubMed 

    Google Scholar 
    Fender, C. K. et al. Investigating particle size-flux relationships and the biological pump across a range of plankton ecosystem states from coastal to oligotrophic. Front. Marine Sci. 6, https://doi.org/10.3389/fmars.2019.00603 (2019).Iversen, M. H., Nowald, N., Ploug, H., Jackson, G. A. & Fischer, G. High resolution profiles of vertical particulate organic matter export off Cape Blanc, Mauritania: Degradation processes and ballasting effects. Deep-Sea Res. Pt I Oceanogr. Res. Papers. 57, 771–784 (2010).Article 
    CAS 

    Google Scholar 
    Griffiths, J. R. et al. The importance of benthic–pelagic coupling for marine ecosystem functioning in a changing world. Glob. Change Biol. 23, 2179–2196 (2017).Article 

    Google Scholar 
    Diaz, R. J. & Rosenberg, R. Spreading dead zones and consequences for marine ecosystems. Science 321, 926–929 (2008).Article 
    CAS 
    PubMed 

    Google Scholar 
    Jenny, J. P. et al. Global spread of hypoxia in freshwater ecosystems during the last three centuries is caused by rising local human pressure. Glob. Chang Biol. 22, 1481–1489 (2016).Article 
    PubMed 

    Google Scholar 
    Carstensen, J., Andersen, J. H., Gustafsson, B. G. & Conley, D. J. Deoxygenation of the Baltic Sea during the last century. Proc. Natl Acad. Sci. 111, 5628–5633 (2014).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Simon, M., Grossart, H. P., Schweitzer, B. & Ploug, H. Microbial ecology of organic aggregates in aquatic ecosystems. Aquat. Microb. Ecol. 28, 175–211 (2002).Article 

    Google Scholar 
    Burd, A. B. & Jackson, G. A. Particle aggregation. Ann. Rev. Mar. Sci. 1, 65–90 (2009).Article 
    PubMed 

    Google Scholar 
    Kiørboe, T., Lundsgaard, C., Olesen, M. & Hansen, J. L. S. Aggregation and sedimentation processes during a spring phytoplankton bloom: A field experiment to test coagulation theory. J. Mar. Res. 52, 297–323 (1994).Article 

    Google Scholar 
    Boyd, P. W. & Trull, T. W. Understanding the export of biogenic particles in oceanic waters: Is there consensus? Prog. Oceanogr. 72, 276–312 (2007).Article 

    Google Scholar 
    Legendre, L. & Rivkin, R. B. Fluxes of carbon in the upper ocean: regulation by food-web control nodes. Mar. Ecol. Prog. Ser. 242, 95–109 (2002).Article 

    Google Scholar 
    Kaneko, H. et al. Eukaryotic virus composition can predict the efficiency of carbon export in the global ocean. iScience 24, 102002 (2021).Article 
    CAS 
    PubMed 

    Google Scholar 
    Guidi, L. et al. Plankton networks driving carbon export in the oligotrophic ocean. Nature 532, 465 (2016).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Grossart, H.-P. et al. Fungi in aquatic ecosystems. Nat. Rev. Microbiol. 17, 339–354 (2019).Article 
    CAS 
    PubMed 

    Google Scholar 
    Amend, A. et al. Fungi in the marine environment: Open questions and unsolved problems. mBio 10, e01189–01118 (2019).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ortiz-Álvarez, R., Triadó-Margarit, X., Camarero, L., Casamayor, E. O. & Catalan, J. High planktonic diversity in mountain lakes contains similar contributions of autotrophic, heterotrophic and parasitic eukaryotic life forms. Sci. Rep. 8, 4457 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Gutiérrez, M. H., Pantoja, S., Tejos, E. & Quiñones, R. A. The role of fungi in processing marine organic matter in the upwelling ecosystem off Chile. Mar. Biol. 158, 205–219 (2011).Article 

    Google Scholar 
    Edgcomb, V. P., Beaudoin, D., Gast, R., Biddle, J. F. & Teske, A. Marine subsurface eukaryotes: The fungal majority. Environ. Microbiol. 13, 172–183 (2011).Article 
    CAS 
    PubMed 

    Google Scholar 
    Frenken, T. et al. Integrating chytrid fungal parasites into plankton ecology: research gaps and needs. Environ. Microbiol. 19, 3802–3822 (2017).Article 
    PubMed 

    Google Scholar 
    Van den Wyngaert, S. et al. Seasonality of parasitic and saprotrophic zoosporic fungi: linking sequence data to ecological traits. ISME J. 16, 2242–2254 (2022).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Gsell, A. S. et al. Long-term trends and seasonal variation in host density, temperature, and nutrients differentially affect chytrid fungi parasitising lake phytoplankton. Freshwat. Biol. https://doi.org/10.1111/fwb.13958 (2022).Gutiérrez, M. H., Jara, A. M. & Pantoja, S. Fungal parasites infect marine diatoms in the upwelling ecosystem of the Humboldt current system off central Chile. Environ. Microbiol. 18, 1646–1653 (2016).Article 
    PubMed 

    Google Scholar 
    Kilias, E. S. et al. Chytrid fungi distribution and co-occurrence with diatoms correlate with sea ice melt in the Arctic Ocean. Commun. Biol. 3, 183 (2020).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Hassett, B. T., Ducluzeau, A. L. L., Collins, R. E. & Gradinger, R. Spatial distribution of aquatic marine fungi across the western Arctic and sub-arctic. Environ. Microbiol. 19, 475–484 (2017).Article 
    CAS 
    PubMed 

    Google Scholar 
    Lepelletier, F. et al. Dinomyces arenysensis gen. et sp. nov. (Rhizophydiales, Dinomycetaceae fam. nov.), a chytrid infecting marine dinoflagellates. Protist 165, 230–244 (2014).Article 
    PubMed 

    Google Scholar 
    Hassett, B. T. & Gradinger, R. Chytrids dominate arctic marine fungal communities. Environ. Microbiol. 18, 2001–2009 (2016).Article 
    CAS 
    PubMed 

    Google Scholar 
    Le Calvez, T., Burgaud, G., Mahé, S., Barbier, G. & Vandenkoornhuyse, P. Fungal diversity in deep-sea hydrothermal ecosystems. Appl. Environ. Microbiol. 75, 6415–6421 (2009).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Richards, T. A. et al. Molecular diversity and distribution of marine fungi across 130 european environmental samples. Proc. R. Soc. B Biol. Sci. 282, 20152243 (2015).Article 

    Google Scholar 
    Taylor, J. D. & Cunliffe, M. Multi-year assessment of coastal planktonic fungi reveals environmental drivers of diversity and abundance. ISME J. 10, 2118–2128 (2016).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Comeau, A. M., Vincent, W. F., Bernier, L. & Lovejoy, C. Novel chytrid lineages dominate fungal sequences in diverse marine and freshwater habitats. Sci. Rep. 6, 30120 (2016).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Wang, Y., Sen, B., He, Y., Xie, N. & Wang, G. Spatiotemporal distribution and assemblages of planktonic fungi in the coastal waters of the Bohai Sea. Front. Microbiol. 9, 584 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Gao, Z., Johnson, Z. I. & Wang, G. Molecular characterization of the spatial diversity and novel lineages of mycoplankton in Hawaiian coastal waters. ISME J. 4, 111–120 (2009).Article 
    PubMed 

    Google Scholar 
    Duan, Y. et al. A high-resolution time series reveals distinct seasonal patterns of planktonic fungi at a temperate coastal ocean site (Beaufort, North Carolina, USA). Appl. Environ. Microbiol. 84, e00967–00918 (2018).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Cleary, A. C., Søreide, J. E., Freese, D., Niehoff, B. & Gabrielsen, T. M. Feeding by Calanus glacialis in a high arctic fjord: Potential seasonal importance of alternative prey. ICES J. Mar. Sci. 74, 1937–1946 (2017).Article 

    Google Scholar 
    Renaud, P. E., Morata, N., Carroll, M. L., Denisenko, S. G. & Reigstad, M. Pelagic–benthic coupling in the western Barents Sea: Processes and time scales. Deep Sea Res. Part II: Topical Stud. Oceanogr. 55, 2372–2380 (2008).Article 
    CAS 

    Google Scholar 
    Lepère, C., Ostrowski, M., Hartmann, M., Zubkov, M. V. & Scanlan, D. J. In situ associations between marine photosynthetic picoeukaryotes and potential parasites – a role for fungi? Environ. Microbiol. Rep. 8, 445–451 (2016).Article 
    PubMed 

    Google Scholar 
    Kagami, M., Gurung, T. B., Yoshida, T. & Urabe, J. To sink or to be lysed? Contrasting fate of two large phytoplankton species in Lake Biwa. Limnol. Oceanogr. 51, 2775–2786 (2006).Article 

    Google Scholar 
    Gerphagnon, M., Colombet, J., Latour, D. & Sime-Ngando, T. Spatial and temporal changes of parasitic chytrids of cyanobacteria. Sci. Rep. 7, 6056 (2017).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ibelings, B. W. et al. Chytrid infections and diatom spring blooms: Paradoxical effects of climate warming on fungal epidemics in lakes. Freshwat. Biol. 56, 754–766 (2011).Article 

    Google Scholar 
    Gsell, A. S. et al. Spatiotemporal variation in the distribution of chytrid parasites in diatom host populations. Freshwat. Biol. 58, 523–537 (2013).Article 

    Google Scholar 
    Grami, B. et al. Functional effects of parasites on food web properties during the spring diatom bloom in Lake Pavin: A linear inverse modeling analysis. PLOS ONE. 6, e23273 (2011).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Klawonn, I. et al. Characterizing the “fungal shunt”: Parasitic fungi on diatoms affect carbon flow and bacterial communities in aquatic microbial food webs. Proc. Natl Acad. Sci. 118, e2102225118 (2021).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Kagami, M., Miki, T. & Takimoto, G. Mycoloop: Chytrids in aquatic food webs. Front. Microbiol. 5, 166 (2014).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Laundon, D. & Cunliffe, M. A call for a better understanding of aquatic chytrid biology. Front. Fungal Biol. 2, https://doi.org/10.3389/ffunb.2021.708813 (2021).Ploug, H., Iversen, M. H. & Fischer, G. Ballast, sinking velocity, and apparent diffusivity within marine snow and zooplankton fecal pellets: Implications for substrate turnover by attached bacteria. Limnol. Oceanogr. 53, 1878–1886 (2008).Article 

    Google Scholar 
    Laurenceau-Cornec, E. C., Trull, T. W., Davies, D. M., De La Rocha, C. L. & Blain, S. Phytoplankton morphology controls on marine snow sinking velocity. Mar. Ecol. Prog. Ser. 520, 35–56 (2015).Article 

    Google Scholar 
    Tréguer, P. et al. Influence of diatom diversity on the ocean biological carbon pump. Nat. Geosci. 11, 27–37 (2018).Article 

    Google Scholar 
    Alldredge, A. L., Gotschalk, C., Passow, U. & Riebesell, U. Mass aggregation of diatom blooms: Insights from a mesocosm study. Deep Sea Res. Part II: Topical Stud. Oceanogr. 42, 9–27 (1995).Article 
    CAS 

    Google Scholar 
    Seto, K., Van den Wyngaert, S., Degawa, Y. & Kagami, M. Taxonomic revision of the genus Zygorhizidium: Zygorhizidiales and Zygophlyctidales ord. nov. (Chytridiomycetes, Chytridiomycota). Fungal Syst. Evol. 5, 17–38 (2020).Article 
    CAS 
    PubMed 

    Google Scholar 
    Engel, A. in Practical Guidelines for the Analysis of Seawater (eds Wurl O & Raton B) (CRC Press, 2009).Cisternas-Novoa, C., Lee, C. & Engel, A. A semi-quantitative spectrophotometric, dye-binding assay for determination of Coomassie Blue stainable particles. Limnol. Oceanogr. Methods. 12, 604–616 (2014).Article 

    Google Scholar 
    Passow, U. & Alldredge, A. L. A dye-binding assay for the spectrophotometric measurement of transparent exopolymer particles (TEP). Limnol. Oceanogr. 40, 1326–1335 (1995).Article 
    CAS 

    Google Scholar 
    Iversen, M. H. & Ploug, H. Temperature effects on carbon-specific respiration rate and sinking velocity of diatom aggregates – potential implications for deep ocean export processes. Biogeosciences 10, 4073–4085 (2013).Article 

    Google Scholar 
    van der Jagt, H., Friese, C., Stuut, J.-B. W., Fischer, G. & Iversen, M. H. The ballasting effect of Saharan dust deposition on aggregate dynamics and carbon export: Aggregation, settling, and scavenging potential of marine snow. Limnol. Oceanogr. 63, 1386–1394 (2018).Article 

    Google Scholar 
    Grossart, H. P. & Ploug, H. Microbial degradation of organic carbon and nitrogen on diatom aggregates. Limnol. Oceanogr. 46, 267–277 (2001).Article 
    CAS 

    Google Scholar 
    Iversen, M. H. & Ploug, H. Ballast minerals and the sinking carbon flux in the ocean: Carbon-specific respiration rates and sinking velocity of marine snow aggregates. Biogeosciences 7, 2613–2624 (2010).Article 
    CAS 

    Google Scholar 
    Ploug, H. & Grossart, H. P. Bacterial growth and grazing on diatom aggregates: Respiratory carbon turnover as a function of aggregate size and sinking velocity. Limnol. Oceanogr. 45, 1467–1475 (2000).Article 
    CAS 

    Google Scholar 
    Belcher, A. et al. Depth-resolved particle-associated microbial respiration in the northeast Atlantic. Biogeosciences 13, 4927–4943 (2016).Article 

    Google Scholar 
    Ploug, H., Grossart, H. P., Azam, F. & Jørgensen, B. B. Photosynthesis, respiration, and carbon turnover in sinking marine snow from surface waters of Southern California Bight: Implications for the carbon cycle in the ocean. Mar. Ecol. Prog. Ser. 179, 1–11 (1999).Article 
    CAS 

    Google Scholar 
    Turner, J. T. Zooplankton fecal pellets, marine snow, phytodetritus and the ocean’s biological pump. Prog. Oceanogr. 130, 205–248 (2015).Article 

    Google Scholar 
    Nguyen, T. T. H. et al. Microbes contribute to setting the ocean carbon flux by altering the fate of sinking particulates. Nat. Commun. 13, 1657 (2022).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Zakem, E. J., Cael, B. B. & Levine, N. M. A unified theory for organic matter accumulation. Proc. Natl Acad. Sci. 118, e2016896118 (2021).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Alcolombri, U. et al. Sinking enhances the degradation of organic particles by marine bacteria. Nat. Geosci. 14, 775–780 (2021).Article 
    CAS 

    Google Scholar 
    Buesseler, K. O. & Boyd, P. W. Shedding light on processes that control particle export and flux attenuation in the twilight zone of the open ocean. Limnol. Oceanogr. 54, 1210–1232 (2009).Article 
    CAS 

    Google Scholar 
    Henson, S., Le Moigne, F. & Giering, S. Drivers of carbon export efficiency in the global ocean. Glob. Biogeochem. Cycles. 33, 891–903 (2019).Article 
    CAS 

    Google Scholar 
    Gsell, A. S., De Senerpont Domis, L. N., Verhoeven, K. J. F., Van Donk, E. & Ibelings, B. W. Chytrid epidemics may increase genetic diversity of a diatom spring-bloom. ISME J. 7, 2057–2059 (2013).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Agha, R., Saebelfeld, M., Manthey, C., Rohrlack, T. & Wolinska, J. Chytrid parasitism facilitates trophic transfer between bloom-forming cyanobacteria and zooplankton (Daphnia). Sci. Rep. 6, 35039 (2016).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Rasconi, S. et al. Parasitic chytrids upgrade and convey primary produced carbon during inedible algae proliferation. Protist 171, 125768 (2020).Article 
    CAS 
    PubMed 

    Google Scholar 
    Guidi, L. et al. Effects of phytoplankton community on production, size, and export of large aggregates: A world-ocean analysis. Limnol. Oceanogr. 54, 1951–1963 (2009).Article 

    Google Scholar 
    Boyd, P. W. & Newton, P. P. Does planktonic community structure determine downward particulate organic carbon flux in different oceanic provinces?. Deep-Sea Res. Pt I Oceanogr. Res. Papers. 46, 63–91 (1999).Article 
    CAS 

    Google Scholar 
    van der Jagt, H., Wiedmann, I., Hildebrandt, N., Niehoff, B. & Iversen, M. H. Aggregate feeding by the copepods Calanus and Pseudocalanus controls carbon flux attenuation in the arctic shelf sea during the productive period. Front. Mar. Sci. 7, 543124 (2020).Article 

    Google Scholar 
    Steinberg, D. K. et al. Bacterial vs. zooplankton control of sinking particle flux in the ocean’s twilight zone. Limnol. Oceanogr. 53, 1327–1338 (2008).Article 

    Google Scholar 
    Cavan, E. L., Henson, S. A., Belcher, A. & Sanders, R. Role of zooplankton in determining the efficiency of the biological carbon pump. Biogeosciences 14, 177–186 (2017).Article 
    CAS 

    Google Scholar 
    Gachon, C. M. M., Küpper, H., Küpper, F. C. & Šetlík, I. Single-cell chlorophyll fluorescence kinetic microscopy of Pylaiella littoralis (Phaeophyceae) infected by Chytridium polysiphoniae (Chytridiomycota). Eur. J. Phycol. 41, 395–403 (2006).Article 

    Google Scholar 
    Senga, Y., Yabe, S., Nakamura, T. & Kagami, M. Influence of parasitic chytrids on the quantity and quality of algal dissolved organic matter (AOM). Water Res. 145, 346––353 (2018).Article 
    PubMed 

    Google Scholar 
    Roberts, C., Allen, R., Bird, K. E. & Cunliffe, M. Chytrid fungi shape bacterial communities on model particulate organic matter. Biol. Lett. 16, 20200368 (2020).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Blackburn, N., Fenchel, T. & Mitchell, J. Microscale nutrient patches in planktonic habitats shown by chemotactic bacteria. Science 282, 2254–2256 (1998).Article 
    CAS 
    PubMed 

    Google Scholar 
    Smriga, S., Fernandez, V. I., Mitchell, J. G. & Stocker, R. Chemotaxis toward phytoplankton drives organic matter partitioning among marine bacteria. Proc. Natl Acad. Sci. 113, 1576–1581 (2016).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Buchan, A., LeCleir, G. R., Gulvik, C. A. & González, J. M. Master recyclers: features and functions of bacteria associated with phytoplankton blooms. Nat. Rev. Microbiol. 12, 686–698 (2014).Article 
    CAS 
    PubMed 

    Google Scholar 
    Shibl, A. A. et al. Diatom modulation of select bacteria through use of two unique secondary metabolites. Proc. Natl Acad. Sci. 117, 27445–27455 (2020).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Guidi, L. et al. Relationship between particle size distribution and flux in the mesopelagic zone. Deep-Sea Res. Part I Oceanogr. Res. Papers. 55, 1364–1374 (2008).Article 
    CAS 

    Google Scholar 
    Jackson, G. A. et al. Particle size spectra between 1 μm and 1 cm at Monterey Bay determined using multiple instruments. Deep-Sea Res. Pt I Oceanogr. Res. Papers. 44, 1739–1767 (1997).Article 

    Google Scholar 
    Frenken, T. et al. Warming accelerates termination of a phytoplankton spring bloom by fungal parasites. Glob. Change Biol. 22, 299–309 (2016).Article 

    Google Scholar 
    Mari, X., Passow, U., Migon, C., Burd, A. B. & Legendre, L. Transparent exopolymer particles: Effects on carbon cycling in the ocean. Prog. Oceanogr. 151, 13–37 (2017).Article 

    Google Scholar 
    Passow, U. Transparent exopolymer particles (TEP) in aquatic environments. Prog. Oceanogr. 55, 287–333 (2002).Article 

    Google Scholar 
    Prieto, L. et al. Scales and processes in the aggregation of diatom blooms: high time resolution and wide size range records in a mesocosm study. Deep-Sea Res. Pt I Oceanogr. Res. Papers. 49, 1233–1253 (2002).Article 

    Google Scholar 
    Kiørboe, T., Andersen, K. P. & Dam, H. G. Coagulation efficiency and aggregate formation in marine phytoplankton. Mar. Biol. 107, 235–245 (1990).Article 

    Google Scholar 
    Vidal-Melgosa, S. et al. Diatom fucan polysaccharide precipitates carbon during algal blooms. Nat. Commun. 12, 1150 (2021).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Gärdes, A., Iversen, M. H., Grossart, H. P., Passow, U. & Ullrich, M. S. Diatom-associated bacteria are required for aggregation of Thalassiosira weissflogii. ISME J. 5, 436–445 (2011).Article 
    PubMed 

    Google Scholar 
    Grossart, H. P. & Simon, M. Interactions of planktonic algae and bacteria: Effects on algal growth and organic matter dynamics. Aquat. Microb. Ecol. 47, 163–176 (2007).Article 

    Google Scholar 
    Short, S. M. The ecology of viruses that infect eukaryotic algae. Environ. Microbiol. 14, 2253–2271 (2012).Article 
    PubMed 

    Google Scholar 
    Carlström, D. The crystal structure of α-chitin (Poly-N-acetyl-d-glucosamine). J. Biophysical Biochemical Cytol. 3, 669–683 (1957).Article 

    Google Scholar 
    Miklasz, K. A. & Denny, M. W. Diatom sinkings speeds: Improved predictions and insight from a modified Stokes’ law. Limnol. Oceanogr. 55, 2513–2525 (2010).Article 

    Google Scholar 
    Bidle, K. D. & Azam, F. Accelerated dissolution of diatom silica by marine bacterial assemblages. Nature 397, 508 (1999).Article 
    CAS 

    Google Scholar 
    Gerphagnon, M. et al. Comparison of sterol and fatty acid profiles of chytrids and their hosts reveals trophic upgrading of nutritionally inadequate phytoplankton by fungal parasites. Environ. Microbiol. 21, 949–958 (2019).Article 
    CAS 
    PubMed 

    Google Scholar 
    Kagami, M., Von Elert, E., Ibelings, B. W., De Bruin, A. & Van Donk, E. The parasitic chytrid, Zygorhizidium, facilitates the growth of the cladoceran zooplankter, Daphnia, in cultures of the inedible alga, Asterionella. Proc. R. Soc. B Biol. Sci. 274, 1561–1566 (2007).Article 

    Google Scholar 
    Carney, L. T. & Lane, T. W. Parasites in algae mass culture. Front. Microbiol. 5, 1–8 (2014).Article 

    Google Scholar 
    Williams, D. M. Synedra, Ulnaria: definitions and descriptions – a partial resolution. Diatom Res. 26, 149–153 (2011).Article 

    Google Scholar 
    Arar, E. J. & Collins, G. B. Method 445.0: In vitro determination of chlorophyll and phaeophytin a in marine and freshwater algae by fluorescence. U.S. Environemental Protection Agency, Cinncinnati, Ohio Revision 1.2, 1–22 (1997).Klawonn, I., Dunker, S., Kagami, M., Grossart, H.-P., Van den Wyngaert, S. Intercomparison of two fluorescent dyes to visualize parasitic fungi (Chytridiomycota) on phytoplankton. Microb. Ecol. 85, 9–23 (2023).Article 
    CAS 
    PubMed 

    Google Scholar 
    Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675 (2012).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Alldredge, A. L. & Gotschalk, C. In situ settling behavior of marine snow. Limnol. Oceanogr. 33, 351 (1988).Article 

    Google Scholar 
    Jackson, G. A. Coagulation in a rotating cylinder. Limnol. Oceanogr. Methods. 13, e10018 (2015).Article 

    Google Scholar 
    Shanks, A. L. & Edmondson, E. W. Laboratory-made artificial marine snow: a biological model of the real thing. Mar. Biol. 101, 463–470 (1989).Article 

    Google Scholar 
    Cowen, R. K. & Guigand, C. M. In situ ichthyoplankton imaging system (ISIIS): system design and preliminary results. Limnol. Oceanogr. Methods. 6, 126–132 (2008).Article 

    Google Scholar 
    Jackson, G. A. & Burd, A. B. Simulating aggregate dynamics in ocean biogeochemical models. Prog. Oceanogr. 133, 55–65 (2015).Article 

    Google Scholar 
    Petrik, C. M., Jackson, G. A. & Checkley, D. M. Aggregates and their distributions determined from LOPC observations made using an autonomous profiling float. Deep-Sea Res. Pt I Oceanogr. Res. Papers. 74, 64–81 (2013).Article 

    Google Scholar 
    Johnson, C. P., Li, X. & Logan, B. E. Settling velocities of fractal aggregates. Environ. Sci. Technol. 30, 1911–1918 (1996).Article 
    CAS 

    Google Scholar 
    Laurenceau-Cornec, E. C. et al. New guidelines for the application of Stokes’ models to the sinking velocity of marine aggregates. Limnol. Oceanogr. 65, 1264–1285 (2020).Article 
    CAS 

    Google Scholar 
    Ploug, H. & Grossart, H. P. Bacterial production and respiration in suspended aggregates – A matter of the incubation method. Aquat. Microb. Ecol. 20, 21–29 (1999).Article 

    Google Scholar 
    Berggren, M., Lapierre, J.-F. & del Giorgio, P. A. Magnitude and regulation of bacterioplankton respiratory quotient across freshwater environmental gradients. ISME J. 6, 984–993 (2012).Article 
    CAS 
    PubMed 

    Google Scholar 
    R.CoreTeam. R: A language and environment for statistical computing. Vienna, Austria. Retrieved from https://www.R-project.org/ (2016). More

  • in

    Rodent activity in municipal waste collection premises in Singapore: an analysis of risk factors using mixed-effects modelling

    Commensal rodents serve as important reservoirs of rodent-borne pathogens. Efforts to reduce the risk of pathogen transmission include decimating rodent populations, altering access pathways, upholding good waste management practices and denying easy access to food sources. In our study, we examined the incidence of rodent activity in waste collection premises in public residential estates in Singapore and examined the factors associated with rodent activity to inform the priority of rodent control measures of resource limited municipal estate managers.Of the three types of waste collection premises, rodent activity had the highest incidence in refuse bin centres followed by CRCs and IRC bin chambers. Refuse bin centres are prone to refuse spillage because refuse is manually transferred from refuse collection carts into bulk bins and refuse compactors located within the centres. Bin centres tend to be larger than CRCs and IRC bin chambers and the storage of bulky waste that provide additional areas of rodent harbourage are a common sight in Singapore. IRC chambers and refuse bin centres in combination far outnumber CRCs, and the former two are a distinct characteristic of older public housing estates in Singapore. This suggests that older public housing estates have a higher propensity for rodent infestation compared to newer ones. Aging infrastructure can also provide a greater number of harbourage areas and alternate access pathways for rodent travel that increase their ability to obtain food sources. Our study findings were in support of previous studies which found that older infrastructure was associated with a greater likelihood of rodent activity22,23.We also found that the number of IRC bin chutes was positively associated with rodent infestation. Fluids from food waste in IRC bin chambers are drained directly into a sanitary line that is common to all other bin chambers within the same building. A possible explanation therefore is that rodents which find their way into the sanitary line can easily access all bin chambers in the same building. This suggests that preventing individual bin chamber access may reduce food availability to rodents which traverse the sanitary line in search of food sources.In the present study, we observed that rodent sightings were relatively higher in some months in the first half of the calendar year compared to the second half. Even though our estimates were positive, those for some months were not statistically significant. In Singapore, end-December, January to February are usually associated with increased food production due to the year-end (Christmas and New Year celebrations) and early-year (Chinese New Year) festivities. A proportionate increase in food waste over that period could improve survivability of rodents that leads to increased mating and reproduction. We therefore postulate that the higher seasonal rodent activity is plausible but recommend that future studies be conducted with sufficient longitude to examine the differences in the seasonal pattern across the three categories of premises more closely. A previous study in Harbin, China27 reported a seasonal pattern in the age composition of R. norvegicus while an ecological study on R. norvegicus in Salvador Brazil did not find any difference in the number of rats trapped between the dry and rainy seasons28. The inconsistent seasonal findings between studies could be due to the differences in the climate, degree of urbanization and environmental conditions of study locations.The relative rise in rodent activity in the first half of the year coupled with older estates being at greater risk of rodent activity suggest that municipal town councils which prioritize regular infrastructural repairs and improvements in older estates and complete them in the second half of each calendar year would help mitigate the anticipated rise in the first half of the new calendar year.In our study, we examined the relations between visual cues and rodent activity to help estate managers prioritise their control efforts. We found that rodent droppings were a common positive predictor of rodent activity across all three categories of waste collection premises. In particular, the odds of droppings in IRC bin chambers were the highest among the three categories of premises. We hypothesize that the probability of rodent dropping sightings was in part related to the accessibility of food waste and thus time spent by rodents within the respective waste collection premises. Each IRC chamber contains an open top bin that receives waste that is disposed down the IRC chamber chute. Food waste in IRC bin chambers are thus more easily accessed by rodents compared to in CRCs where waste is stored in a compactor and in bin centres where bulk bins are covered until the waste is compacted or collected.In Salvador, Brazil, the presence of Rattus norvegicus droppings were independently associated with an increased risk of Leptospira infection in humans29. Further research on site-specific Leptospira infection risks in Singapore are required to affirm the utility of droppings as an indicator for Leptospira infection risk. In addition, rub marks and gnaw marks were also positive predictors of rodent activity in CRCs and IRC bin chambers. A study in Chile reported that gnaw marks and holes, as well as grease or rub marks left behind by rodent travel were indicators of rodent activity30. A previous study carried out in an urban city in Taiwan reported that rodent droppings and rub marks were well correlated with rodent infestation31. Our findings, which were in support of these previous studies, suggest that estate managers can maximise the cost effectiveness of their resources by focusing their control efforts based on visual cues without relying solely on trapping activities for surveillance.We found a positive relationship between the number of rodent burrows and rodent activity in all three waste collection premises, though this was only significant for refuse bin centres. That the direction of effect for burrows was consistent these three premises, was a reassuring observation. It is possible that we did not have enough study power to establish the observed positive relations in CRCs and IRC bin chambers. Therefore future studies should seek to confirm our findings. R. norvegicus excavate extensive burrow systems that are able to house a large number of rats32. They exhibit a strong preference for creating burrows in loose soil and on sloping terrain33 and construct shallow burrows in close proximity to water bodies and food sources34. As rodent burrows are primarily used for nesting, food storage and harbourage purposes35, burrows can provide important information about the extent of rodent activity in an area and may be used as an indicator for estate managers to focus their investigations.A previous study in New York, United States found that the presence of numerous restaurants, or having older infrastructure were associated with increased levels of R. norvegicus22. Unexpectedly, we did not find any evidence that the number of dining establishments was associated with rodent activity. However, instances of rodent activity have been reported in food establishments in Singapore36,37,38. We hypothesize that rodent movement is restricted to the surrounding area of the food establishments due to the plethora of food available, with little reason for rodents to venture into waste collection premises. Future studies examining the relationship between rodent activity in food establishments and waste collection premises are required to confirm this.In our study, the presence of gnaw marks (aOR: 5.61), rub marks (aOR: 5.04) in CRCs and rodent droppings in CRCs (aOR: 6.20), IRC bin chambers (aOR: 90.84) and bin centres (aOR: 3.61) had the largest strengths of association with rodent activity. Comparatively, in a study in Johannesburg, South Africa, predictors such as dampness (aOR: 2.54) and cracks (aOR: 1.92) in homes had relatively smaller effects on rodent activity20, while a study in Salvador, Brazil found relatively larger effects of homes with dilapidated fences and walls (aOR: 8.95) and those built on earthen slopes (aOR: 4.95)21. This suggests that rodent activity can be strongly influenced by site- and setting-specific factors, and supports the body of evidence on the strong adaptability of rodents in our urban environment”.Urban environments have the capacity to alter the biology of the pathogens, hosts and vectors, which can influence disease transmission39. The proximate setting of dense urban environments allows for close contact between humans and synanthropic rodents, thereby increasing the transmission risk of zoonotic diseases4. In addition to causing diseases in human populations, urban rats are also known to compromise food safety, damage infrastructure and cause mental health distress25,40. The responsibility of rodent control in residential estates is important but may be one among many other competing public health and estate management responsibilities that municipal town councils have to undertake. Consequently, estate managers have to prioritize their limited resources in order to maximise the cost effectiveness of their resource allocation choices. Based on our study findings, we recommend that estate managers adopt a risk-based approach in vector control resource allocation in waste collection premises according to infrastructural age and visual cues for rodent activity.IRC bin chambers which are a distinct feature of the oldest residential buildings, were observed with a substantially higher odds of rodent activity compared to the other categories of waste collection premises. This suggests that rodent control resource allocation should be prioritized in older residential estates. The clear seasonal pattern of rodent activity in CRCs suggests that estate managers can increase their rodent control activities thereat in the first half of the year. Finally, easy access to food waste directly increases the probability of survival and consequently the rodent population size. Future research should examine the quality of municipal solid waste management and the waste processing flow in residential estates to determine how rodent access to food waste can be further minimized to reduce the population of rodents.Study strengths and limitationsWe analysed data from all public residential estates in Singapore; our findings are thus generalizable at the national level. The use of outcomes and independent measures from individual waste collection premises over multiple cycles of inspection provided stronger evidence for causal inferences. We analysed data over 12 months to account for within-year variations that could influence the outcome measure. Rodents were visually identified without molecular speciation because no trapping was carried out. Though the majority of rodents were observed to be Rattus norvegicus, which is the most common species of rodents in public housing estates in Singapore, we could not rule out misclassification of rodents. However, our findings remain relevant for municipal authorities seeking to prioritize resources for vector control in waste collection premises under their care. More

  • in

    Directional asymmetry in gonad length indicates moray eels (Teleostei, Anguilliformes, Muraenidae) are “right-gonadal”

    Graham, J. H., Raz, S., Hel-Or, H. & Nevo, E. Fluctuating asymmetry: Methods, theory, and applications. Symmetry 2(2), 466–540 (2010).ADS 
    MathSciNet 

    Google Scholar 
    Graham, J. H., Emlen, J. M., Freeman, D. C., Leamy, L. J. & Kieser, J. A. Directional asymmetry and the measurement of developmental instability. Biol. J. Lin. Soc. 64(1), 1–16 (1998).
    Google Scholar 
    Dongen, V., Lensm, L. & Molenberghs, G. Mixture analysis of asymmetry: Modelling directional asymmetry, antisymmetry and heterogeneity in fluctuating asymmetry. Ecol. Lett. 2(6), 387–396 (1999).
    Google Scholar 
    Palmer, A. R. Symmetry breaking and the evolution of development. Science 306(5697), 828–833 (2004).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Møller, A. P. Directional selection on directional asymmetry: Testes size and secondary sexual characters in birds. Proc. R. Soc. Lond. Ser. B Biol. Sci. 258(1352), 147–151 (1994).ADS 

    Google Scholar 
    Allenbach, D. M. Fluctuating asymmetry and exogenous stress in fishes: A review. Rev. Fish Biol. Fish. 21(3), 355–376 (2011).
    Google Scholar 
    Werner, Y. L., Rothenstein, D. & Sivan, N. Directional asymmetry in reptiles (Sauria: Gekkonidae: Ptyodactylus) and its possible evolutionary role, with implications for biometrical methodology. J. Zool. 225(4), 647–658 (1991).
    Google Scholar 
    Loehr, J. et al. Asymmetry in threespine stickleback lateral plates. J. Zool. 289(4), 279–284 (2013).
    Google Scholar 
    Bell, M. A., Khalef, V. & Travis, M. P. Directional asymmetry of pelvic vestiges in threespine stickleback. J. Exp. Zool. B Mol. Dev. Evol. 308(2), 189–199 (2007).PubMed 

    Google Scholar 
    Somarakis, S., Kostikas, I. & Tsimenides, N. Fluctuating asymmetry in the otoliths of larval fish as an indicator of condition: Conceptual and methodological aspects. J. Fish Biol. 51, 30–38 (1997).
    Google Scholar 
    Ratty, F. J., Laurs, R. M. & Kelly, R. M. Gonad morphology, histology, and spermatogenesis in South Pacific albacore tuna Thunnus alalunga (Scombridae). Fish. Bull. 88, 207–216 (1989).
    Google Scholar 
    Harrod, C. & Griffiths, D. Parasitism, space constraints, and gonad asymmetry in the pollan (Coregonus autumnalis). Can. J. Fish. Aquat. Sci. 62(12), 2796–2801 (2005).
    Google Scholar 
    Park, I. S., Zhang, C. I., Kim, Y. J. & Bang, I. C. Directional asymmetry of gonadal development in Ayu (Plecoglossus altivelis). Fish. Aquat. Sci. 8(4), 207–212 (2005).
    Google Scholar 
    Bernet, D., Wahli, T., Kueng, C. & Segner, H. Frequent and unexplained gonadal abnormalities in whitefish (central alpine Coregonus sp.) from an alpine oligotrophic lake in Switzerland. Dis. Aquat. Org. 61(1–2), 137–148 (2004).CAS 

    Google Scholar 
    Bittner, D. et al. How normal is abnormal? Discrimination between deformations and natural variation in gonad morphology of European whitefish Coregonus lavaretus. J. Fish Biol. 74(7), 1594–1614 (2009).CAS 
    PubMed 

    Google Scholar 
    Fricke, R., Eschmeyer, W. N. & R. van der Laan (eds) 2022. Eschmeyer’s Catalog of Fishes: Genera, Species, References. (http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp). Electronic version Accessed 31 12 2022).Chen, H. M., Shao, K. T. & Chen, C. T. A review of the muraenid eels (Family Muraenidae) from Taiwan with descriptions of twelve new records. Zool. Stud. 33(1), 44–64 (1994).
    Google Scholar 
    Chen, H. M., Loh, K. H. & Shao, K. T. A new species of moray eel, Gymnothorax taiwanensis (Anguilliformes: Muraenidae) from eastern Taiwan. Raffles Bull. Zool. 19, 131–134 (2008).
    Google Scholar 
    Loh, K. H., Shao, K. T. & Chen, H. M. Gymnothorax melanosomatus, a new moray eel (Teleostei: Anguilliformes: Muraenidae) from southeastern Taiwan. Zootaxa 3134(1), 43–52 (2011).
    Google Scholar 
    Loh, K. H., Shao, K. T., Ho, H. C., Lim, P. E. & Chen, H. M. A new species of moray eel (Anguilliformes: Muraenidae) from Taiwan, with comments on related elongate unpatterned species. Zootaxa 4060(1), 30–40 (2015).PubMed 

    Google Scholar 
    Huang, W. C., Mohapatra, A., Thu, P. T., Chen, H. M. & Liao, T. Y. A review of the genus Strophidon (Anguilliformes: Muraenidae), with description of a new species. J. Fish Biol. 97(5), 1462–1480 (2020).PubMed 

    Google Scholar 
    Huang, W. C., Smith, D. G., Loh, K. H. & Liao, T. Y. Two New Moray Eels of Genera Diaphenchelys and Gymnothorax (Anguilliformes: Muraenidae) from Taiwan and the Philippines. Zool. Stud. 60, e24 (2021).Matić-Skoko, S. et al. Mediterranean moray eel Muraena helena (Pisces: Muraenidae): biological indices for life history. Aquat. Biol. 13(3), 275–284 (2011).
    Google Scholar 
    Fishelson, L. Comparative gonad morphology and sexuality of the Muraenidae (Pisces, Teleostei). Copeia 1992, 197–209 (1992).Froese, R. & D. Pauly. Editors. 2022.FishBase. World Wide Web electronic publication. www.fishbase.org. Accessed March 2022.Almany, G. R. Differential effects of habitat complexity, predators and competitors on abundance of juvenile and adult coral reef fishes. Oecologia 141(1), 105–113 (2004).ADS 
    PubMed 

    Google Scholar 
    Hixon, M. A. & Beets, J. P. Predation, prey refuges, and the structure of coral-reef fish assemblages. Ecol. Monogr. 63(1), 77–101 (1993).
    Google Scholar 
    Muñoz, R. C. Evidence of natural predation on invasive lionfish, Pterois s, by the spotted moray eel, Gymnothorax moringa. Bull. Marine Sci. 93(3), 789–790 (2017).
    Google Scholar 
    Bos, A. R., Sanad, A. M. & Elsayed, K. Gymnothorax spp. (Muraenidae) as natural predators of the lionfish Pterois miles in its native biogeographical range. Environ. Biol. Fish. 100(6), 745–748 (2017).
    Google Scholar 
    Bshary, R., Hohner, A., Ait-el-Djoudi, K. & Fricke, H. Interspecific communicative and coordinated hunting between groupers and giant moray eels in the Red Sea. PLoS Biol. 4(12), e431 (2006).PubMed 
    PubMed Central 

    Google Scholar 
    Hedrick, B. P., Antalek-Schrag, P., Conith, A. J., Natanson, L. J. & Brennan, P. L. Variability and asymmetry in the shape of the spiny dogfish vagina revealed by 2D and 3D geometric morphometrics. J. Zool. 308(1), 16–27 (2019).
    Google Scholar 
    Winters, G. H. Fecundity of the left and right ovaries of Grand Bank capelin (Mallotus villosus). J. Fish. Board Can. 28(7), 1029–1033 (1971).
    Google Scholar 
    Huang, L.Y. Reproductive biology of Gymnothorax reticularis from the waters off northeastern Taiwan. Master Thesis, Department of Aquaculture, College of Life Sciences, National Taiwan Ocean University, Keelung, Taiwan (2008).Loh, K.H. Molecular phylogeny and reproductive biology of moray eels (Muraenidae) around Taiwan. Ph.D. Thesis, Department of Aquaculture, College of Life Sciences, National Taiwan Ocean University, Keelung, Taiwan (2009).Calhim, S. & Birkhead, T. R. Intraspecific variation in testis asymmetry in birds: evidence for naturally occurring compensation. Proc. R. Soc. B Biol. Sci. 276(1665), 2279–2284 (2009).
    Google Scholar 
    Palmer, A. R. What determines direction of asymmetry: Genes, environment or chance?. Philos. Trans. R. Soc. B Biol. Sci. 371(1710), 20150417 (2016).
    Google Scholar 
    Calhim, S. & Montgomerie, R. Testis asymmetry in birds: The influences of sexual and natural selection. J. Avian Biol. 46(2), 175–185 (2015).
    Google Scholar 
    Johnson, G. D. Revisions of anatomical descriptions of the pharyngeal jaw apparatus in moray eels of the family Muraenidae (Teleostei: Anguilliformes). Copeia 107(2), 341–357 (2019).MathSciNet 

    Google Scholar 
    Blackburn, D. G. Structure, function, and evolution of the oviducts of squamate reptiles, with special reference to viviparity and placentation. J. Exp. Zool. 282(4–5), 560–617 (1998).CAS 
    PubMed 

    Google Scholar 
    Guioli, S. et al. Gonadal asymmetry and sex determination in birds. Sex. Dev. 8(5), 227–242 (2014).CAS 
    PubMed 

    Google Scholar 
    Witschi, E. Origin of asymmetry in the reproductive system of birds. Am. J. Anat. 56(1), 119–141 (1935).
    Google Scholar 
    Ramirez-Llodra, E. et al. Deep, diverse and definitely different: Unique attributes of the world’s largest ecosystem. Biogeosciences 7(9), 2851–2899 (2010).ADS 

    Google Scholar 
    Calhim, S., Pruett-Jones, S., Webster, M. S. & Rowe, M. Asymmetries in reproductive anatomy: insights from promiscuous songbirds. Biol. J. Lin. Soc. 128(3), 569–582 (2019).
    Google Scholar 
    Quillet, E., Labbe, L. & Queau, I. Asymmetry in sexual development of gonads in intersex rainbow trout. J. Fish Biol. 64(4), 1147–1151 (2004).
    Google Scholar 
    Burnham, K. P. & Anderson, D. R. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach 2nd edn. (Springer, 2002).MATH 

    Google Scholar 
    R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ (2022).Lin, Y. J., Qurban, M. A., Shen, K. N. & Chao, N. L. Delimitation of Tiger-tooth croaker Otolithes species (Teleostei: Sciaenidae) from the Western Arabian Gulf using an integrative approach, with a description of Otolithes arabicus sp. nov. Zool. Stud. 58, 10 (2019).
    Google Scholar 
    Bodenhofer, U., Bonatesta, E., Horejs-Kainrath, C. & Hochreiter, S. msa: An R package for multiple sequence alignment. Bioinformatics 31(24), 3997–9999 (2015).CAS 
    PubMed 

    Google Scholar 
    Paradis, E. & Schliep, K. ape 5.0: An environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35, 526–528 (2019).CAS 
    PubMed 

    Google Scholar 
    Oksanen, J., Blanchet, F. G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P. R., O’Hara, R. B., Simpson, G. L., Solymos, P., Stevens, M. H. H., Szoecs E. & Wagner, H. vegan: Community Ecology Package. R package version 2.5–7. https://CRAN.R-project.org/package=vegan (2020).Clarke, K. R. & Warwick, R. M. A taxonomic distinctness index and its statistical properties. J. Appl. Ecol. 35(4), 523–531 (1998).
    Google Scholar 
    Murtagh, F. & Legendre, P. Ward’s hierarchical agglomerative clustering method: which algorithms implement Ward’s criterion?. J. Classif. 31(3), 274–295 (2014).MathSciNet 
    MATH 

    Google Scholar 
    Legendre, P. & Legendre, L. Numerical Ecology (Elsevier, 2012).MATH 

    Google Scholar  More

  • in

    Impacts of water hardness and road deicing salt on zooplankton survival and reproduction

    Herbert, E. R. et al. A global perspective on wetland salinization: Ecological consequences of a growing threat to freshwater wetlands. Ecosphere. https://doi.org/10.1890/es14-00534.1 (2015).Article 

    Google Scholar 
    Kelly, V. R. et al. Long-term sodium chloride retention in a rural watershed: Legacy effects of road salt on streamater concentration. Environ. Sci. Tech. 42, 410–415. https://doi.org/10.1021/es071391l (2008).Article 
    CAS 

    Google Scholar 
    Tiwari, A. & Rachlin, J. W. A review of road salt ecological impacts. Northeast. Nat. 25, 123–142. https://doi.org/10.1656/045.025.0110 (2018).Article 

    Google Scholar 
    Hintz, W. D. & Relyea, R. A. A review of the species, community, and ecosystem impacts of road salt salinisation in fresh waters. Freshwater Biol. 64, 1081–1097. https://doi.org/10.1111/fwb.13286 (2019).Article 

    Google Scholar 
    Dugan, H. A. et al. Salting our freshwater lakes. Proc. Natl. Acad. of Sci. U.S.A 114, 4453–4458. https://doi.org/10.1073/pnas.1620211114 (2017).Article 
    ADS 
    CAS 

    Google Scholar 
    Kaushal, S. S. et al. Increased salinization of fresh water in the northeastern United States. Proc. Natl. Acad. of Sci. U.S.A. 102, 13517–13520. https://doi.org/10.1073/pnas.0506414102 (2005).Article 
    ADS 
    CAS 

    Google Scholar 
    Kaushal, S. S. et al. Freshwater salinization syndrome: from emerging global problem to managing risks. Biogeochemistry 154, 255–292. https://doi.org/10.1007/s10533-021-00784-w (2021).Article 

    Google Scholar 
    Kaushal, S. S. et al. Freshwater salinization syndrome on a continental scale. Proc. Natl. Acad. of Sci. U.S.A. 115, E574–E583. https://doi.org/10.1073/pnas.1711234115 (2018).Article 
    CAS 

    Google Scholar 
    Hintz, W. D., Fay, L. & Relyea, R. A. Road salts, human safety, and the rising salinity of our fresh waters. Front. Ecol. Environ. 9, 22–30. https://doi.org/10.1002/fee.2433 (2022).Article 

    Google Scholar 
    Petranka, J. W. & Doyle, E. J. Effects of road salts on the composition of seasonal pond communities: Can the use of road salts enhance mosquito recruitment?. Aquat. Ecol. 44, 155–166. https://doi.org/10.1007/s10452-009-9286-z (2010).Article 
    CAS 

    Google Scholar 
    Petranka, J. W. & Francis, R. A. Effects of road salts on seasonal wetlands: Poor prey performance may compromise growth of predatory salamanders. Wetlands 33, 707–715. https://doi.org/10.1007/s13157-013-0428-7 (2013).Article 

    Google Scholar 
    Searle, C. L., Shaw, C. L., Hunsberger, K. K., Prado, M. & Duffy, M. A. Salinization decreases population densities of the freshwater crustacean Daphnia dentifera. Hydrobiologia 770, 165–172. https://doi.org/10.1007/s10750-015-2579-4 (2016).Article 
    CAS 

    Google Scholar 
    Hebert, M. P. et al. Lake salinization drives consistent losses of zooplankton abundance and diversity across coordinated mesocosm experiments. Limnol. Oceanogr. Let. https://doi.org/10.1002/lol2.10239 (2022).Article 

    Google Scholar 
    Collins, S. J. & Russell, R. W. Toxicity of road salt to nova scotia amphibians. Environ. Pollut. 157, 320–324. https://doi.org/10.1016/j.envpol.2008.06.032 (2009).Article 
    CAS 
    PubMed 

    Google Scholar 
    Milotic, D., Milotic, M. & Koprivnikar, J. Effects of road salt on larval amphibian susceptibility to parasitism through behavior and immunocompetence. Aquat. Toxicol. 189, 42–49. https://doi.org/10.1016/j.aquatox.2017.05.015 (2017).Article 
    CAS 
    PubMed 

    Google Scholar 
    Sanzo, D. & Hecnar, S. J. Effects of road de-icing salt (NaCl) on larval wood frogs (Rana sylvatica). Environ. Pollut. 140, 247–256. https://doi.org/10.1016/j.envpol.2005.07.013 (2006).Article 
    CAS 
    PubMed 

    Google Scholar 
    Arnott, S. E. et al. Road salt impacts freshwater zooplankton at concentrations below current water quality guidelines. Envir. Sci. Tech. 54, 9398–9407. https://doi.org/10.1021/acs.est.0c02396 (2020).Article 
    CAS 

    Google Scholar 
    Elphick, J. R. F., Bergh, K. D. & Bailey, H. C. Chronic toxicity of chloride to freshwater species effects of hardness and implications for water quality guidelines. Environ. Toxicol. Chem. 30, 239–246. https://doi.org/10.1002/etc.365 (2011).Article 
    CAS 
    PubMed 

    Google Scholar 
    Mount, D. R. et al. The acute toxicity of major ion salts to Ceriodaphnia dubia: I. Influence of background water chemistry. Environ. Toxicol. Chem. 35, 3039–3057. https://doi.org/10.1002/etc.3487 (2016).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Soucek, D. J. Comparison of hardness- and chloride-regulated acute effects of sodium sulfate on two freshwater crustaceans. Environ. Toxicol. Chem. 26, 773–779. https://doi.org/10.1897/06-229r.1 (2007).Article 
    CAS 
    PubMed 

    Google Scholar 
    Bhateria, R. & Jain, D. Water quality assessment of lake water: A review. Sustain. Wat. Res. Manag. 2, 161–173. https://doi.org/10.1007/s40899-015-0014-7 (2016).Article 

    Google Scholar 
    USGS. Hardness of Water. https://www.usgs.gov/special-topics/water-science-school/science/hardness-water#overview, Accessed: 1 August 2022 (2018).Brown, A. H. & Yan, N. D. Food quantity affects the sensitivity of Daphnia to Road Salt. Environ. Sci. Tech. 49, 4673–4680. https://doi.org/10.1021/es5061534 (2015).Article 
    CAS 

    Google Scholar 
    Smith, D. W. & Cooper, S. D. Competition among cladocera. Ecology 63, 1004–1015. https://doi.org/10.2307/1937240 (1982).Article 

    Google Scholar 
    Soucek, D. J. et al. Influence of water hardness and sulfate on the acute toxicity of chloride to sensitive freshwater invertebrates. Environ. Toxicol. Chem. 30, 930–938. https://doi.org/10.1002/etc.454 (2011).Article 
    CAS 
    PubMed 

    Google Scholar 
    Gust, K. A. et al. Daphnia magna’s sense of competition: Intra-specific interactions (ISI) alter life history strategies and increase metals toxicity. Ecotoxicology 25, 1126–1135. https://doi.org/10.1007/s10646-016-1667-1 (2016).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Liu, X. & Steiner, C. F. Ecotoxicology of salinity tolerance in Daphnia pulex: Interactive effects of clonal variation, salinity stress and predation. J. Plankton Res. 39, 687–697. https://doi.org/10.1093/plankt/fbx027 (2017).Article 
    CAS 

    Google Scholar 
    Evans, M. & Frick, C. The effects of road salts on aquatic ecosystems. Report No. 02-308, (Environment Canada – Water Science and Technology Directorate, 2001).USEPA. (U.S. Environmental Protection Agency, 1988).Schuler, M. S. et al. Regulations are needed to protect freshwater ecosystems from salinization. Phil. Trans. R. Soc. B. https://doi.org/10.1098/rstb.2018.0019 (2019).Article 

    Google Scholar 
    Canadian Council of Ministers for the Environment. Candadian water Quality Guidelines for the Protection of Aquatic Life: Chloride. (Environment Canada, Gatineau, Canada, 2011).Valleau, R. E., Paterson, A. M. & Smol, J. P. Effects of road-salt application on Cladocera assemblages in shallow precambrian shield lakes in south-central Ontario, Canada. Freshwat. Sci. 39, 824–836. https://doi.org/10.1086/711666 (2020).Article 

    Google Scholar 
    Hintz, W. D. et al. Current water quality guidelines across North America and Europe do not protect lakes from salinization. Proc. Natl. Acad. of Sci. U.S.A. https://doi.org/10.1073/pnas.2115033119 (2022).Article 

    Google Scholar 
    Valleau, R. E., Celis-Salgado, M. P., Arnott, S. E., Paterson, A. M. & Smol, J. P. Assessing the effect of salinization (NaCl) on the survival and reproduction of two ubiquitous cladocera species (Bosmina longirostris and Chydorus brevilabris). Wat. Air Soil Pollut. 233, 135. https://doi.org/10.1007/s11270-021-05482-9 (2022).Article 
    ADS 
    CAS 

    Google Scholar 
    Celis-Salgado, M. P., Cairns, A., Kim, N. & Yan, N. D. The FLAMES medium: A new, soft-water culture and bioassay medium for Cladocera. SIL Proc. 1922–2010(30), 265–271. https://doi.org/10.1080/03680770.2008.11902123 (2008).Article 

    Google Scholar 
    USEPA. Methods for measuring the acute toxicity of effluents and receiving waters to freshwater and marine organisms, 5th ed. Office of Water Washington, DC (2002).Hintz, W. D. et al. Concurrent improvement and deterioration of epilimnetic water quality in an oligotrophic lake over 37 years. Limnol. Oceanogr. 65, 927–938. https://doi.org/10.1002/lno.11359 (2020).Article 
    ADS 
    CAS 

    Google Scholar 
    Winner, R. W. Interactive effects of water hardness and humic acid on the chronic toxicity of cadmium to Daphnia pulex. Aquat. Toxicol. 8, 281–293. https://doi.org/10.1016/0166-445X(86)90080-9 (1986).Article 
    CAS 

    Google Scholar 
    Kaushal, S. S. et al. Novel “chemical cocktails” in inland waters are a consequence of the freshwater salinization syndrome. Phil. Trans. R. Soc. B. https://doi.org/10.1098/rstb.2018.0017 (2019).Article 

    Google Scholar 
    Kaushal, S. S. et al. Making “chemical cocktails”: Evolution of urban geochemical processes across the periodic table of elements. Appl. Geochem. https://doi.org/10.1016/j.apgeochem.2020.104632 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Cremona, F. et al. How warming and other stressors affect zooplankton abundance, biomass and community composition in shallow eutrophic lakes. Clim. Change 159, 565–580. https://doi.org/10.1007/s10584-020-02698-2 (2020).Article 
    ADS 
    CAS 

    Google Scholar 
    Lind, L. et al. Salty fertile lakes: How salinization and eutrophication alter the structure of freshwater communities. Ecosphere. https://doi.org/10.1002/ecs2.2383 (2018).Article 

    Google Scholar 
    Stoler, A. B. et al. Effects of a common insecticide on wetland communities with varying quality of leaf litter inputs. Environ. Pollut. 226, 452–462. https://doi.org/10.1016/j.envpol.2017.04.019 (2017).Article 
    CAS 
    PubMed 

    Google Scholar 
    Riessen, H. P. & Sprules, W. G. Demographic costs of antipredator defenses in Daphnia pulex. Ecology 71, 1536–1546. https://doi.org/10.2307/1938290 (1990).Article 

    Google Scholar  More