Ecology

1.Hubbell, S. The Unified Neutral Theory of Biodiversity and Biogeography (Princeton Univ. Press, 2001).2.Tilman, D. et al. Diversity and productivity in a long-term grassland experiment. Science 294, 843–845 (2001).CAS 
PubMed 
Article 

Google Scholar 
3.Hutchinson, G. E. The paradox of the plankton. Am. Nat. 95, 137–145 (1961).Article 

Google Scholar 
4.Koskella, B., Hall, L. J. & Metcalf, C. J. E. The microbiome beyond the horizon of ecological and evolutionary theory. Nat. Ecol. Evol. 1, 1606–1615 (2017).PubMed 
Article 

Google Scholar 
5.Flemming, H. C. & Wuertz, S. Bacteria and archaea on Earth and their abundance in biofilms. Nat. Rev. Microbiol. 17, 247–260 (2019).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
6.Hug, L. A. et al. A new view of the tree of life. Nat. Microbiol. 1, 16048 (2016).CAS 
PubMed 
Article 

Google Scholar 
7.Salazar, G. & Sunagawa, S. Marine microbial diversity. Curr. Biol. 27, R489–R494 (2017).CAS 
PubMed 
Article 

Google Scholar 
8.Huttenhower, C. et al. Structure, function and diversity of the healthy human microbiome. Nature 486, 207–214 (2012).CAS 
Article 

Google Scholar 
9.Falkowski, P. G., Fenchel, T. & Delong, E. F. The microbial engines that drive earth’s biogeochemical cycles. Science 320, 1034–1039 (2008).CAS 
PubMed 
Article 

Google Scholar 
10.Kau, A. L., Ahern, P. P., Griffin, N. W., Goodman, A. L. & Gordon, J. I. Human nutrition, the gut microbiome and the immune system. Nature 474, 327–336 (2011).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
11.Cavicchioli, R. et al. Scientists’ warning to humanity: microorganisms and climate change. Nat. Rev. Microbiol. 17, 569–586 (2019).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
12.Blasche, S. et al. Metabolic cooperation and spatiotemporal niche partitioning in a kefir microbial community. Nat. Microbiol. 6, 196–208 (2021).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
13.Gude, S. et al. Bacterial coexistence driven by motility and spatial competition. Nature 578, 588–592 (2020).CAS 
PubMed 
Article 

Google Scholar 
14.Kommineni, S. et al. Bacteriocin production augments niche competition by enterococci in the mammalian gastrointestinal tract. Nature 526, 719–722 (2015).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
15.Granato, E. T., Meiller-Legrand, T. A. & Foster, K. R. The evolution and ecology of bacterial warfare. Curr. Biol. 29, R521–R537 (2019).CAS 
PubMed 
Article 

Google Scholar 
16.Ratzke, C., Barrere, J. & Gore, J. Strength of species interactions determines biodiversity and stability in microbial communities. Nat. Ecol. Evol. 4, 376–383 (2020).PubMed 
Article 

Google Scholar 
17.Hoek, T. A. et al. Resource availability modulates the cooperative and competitive nature of a microbial cross-feeding mutualism. PLoS Biol. 14, e1002540 (2016).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
18.Goldford, J. E. et al. Emergent simplicity in microbial community assembly. Science 361, 469–474 (2018).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
19.Tilman, D. Resource Competition and Community Structure Vol. 17 (Princeton Univ. Press, 1982).20.Gause, G. F. The Struggle for Existence (Hafner Press, 1934).21.MacArthur, R. Species packing and competitive equilibrium for many species. Theor. Popul. Biol. 1, 1–11 (1970).CAS 
PubMed 
Article 

Google Scholar 
22.Levin, S. A. Community equilibria and stability, and an extension of the competitive exclusion principle. Am. Nat. 104, 413–423 (1970).Article 

Google Scholar 
23.Estrela, S. et al. Metabolic rules of microbial community assembly. Preprint at bioRxiv https://doi.org/10.1101/2020.03.09.984278 (2020).24.Enke, T. N. et al. Modular assembly of polysaccharide-degrading marine microbial communities. Curr. Biol. 29, 1528–1535 (2019).CAS 
PubMed 
Article 

Google Scholar 
25.Fu, H., Uchimiya, M., Gore, J. & Moran, M. A. Ecological drivers of bacterial community assembly in synthetic phycospheres. Proc. Natl Acad. Sci. USA 117, 3656–3662 (2020).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
26.Gralka, M., Szabo, R., Stocker, R. & Cordero, O. X. Trophic interactions and the drivers of microbial community assembly. Curr. Biol. 30, R1176–R1188 (2020).CAS 
PubMed 
Article 

Google Scholar 
27.Enke, T. N. et al. Modular assembly of polysaccharide-degrading marine microbial communities. Curr. Biol. 29, 1528–1535.e6 (2019).CAS 
PubMed 
Article 

Google Scholar 
28.Martiny, J. B. H., Jones, S. E., Lennon, J. T. & Martiny, A. C. Microbiomes in light of traits: a phylogenetic perspective. Science 350, aac9323 (2015).PubMed 
Article 
CAS 

Google Scholar 
29.Naylor, D. et al. Deconstructing the soil microbiome into reduced-complexity functional modules. mBio 11, e01349-20 (2020).PubMed 
PubMed Central 
Article 

Google Scholar 
30.MacArthur, R. H. Geographical Ecology. Patterns in the Distribution of Species (Harper & Row, 1972) .31.Kanehisa, M. & Goto, S. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28, 27–30 (2000).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
32.Caspi, R. et al. The MetaCyc database of metabolic pathways and enzymes. Nucleic Acids Res. 46, D633–D639 (2018).CAS 
PubMed 
Article 

Google Scholar 
33.Wang, T., Goyal, A., Dubinkina, V. & Maslov, S. Evidence for a multi-level trophic organization of the human gut microbiome. PLoS Comput. Biol. 15, e1007524 (2019).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
34.Goyal, A. & Maslov, S. Diversity, stability, and reproducibility in stochastically assembled microbial ecosystems. Phys. Rev. Lett. 120, 158102 (2018).CAS 
PubMed 
Article 

Google Scholar 
35.Marsland, R. et al. Available energy fluxes drive a transition in the diversity, stability, and functional structure of microbial communities. PLoS Comput. Biol. 15, e1006793 (2019).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
36.Levine, J. M. & HilleRisLambers, J. The importance of niches for the maintenance of species diversity. Nature 461, 254–257 (2009).CAS 
PubMed 
Article 

Google Scholar 
37.Tromas, N. et al. Niche separation increases with genetic distance among bloom-forming Cyanobacteria. Front. Microbiol. 9, 438 (2018).PubMed 
PubMed Central 
Article 

Google Scholar 
38.Sriswasdi, S., Yang, C. C. & Iwasaki, W. Generalist species drive microbial dispersion and evolution. Nat. Commun. 8, 1162 (2017).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
39.Logares, R. et al. Biogeography of bacterial communities exposed to progressive long-term environmental change. ISME J. 7, 937–948 (2013).CAS 
PubMed 
Article 

Google Scholar 
40.Monard, C., Gantner, S., Bertilsson, S., Hallin, S. & Stenlid, J. Habitat generalists and specialists in microbial communities across a terrestrial-freshwater gradient. Sci. Rep. 6, 37719 (2016).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
41.Székely, A. J. & Langenheder, S. The importance of species sorting differs between habitat generalists and specialists in bacterial communities. FEMS Microbiol. Ecol. 87, 102–112 (2014).PubMed 
Article 
CAS 

Google Scholar 
42.Pandit, S. N., Kolasa, J. & Cottenie, K. Contrasts between habitat generalists and specialists: an empirical extension to the basic metacommunity framework. Ecology 90, 2253–2262 (2009).PubMed 
Article 

Google Scholar 
43.Muscarella, M. E., Boot, C. M., Broeckling, C. D. & Lennon, J. T. Resource heterogeneity structures aquatic bacterial communities. ISME J. 13, 2183–2195 (2019).PubMed 
PubMed Central 
Article 

Google Scholar 
44.Roller, B. R. K., Stoddard, S. F. & Schmidt, T. M. Exploiting rRNA operon copy number to investigate bacterial reproductive strategies. Nat. Microbiol. 1, 16160 (2016).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
45.Goldfarb, K. C. et al. Differential growth responses of soil bacterial taxa to carbon substrates of varying chemical recalcitrance. Front. Microbiol. 2, 94 (2011).PubMed 
PubMed Central 
Article 

Google Scholar 
46.Klappenbach, J. A., Dunbar, J. M. & Schmidt, T. M. rRNA operon copy number reflects ecological strategies of bacteria. Appl. Environ. Microbiol. 66, 1328–1333 (2000).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
47.Rojo, F. Carbon catabolite repression in Pseudomonas: optimizing metabolic versatility and interactions with the environment. FEMS Microbiol. Rev. 34, 658–684 (2010).CAS 
PubMed 
Article 

Google Scholar 
48.Mills, C. G., Allen, R. J. & Blythe, R. A. Resource spectrum engineering by specialist species can shift the specialist-generalist balance. Theor. Ecol. 13, 149–163 (2020).Article 

Google Scholar 
49.Bajic, D. & Sanchez, A. The ecology and evolution of microbial metabolic strategies. Curr. Opin. Biotechnol. 62, 123–128 (2020).CAS 
PubMed 
Article 

Google Scholar 
50.Basan, M. et al. A universal trade-off between growth and lag in fluctuating environments. Nature 584, 470–474 (2020).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
51.Paczia, N. et al. Extensive exometabolome analysis reveals extended overflow metabolism in various microorganisms. Microb. Cell Fact. 11, 122 (2012).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
52.Pinu, F. R. et al. Metabolite secretion in microorganisms: the theory of metabolic overflow put to the test. Metabolomics 14, 43 (2018).PubMed 
Article 
CAS 

Google Scholar 
53.Douglas, A. E. The microbial exometabolome: ecological resource and architect of microbial communities. Phil. Trans. R. Soc. B 375, 20190250 (2020).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
54.Machado, D., Andrejev, S., Tramontano, M. & Patil, K. R. Fast automated reconstruction of genome-scale metabolic models for microbial species and communities. Nucleic Acids Res. 46, 7542–7553 (2018).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
55.Zelezniak, A. et al. Metabolic dependencies drive species co-occurrence in diverse microbial communities. Proc. Natl Acad. Sci. USA 112, 6449–6454 (2015).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
56.Diener, C., Gibbons, S. M. & Resendis-Antonio, O. MICOM: metagenome-scale modeling to infer metabolic interactions in the gut microbiota. mSystems 5, e00606-19 (2020).PubMed 
PubMed Central 
Article 

Google Scholar 
57.Garza, D. R., van Verk, M. C., Huynen, M. A. & Dutilh, B. E. Towards predicting the environmental metabolome from metagenomics with a mechanistic model. Nat. Microbiol. 3, 456–460 (2018).CAS 
PubMed 
Article 

Google Scholar 
58.Pacheco, A. R., Osborne, M. L. & Segrè, D. Non-additive microbial community responses to environmental complexity. Nat Commun. 12, 2365 (2021).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
59.Wang, X., Xia, K., Yang, X. & Tang, C. Growth strategy of microbes on mixed carbon sources. Nat. Commun. 10, 1279 (2019).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
60.Louca, S. et al. High taxonomic variability despite stable functional structure across microbial communities. Nat. Ecol. Evol. 1, 0015 (2017).Article 

Google Scholar 
61.Callahan, B. J. et al. DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583 (2016).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
62.Callahan, B. J., Sankaran, K., Fukuyama, J. A., McMurdie, P. J. & Holmes, S. P. Bioconductor workflow for microbiome data analysis: from raw reads to community analyses. F1000Research 5, 1492 (2016).PubMed 
PubMed Central 
Article 

Google Scholar 
63.Quast, C. et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596 (2013).CAS 
Article 

Google Scholar 
64.Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
65.R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2019).66.McMurdie, P. J. & Holmes, S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8, e61217 (2013).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
67.Chao, A. et al. Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecol. Monogr. 84, 45–67 (2014).Article 

Google Scholar 
68.Chao, A., Chiu, C. H. & Jost, L. Phylogenetic diversity measures based on Hill numbers. Phil. Trans. R. Soc. B 365, 3599–3609 (2010).PubMed 
PubMed Central 
Article 

Google Scholar 
69.Underwood, A. J. Experiments in Ecology (Cambridge Univ. Press, 1996); https://doi.org/10.1017/cbo978051180640770.Saeedghalati, M. et al. Quantitative comparison of abundance structures of generalized communities: from B-cell receptor repertoires to microbiomes. PLoS Comput. Biol. 13, e1005362 (2017).PubMed 
PubMed Central 
Article 

Google Scholar 
71.Goldford, J. E., Hartman, H., Smith, T. F. & Segrè, D. Remnants of an ancient metabolism without phosphate. Cell 168, 1126–1134.e9 (2017).CAS 
PubMed 
Article 

Google Scholar 
72.Raymond, J. & Segrè, D. The effect of oxygen on biochemical networks and the evolution of complex life. Science 311, 1764–1767 (2006).CAS 
PubMed 
Article 

Google Scholar 
73.Handorf, T., Ebenhoh, O. E. & Heinrich, R. Expanding metabolic networks: scopes of compounds, robustness, and evolution. J. Mol. Evol. 61, 498–512 (2005).CAS 
PubMed 
Article 

Google Scholar 
74.Ebenhoh, O., Handorf, T. & Heinrich, R. Structural analysis of expanding metabolic networks. Genome Inform. 15, 35–45 (2004).PubMed 

Google Scholar 
75.Orth, J. D., Thiele, I. & Palsson, B. O. What is flux balance analysis? Nat. Biotechnol. 28, 245–248 (2010).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
76.Johnson, M. et al. NCBI BLAST: a better web interface. Nucleic Acids Res. 36, 5–9 (2008).Article 
CAS 

Google Scholar 
77.Machado, D. et al. Polarization of microbial communities between competitive and cooperative metabolism. Nat. Ecol. Evol. 5, 195–203 (2021).PubMed 
PubMed Central 
Article 

Google Scholar 
78.Stoddard, S. F., Smith, B. J., Hein, R., Roller, B. R. K. & Schmidt, T. M. rrnDB: improved tools for interpreting rRNA gene abundance in bacteria and archaea and a new foundation for future development. Nucleic Acids Res. 43, D593–D598 (2015).CAS 
PubMed 
Article 

Google Scholar 
79.Douglas, G. M. et al. PICRUSt2: an improved and extensible approach for metagenome inference. Preprint at bioRxiv https://doi.org/10.1101/672295 (2019).80.Chen, T. & Guestrin, C. XGBoost: a scalable tree boosting system. In Proc. ACM SIGKDD International Conference on Knowledge Discovery and Data Mining 785–794 (Association for Computing Machinery, 2016).81.Hastie, T., Tibshirani, R. & Friedman, J. The Elements of Statistical Learning: Data Mining, Inference, and Prediction 2nd edn. (Springer Series in Statistics, Springer, 2009).82.Lundberg, S. M. et al. From local explanations to global understanding with explainable AI for trees. Nat. Mach. Intell. 2, 56–67 (2020).PubMed 
PubMed Central 
Article 

Google Scholar  More

1.Schipper, J. et al. The status of the world’s land and marine mammals: Diversity, threat, and knowledge. Science 322, 225–230 (2008).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
2.Cushman, S. A. Effects of habitat loss and fragmentation on amphibians: A review and prospectus. Biol. Conserv. 128, 231–240 (2006).Article 

Google Scholar 
3.Díaz, S. et al. Pervasive human-driven decline of life on Earth points to the need for transformative change. Science 366, 6471 (2019).Article 
CAS 

Google Scholar 
4.Geary, W. L., Nimmo, D. G., Doherty, T. S., Ritchie, E. G. & Tulloch, A. I. T. Threat webs: Reframing the co-occurrence and interactions of threats to biodiversity. J. Appl. Ecol. 56, 1992–1997 (2019).
Google Scholar 
5.Halpern, B. S. et al. A global map of human impact on marine ecosystems. Science 319, 948–952 (2008).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
6.Johnson, C. N. et al. Biodiversity losses and conservation responses in the Anthropocene. Science 356, 270–275 (2017).ADS 
CAS 
PubMed 
Article 

Google Scholar 
7.Di Prisco, G. et al. A mutualistic symbiosis between a parasitic mite and a pathogenic virus undermines honey bee immunity and Health. Proc. Natl. Acad. Sci. USA. 113, 3203–3208 (2016).ADS 
PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
8.Grant, E. H. C. et al. Identifying management-relevant research priorities for responding to disease-associated amphibian declines. Glob. Ecol. Conserv. 16, 00441 (2018).
Google Scholar 
9.Schindler, D. W. The cumulative effects of climate warming and other human stresses on Canadian freshwaters in the new millennium. Can. J. Fish. Aquat. Sci. 58, 18–29 (2001).Article 

Google Scholar 
10.Cumulative Effects in Wildlife Management: Impact Mitigation. https://doi.org/10.1017/CBO9781107415324.004 (CRC Press, 2011). 11.Frid, A. & Dill, L. Human-caused disturbance stimuli as a form of predation risk. Conserv. Ecol. 6, 11 (2002).
Google Scholar 
12.Rolland, R. M., Hunt, K. E., Kraus, S. D. & Wasser, S. K. Assessing reproductive status of right whales (Eubalaena glacialis) using fecal hormone metabolites. Gen. Comp. Endocrinol. 142, 308–317 (2005).CAS 
PubMed 
Article 

Google Scholar 
13.Sheriff, M. J., Dantzer, B., Delehanty, B., Palme, R. & Boonstra, R. Measuring stress in wildlife: Techniques for quantifying glucocorticoids. Oecologia 166, 869–887 (2011).ADS 
PubMed 
Article 

Google Scholar 
14.Crain, C. M., Kroeker, K. & Halpern, B. S. Interactive and cumulative effects of multiple human stressors in marine systems. Ecol. Lett. 11, 1304–1315 (2008).PubMed 
Article 

Google Scholar 
15.Beal, A., Rodriguez-Casariego, J., Rivera-Casas, C., Suarez-Ulloa, V. & Eirin-Lopez, J. M. Environmental epigenomics and its applications in marine organisms. in Population Genomics: Marine Organisms (eds. Oleksiak, M. F. & Rajora, O. P.) 325–359. https://doi.org/10.1007/13836_2018_28 (Springer, 2018). 16.Eirin-Lopez, J. M. & Putnam, H. M. Marine environmental epigenetics. Ann. Rev. Mar. Sci. 11, 335–368 (2019).PubMed 
Article 

Google Scholar 
17.Laird, P. W. The power and the promise of DNA methylation markers. Nat. Rev. Cancer 3, 253–266 (2003).CAS 
PubMed 
Article 

Google Scholar 
18.Bird, A. P. CpG-rich islands and the function of DNA methylation. Nature 321, 209–213 (1986).ADS 
CAS 
PubMed 
Article 

Google Scholar 
19.Cedar, H. & Bergman, Y. Linking DNA methylation and histone modification: patterns and paradigms. Nat. Rev. Genet. 10, 295–304 (2009).CAS 
PubMed 
Article 

Google Scholar 
20.Matosin, N., Cruceanu, C. & Binder, E. B. Preclinical and clinical evidence of DNA methylation changes in response to trauma and chronic stress. Chronic Stress 1, 247054701771076 (2017).Article 

Google Scholar 
21.Radtke, K. M. et al. Transgenerational impact of intimate partner violence on methylation in the promoter of the glucocorticoid receptor. Transl. Psychiatry 1, e21–e26 (2011).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
22.Mueller, B. R. & Bale, T. L. Sex-specific programming of offspring emotionality after stress early in pregnancy. J. Neurosci. 28, 9055–9065 (2008).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
23.Elliott, E., Ezra-Nevo, G., Regev, L., Neufeld-Cohen, A. & Chen, A. Resilience to social stress coincides with functional DNA methylation of the Crf gene in adult mice. Nat. Neurosci. 13, 1351–1353 (2010).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
24.Boersma, G. J. et al. Prenatal stress decreases Bdnf expression and increases methylation of Bdnf exon IV in rats. Epigenetics 9, 437–447 (2013).PubMed 
PubMed Central 
Article 

Google Scholar 
25.Turecki, G. & Meaney, M. J. Effects of the social environment and stress on glucocorticoid receptor gene methylation: A systematic review. Biol. Psychiatry 79, 87–96 (2016).CAS 
PubMed 
Article 

Google Scholar 
26.Sterrenburg, L. et al. Chronic stress induces sex-specific alterations in methylation and expression of corticotropin-releasing factor gene in the rat. PLoS ONE 6, 1–14 (2011).Article 
CAS 

Google Scholar 
27.Reeder, D. A. M. & Kramer, K. M. Stress in free-ranging mammals: Integrating physiology, ecology, and natural history. J. Mammal. 86, 225–235 (2005).Article 

Google Scholar 
28.Jeanneteau, F. D. et al. BDNF and glucocorticoids regulate corticotrophin-releasing hormone (CRH) homeostasis in the hypothalamus. Proc. Natl. Acad. Sci. USA. 109, 1305–1310 (2012).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
29.Smith, S. M. & Vale, W. W. The role of the hypothalamic-pituitary-adrenal axis in neuroendocrine responses to stress. Dialogues Clin. Neurosci. 8, 383–395 (2006).PubMed 
PubMed Central 
Article 

Google Scholar 
30.Turner, J. D. & Muller, C. P. Structure of the glucocorticoid receptor (NR3C1) gene 5′ untranslated region: Identification, and tissue distribution of multiple new human exon 1. J. Mol. Endocrinol. 35, 283–292 (2005).CAS 
PubMed 
Article 

Google Scholar 
31.Bakusic, J., Schaufeli, W., Claes, S. & Godderis, L. Stress, burnout and depression: A systematic review on DNA methylation mechanisms. J. Psychosom. Res. 92, 34–44 (2017).PubMed 
Article 

Google Scholar 
32.Center for Whale Research. Population. https://www.whaleresearch.com. Accessed 11 Jan 2021 (2020).33.Fisheries and Oceans Canada. Recovery Strategy for the Northern and Southern Resident Killer Whales (Orcinus orca) in Canada [Proposed]. Species at Risk Act Recovery Strategy Series, Fisheries & Oceans Canada, Ottawa, x + 84 pp.(2018).34.DFO. Population Status Update for the Northern Resident Killer Whale (Orcinus orca) in 2018. DFO Can. Sci. Advis. Sec. Sci. Resp. 2019/025. (2019).35.Bigg, M. A., Olesiuk, P. F., Ellis, G. M., Ford, J. K. B. & Balcomb, K. C. Social organization and genealogy of resident killer whales (Orcinus orca) in the coastal waters of British Columbia and Washington State. Reports Int. Whal. Comm. 12, 383–405 (1990).
Google Scholar 
36.Ford, J. K. B. & Ellis, G. M. Selective foraging by fish-eating killer whales Orcinus orca in British Columbia. Mar. Ecol. Prog. Ser. 316, 185–199 (2006).ADS 
Article 

Google Scholar 
37.Chen, I.-H. et al. Selection of reference genes for RT-qPCR studies in blood of beluga whales (Delphinapterus leucas). PeerJ 4, e1810 (2016).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
38.Horvath, S. & Raj, K. DNA methylation-based biomarkers and the epigenetic clock theory of ageing. Nat. Rev. Genet. 19, 371–384 (2018).CAS 
PubMed 
Article 

Google Scholar 
39.Hoelzel, A. R., Dahlheim, M. E. & Stern, S. J. Low genetic variation among killer whales (Orcinus orca) in the eastern north Pacific and genetic differentiation between foraging specialists. J. Hered. 89, 121–128 (1998).CAS 
PubMed 
Article 

Google Scholar 
40.Yao, M., Stenzel-Poore, M. & Denver, R. J. Structural and functional conservation of vertebrate corticotropin- releasing factor genes: Evidence for a critical role for a conserved cyclic AMP response element. Endocrinology 148, 2518–2531 (2007).CAS 
PubMed 
Article 

Google Scholar 
41.Aguiniga, L. M., Yang, W., Yaggie, R. E., Schaeffer, A. J. & Klumpp, D. J. Acyloxyacyl hydrolase modulates depressive-like behaviors through aryl hydrocarbon receptor. Am. J. Physiol. Regul. Integr. Comp. Physiol. 317, R289–R300 (2019).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
42.Hankinson, O. The aryl hydrocarbon receptor complex. Annu. Rev. Pharmacol. Toxicol. 35, 307–340 (1995).CAS 
PubMed 
Article 

Google Scholar 
43.Lundin, J. I. et al. Pre-oil spill baseline profiling for contaminants in Southern Resident killer whale fecal samples indicates possible exposure to vessel exhaust. Mar. Pollut. Bull. 136, 448–453 (2018).CAS 
PubMed 
Article 

Google Scholar 
44.MacDonald, L. H. Evaluating and managing cumulative effects: Process and constraints. Environ. Manag. 26, 299–315 (2000).CAS 
Article 

Google Scholar 
45.National Academies of Sciences Engineering and Medicine. Approaches to Understanding the Cumulative Effects of Stressors on Marine Mammals. https://doi.org/10.17226/23479 (National Academies Press, 2017). 46.Barrett-Lennard, L. G., Smith, T. G. & Ellis, G. M. A cetacean biopsy system using lightweight pneumatic darts, and its effect on the behavior of killer whales. Mar. Mammal Sci. 12, 14–27 (1996).Article 

Google Scholar 
47.Sambrook, J., Fritsch, E. F. & Maniatis, H. Molecular Cloning: A Laboratory Manual (Cold Springs Harbor Laboratory Press, 1989).
Google Scholar 
48.Illumina. 16S Metagenomic Sequencing Library Preparation. Illumina.com 1–28 (2013).49.Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.j 17, 10–12 (2011).Article 

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

Google Scholar 
51.Magoč, T. & Salzberg, S. L. FLASH: Fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27, 2957–2963 (2011).PubMed 
PubMed Central 
Article 
CAS 

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

Google Scholar 
53.Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar  More

1.Arnold, M. L. Natural Hybridization and Evolution (Oxford University Press, 1997).
Google Scholar 
2.Stelkens, R. & Seehausen, O. Genetic distance between species predicts novel trait expression in their hybrids. Evolution 63, 884–897 (2009).PubMed 
Article 
PubMed Central 

Google Scholar 
3.Grant, P. R. & Grant, B. R. Hybridization of bird species. Science 256, 193–197 (1992).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
4.Saino, N. & Villa, S. Pair composition and reproductive success across a hybrid zone of carrion crows and hooded crows. Auk 109, 543–555 (1992).
Google Scholar 
5.Good, T. P., Ellis, J. C., Annett, C. A. & Pierotti, R. Bounded hybrid superiority in an avian hybrid zone: effects of mate, diet, and habitat choice. Evolution 54, 1774–1783 (2000).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
6.Bartley, D. M., Rana, K. & Immink, A. J. The use of inter-specific hybrids in aquaculture and fisheries. Rev. Fish Biol. Fisher. 10, 325–337 (2001).Article 

Google Scholar 
7.Rosenfield, J. A., Nolasco, S., Lindauer, S., Sandoval, C. & Kodric-Brown, A. The role of hybrid vigor in the replacement of Pecos pupfish by its hybrids with sheepshead minnow. Conserv. Biol. 18, 1589–1598 (2004).Article 

Google Scholar 
8.Sun, Y. et al. Comparative transcriptomic study of muscle provides new insights into the growth superiority of a novel grouper hybrid. PLoS ONE 11, e0168802 (2016).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
9.Scribner, K. T., Page, K. S. & Bartron, M. L. Hybridization in freshwater fishes: A review of case studies and cytonuclear methods of biological inference. Rev. Fish Biol. Fisher. 10, 293–323 (2001).Article 

Google Scholar 
10.Ottová, E. et al. Evolution and trans-species polymorphism of MHC class IIB genes in cyprinid fish. Fish Shellfish Immun. 18, 199–222 (2005).Article 
CAS 

Google Scholar 
11.Šimková, A. et al. Does invasive Chondrostoma nasus shift the parasite community structure of endemic Parachondrostoma toxostoma in sympatric zones?. Parasite. Vector. 5, 200 (2012).Article 

Google Scholar 
12.Klein, J. & OhUigin, C. MHC polymorphism and parasites. Philos. Trans. R. Soc. Lond. B Biol. Sci. 346, 351–358 (1994).ADS 
CAS 
PubMed 
Article 

Google Scholar 
13.Klein, J., Klein, D., Figueroa, F., OhUigin, C. & Sato, A. Major histocompatibility complex genes in the study of fish phylogeny. In Molecular Systematic of Fishes (eds Kocher, T. D. & Stepien, C. A.) 271–283 (Academic Press, 1997).Chapter 

Google Scholar 
14.Hughes, A. L. & Nei, M. Nucleotide substitution at major histocompatibility complex class II loci: Evidence for overdominant selection. Proc. Nat. Acad. Sci. USA 56, 958–962 (1989).ADS 
Article 

Google Scholar 
15.Klein, J. & OhUigin, C. Composite origin of major histocompatibility complex genes. Curr. Opin. Genet. Dev. 3, 923–930 (1993).CAS 
PubMed 
Article 

Google Scholar 
16.Hughes, A. L. & Nei, M. Models of host-parasite interactions and MHC polymorphism. Genetics 132, 863–864 (1992).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
17.Klein, J. Of HLA, tryps, and selection? An essay on coevolution of MHC and parasites. Hum. Immunol. 30, 247–258 (1991).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
18.Hughes, A. L., Hughes, M. K., Howell, C. Y. & Nei, M. Natural selection at the class II major histocompatibility complex loci of mammals. Philos. Trans. R. Soc. Lond. B Biol. Sci. 346, 359–367 (1994).ADS 
CAS 
Article 

Google Scholar 
19.Hedrick, P. W. Pathogen resistence and genetic variation at MHC loci. Evolution 56, 1902–1908 (2002).PubMed 
Article 
PubMed Central 

Google Scholar 
20.Nowak, M. A., Tarczy-Hornoch, K. & Austyn, J. M. The optimal number of major histocompatibility complex molecules in an individual. Proc. Nat. Acad. Sci. U.S.A. 89, 10896–10899 (1992).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
21.Wegner, K. M., Reusch, T. B. H. & Kalbe, M. Multiple parasites are driving major histocompatibility complex polymorphism in the wild. J. Evol. Biol. 16, 224–232 (2003).CAS 
PubMed 
Article 

Google Scholar 
22.Eizaguirre, C., Lenz, T. L., Traulsen, A. & Milinski, M. Speciation accelerated and stabilized by pleiotropic major histocompatibility complex immunogenes. Ecol. Lett. 12, 5–12 (2009).PubMed 
Article 

Google Scholar 
23.Nadachowska-Brzyska, K., Zielinski, P., Radwan, J. & Babiks, W. Interspecific hybridization increases MHC class II diversity in two sister species of newts. Mol. Ecol. 21, 887–906 (2012).CAS 
PubMed 
Article 

Google Scholar 
24.Wegner, K. M. & Eizaguirre, C. New(t)s and views from hybridizing MHC genes: Introgression rather than trans-species polymorphism may shape allelic repertoires. Mol. Ecol. 21, 779–781 (2012).CAS 
PubMed 
Article 

Google Scholar 
25.Dudek, K., Gaczorek, T. S., Zielinski, P. & Babik, W. Massive introgression of major histocompatibility complex (MHC) genes in newt hybrid zones. Mol. Ecol. 28, 4798–4810 (2019).CAS 
PubMed 
Article 

Google Scholar 
26.Šimková, A., Civáňová, K., Gettová, L. & Gilles, A. Genomic porosity between invasive Chondrostoma nasus and endangered endemic Parachondrostoma toxostoma (Cyprinidae): The evolution of MHC IIB genes. PLoS ONE 8, e65883 (2013).ADS 
PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
27.Zhang, S., Wang, Z. & Wang, H. Maternal immunity in fish. Dev. Comp. Immunol. 39, 72–78 (2013).ADS 
PubMed 
Article 
CAS 

Google Scholar 
28.Šimková, A., Vojtek, L., Halačka, K., Hyršl, P. & Vetešník, L. The effect of hybridization on fish physiology, immunity and blood biochemistry: A case study in hybridizing Cyprinus carpio and Carassius gibelio (Cyprinidae). Aquaculture 435, 381–389 (2015).Article 
CAS 

Google Scholar 
29.Cowx, I. G. The biology of bream, Abramis brama (L), and its natural hybrid with roach, Rutilus rutilus (L), in the River Exe. J. Fish Biol. 22, 631–646 (1983).Article 

Google Scholar 
30.Economidis, P. S. & Wheeler, A. Hybrids of Abramis brama with Scardinius erythrophthalmus and Rutilus rutilus from Lake Volvi, Macedonia, Greece. J. Fish Biol. 35, 295–299 (1989).Article 

Google Scholar 
31.Toscano, B. J. et al. An ecomorphological framework for the coexistence of two cyprinid fish and their hybrids in a novel environment. Biol. J. Linn. Soc. 99, 768–783 (2010).Article 

Google Scholar 
32.Hayden, B. et al. Hybridisation between two cyprinid fishes in a novel habitat: Genetics, morphology and life-history traits. BMC Evol. Biol. 10, 169 (2010).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
33.Kuparinen, A., Vinni, M., Teacher, A. G. F., Kähkönen, K. & Merilä, J. Mechanism of hybridization between bream Abramis brama and roach Rutilus rutilus in their native range. J. Fish Biol. 84, 237–242 (2014).CAS 
PubMed 
Article 

Google Scholar 
34.Konopinski, M. K. & Amirowicz, A. Genetic composition of a population of natural common bream Abramis brama x roach Rutilus rutilus hybrids and their morphological characteristics in comparison with parent species. J. Fish Biol. 92, 365–385 (2018).CAS 
PubMed 
Article 

Google Scholar 
35.Krasnovyd, V., Vetešník, L., Gettová, L., Civáňová, K. & Šimková, A. Patterns of parasite distribution in the hybrids of non-congeneric cyprinid fish species: Is asymmetry in parasite infection the result of limited coadaptation?. Int. J. Parasitol. 47, 471–483 (2017).PubMed 
Article 
PubMed Central 

Google Scholar 
36.Hayden, B. et al. Trophic dynamics within a hybrid zone—interactions between an abundant cyprinid hybrid and sympatric parental species. Freshwater Biol. 56, 1723–1735 (2011).Article 

Google Scholar 
37.Nzau Matondo, B. et al. Hybridization success of three common European cyprinid species, Rutilus rutilus, Blicca bjoerkna and Abramis brama and larval resistance to stress tests. Fish. Sci. 73, 1137–1146 (2007).Article 
CAS 

Google Scholar 
38.Hayden, B., McLoone, P., Coyne, J. & Caffrey, J. M. Extensive hybridization between roach, Rutilus rutilus L., and common bream, Abramis brama L. Irish lakes and rivers. Biol. Environ. 114B, 35–39 (2014).
Google Scholar 
39.Eizaguirre, C. et al. Parasite diversity, patterns of MHC II variation and olfactory based mate choice in diverging threespined stickleback ecotypes. Evol. Ecol. 25, 605–622 (2011).Article 

Google Scholar 
40.Hubbs, C. L. Hybridization between fish species in nature. Syst. Zool. 4, 1–20 (1955).Article 

Google Scholar 
41.Rauch, G., Kalbe, M. & Reusch, T. B. H. Relative importance of MHC and genetic background for parasite load in a field experiment. Evol. Ecol. Res. 8, 373–386 (2006).
Google Scholar 
42.Eizaguirre, C., Lenz, T. L., Kalbe, M. & Milinski, M. Divergent selection on locally adapted major histocompatibility complex immune genes experimentally proven in the field. Ecol. Lett. 15, 723–731 (2012).PubMed 
PubMed Central 
Article 

Google Scholar 
43.Šimková, A., Dávidová, M., Papoušek, I. & Vetešník, L. Does interspecies hybridization affect the host specificity of parasites in cyprinid fish?. Parasite. Vector. 6, 95 (2013).Article 

Google Scholar 
44.Seifertová, M., Jarkovský, J. & Šimková, A. Does the parasite-mediated selection drive the MHC class IIB diversity in wild populations of European chub (Squalius cephalus)?. Parasitol. Res. 115, 1401–1415 (2016).PubMed 
Article 
PubMed Central 

Google Scholar 
45.Nzau Matondo, B., Ovidio, M., Philippart, J. C. & Poncin, P. Reproductive behaviour and sexual production in the first-generation hybrids of roach Rutilus rutilus L. × common bream Abramis brama L. J. Appl. Ichthyol. 27, 859–867 (2011).Article 

Google Scholar 
46.Graser, R., OhUigin, C., Vincek, V., Meyer, A. & Klein, J. Trans-species polymorphism of class II Mhc loci in danio fishes. Immunogenetics 44, 36–48 (1996).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
47.Figueroa, F. et al. MHC class IIB gene evolution in East African cichlid fishes. Immunogenetics 51, 556–575 (2000).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
48.Migalska, M., Sebastian, A. & Radwan, J. Major histocompatibility complex class I diversity limits the repertoire of T cell
receptors.Proc. Natl. Acad. Sci. USA 116, 5021–5026 (2019).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
49.Šimková, A., Košař, M., Vetešník, L. & Vyskočilová, M. MHC genes and parasitism in Carassius gibelio, a diploid-triploid fish species with dual reproduction strategies. BMC Evol. Biol. 13, 122 (2013).PubMed 
PubMed Central 
Article 

Google Scholar 
50.Borghans, J. A. M., Beltman, J. B. & De Boer, J. B. MHC polymorphism under host-pathogen coevolution. Immunogenetics 55, 732–739 (2004).CAS 
PubMed 
Article 

Google Scholar 
51.Ejsmond, M. J. & Radwan, J. Red queen processes drive positive selection on major histocompatibility complex (MHC) genes. PLoS Comput. Biol. 11, e1004627 (2015).ADS 
PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
52.Phillips, K. P. et al. Immunogenetic novelty confers a selective advantage in host-pathogen coevolution. Proc. Natl. Acad. Sci. USA 115, 1552–1557 (2018).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
53.Gaigher, A., Burri, R., San-Jose, L. M., Roulin, A. & Fumagalli, L. Lack of statistical power as a major limitation in understanding MHC-mediated immunocompetence in wild vertebrate populations. Mol. Ecol. 28, 5115–5132 (2019).PubMed 
Article 

Google Scholar 
54.Šimková, A., Ottová, E. & Morand, S. MHC variability, life-traits and parasite diversity of European cyprinid fish. Evol. Ecol. 20, 465–477 (2006).Article 

Google Scholar 
55.Clarke, B. & Kirby, D. R. S. Maintenance of histocompatibility polymorphisms. Nature 211, 999–1000 (1966).ADS 
CAS 
PubMed 
Article 

Google Scholar 
56.Meglécz, E. et al. SESAME (SEquence Sorter & AMplicon Explorer): Genotyping based on high throughput multiplex amplicon sequencing. Bioinformatics 27, 277–278 (2011).PubMed 
Article 
CAS 

Google Scholar 
57.Zagalska-Neubauer, M. et al. 454 sequencing reveals extreme complexity of the class II major histocompatibility complex in the collared flycatcher. BMC Evol. Biol. 10, 395 (2010).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
58.Van Erp, S. H. M., Egberts, E. & Stet, R. J. M. Characterization of class II A and B genes in a gynogenetic carp clone. Immunogenetics 44, 192–202 (1996).PubMed 
Article 

Google Scholar 
59.Šimková, A. Major histocompatibility complex genes and parasites in cyprinid fish. Vie Milieu 67, 139–148 (2017).
Google Scholar 
60.Klein, J. et al. Nomenclature for the major histocompatibility complexes of different species: A proposal. Immunogenetics 31, 217–219 (1990).CAS 
PubMed 
PubMed Central 

Google Scholar 
61.Dixon, B., Nagelkerke, L. A. J., Sibbing, F. A., Egberts, E. & Stet, R. J. M. Evolution of MHC class II beta chain-encoding genes in the Lake Tana barbel species flock (Barbus intermedius complex). Immunogenetics 44, 419–431 (1996).CAS 
PubMed 

Google Scholar 
62.Rakus, K. L. et al. Major histocompatibility (MH) class IIB gene polymorphism influences disease resistance of common carp (Cyprinus carpio L). Aquaculture 288, 44–50 (2009).CAS 
Article 

Google Scholar 
63.Seifertová, M. & Šimková, A. Structure, diversity and evolutionary patterns of expressed MHC class IIB genes in chub (Squalius cephalus), a cyprinid fish species from Europe. Immunogenetics 63, 167–181 (2011).PubMed 
Article 

Google Scholar 
64.Ronquist, F. et al. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across large model space. Syst. Biol. 61, 539–542 (2012).PubMed 
PubMed Central 
Article 

Google Scholar 
65.Darriba, D., Taboala, G. L., Doallo, R. & Posada, D. J. ModelTest2: More models, new heuristics and parallel computing. Nat. Methods 9, 772 (2012).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
66.Yang, Z. H. PAML4: Phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586–1591 (2007).CAS 
PubMed 
Article 

Google Scholar 
67.Doledec, S. & Chessel, D. Co-inertia analysis—an alternative method for studying species environment relationships. Freshwater Biol. 31, 277–294 (1994).Article 

Google Scholar 
68.Dray, S., Chessel, D. & Thioulouse, J. Co-inertia analysis and the linking of ecological data tables. Ecology 84, 3078–3089 (2003).Article 

Google Scholar 
69.Deter, J. et al. Association between the DQA MHC class II gene and puumala virus infection in Myodes glareolus, the bank vole. Infect. Genet. Evol. 8, 450–458 (2008).CAS 
PubMed 
Article 

Google Scholar 
70.Evans, M. L. & Neff, B. D. Major histocompatibility complex heterozygote advantage and widespread bacterial infections in populations of Chinook salmon (Oncorhynchus tshawytscha). Mol. Ecol. 18, 4716–4729 (2009).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
71.Zuur, A. et al. Mixed Effects Models and Extensions in Ecology With R (Springer, 2009).MATH 
Book 

Google Scholar 
72.Burnham, K. P. & Anderson, D. R. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach 2nd edn. (Springer, 2002).MATH 

Google Scholar 
73.R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/(2018).74.Bates, D., Maechler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).Article 

Google Scholar 
75.Bartoń, K. MuMIn: Multi-Model Inference. R package version 1.15.1. http://CRAN.R-project.org/package=MuMIn (2018).76.Thioulouse, J. & Dray, S. Interactive multivariate data analysis in R with the ade4 and ade4tkgui packages. J. Stat. Softw. 22, 1–14 (2007).Article 

Google Scholar  More

The location, diameter, height and circumference of the coral were measured (Table 1, Fig. 2). The Porites was brown to cream in colour and hemispherical in shape (Fig. 2). It was identified as either Porites lutea (Hump or Pore coral) or P. lobata (Lobe coral)14.The primary habitat on the Porites was live coral (70%), followed by sponge, live coral rock and a small amount of macroalgae (Table 2). No recently dead coral, coral rubble or sand was recorded (Table 2). We observed competition between the Porites and other species of coral and invertebrate including encrusting sponge, plating and branching Acropora spp., Montipora, Chlorodesmis, soft coral and zoanthids (Table 2, Figs. 3, 4).Table 2 Reef Health Impact Survey (RHIS) of habitat and species categories on Porites sp.Full size tableFigure 3Detail of the sub-habitats and competitive interactions Porites sp. and boring sponge Cliona viridis (left) and live coral Porites sp. and Montipora sp. (right) along interspecific contact zones.Full size imageFigure 4Detail of Reef Health Impact Survey (RHIS) of Porites.Full size imageThe boring sponge, Cliona viridis, is abundant on the Great Barrier Reef15. It is a common bioeroding species advancing laterally at around 1 cm and to a depth of 1.2 cm per annum15. Abundance of Cliona viridis is often correlated to substrate availability and water energy with the greatest abundance often on the windward side of bommies15. This correlates to our observations as the large proportion of the substrate estimated to cover the bommie (15%) was on the windward side. The sponge’s advances will likely continue to compromise the colony size and health.We recorded marine debris at the base of the Porites. The debris was 2–3 m of rope that appeared to have been wrapped around the base of an adjacent coral. Adjacent to the bommie were three concrete blocks.How big is the Porites coral at Goolboodi compared to other big corals in the GBR, and the world? Potts et al.6 reported a very large, rounded Porites colony, 6.9 m in diameter which is 3.1 m smaller than this study. Lough et al.16 reported coral cores from colonies between 1.6–8.0 m in height with the largest corals of 6.0 m at Havannah, North Molle and Masthead Islands, 7.5 m at Abraham Reef and 8.0 m at Sanctuary Reef. Recognising the limitations of published data, the Porites coral at Goolboodi is the largest diameter coral that has been measured, and the 6th tallest in the GBR. It is unknown if the other corals are still alive or dead.Other comparatively large massive Porites have previously been located throughout the Pacific. These have included multiple bommies measuring more than 10 m4 and one exceptionally large colony observed measuring 17 m × 12 m in American Samoa17. Additionally, large Porites sp. bommies have been observed at Green Island, 30 km east of Taiwan18 as well as an 11 m diameter Porites australiensis at Sesoko Island, Okinawa, Japan19.How old is this massive Porites? In discussions with the Australian Institute of Marine Science (AIMS), there is a robust, linear relationship ( > 80% variance explained) between Porites average linear extension rate and average annual sea surface temperature (SST)20,21 that provides an estimate of colony age from its height. Using average annual SST at 18.5S, 146.5E of 26.12C (from HadiSST data set), the estimated linear extension rate is determined by (2.97 × 26.12) − 65.46 = 1.21 cm/year. Given the colony height of 5.1–5.3 m, this gives an estimated age of 421–438 years. This is well before European exploration and settlement of Australia. AIMS has investigated over 328 colonies of massive Porites corals from 69 reefs along the GBR and has aged them as being from 10–436 years21. AIMS has not investigated this coral (pers. comm Neal Cantin). Based on limitations of published data, the Porites coral at Goolboodi is one of the oldest corals on the GBR.Why is the Porites partially dead on top and living on the side? The proportion of live coral tissue on a colony reflects the cumulative, integrated effect of both beneficial and adverse environmental factors. Substantial portions of coral tissue can die from exposure to sun at low tides or warm water without lethal consequences to the colony as a whole10. Partial mortality of large bommies provides available real estate for opportunistic, fast growing sessile organisms. In this instance, multiple species of tabulate and branching Acropora sp., encrusting Montipora sp. and encrusting sponges are among the benthic organisms to have colonised 30% of the coral bommies’ surface area. Intraspecific competition is also evident from the skeletal barriers created along contact zones22 (Fig. 3). There was no observation of disease or coral bleaching.The Porites is located in a relatively remote, rarely visited and highly protected Marine National Park (green) zone. Its location had not been previously reported and there is no existing database for significant corals in Australia or globally. Cataloguing the location of massive and long-lived corals can have multiple benefits. Scientific benefits include geochemical and isotopic analyses in coral skeletal cores which can help understand century-scale changes in oceanographic events and can be used to verify climate models. Social and economic benefits can include diving tourism, citizen science23 culture and stewardship. Perhaps the Significant Trees Register, which was designed by the National Trust24 to protect and celebrate Australia’s heritage could be considered as a model. There are risks of cataloguing the location of massive corals. It could be damaged by direct and indirect human uses including anchoring, research and pollution.Indigenous languages are an integral part of Indigenous culture, spirituality, and connection to country. We consulted Manbarra Traditional Owners about protocol and an appropriate cultural name for the Porites and they considered: Big (Muga), Home (Wanga), Coral reef (Muugar), Coral (Dhambi), Old (Anki, Gurgu), Old man (Gulula) and Old person (Gurgurbu)25. The recommendation by Manbarra Traditional Owners is that the Porites is named as Muga dhambi (Big coral). The feedback from the process of consultation was very positive with acknowledgement of the respect that the scientists have demonstrated to acknowledge Traditional Owners in this way.The large Porites coral at Goolboodi (Orpheus) Island is unusually rare and resilient. It has survived coral bleaching, invasive species, cyclones, severely low tides and human activities for almost 500 years. In an attempt to contextualise the resilience of these individual Porites we have reviewed major historic disturbances such as coral bleaching which has occurred since at least 1575 and potentially 99 bleaching events in the GBR over the past 400 plus years26. Other indicators such as high-density ‘stress bands’ were recorded from 1877 and are significantly more frequent in the late twentieth and early twenty-first centuries in accordance with rising temperatures from anthropogenic global warming27. In addition there have been an average of 1–2 tropical cyclones per decade (40–80 in total) that have potentially impacted the coral adjacent to Goolboodi Island28,29; 46 tropical cyclones impacted the area between Ingham and Townsville from 1858 to 200830. The cumulative impact of almost 100 bleaching events and up to 80 major cyclones over a period of four centuries, plus declining nearshore water quality contextualise the high resilience of this Porites coral. Looking to the future there is real concern for corals in the GBR due to many impacts including climate change, declining water quality, overfishing and coastal development31,32. This field note provides important geospatial, environmental, and cultural information of a rare coral that can be monitored, appreciated, potentially restored and hopefully inspire future generations to care more for our reefs and culture. More

1.Chapman, B. B. et al. Partial migration in fishes: Causes and consequences. J. Fish Biol. 81, 456–478 (2012).CAS 
Article 

Google Scholar 
2.Araújo, C. V. M. et al. Habitat fragmentation caused by contaminants: Atrazine as a chemical barrier isolating fish populations. Chemosphere 193, 24–31 (2018).ADS 
Article 

Google Scholar 
3.Flitcroft, R. L., Arismendi, I. & Santelmann, M. V. A review of habitat connectivity research for pacific salmon in marine, estuary, and freshwater environments. J. Am. Water Resour. Assoc. 55, 430–441 (2019).ADS 
Article 

Google Scholar 
4.Maire, A., Thierry, E., Viechtbauer, W. & Daufresne, M. Poleward shift in large-river fish communities detected with a novel meta-analysis framework. Freshw. Biol. 64, 1143–1156 (2019).Article 

Google Scholar 
5.van Vliet, M. T. H. et al. Coupled daily streamflow and water temperature modelling in large river basins. Hydrol. Earth Syst. Sci. 16, 4303–4321 (2012).ADS 
Article 

Google Scholar 
6.Palmer, M. A. et al. Climate change and the world’s river basins: Anticipating management options. Front. Ecol. Environ. 6, 81–89 (2008).Article 

Google Scholar 
7.Jonsson, B. & Jonsson, N. A review of the likely effects of climate change on anadromous Atlantic salmon Salmo salar and brown trout Salmo trutta, with particular reference to water temperature and flow. J. Fish Biol. 75, 2381–2447 (2009).CAS 
Article 

Google Scholar 
8.Arevalo, E. et al. An innovative bivariate approach to detect joint temporal trends in environmental conditions: Application to large French rivers and diadromous fish. Sci. Total Environ. 748, 141260 (2020).ADS 
CAS 
Article 

Google Scholar 
9.Hughes, L. Biological consequences of global warming: Is the signal already apparent?. Trends Ecol. Evol. 15, 56–61 (2000).CAS 
Article 

Google Scholar 
10.Tesch, F.-W. & Bartsch, P. The Eel (Blackwell Science, 2003).Book 

Google Scholar 
11.Durif, C. M. F. et al. Age of European silver eels during a period of declining abundance in Norway. Ecol. Evol. 10, 4801–4815 (2020).Article 

Google Scholar 
12.Poole, R. W. & Reynolds, J. D. Growth rate and age at migration of Anguilla anguilla. J. Fish Biol. 48, 633–642 (1996).
Google Scholar 
13.Durif, C. M. F., Travade, F., Rives, J., Elie, P. & Gosset, C. Relationship between locomotor activity, environmental factors, and timing of the spawning migration in the European eel Anguilla anguilla. Aquat. Living Resour. 21, 163–170 (2008).Article 

Google Scholar 
14.Fontaine, M. Physiological mechanisms in the migration of marine and amphihaline fish. Adv. Mar. Biol. 13, 241–355 (1975).Article 

Google Scholar 
15.Bruijs, M. C. M. & Durif, C. M. F. Silver Eel migration and behaviour. Spawning Migr. Eur. Eel https://doi.org/10.1007/978-1-4020-9095-0_4 (2009).Article 

Google Scholar 
16.ICES. Workshop on the temporal migration patterns of European eel (WKEELMIGRATION). vol. 2 http://doi.org/https://doi.org/10.17895/ices.pub.5993 (2020).17.Vøllestad, L. A., Jonsson, B., Hvidsten, N. A. & Naesje, T. F. Experimental test of environmental factors influencing the seaward migration of European silver eels. J. Fish Biol. 45, 641–651 (1994).Article 

Google Scholar 
18.Sandlund, O. T. et al. Timing and pattern of annual silver eel migration in two European watersheds are determined by similar cues. Ecol. Evol. 7, 5956–5966 (2017).Article 

Google Scholar 
19.Drouineau, H. et al. Freshwater eels: A symbol of the effects of global change. Fish Fish. 19, 903–930 (2018).Article 

Google Scholar 
20.Pike, C., Crook, V., & Gollock, M. Anguilla anguilla. The IUCN Red List of Treatened Species 2020. https://dx.doi.org/https://doi.org/10.2305/IUCN.UK.2020-539 2.RLTS.T60344A152845178.en (2020).21.Dankers, R. & Feyen, L. Climate change impact on flood hazard in Europe: An assessment based on high-resolution climate simulations. J. Geophys. Res. Atmos. 113, 1–17 (2008).Article 

Google Scholar 
22.Reid, A. J. et al. Emerging threats and persistent conservation challenges for freshwater biodiversity. Biol. Rev. 94, 849–873 (2019).Article 

Google Scholar 
23.Trenberth, K. E. et al. Global warming and changes in drought. Nat. Clim. Chang. 4, 17–22 (2014).ADS 
Article 

Google Scholar 
24.Durif, C., Elie, P., Gosset, C. & Rives, J. Behavioral Study of Downstream Migrating Eels by Radio-telemetry at a Small Hydroelectric Power Plant. Am. Fish. Soc. Symp. 1–14 (2002).25.Flitcroft, R. L. et al. Linking hydroclimate to fish phenology and habitat use with ichthyographs. PLoS ONE 11, 1–12 (2016).Article 

Google Scholar 
26.Bossard, M., Feranec, J. & Othael, J. CORINE Land Cover Technical Guide – Addendum 2000. European Environment Agency. Technical Report. Available online at: http://www.eea.europa.eu/publications/tech40add. (2000).27.de Eyto, E. et al. Characterisation of salmonid food webs in the rivers and lakes of an Irish peatland ecosystem. Biol. Environ. Proc. R. Irish Acad. 120, 1–17 (2020).
Google Scholar 
28.Poole, W. R., Reynolds, J. D. & Moriarty, C. Observations on the Silver Eel Migrations of the Burrishoole River System, Ireland, 1959 to 1988. Int. Rev. der gesamten Hydrobiol. und Hydrogr 75, 807–815 (1990).Article 

Google Scholar 
29.Poole, W. R. et al. Long-term variation in numbers and biomass of silver eels being produced in two European river systems. ICES J. Mar. Sci. 75, 1627–1637 (2018).Article 

Google Scholar 
30.Chacón, J. E. & Duong, T. Multivariate plug-in bandwidth selection with unconstrained pilot bandwidth matrices. TEST 19, 375–398 (2010).MathSciNet 
Article 

Google Scholar 
31.Lechowicz, M. The sampling characteristics of electivity indices. Oecologia 52, 22–30 (1982).ADS 
Article 

Google Scholar 
32.Ivlev, V. S. Experimental ecology of the feeding fishes (Yale University Press, 1961).
Google Scholar 
33.R Development Core Team. R: A Language and Environment for Statistical Computing. (2020).34.Drouineau, H., Arevalo, E., Lassalle, G., Tétard, S. & Maire, A. chocR: Exploring the temporal CHange of OCcurence of events in multivariate time series. R package version 0.0.0.9000. (2020).35.Hutchinson, G. E. Concluding Remarks. in Cold Spring Harbor Symposia on Quantitative Biology 415–442 (1957).36.Schneider, C., Laizé, C. L. R., Acreman, M. C. & Flörke, M. How will climate change modify river flow regimes in Europe?. Hydrol. Earth Syst. Sci. 17, 325–339 (2013).ADS 
Article 

Google Scholar 
37.Hannaford, J., Laize, C. L. R. & Marsh, T. J. An assessment of runoff trends in undisturbed catchments in the Celtic regions of North West Europe. IAHS-AISH Publ. 78–85 (2007).38.Engen-Skaugen, T. Refinement of dynamically downscaled precipitation and temperature scenarios. Clim. Change 84, 365–382 (2007).ADS 
Article 

Google Scholar 
39.Lawrence, D. & Hisdal, H. Hydrological projections for floods in Norway under a future climate. NVE Report http://webby.nve.no/publikasjoner/report/2011/report2011_05.pdf (2011).40.Woolway, R. I. et al. Substantial increase in minimum lake surface temperatures under climate change. Clim. Change 155, 81–94 (2019).ADS 
CAS 
Article 

Google Scholar 
41.Fealy, R. et al. RESCALE : Review and Simulate Climate and Catchment Responses at Burrishoole. Review Literature and Arts of the Americas (2014).42.Als, T. D. et al. All roads lead to home: Panmixia of European eel in the Sargasso Sea. Mol. Ecol. 20, 1333–1346 (2011).Article 

Google Scholar 
43.Acou, A., Laffaille, P., Legault, A. & Feunteun, E. Migration pattern of silver eel (Anguilla anguilla, L.) in an obstructed river system. Ecol. Freshw. Fish 17, 432–442 (2008).Article 

Google Scholar 
44.Fernandes, W. P. A. et al. Does relatedness influence migratory timing and behaviour in Atlantic salmon smolts?. Anim. Behav. 106, 191–199 (2015).Article 

Google Scholar 
45.Vøllestad, L. A. et al. Environmental Factors Regulating the Seaward Migration of European Silver Eels (Anguilla anguilla). Can. J. Fish. Aquat. Sci. 43, 1909–1916 (1986).Article 

Google Scholar 
46.Daverat, F. et al. One century of eel growth: Changes and implications. Ecol. Freshw. Fish 21, 325–336 (2012).Article 

Google Scholar 
47.Vøllestad, L. A. Geographic variation in age and length at metamorphosis of maturing European eel: Environmental effects and phenotypic plasticity. J. Anim. Ecol. 61, 41 (1992).Article 

Google Scholar 
48.Vaughan, L. et al. Growth rates in a European eel Anguilla anguilla (L., 1758) population show a complex relationship with temperature over a seven-decade otolith biochronology. ICES J. Mar. Sci. (2021).49.Lassalle, G. & Rochard, E. Impact of twenty-first century climate change on diadromous fish spread over Europe, North Africa and the Middle East. Glob. Chang. Biol. 15, 1072–1089 (2009).ADS 
Article 

Google Scholar 
50.Monteiro, R. M. et al. Migration and escapement of silver eel males, Anguilla anguilla, from a southwestern European river. Ecol. Freshw. Fish https://doi.org/10.1111/eff.12545 (2020).Article 

Google Scholar 
51.Mateo, M. et al. Cause or consequence? Exploring the role of phenotypic plasticity and genetic polymorphism in the emergence of phenotypic spatial patterns of the European eel. Can. J. Fish. Aquat. Sci. 74, 987–999 (2017).Article 

Google Scholar  More

1.Irwin AJ, Oliver MJ. Are ocean deserts getting larger? Geophys Res Lett. 2009;36:L18609.Article 

Google Scholar 
2.McClain CR, Signorini SR, Christian JR. Subtropical gyre variability observed by ocean-color satellites. Deep Sea Res Part II Topical Stud Oceanogr. 2004;51:281–301.CAS 
Article 

Google Scholar 
3.Signorini SR, Franz BA, McClain CR. Chlorophyll variability in the oligotrophic gyres: Mechanisms, seasonality and trends. Front Mar Sci. 2015;2:1–11.Article 

Google Scholar 
4.Polovina JJ, Howell EA, Abecassis M. Ocean’s least productive waters are expanding. Geophys Res Lett. 2008;35:L03618.Article 

Google Scholar 
5.Sharma P, Marinov I, Cabre A, Kostadinov T, Singh A. Increasing biomass in the warm oceans: unexpected new insights from SeaWIFS. Geophys Res Lett. 2019;46:3900–10.Article 

Google Scholar 
6.Flombaum P, Wang W-L, Primeau FW, Martiny AC. Global picophytoplankton niche partitioning predicts overall positive response to ocean warming. Nat Geosci. 2020;13:116–20.CAS 
Article 

Google Scholar 
7.Carr M-E, Friedrichs MAM, Schmeltz M, Noguchi Aita M, Antoine D, Arrigo KR, et al. A comparison of global estimates of marine primary production from ocean color. Deep Sea Res Part II Topical Stud Oceanogr. 2006;53:741–70.Article 

Google Scholar 
8.Field CB, Behrenfeld MJ, Randerson JT, Falkowski P. Primary production of the biosphere: Integrating terrestrial and oceanic components. Science. 1998;281:237–40.CAS 
PubMed 
Article 

Google Scholar 
9.DeVries T, Primeau F, Deutsch C. The sequestration efficiency of the biological pump. Geophys Res Lett. 2012;39:L13601.Article 
CAS 

Google Scholar 
10.Cabré A, Marinov I, Leung S. Consistent global responses of marine ecosystems to future climate change across the IPCC AR5 earth system models. Clim Dyn. 2015;45:1253–80.Article 

Google Scholar 
11.Behrenfeld MJ, O’Malley RT, Boss ES, Westberry TK, Graff JR, Halsey KH, et al. Revaluating ocean warming impacts on global phytoplankton. Nat Clim Change. 2015;6:323–30.Article 

Google Scholar 
12.Richardson K, Bendtsen J. Vertical distribution of phytoplankton and primary production in relation to nutricline depth in the open ocean. Mar Ecol Prog Ser. 2019;620:33–46.CAS 
Article 

Google Scholar 
13.Roshan S, DeVries T. Efficient dissolved organic carbon production and export in the oligotrophic ocean. Nat Commun. 2017;8:1–8.CAS 
Article 

Google Scholar 
14.Marañón E, Holligan PM, Barciela R, González N, Mouriño B, Pazó MJ, et al. Patterns of phytoplankton size structure and productivity in contrasting open-ocean environments. Mar Ecol Prog Ser. 2001;216:43–56.Article 

Google Scholar 
15.Pérez V, Fernández E, Marañón E, Morán XAG, Zubkov MV. Vertical distribution of phytoplankton biomass, production and growth in the Atlantic subtropical gyres. Deep Sea Res Part I Oceanographic Res Pap. 2006;53:1616–34.Article 

Google Scholar 
16.Teira E, Mouriño B, Marañón E, Pérez V, Pazó MJ, Serret P, et al. Variability of chlorophyll and primary production in the Eastern North Atlantic subtropical gyre: potential factors affecting phytoplankton activity. Deep Sea Res Part I Oceanographic Res Pap. 2005;52:569–88.CAS 
Article 

Google Scholar 
17.Chisholm SW, Frankel SL, Goericke R, Olson RJ, Palenik B, Waterbury JB, et al. Prochlorococcus marinus nov. Gen. Nov. Sp.: an oxyphototrophic marine prokaryote containing divinyl chlorophyll a and b. Arch Microbiol. 1992;157:297–300.CAS 
Article 

Google Scholar 
18.Flombaum P, Gallegos JL, Gordillo RA, Rincón J, Zabala LL, Jiao N, et al. Present and future global distributions of the marine cyanobacteria Prochlorococcus and Synechococcus. PNAS. 2013;110:9824–9.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
19.Partensky F, Hess WR, Vaulot D. Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol Mol Biol Rev. 1999;63:106–27.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
20.Li WK. Primary production of prochlorophytes, cyanobacteria, and eucaryotic ultraphytoplankton: Measurements from flow cytometric sorting. Limnol Oceanogr. 1994;39:169–75.CAS 
Article 

Google Scholar 
21.Jardillier L, Zubkov MV, Pearman J, Scanlan DJ. Significant CO2 fixation by small prymnesiophytes in the subtropical and tropical Northeast Atlantic Ocean. ISME J. 2010;4:1180–92.CAS 
PubMed 
Article 

Google Scholar 
22.Irion S, Christaki U, Berthelot H, L’Helguen S, Jardillier L. Small phytoplankton contribute greatly to CO2-fixation after the diatom bloom in the Southern Ocean. ISME J. 2021;15:1–14.Article 
CAS 

Google Scholar 
23.Liu K, Suzuki K, Chen B, Liu H. Are temperature sensitivities of Prochlorococcus and Synechococcus impacted by nutrient availability in the subtropical Northwest Pacific? Limnol Oceanogr. 2020;66:639–51.Article 
CAS 

Google Scholar 
24.D’Hondt S, Spivack AJ, Pockalny R, Ferdelman TG, Fischer JP, Kallmeyer J, et al. Subseafloor sedimentary life in the South Pacific gyre. PNAS. 2009;106:11651–6.PubMed 
PubMed Central 
Article 

Google Scholar 
25.Longhurst A, Sathyendranath S, Platt T, Caverhill C. An estimate of global primary production in the ocean from satellite radiometer data. J Plankton Res. 1995;17:1245–71.Article 

Google Scholar 
26.Morel A, Gentili B, Claustre H, Babin M, Bricaud A, Ras J, et al. Optical properties of the “clearest” natural waters. Limnol Oceanogr. 2007;52:217–29.CAS 
Article 

Google Scholar 
27.Halm H, Lam P, Ferdelman TG, Lavik G, Dittmar T, LaRoche J, et al. Heterotrophic organisms dominate nitrogen fixation in the south pacific gyre. ISME J. 2012;6:1238–49.CAS 
PubMed 
Article 

Google Scholar 
28.Raimbault P, Garcia N. Evidence for efficient regenerated production and dinitrogen fixation in nitrogen-deficient waters of the South Pacific Ocean: impact on new and export production estimates. Biogeosciences. 2008;5:323–38.CAS 
Article 

Google Scholar 
29.Shiozaki T, Bombar D, Riemann L, Sato M, Hashihama F, Kodama T, et al. Linkage between dinitrogen fixation and primary production in the oligotrophic South Pacific Ocean. Glob Biogeochem Cyc. 2018;32:1028–44.CAS 
Article 

Google Scholar 
30.Reintjes G, Tegetmeyer HE, Bürgisser M, Orlić S, Tews I, Zubkov M, et al. On-site analysis of bacterial communities of the ultraoligotrophic South Pacific gyre. Appl Environ Microbiol. 2019;85:e00184–19.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
31.Zielinski O, Henkel R, Voß D, Ferdelman TG. Physical oceanography during Sonne cruise SO245 (Ultrapac). PANGAEA. 2018. https://doi.org/10.1594/PANGAEA.890394.32.Ferdelman TG, Klockgether G, Downes P, Lavik G. Nutrient data from CTD Nisken bottles from Sonne expedition SO-245 “Ultrapac”. PANGAEA. 2019. https://doi.org/10.1594/PANGAEA.899228.33.Arar EJ, Collins GB. Method 445.0: In vitro determination of chlorophyll a and pheophytin a in marine and freshwater algae by fluorescence: U.S. Environmental Protection Agency, Washington, DC; 1997. https://cfpub.epa.gov/si/si_public_record_report.cfm?Lab=NERL&dirEntryId=309417.34.Welschmeyer N, Naughton S. Improved chlorophyll a analysis: single fluorometric measurement with no acidification. Lake Reserv Manag. 1994;9:123.
Google Scholar 
35.Osterholz H, Kilgour D, Storey DS, Lavik G, Ferdelman T, Niggemann J, et al. Accumulation of DOC in the South Pacific subtropical gyre from a molecular perspective. Mar Chem. 2021;231:103955.CAS 
Article 

Google Scholar 
36.Voß D, Henkel R, Wollschläger J, Zielinski O. Hyperspectral underwater light field measured during the cruise SO245 with R/V Sonne. PANGAEA. 2020. https://doi.org/10.1594/PANGAEA.911558.37.Martínez-Pérez C, Mohr W, Löscher CR, Dekaezemacker J, Littmann S, Yilmaz P, et al. The small unicellular diazotrophic symbiont, UCYN-A, is a key player in the marine nitrogen cycle. Nat Microbiol. 2016;1:1–7.Article 
CAS 

Google Scholar 
38.Marra J. Net and gross productivity: weighing in with 14C. Aquat Microb Ecol. 2009;56:123–31.Article 

Google Scholar 
39.Ribeiro CG, Marie D, Santos ALD, Brandini FP, Vaulot D. Estimating microbial populations by flow cytometry: comparison between instruments. Limnol Oceanogr Methods. 2016;14:750–8.Article 

Google Scholar 
40.Pernthaler A, Pernthaler J, Amann R. Fluorescence in situ hybridization and catalyzed reporter deposition for the identification of marine bacteria. Appl Environ Microbiol. 2002;68:3094–101.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
41.West NJ, Schönhuber WA, Fuller NJ, Amann RI, Rippka R, Post AF, et al. Closely related Prochlorococcus genotypes show remarkably different depth distributions in two oceanic regions as revealed by in situ hybridization using 16 S rRNA-targeted oligonucleotides. Microbiology. 2001;147:1731–44.CAS 
PubMed 
Article 

Google Scholar 
42.Polerecky L, Adam B, Milucka J, Musat N, Vagner T, Kuypers MMM. Look@NanoSIMS—a tool for the analysis of nanoSIMS data in environmental microbiology. Environ Microbiol. 2012;14:1009–23.CAS 
PubMed 
Article 

Google Scholar 
43.Verity PG, Robertson CY, Tronzo CR, Andrews MG, Nelson JR, Sieracki ME. Relationships between cell volume and the carbon and nitrogen content of marine photosynthetic nanoplankton. Limnol Oceanogr. 1992;37:1434–46.CAS 
Article 

Google Scholar 
44.Khachikyan A, Milucka J, Littmann S, Ahmerkamp S, Meador T, Könneke M, et al. Direct cell mass measurements expand the role of small microorganisms in nature. Appl Environ Microbiol. 2019;85:AEM00493–19.Article 

Google Scholar 
45.Walters W, Hyde ER, Berg-Lyons D, Ackermann G, Humphrey G, Parada A, et al. Improved bacterial 16 S rRNA gene (v4 and v4-5) and fungal internal transcribed spacer marker gene primers for microbial community surveys. MSystems. 2016;1:e00009–15.PubMed 
Article 

Google Scholar 
46.Parada AE, Needham DM, Fuhrman JA. Every base matters: assessing small subunit rrna primers for marine microbiomes with mock communities, time series and global field samples. Environ Microbiol. 2016;18:1403–14.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
47.Comeau AM, Douglas GM, Langille MG. Microbiome helper: a custom and streamlined workflow for microbiome research. MSystems. 2017;2:e00127–16.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
48.Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. Qiime allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
49.Haas S, Desai DK, LaRoche J, Pawlowicz R, Wallace DW. Geomicrobiology of the carbon, nitrogen and sulphur cycles in Powell Lake: a permanently stratified water column containing ancient seawater. Environ Microbiol. 2019;21:3927–52.CAS 
PubMed 
Article 

Google Scholar 
50.Zhang J, Kobert K, Flouri T, Stamatakis A. Pear: a fast and accurate Illumina paired-end read merger. Bioinformatics. 2013;30:614–20.51.Rognes T, Flouri T, Nichols B, Quince C, Mahé F. Vsearch: a versatile open source tool for metagenomics. PeerJ. 2016;4:e2584.PubMed 
PubMed Central 
Article 

Google Scholar 
52.Kopylova E, Noé L, Touzet H. Sortmerna: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics. 2012;28:3211–7.CAS 
PubMed 
Article 

Google Scholar 
53.Mercier C, Boyer F, Bonin A, Coissac E (eds). Sumatra and Sumaclust: fast and exact comparison and clustering of sequences. SeqBio 2013 Workshop 2013: (abstract).54.DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, et al. Greengenes, a chimera-checked 16 S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol. 2006;72:5069–72.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
55.Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2012;41:D590–6.PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
56.Decelle J, Romac S, Stern RF, Bendif EM, Zingone A, Audic S, et al. PhytoREF: A reference database of the plastidial 16 S rRNA gene of photosynthetic eukaryotes with curated taxonomy. Molec Ecol Res. 2015;15:1435–45.CAS 
Article 

Google Scholar 
57.Guillou L, Bachar D, Audic S, Bass D, Berney C, Bittner L, et al. The protist ribosomal reference database (PR2): a catalog of unicellular eukaryote small sub-unit rRNA sequences with curated taxonomy. Nucleic Acids Res. 2012;4:D597–604.Article 
CAS 

Google Scholar 
58.Del Campo J, Kolisko M, Boscaro V, Santoferrara LF, Nenarokov S, Massana R, et al. EukRef: phylogenetic curation of ribosomal RNA to enhance understanding of eukaryotic diversity and distribution. PLoS Biol. 2018;16:e2005849.PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
59.Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar, et al. ARB: A software environment for sequence data. Nucleic Acids Res. 2004;32:1363–71.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
60.Gruber-Vodicka HR, Seah BK, Pruesse E. Phyloflash: rapid small-subunit rRNA profiling and targeted assembly from metagenomes. Msystems. 2020;5:e00920.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
61.Farrant GK, Doré H, Cornejo-Castillo FM, Partensky F, Ratin M, Ostrowski M, et al. Delineating ecologically significant taxonomic units from global patterns of marine picocyanobacteria. PNAS. 2016;113:E3365–74.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
62.Oggerin de Orube M, Fuchs BM. Personal communication: Unpublished shotgun metagenomes collected from in situ pump samples during R/V Sonne expedition SO245. Bremen, Germany. 2021.63.Schlitzer R. Ocean Data View. Bremerhaven, Germany. 2021. https://odv.awi.de.64.R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing,Vienna, Austria. 2017. https://www.R-project.org/.65.Wickham H. Ggplot2: elegant graphics for data analysis. Springer-Verlag, New York. 2016.66.McMurdie PJ, Holmes S. Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLOS ONE. 2013;8:e61217.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
67.Oksanen J, Kindt R, Legendre P, O’Hara B, Stevens MHH, Oksanen MJ, et al. The vegan package: community ecology package. R package version 2.5–7. 2019. https://CRAN.R-project.org/package=vegan.68.Chaigneau A, Pizarro O. Surface circulation and fronts of the South Pacific Ocean, east of 120°W. Geophys Res Lett. 2005;32:L08605.69.Logares R, Sunagawa S, Salazar G, Cornejo‐Castillo FM, Ferrera I, Sarmento H, et al. Metagenomic 16 S rRNA Illumina tags are a powerful alternative to amplicon sequencing to explore diversity and structure of microbial communities. Environ Microbiol. 2014;16:2659–71.CAS 
PubMed 
Article 

Google Scholar 
70.Shi XL, Lepère C, Scanlan DJ, Vaulot D. Plastid 16 s rRNA gene diversity among eukaryotic picophytoplankton sorted by flow cytometry from the South Pacific Ocean. PLOS ONE. 2011;6:e18979.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
71.Fuller NJ, Campbell C, Allen DJ, Pitt FD, Zwirglmaier K, Le Gall F, et al. Analysis of photosynthetic picoeukaryote diversity at open ocean sites in the Arabian Sea using a pcr biased towards marine algal plastids. Aquat Micro Ecol. 2006;43:79–93.Article 

Google Scholar 
72.Raes EJ, Bodrossy L, Kamp JVD, Bissett A, Ostrowski M, Brown MV, et al. Oceanographic boundaries constrain microbial diversity gradients in the South Pacific Ocean. PNAS. 2018;115:E8266–75.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
73.Campbell L, Liu H, Nolla HA, Vaulot D. Annual variability of phytoplankton and bacteria in the subtropical North Pacific Ocean at station ALOHA during the 1991-4 ENSO event. Deep Sea Res Part I Oceanogr Res Pap. 1997;44:167–92.CAS 
Article 

Google Scholar 
74.Viviani DA, Church MJ. Decoupling between bacterial production and primary production over multiple time scales in the North Pacific subtropical gyre. Deep Sea Res Part I Oceanogr Res Pap. 2017;121:132–42.CAS 
Article 

Google Scholar 
75.Rii YM, Duhamel S, Bidigare RR, Karl DM, Repeta DJ, Church MJ. Diversity and productivity of photosynthetic picoeukaryotes in biogeochemically distinct regions of the south east pacific ocean. Limnol Oceanogr. 2016;61:806–24.Article 

Google Scholar 
76.Shi XL, Marie D, Jardillier L, Scanlan DJ, Vaulot D. Groups without cultured representatives dominate eukaryotic picophytoplankton in the oligotrophic South East Pacific Ocean. PLOS ONE. 2009;4:e7657.PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
77.Kirkham AR, Lepere C, Jardillier LE, Not F, Bouman H, Mead A, et al. A global perspective on marine photosynthetic picoeukaryote community structure. ISME J. 2013;7:922–36.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
78.Lepère C, Vaulot D, Scanlan DJ. Photosynthetic picoeukaryote community structure in the South East Pacific Ocean encompassing the most oligotrophic waters on earth. Environ Microbiol. 2009;11:3105–17.PubMed 
Article 
CAS 

Google Scholar 
79.Bender ML, Jönsson B. Is seasonal net community production in the South Pacific subtropical gyre anomalously low? Geophys Res Lett. 2016;43:9757–63.Article 

Google Scholar 
80.Montégut CDB, Madec G, Fischer AS, Lazar A, Iudicone D. Mixed layer depth over the global ocean: an examination of profile data and a profile-based climatology. J Geophys Res Oceans. 2004;109:C12003.Article 

Google Scholar 
81.Liu Q, Lu Y. Role of horizontal density advection in seasonal deepening of the mixed layer in the subtropical Southeast Pacific. Adv Atmospher Sci. 2016;33:442–51.Article 

Google Scholar 
82.Sato K, Suga T. Structure and modification of the South Pacific eastern subtropical mode water. J Phys Oceanogr. 2009;39:1700–14.Article 

Google Scholar 
83.Jung J, Furutani H, Uematsu M. Atmospheric inorganic nitrogen in marine aerosol and precipitation and its deposition to the north and south pacific oceans. J Atmospher Chem. 2011;68:157–81.CAS 
Article 

Google Scholar 
84.Pavia FJ, Anderson RF, Winckler G, Fleisher MQ. Atmospheric dust inputs, iron cycling, and biogeochemical connections in the South Pacific Ocean from thorium isotopes. Glob Biogeochem Cycles. 2020;34:e2020GB006562.CAS 

Google Scholar 
85.Bonnet S, Guieu C, Bruyant F, Prášil O, Van Wambeke F, Raimbault P, et al. Nutrient limitation of primary productivity in the Southeast Pacific (Biosope Cruise). Biogeosciences. 2008;5:215–25.CAS 
Article 

Google Scholar 
86.Mahaffey C, Björkman KM, Karl DM. Phytoplankton response to deep seawater nutrient addition in the North Pacific subtropical gyre. Mar Ecol Prog Ser. 2012;460:13–34.CAS 
Article 

Google Scholar 
87.Grob C, Jardillier L, Hartmann M, Ostrowski M, Zubkov MV, Scanlan DJ. Cell-specific CO2 fixation rates of two distinct groups of plastidic protists in the Atlantic Ocean remain unchanged after nutrient addition. Environ Microbiol Rep. 2015;7:211–8.CAS 
PubMed 
Article 

Google Scholar 
88.Vaulot D, Marie D, Olson RJ, Chisholm SW. Growth of Prochlorococcus, a photosynthetic prokaryote, in the equatorial pacific ocean. Science. 1995;268:1480–2.CAS 
PubMed 
Article 

Google Scholar 
89.Grob C, Hartmann M, Zubkov MV, Scanlan DJ. Invariable biomass-specific primary production of taxonomically discrete picoeukaryote groups across the Atlantic Ocean. Environ Microbiol. 2011;13:3266–74.PubMed 
Article 

Google Scholar 
90.Berthelot H, Duhamel S, L’Helguen S, Maguer J-F, Wang S, Cetinić I, et al. NanoSIMS single cell analyses reveal the contrasting nitrogen sources for small phytoplankton. ISME J. 2019;13:651.CAS 
PubMed 
Article 

Google Scholar 
91.Zubkov MV, Fuchs BM, Tarran GA, Burkill PH, Amann R. High rate of uptake of organic nitrogen compounds by Prochlorococcus cyanobacteria as a key to their dominance in oligotrophic oceanic waters. Appl Environ Microbiol. 2003;69:1299–304.CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
92.Muñoz-Marín MC, Gómez-Baena G, López-Lozano A, Moreno-Cabezuelo JA, Díez J, García-Fernández JM. Mixotrophy in marine picocyanobacteria: use of organic compounds by Prochlorococcus and Synechococcus. ISME J. 2020;14:1065–73.PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
93.Timmermans K, Van der Wagt B, Veldhuis M, Maatman A, De Baar H. Physiological responses of three species of marine pico-phytoplankton to ammonium, phosphate, iron and light limitation. J Sea Res. 2005;53:109–20.CAS 
Article 

Google Scholar 
94.Vaulot D, Eikrem W, Viprey M, Moreau H. The diversity of small eukaryotic phytoplankton (≤ 3 μm) in marine ecosystems. FEMS Microbiol Rev. 2008;32:795–820.CAS 
PubMed 
Article 

Google Scholar 
95.Worden AZ, Janouskovec J, McRose D, Engman A, Welsh RM, Malfatti S, et al. Global distribution of a wild alga revealed by targeted metagenomics. Curr Biol. 2012;22:R675–7.CAS 
PubMed 
Article 

Google Scholar 
96.Le Gall F, Rigaut-Jalabert F, Marie D, Garczarek L, Viprey M, Gobet A, et al. Picoplankton diversity in the South-east Pacific Ocean from cultures. Biogeosciences. 2008;5:203–14.Article 

Google Scholar 
97.NASA Goddard Space Flight Center, Ocean Ecology Laboratory, Ocean Biology Processing Group. Moderate-resolution Imaging Spectroradiometer (MODIS) Aqua Chlorophyll Data; Reprocessing. NASA OB.DAAC, Greenbelt, MD, USA. 2018. https://oceancolor.gsfc.nasa.gov/data/10.5067/AQUA/MODIS/L3M/CHL/2018/ Accessed 2019/08/01. More

1.Roberts, P. & Stewart, B. A. Defining the ‘generalist specialist’ niche for Pleistocene Homo sapiens. Nat. Hum. Behav. 2, 542–550 (2018).PubMed 
Article 
PubMed Central 

Google Scholar 
2.Heaney, L. R. A synopsis of climatic and vegetational change in Southeast Asia. Clim. Change 19, 53–61 (1991).ADS 
Article 

Google Scholar 
3.Morley, R. J. Origin and Evolution of Tropical Rain Forests (Wiley, 2000).
Google Scholar 
4.Bird, M. I., Taylor, D. & Hunt, C. Palaeoenvironments of insular Southeast Asia during the last Glacial Period: a savanna corridor in Sundaland?. Quat. Sci. Rev. 24, 2228–2242 (2005).ADS 
Article 

Google Scholar 
5.Wurster, C. M., Rifai, H., Zhou, B., Haig, J. & Bird, M. I. Savanna in equatorial Borneo during the late Pleistocene. Sci. Rep. 9, 6392. https://doi.org/10.1038/s41598-019-42670-4 (2019).ADS 
CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
6.Wurster, C. M. & Bird, M. I. Barriers and bridges: early human dispersals in equatorial SE Asia. Geol. Soc. Spec. Publ. 411, 235–250 (2016).ADS 
Article 

Google Scholar 
7.Zaim, Y. Geological evidence for the earliest appearance of hominins in Indonesia. In Out of Africa I: The First Hominin Colonization of Eurasia (eds Fleagle, J. G. et al.) 97–110 (Springer, 2010).Chapter 

Google Scholar 
8.Cannon, C. H., Morley, R. J. & Bush, A. B. G. The current refugial rainforests of Sundaland are unrepresentative of their biogeographic past and highly vulnerable to disturbance. Proc. Natl. Acad. Sci. USA 106, 11188–11193 (2009).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
9.Raes, N. et al. Historical distribution of Sundaland’s Dipterocarp rainforests at Quaternary glacial maxima. Proc. Natl. Acad. Sci. USA 111, 16790–16795 (2014).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
10.Suraprasit, K., Jongautchariyakul, S., Yamee, C., Pothichaiya, C. & Bocherens, H. New fossil and isotope evidence for the Pleistocene zoogeographic transition and hypothesized savanna corridor in peninsular Thailand. Quat. Sci. Rev. 221, 1055861 (2019).Article 

Google Scholar 
11.Pookajorn, S. Human activities and environmental changes during the late pleistocene to middle holocene in Southern Thailand and Southeast Asia. In Humans at the End of the Ice Age: The Archaeology of the Pleistocene—Holocene Transition, Interdisciplinary Contributions to Archaeology (eds Straus, L. G. et al.) 201–213 ( Springer, 1996).Chapter 

Google Scholar 
12.Schepartz, L. A., Miller-Antonio, S. & Bakken, D. A. Upland resources and the early palaeolithic occupation of Southern China, Vietnam, Laos Thailand and Burma. World Archaeol. 32, 1–13 (2000).Article 

Google Scholar 
13.Mudar, K. & Anderson, D. New evidence for Southeast Asian pleistocene foraging economies: faunal remains from the early levels of Lang Rongrien Rockshelter, Krabi, Thailand. Asian Perspect. 46, 298–334 (2007).Article 

Google Scholar 
14.Shoocongdej, R. Late Pleistocene activities at the Tham Lod rockshelter in Highland Pang Mapha, Mae Hong Son province, Norhwestern Thailand. In Uncovering Southeast Asia’s Past (eds Bacus, E. et al.) 22–37 (NUS Press, 2006).
Google Scholar 
15.Shoocongdej, R. et al. Final report of Highland Archaeology Project in Pang Mapha District, Mae Hong Son Province Phase 2, Vol. 2 (Thailand Research Fund, 2007).16.Demeter, F. et al. Anatomically modern human in Southeast Asia (Laos) by 46 ka. Proc. Natl. Acad. Sci. USA 109, 14375–14380 (2012).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
17Demeter, F. et al. Early modern humans and morphological variation in Southeast Asia: fossil evidence from Tam Pa Ling. Laos. PLoS ONE 10, e0121193. https://doi.org/10.1371/journal.pone.0121193 (2015).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
18.Viet, N. First archaeological evidence of symbolic activities from the Pleistocene of Vietnam. In Emergence and Diversity of Human Behavior Paleolithic Asia (ed. Kaifu, Y.) 133–139 (Texas A&M University Press, 2015).
Google Scholar 
19.Higham, C. F. & Thosarat, R. An early hunter-gatherer site at Ban Non Wat, Northeast Thailand. J. Indo. Pacif. Archaeol. 43, 93–96 (2019).Article 

Google Scholar 
20.Gorman, C. F. Excavations at Spirit Cave, North Thailand: Some Interim Interpretations. Asian Perspect. 13, 79–107 (1970).
Google Scholar 
21.Tayles, N., Halcrow, S. E., Sayavongkhamdy, T. & Souksavatdy, V. A prehistoric flexed human burial from Pha Phen, Middle Mekong Valley, Laos: its context in Southeast Asia. Anthropol. Sci. 123, 1–12 (2015).Article 

Google Scholar 
22.Conrad, C., Higham, C., Eda, M. & Marwick, B. Palaeoecology and forager subsistence strategies during the Pleistocene—Holocene transition: A reinvestigation of the zooarchaeological assemblage from Spirit Cave, Mae Hong Son Province, Thailand. Asian Perspect. 5, 2–27 (2016).Article 

Google Scholar 
23.Zeitoun, V. D. et al. Discovery of an outstanding Hoabinhian site from the Late Pleistocene at Doi Pha Kan (Lampang province, northern Thailand). Archaeol. Res. Asia 18, 1–16 (2019).Article 

Google Scholar 
24.Shoocongdej, R. Forager mobility organization in seasonal tropical environments of western Thailand. World Archaeol. 32, 14–40 (2000).Article 

Google Scholar 
25.Forestier, H. et al. The Hoabinhian from Laang Spean Cave in its stratigraphic, chronological, typo-technological and environmental context (Cambodia, Battambang province). J. Archaeol. Sci. Rep. 3, 194–206 (2015).
Google Scholar 
26.Chitkament, T., Gaillard, C. & Shoocongdej, R. Tham Lod rockshelter (Pang Mapha district, north-western Thailand): Evolution of the lithic assemblages during the late Pleistocene. Quat. Int. 416, 151–161 (2016).Article 

Google Scholar 
27.Marwick, B. The Hoabinhian of Southeast Asia and its relationship to regional Pleistocene lithic technologies. In Lithic Technological Organization and Paleoenvironmental Change Global and Diachronic Perspectives (eds Robinson, E. & Sellet, F.) 63–78 (Springer, 2018).Chapter 

Google Scholar 
28.Marwick, B. & Gagan, M. K. Late Pleistocene monsoon variability in northwest Thailand: an oxygen isotope sequence from the bivalve Margaritanopsis laosensis excavated in Mae Hong Son province. Quat. Sci. Rev. 30, 3088–3098 (2011).ADS 
Article 

Google Scholar 
29.Marwick, B. Multiple Optima in Hoabinhian flaked stone artefact palaeoeconomics and palaeoecology at two archaeological sites in Northwest Thailand. J. Anthropol. Archaeol. 32, 553–564 (2013).Article 

Google Scholar 
30.Wattanapituksakul, A., Filoux, A., Amphansri, A. & Tumpeesuwan, S. Late Pleistocene Caprinae assemblages of Tham Lod Rockshelter (Mae Hong Son Province, Northwest Thailand). Quat. Int. 493, 212–226 (2018).Article 

Google Scholar 
31.Shoocongdej, R. & Wattanapituksakul, A. Faunal assemblages and demography during the Late Pleistocene (MIS 2–1) to Early Holocene in Highland Pang Mapha, Northwest Thailand. Quat. Int. 563, 51–63 (2020).Article 

Google Scholar 
32.DeNiro, M. J. & Epstein, S. Influence of diet on the distribution of carbon isotopes in animals. Geochim. Cosmochim. Acta 42, 495–506 (1978).ADS 
CAS 
Article 

Google Scholar 
33.Van Der Merwe, N. J. & Vogel, J. C. 13C Content of human collagen as a measure of prehistoric diet in woodland North America. Nature 276, 815–816 (1978).ADS 
PubMed 
Article 
PubMed Central 

Google Scholar 
34.Cerling, T. E. & Harris, J. M. Carbon isotope fractionation between diet and bioapatite in ungulate mammals and implications for ecological and paleoecological studies. Oecologia 120, 347–363 (1999).ADS 
PubMed 
Article 
PubMed Central 

Google Scholar 
35.Cerling, T. E., Hart, J. A. & Hart, T. B. Stable isotope ecology in the Ituri Forest. Oecologia 138, 5–12 (2004).ADS 
PubMed 
Article 
PubMed Central 

Google Scholar 
36.Bourgon, N. et al. Zinc isotopes in Late Pleistocene fossil teeth from a Southeast Asian cave setting preserve paleodietary information. Proc. Natl. Acad. Sci. USA 117, 4675–4681 (2020).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
37.van Klinken, G. J. Bone Collagen quality indicators for palaeodietary and radiocarbon measurements. J. Archaeol. Sci. 26, 687–695 (1999).Article 

Google Scholar 
38.Pestle, W. J. & Colvard, M. Bone collagen preservation in the tropics: a case study from ancient Puerto Rico. J. Archaeol. Sci. 39, 2079–2090 (2012).CAS 
Article 

Google Scholar 
39.Ecker, M. et al. Middle Pleistocene ecology and Neanderthal subsistence: Insights from stable isotope analyses in Payre (Ardèche, southeastern France). J. Hum. Evol. 65, 363–373 (2013).PubMed 
Article 
PubMed Central 

Google Scholar 
40Kohn, M. & Cerling, T. E. Stable isotope compositions of biological apatite. In Phosphates—Geochemical Geobiological and Materials Importance Reviews in Mineralogy and Geochemistry Vol. 48 (eds Kohn, M. et al.) 455–488 (Mineralogical Society of America, 2002).Chapter 

Google Scholar 
41.Biasatti, D., Wang, Y., Gao, F., Xu, Y. & Flynn, L. Paleoecologies and paleoclimates of late cenozoic mammals from Southwest China: evidence from stable carbon and oxygen isotopes. J. Asian Earth Sci. 44, 48–61 (2012).ADS 
Article 

Google Scholar 
42.Clementz, M. T., Fox-Dobbs, K., Wheatley, P.-V., Koch, P. L. & Doak, D. F. Revisiting old bones: coupled carbon isotope analysis of bioapatite and collagen as an ecological and palaeoecological tool. Geol. J. 44, 605–620 (2009).CAS 
Article 

Google Scholar 
43.Domingo, M. S., Domingo, L., Badgley, C., Sanisidro, O. & Morales, J. Resource partitioning among top predators in a Miocene food web. Proc. R. Soc. B 280, 20122138. https://doi.org/10.1098/rspb.2012.2138 (2013).Article 
PubMed 
PubMed Central 

Google Scholar 
44.Codron, D., Clauss, M., Codron, J. & Tütken, T. Within trophic level shifts in collagen–carbonate stable carbon isotope spacing are propagated by diet and digestive physiology in large mammal herbivores. Ecol. Evol. 8, 3983–3995 (2018).PubMed 
PubMed Central 
Article 

Google Scholar 
45Tejada-Lara, J. V. et al. Body mass predicts isotope enrichment in herbivorous mammals. Proc. R. Soc. B 285, 20181020. https://doi.org/10.1098/rspb.2018.1020 (2018).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
46.Cerling, T. E. et al. Stable isotope-based diet reconstructions of Turkana Basin hominins. Proc. Natl. Acad. Sci. USA 110, 10501–10506 (2013).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
47.Ayliffe, L. K. & Chivas, A. R. Oxygen isotope composition of the bone phosphate of Australian kangaroos: potential as a palaeoenvironmental recorder. Geochim. Cosmochim. Acta 54, 2603–2609 (1990).ADS 
CAS 
Article 

Google Scholar 
48.Levin, N. E., Cerling, T. E., Passey, B. H., Harris, J. M. & Ehleringer, J. R. A stable isotope aridity index for terrestrial environments. Proc. Natl. Acad. Sci. USA 103, 11201–11205 (2006).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
49.Bocherens, H., Koch, P., Mariotti, A., Geraads, D. & Jaeger, J.-J. Isotopic biogeochemistry (13C, 18O) of mammalian enamel from African Pleistocene hominoid sites. Palaios 11, 306–308 (1996).ADS 
Article 

Google Scholar 
50.Hambali, K., Ismail, A., Md-Zain, B. M., Amir, A. & Karim, F. A. Diet of long-tailed macaques (Macaca fascicularis) at the entrance of Kuala Selangor Nature Park (anthropogenic habitat): food selection that leads to human-macaque conflict. Acta Biol. Malay. 3, 58–68 (2014).
Google Scholar 
51.Nila, S., Suryobroto, B. & Widayati, K. A. Dietary variation of long tailed macaques (Macaca fascicularis) in Telaga Warna, Bogor, West Java. HAYATI J. Biosci. 21, 8–14 (2014).Article 

Google Scholar 
52.Lekagul, B. & McNeely, J. A. Mammals of Thailand: Association for the Conservation of Wildlife (Kurusapa Ladproa Press, 1988).
Google Scholar 
53.Suraprasit, K., Bocherens, H., Chaimanee, Y., Panha, S. & Jaeger, J.-J. Late Middle Pleistocene ecology and climate in Northeastern Thailand inferred from the stable isotope analysis of Khok Sung herbivore tooth enamel and the land mammal cenogram. Quat. Sci. Rev. 193, 24–42 (2018).ADS 
Article 

Google Scholar 
54Suraprasit, K. et al. Long-term isotope evidence on the diet and habitat breadth of pleistocene to holocene caprines in Thailand: implications for the extirpation and conservation of Himalayan Gorals. Front. Ecol. Evol. 8, 67. https://doi.org/10.3389/fevo.2020.00067 (2020).Article 

Google Scholar 
55.Kohn, M. J. Predicting animal δ18O: Accounting for diet and physiological adaptation. Geochim. Cosmochim. Acta 60, 4811–4829 (1996).ADS 
CAS 
Article 

Google Scholar 
56.Kohn, M. J., Schoeninger, M. J. & Valley, J. W. Herbivore tooth oxygen isotope compositions: effects of diet and physiology. Geochim. Cosmochim. Acta 60, 3889–3896 (1996).ADS 
CAS 
Article 

Google Scholar 
57.Dunbar, J. & Wilson, T. Oxygen and hydrogen isotopes in fruits and vegetable juices. Plant Physiol. 72, 725–727 (1983).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
58.Yakir, D. Variations in the natural abundances of oxygen-18 and deuterium in plant carbohydrates. Plant Cell Environ. 15, 1005–1020 (1992).CAS 
Article 

Google Scholar 
59.Fricke, H. C. & O’Neil, J. R. Inter- and intra-tooth variation in the oxygen isotope composition of mammalian tooth enamel phosphate: implications for palaeoclimatological and palaeobiological research. Palaeogeogr. Palaeoclimatol. Palaeoecol. 126, 91–99 (1996).Article 

Google Scholar 
60.Fricke, H. C., Clyde, W. C. & O’Neil, J. R. Intra-tooth variations in δ18O (PO4) of mammalian tooth enamel as a record of seasonal variations in continental climate variables. Geochem. Cosmochim. Acta 62, 1839–1850 (1998).ADS 
CAS 
Article 

Google Scholar 
61.Balasse, M., Ambrose, S. H., Smith, A. B. & Price, T. D. The seasonal mobility model for prehistoric herders in the south-western Cape of South Africa assessed by isotopic analysis of sheep tooth enamel. J. Archaeol. Sci. 29, 917–932 (2002).Article 

Google Scholar 
62Ratnam, J., Tomlinson, K. W., Rasquinha, D. N. & Sankaran, M. Savannahs of Asia: antiquity, biogeography, and an uncertain future. Philos. Trans. R. Soc. Lond. B Biol. Sci. 371, 2015305. https://doi.org/10.1098/rstb.2015.0305 (2016).CAS 
Article 

Google Scholar 
63.Pushkina, D., Bocherens, H., Chaimanee, Y. & Jaeger, J.-J. Stable carbon isotope reconstructions of diet and paleoenvironment from the late middle Pleistocene Snake Cave in Northeastern Thailand. Naturwissenschaften 97, 299–309 (2010).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
64.Louys, J. & Roberts, P. Environmental drivers of megafauna and hominin extinction in Southeast Asia. Nature 586, 402–406 (2020).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
65.Passey, B. H. et al. Carbon isotope fractionation between diet, breath CO2, and bioapatite in different mammals. J. Archaeol. Sci. 32, 1459–1470 (2005).Article 

Google Scholar 
66.Dutt, S. et al. Abrupt changes in Indian summer monsoon strength during 33,800 to 5500 years B.P. Geophys. Res. Lett. 42, 5526–5532 (2015).ADS 
Article 

Google Scholar 
67.Ronay, E. R., Breitenbach, S. F. M. & Oster, J. L. Sensitivity of speleothem records in the Indian Summer Monsoon region to dry season infiltration. Sci. Rep. 9, 5091. https://doi.org/10.1038/s41598-019-41630-2 (2019).ADS 
CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
68Liu, G. et al. On the glacial-interglacial variability of the Asian monsoon in speleothem δ18O records. Sci. Adv. 6, 8eaay8189. https://doi.org/10.1126/sciadv.aay8189 (2020).CAS 
Article 

Google Scholar 
69.Lambeck, K., Rouby, H., Purcell, A., Sun, Y. & Sambridge, M. Sea level and global ice volumes from the Last Glacial Maximum to the Holocene. Proc. Natl. Acad. Sci. USA 111, 15296–15303 (2014).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
70Rabett, R. J. Human Adaptation in the Asian Palaeolithic: hominin dispersal and behaviour during the late quaternary (Cambridge University Press, 2012).Book 

Google Scholar 
71.Bailey, R. C. et al. Hunting and gathering in tropical rain forest: Is it possible?. Am. Anthropol. 91, 59–82 (1989).Article 

Google Scholar 
72.Mercader, J. Forest people: the role of African rainforests in human evolution and dispersal. Evol. Anthropol. 11, 117–124 (2002).Article 

Google Scholar 
73.Mercader, J. Under the Canopy: The Archaeology of Tropical Rainforests (Rutgers University Press, 2002).
Google Scholar 
74.Mercader, J. Foragers of the Congo: the early settlement of the Ituri forest. In Under the Canopy: The Archeology of Tropical Rain Forests (ed. Mercader, J.) 93–116 (Rutgers University Press, London, 2003).
Google Scholar 
75.Perera, N. et al. People of the ancient rainforest: Late Pleistocene foragers at the Batadomba-lena rockshelter, Sri Lanka. J. Hum. Evol. 61, 254–269 (2011).PubMed 
Article 
PubMed Central 

Google Scholar 
76.Roberts, P. et al. Direct evidence for human reliance on rainforest resources in late Pleistocene Sri Lanka. Science 347, 1246–1249 (2015).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
77.Roberts, P. et al. Fruits of the forest: human stable isotope ecology and rainforest adaptations in Late Pleistocene and Holocene (~36 to 3 ka) Sri Lanka. J. Hum. Evol. 106, 102–118 (2017).PubMed 
Article 
PubMed Central 

Google Scholar 
78Wedage, O. et al. Specialized rainforest hunting by Homo sapiens ~45,000 years ago. Nat. Commun. 10, 739. https://doi.org/10.1038/s41467-019-08623-1 (2019).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
79.Ji, X. et al. The oldest Hoabinhian technocomplex in Asia (43.5 ka) at Xiaodong rockshelter, Yunnan Province, southwest China. Quat. Int. 400, 166–174 (2016).Article 

Google Scholar 
80.Olsen, J. W. & Ciochon, R. L. A review of evidence for postulated Middle Pleistocene occupations in Viet Nam. J. Hum. Evol. 19, 761–788 (1990).Article 

Google Scholar 
81.Rabett, R. et al. The Tràng An Project: Late-to-Post-Pleistocene Settlement of the Lower Song Hong Valley, North Vietnam. J. R. Asiat. Soc. 19, 83–109 (2009).Article 

Google Scholar 
82.Rabett, R. et al. Tropical limestone forest resilience and late Pleistocene foraging during MIS-2 in the Tràng An massif, Vietnam. Quat. Int. 448, 62–81 (2017).Article 

Google Scholar 
83.Barker, G. et al. The ‘Human Revolution’ in lowland tropical Southeast Asia: the antiquity and behavior of anatomically modern humans at Niah Cave (Sarawak, Borneo). J. Hum. Evol. 52, 243–261 (2007).PubMed 
Article 
PubMed Central 

Google Scholar 
84.Piper, P. & Rabett, R. Hunting in a tropical rainforest: evidence from the terminal Pleistocene at Lobang Hangus, Niah Caves, Sarawak. Int. J. Osteoarchaeol. 19, 551–565 (2009).Article 

Google Scholar 
85.Hunt, C. O., Gilbertson, D. D. & Rushworth, G. A 50,000-year record of late Pleistocene tropical vegetation and human impact in lowland Borneo. Quat. Sci. Rev. 37, 61–80 (2012).ADS 
Article 

Google Scholar 
86.de Vos, J. The Pongo faunas from Java and Sumatra and their significance for biostratigraphical and paleoecological interpretations. Proc. K. Ned. Akad. Wet. B. 86, 417–425 (1983).
Google Scholar 
87.Westaway, K. E. An early modern human presence in Sumatra 73000–63000 years ago. Nature 548, 322–325 (2017).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
88.Storm, P. et al. Late Pleistocene Homo Sapiens in a tropical rainforest Fauna in East Java. J. Hum. Evol. 49, 536–545 (2005).PubMed 
Article 
PubMed Central 

Google Scholar 
89.Storm, P. & de Vos, J. Rediscovery of the late Pleistocene Punung Hominin Sites and the Discovery of a New Site Gunung Dawung in East Java. Senck. Leth. 86, 271–281 (2006).Article 

Google Scholar 
90Roberts, P. et al. Isotopic evidence for initial coastal colonization and subsequent diversification in the human occupation of Wallacea. Nat. Commun. 11, 2068. https://doi.org/10.1038/s41467-020-15969-4 (2020).ADS 
CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
91.Pasveer, J. M., Clarke, S. J. & Miller, G. H. Late Pleistocene human occupation of inland rainforest, Bird’s Head, Papua. Archaeol. Oceania 37, 92–95 (2002).Article 

Google Scholar 
92.Summerhayes, G. R. et al. Human adaptation and plant use in highland New Guinea 49,000 to 44,000 Years Ago. Science 330, 78–81 (2010).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
93.Summerhayes, G. R., Field, J. H., Shaw, B. & Gaffney, D. The archaeology of forest exploitation and change in the tropics during the Pleistocene: the case of Northern Sahul (Pleistocene New Guinea). Quat. Int. 448, 14–30 (2017).Article 

Google Scholar 
94.Roberts, P., Gaffney, D., Lee-Thorp, J. A. & Summerhayes, G. R. Persistent tropical foraging in the highlands of terminal Pleistocene/Holocene New Guinea. Nature Ecol. Evol. 1, 1–6 (2017).CAS 
Article 

Google Scholar 
95.Wedage, O. et al. Microliths in the South Asian rainforest ~45–4 ka: New insights from Fa-Hien Lena Cave, Sri Lanka. PLoS ONE https://doi.org/10.1371/journal.pone.0222606 (2019).Article 
PubMed 
PubMed Central 

Google Scholar 
96.Bettis, E. A. et al. Way out of Africa: early Pleistocene paleoenvironments inhabited by Homo erectus in Sangiran, Java. J. Hum. Evol. 56, 11–24 (2009).PubMed 
Article 
PubMed Central 

Google Scholar 
97.Brumm, A. et al. Age and context of the oldest known hominin fossils from Flores. Nature 534, 249–253 (2016).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
98.Hammer, Ø., Harper, D. A. T. & Ryan, P. D. PAST: Paleontological statistics software package for education and data analysis. Palaeontol. Electron. 4, 1–9 (2001).
Google Scholar  More

1.McLean, J. E., Pabst, M. W., Miller, C. D., Dimkpa, C. O. & Anderson, A. J. Effect of complexing ligands on the surface adsorption, internalization, and bioresponse of copper and cadmium in a soil bacterium, Pseudomonas Putida. Chemosphere 91(3), 374–382. https://doi.org/10.1016/j.chemosphere.2012.11.071 (2013).ADS 
CAS 
Article 
PubMed 

Google Scholar 
2.Clemens, S. Metal ligands in micronutrient acquisition and homeostasis. Plant. Cell Environ. 42(10), 2902–2912. https://doi.org/10.1111/pce.13627 (2019).CAS 
Article 
PubMed 

Google Scholar 
3.Ma, H. et al. Elucidation of the mechanisms into effects of organic acids on soil fertility, cadmium speciation and ecotoxicity in contaminated soil. Chemosphere 239, 124706. https://doi.org/10.1016/j.chemosphere.2019.124706 (2020).ADS 
CAS 
Article 
PubMed 

Google Scholar 
4.Ahmed, E. & Holmström, S. J. M. Siderophores in environmental research: Roles and applications. Microb. Biotechnol. 7(3), 196–208. https://doi.org/10.1111/1751-7915.12117 (2014).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
5.Butler, A. & Theisen, R. M. Iron(III)-siderophore coordination chemistry: Reactivity of marine siderophores. Coord. Chem. Rev. 254(3–4), 288–296. https://doi.org/10.1016/j.ccr.2009.09.010 (2010).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
6.Hider, R. C. & Kong, X. Chemistry and biology of siderophores. Nat. Prod. Rep. 27(5), 637. https://doi.org/10.1039/b906679a (2010).CAS 
Article 
PubMed 

Google Scholar 
7.Kirby, M. E., Sonnenberg, J. L., Simperler, A. & Weiss, D. J. Stability series for the complexation of six key siderophore functional groups with uranyl using density functional theory. J. Phys. Chem. A 124(12), 2460–2472. https://doi.org/10.1021/acs.jpca.9b10649 (2020).CAS 
Article 
PubMed 

Google Scholar 
8.Harrington, J. et al. Structural dependence of Mn complexation by siderophores: Donor group dependence on complex stability and reactivity. GCA. 88, 106–119 (2012).ADS 
CAS 

Google Scholar 
9.McRose, D. L., Seyedsayamdost, M. R. & Morel, F. M. M. Multiple siderophores: Bug or feature?. JBIC J. Biol. Inorg. Chem. 23(7), 983–993. https://doi.org/10.1007/s00775-018-1617-x (2018).CAS 
Article 
PubMed 

Google Scholar 
10.Johnstone, T. C., Nolan, E. M. Beyond iron: Non-classical biological functions of bacterial siderophores. In Dalton Transactions. Royal Society of Chemistry April 14, 2015, pp 6320–6339. https://doi.org/10.1039/c4dt03559c.11.Northover, G. H. R., Garcia-España, E. & Weiss, D. J. Unravelling the modus operandi of phytosiderophores during zinc uptake in rice: The importance of geochemical gradients and accurate stability constants. J. Exp. Bot. https://doi.org/10.1093/jxb/eraa580 (2020).Article 

Google Scholar 
12.Ghavami, N., Alikhani, H. A., Pourbabaee, A. A. & Besharati, H. Study the effects of siderophore-producing bacteria on zinc and phosphorous nutrition of canola and maize plants. Commun. Soil Sci. Plant Anal. 47(12), 1517–1527. https://doi.org/10.1080/00103624.2016.1194991 (2016).CAS 
Article 

Google Scholar 
13.Weiss, D. et al. Isotope fractionation of zinc in the paddy rice soil-water environment and the role of 2’deoxymugineic acid (DMA) as zincophore under Zn limiting conditions. Chem. Geol. 577, 120271. https://doi.org/10.1016/j.chemgeo.2021.120271 (2021).ADS 
CAS 
Article 

Google Scholar 
14.Suzuki, M. et al. Biosynthesis and secretion of mugineic acid family phytosiderophores in zinc-deficient barley. Plant J. 48(1), 85–97. https://doi.org/10.1111/j.1365-313X.2006.02853.x (2006).CAS 
Article 
PubMed 

Google Scholar 
15.Zaman, M. , Shahid, S. A., Heng, L., Shahid, S. A., Zaman, M., Heng, L. Soil salinity: Historical perspectives and a world overview of the problem. In Guideline for Salinity Assessment, Mitigation and Adaptation Using Nuclear and Related Techniques 43–53 (Springer, 2018). https://doi.org/10.1007/978-3-319-96190-3_2.16.Alfarrah, N. & Walraevens, K. Groundwater overexploitation and seawater intrusion in coastal areas of arid and semi-arid regions. Water 10(2), 143. https://doi.org/10.3390/w10020143 (2018).CAS 
Article 

Google Scholar 
17.Trenberth, K. Changes in precipitation with climate change. Clim. Res. 47(1), 123–138. https://doi.org/10.3354/cr00953 (2011).Article 

Google Scholar 
18.Pendergrass, A. G., Knutti, R., Lehner, F., Deser, C. & Sanderson, B. M. Precipitation variability increases in a warmer climate. Sci. Rep. 7(1), 1–9. https://doi.org/10.1038/s41598-017-17966-y (2017).CAS 
Article 

Google Scholar 
19.Errabii, T., Gandonou, C. H., Essalmani, H., Jamal; Senhaji, N. S. Effects of NaCl and mannitol induced stress on sugarcane (Saccharum Sp.) Callus Cultures. https://doi.org/10.1007/s11738-006-0006-1.20.Saboora, A., Hajihashemi, S. & Khatam, B. NaCl tolerance of wheat genotypes at germination and early seedling growth article in Pakistan. J. Biol. Sci. https://doi.org/10.3923/pjbs.2006.2009.2021 (2006).Article 

Google Scholar 
21.Chand, M., Randhawa, N. S. & Bhumbla, D. R. Effectiveness of zinc chelates in zinc nutrition of greenhouse rice crop in a saline-sodic soil. Plant Soil 59(2), 217–225. https://doi.org/10.1007/BF02184195 (1981).CAS 
Article 

Google Scholar 
22.Lores, E. M. & Pennock, J. R. The effect of salinity on binding of Cd, Cr, Cu and Zn to dissolved organic matter. Chemosphere 37(5), 861–874. https://doi.org/10.1016/S0045-6535(98)00090-3 (1998).ADS 
CAS 
Article 

Google Scholar 
23.Cigala, R. M. et al. Zinc(II) complexes with hydroxocarboxylates and mixed metal species with Tin(II) in different salts aqueous solutions at different ionic strengths: Formation, stability, and weak interactions with supporting electrolytes. Monatshefte fur Chemie 146(4), 527–540. https://doi.org/10.1007/s00706-014-1394-3 (2015).CAS 
Article 

Google Scholar 
24.Laird, D. A., Koskinen, I. W. C. Triazine Soil Interactions. In The Triazine Herbicides 275–299 (Elsevier, 2008). https://doi.org/10.1016/B978-044451167-6.50024-6.25.Cigala, R. M. et al. Speciation of Tin(II) in aqueous solution: Thermodynamic and spectroscopic study of simple and mixed hydroxocarboxylate complexes. Monatshefte fur Chemie 144(6), 761–772. https://doi.org/10.1007/s00706-013-0961-3 (2013).CAS 
Article 

Google Scholar 
26.Daniele, P. G., Rigano, C. & Sammartano, S. Ionic strength dependence of formation constants-I protonation constants of organic and inorganic acids. Talanta 30(2), 81–87. https://doi.org/10.1016/0039-9140(83)80023-X (1983).CAS 
Article 
PubMed 

Google Scholar 
27.Bretti, C., Foti, C. & Sammartano, S. A new approach in the use of sit in determining the dependence on ionic strength of activity coefficients. Application to Some Chloride Salts Of Interest In The Speciation Of Natural Fluids. Chem. Speciat. Bioavailab. 16(3), 105–110. https://doi.org/10.3184/095422904782775036 (2004).CAS 
Article 

Google Scholar 
28.Bretti, C., De Stefano, C., Foti, C. & Sammartano, S. Critical evaluation of protonation constants. Literature analysis and experimental potentiometric and calorimetric data for the thermodynamics of phthalate protonation in different ionic media. J. Solution Chem. 35(9), 1227–1244. https://doi.org/10.1007/s10953-006-9057-6 (2006).CAS 
Article 

Google Scholar 
29.Cigala, R. M. et al. Quantitative study on the interaction of Sn2+ and Zn2+ with some phosphate ligands, in aqueous solution at different ionic strengths. J. Mol. Liq. 165, 143–153. https://doi.org/10.1016/j.molliq.2011.11.002 (2012).CAS 
Article 

Google Scholar 
30.Northover, G. H. R., Mao, Y., Hanif M. D., Blasco, S., Vilar, R., Garcia-Espana, E. & Weiss, D. J. The control of pH and ionic strength gradients on the interaction of low-molecular-weight organic acids and siderophores. ChemRxiv. Preprint (2021). https://doi.org/10.26434/chemrxiv.14706036.v1.31.Domenico, P. A., Harris, D. R., Schwartz, F. W., Wiley, J., Chichester, N. Y., Brisbane, W. & Singapore, T. Physical and Chemical Hydrogeology 2nd edn.32.Pankow, J.; Taylor & Francis Group. Aquatic Chemistry Concepts 2nd edn.33.Graziano, G. Role of salts on the strength of pairwise hydrophobic interaction. Chem. Phys. Lett. 483(1–3), 67–71. https://doi.org/10.1016/j.cplett.2009.10.040 (2009).ADS 
CAS 
Article 

Google Scholar 
34.Mancera, R. L. Does salt increase the magnitude of the hydrophobic effect? A computer simulation study. Chem. Phys. Lett. 296(5–6), 459–465. https://doi.org/10.1016/S0009-2614(98)01080-X (1998).ADS 
CAS 
Article 

Google Scholar 
35.Mancera, R. L. Computer simulation of the effect of salt on the hydrophobic effect. J. Chem. Soc. Faraday Trans. 94(24), 3549–3559. https://doi.org/10.1039/a806899b (1998).CAS 
Article 

Google Scholar 
36.Ghosh, T., Kalra, A. & Garde, S. On the salt-induced stabilization of pair and many-body hydrophobic interactions. J. Phys. Chem. B 109(1), 642–651. https://doi.org/10.1021/jp0475638 (2005).CAS 
Article 
PubMed 

Google Scholar 
37.Papaneophytou, C. P., Grigoroudis, A. I., McInnes, C. & Kontopidis, G. Quantification of the effects of ionic strength, viscosity, and hydrophobicity on protein-ligand binding affinity. ACS Med. Chem. Lett. 5(8), 931–936. https://doi.org/10.1021/ml500204e (2014).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
38.Ghafoor, K., AL-Juhaimi, F., Ozcan, M. M. & Jahurul, M. H. A. Some nutritional characteristics and mineral contents in Barley (Hordeum Vulgare L.) seeds cultivated under salt stress. Qual. Assur. Saf. Crop. Foods 7(3), 363–368. https://doi.org/10.3920/QAS2013.0380 (2015).CAS 
Article 

Google Scholar 
39.Akman, Z. Effects of plant growth regulators on nutrient content of young wheat and barley plants under
saline conditions. J. Anim. Vet. Adv. 8(10), 2018–2021 (2009).CAS 

Google Scholar 
40.Yousfi, S., Houmani, H., Zribi, F., Abdelly, C. & Gharsalli, M. Physiological responses of wild and cultivated barley to the interactive effect of salinity and iron deficiency. (2012). https://doi.org/10.5402/2012/121983.41.Alderighi, L. et al. Hyperquad simulation and speciation (HySS): A utility program for the investigation of equilibria involving soluble and partially soluble species. Coord. Chem. Rev. 184(1), 311–318. https://doi.org/10.1016/S0010-8545(98)00260-4 (1999).CAS 
Article 

Google Scholar 
42.Gans, P. & O’Sullivan, B. GLEE: A new computer program for glass electrode calibration. Talanta 51(1), 33–37. https://doi.org/10.1016/s0039-9140(99)00245-3 (2000).CAS 
Article 
PubMed 

Google Scholar 
43.Gans, P., Sabatini, A. & Vacca, A. Investigation of equilibria in solution. Determination of equilibrium constants with the HYPERQUAD suite of programs. Talanta 43(10), 1739–1753. https://doi.org/10.1016/0039-9140(96)01958-3 (1996).CAS 
Article 
PubMed 

Google Scholar 
44.Hu, W., Xie, J., Chau, H. W. & Si, B. C. Evaluation of parameter uncertainties in nonlinear regression using Microsoft excel spreadsheet. Environ. Syst. Res. 4(1), 1–12. https://doi.org/10.1186/s40068-015-0031-4 (2015).ADS 
CAS 
Article 

Google Scholar 
45.Harris, W. R., Raymond, K. N. & Weitl, F. L. Ferric ion sequestering agents. 6. The spectrophotometric and potentiometric evaluation of sulfonated tricatecholate ligands. J. Am. Chem. Soc. 103(10), 2667–2675. https://doi.org/10.1021/ja00400a030 (1981).CAS 
Article 

Google Scholar 
46.Bravin, M. N., Tentscher, P., Rose, J. & Hinsinger, P. Rhizosphere PH Gradient Controls Copper Availability in a Strongly Acidic Soil. Environ. Sci. Technol. 43(15), 5686–5691. https://doi.org/10.1021/es900055k (2009).ADS 
CAS 
Article 
PubMed 

Google Scholar 
47.Gollany, H. T. & Schumacher, T. E. Combined use of colorimetric and microelectrode methods for evaluating rhizosphere PH. Plant Soil 154(2), 151–159. https://doi.org/10.1007/BF00012520 (1993).CAS 
Article 

Google Scholar 
48.Kirk, G. J. D. Root ventilation, rhizosphere modification, and nutrient uptake by rice. In Systems Approaches for Agricultural Development 221–232 (Springer, Netherlands, 1993). https://doi.org/10.1007/978-94-011-2842-1_13.49.Li, J. & Heap, A. D. Spatial interpolation methods applied in the environmental sciences: A review. In Environmental Modelling and Software 173–189 (Elsevier, 2014). https://doi.org/10.1016/j.envsoft.2013.12.008.50.Gergely, A., Kiss, T. & Deák, G. Complexes of 3,4-dihydroxyphenyl derivatives. II. Complex formation processes in the Nickel(II)-L-DOPA and Zinc(II)-L-DOPA systems. Inorganica Chim. Acta 36(1), 113–120. https://doi.org/10.1016/S0020-1693(00)89379-2 (1979).CAS 
Article 

Google Scholar 
51.Griesser, R. & Sigel, H. Ternary complexes in solution. XI. complex formation between the cobalt(h)-, nickel(ii)-, copper(ii)-, and zinc(II)-2,2′-bipyridyl 1:1 complexes and ethylenediamine, glycinate, or pyrocatecholate. Inorg. Chem. 10(10), 2229–2232. https://doi.org/10.1021/ic50104a028 (1971).CAS 
Article 

Google Scholar 
52.Das, A. K. Studies on mixed ligand complexes of cobalt(II), nickel(II), copper(II) and zinc(II) involving 8-hydroxyquinoline-5-sulphonic acid as a primary ligand and substituted catechols as secondary ligands. Transition Met. Chem. 14, 200–209 (1989).CAS 
Article 

Google Scholar 
53.Das, A. K. Astatistical aspects of the stabilities of ternary complexes of cobalt(II), nickel(II), copper(II) and zinc(II) involving amino-polycarboxylic acids and heteroaromatic N-bases as primary ligands and acetohydroxamic acid as a secondary ligand. Transition Met. Chem. 14, 66–68 (1989).CAS 
Article 

Google Scholar 
54.Cannan, R. K. & Kibrick, A. Complex formation between carboxylic acids and divalent metal cations. J. Am. Chem. Soc. 60(10), 2314–2320. https://doi.org/10.1021/ja01277a012 (1938).CAS 
Article 

Google Scholar 
55.Farkas, E., Brown, D. A., Cittaro, R. & Glass, W. K. Metal complexes of glutamic acid-γ-hydroxamic acid (Glu-γ-Ha) (N-hydroxyglutamine) in aqueous solution. J. Chem. Soc. Dalt. Trans. 18, 2803–2807. https://doi.org/10.1039/DT9930002803 (1993).Article 

Google Scholar 
56.Farkas, E., Enyedy, É. A. & Csóka, H. Some factors affecting metal ion-monohydroxamate interactions in aqueous solution. J. Inorg. Biochem. 79(1–4), 205–211. https://doi.org/10.1016/S0162-0134(99)00158-0 (2000).CAS 
Article 
PubMed 

Google Scholar 
57.Warnke, Z. Investigation on divalent metal complexes with oxyacids in aqueous solutions. 6. Potentiometric investigation on copper(II), zinc(II), and cadmium(II) complexes with glycolic acd. Rocz. Chem. 43, 1939 (1969).CAS 

Google Scholar 
58.Lengyel, T. Investigations on ion exchange equilibria with radioactive tracer method. 15. Liquid ion exchange technique for investigating mixed complex species of zinc with glycolic and alpha-hydroxyisobutyric acid. Acta Chim. Acad. Sci. Hung. 60, 373 (1969).CAS 

Google Scholar 
59.Athavale, V. T., Prabhu, L. H. & Vartak, D. G. Solution stability constants of some metal complexes of derivatives of catechol. J. Inorg. Nucl. Chem. 28(5), 1237–1249. https://doi.org/10.1016/0022-1902(66)80450-5 (1966).CAS 
Article 

Google Scholar 
60.Portanova, R., Lajunen, L. H. J., Tolazzi, M. & Piispanen, J. Critical evaluation of stability constants for α-hydroxycarboxylic acid complexes with protons and metal ions and the accompanying enthalpy changes: Part II. Aliphatic 2-hydroxycarboxylic acids (IUPAC technical report). Pure Appl. Chem. 75(4), 495–540. https://doi.org/10.1351/pac200375040495 (2003).CAS 
Article 

Google Scholar 
61.Krężel, A. & Maret, W. The biological inorganic chemistry of zinc ions. Arch. Biochem. Biophys. 611, 3–19. https://doi.org/10.1016/j.abb.2016.04.010 (2016).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
62.Al-Sogair, F. M.; Operschall, B. P.; Sigel, A.; Sigel, H.; Schnabl, J.; Sigel, R. K. O. Probing the Metal-Ion-Binding Strength of the Hydroxyl Group. In Chemical Reviews. American Chemical Society August 10, 964–5003 (2011). https://doi.org/10.1021/cr100415s.63.Gries, D., Brunn, S., Crowley, D. E. & Parker, D. R. Phytosiderophore release in relation to micronutrient metal deficiencies in Barley. Plant Soil 172(2), 299–308. https://doi.org/10.1007/BF00011332 (1995).CAS 
Article 

Google Scholar 
64.Welch, R. M. & Shuman, L. Micronutrient nutrition of plants. CRC Crit. Rev. Plant Sci. 14(1), 49–82. https://doi.org/10.1080/07352689509701922 (1995).CAS 
Article 

Google Scholar 
65.Arnold, T. et al. Evidence for the mechanisms of zinc uptake by rice using isotope fractionation. Plant. Cell Environ. 33(3), 370–381. https://doi.org/10.1111/j.1365-3040.2009.02085.x (2010).CAS 
Article 
PubMed 

Google Scholar 
66.Haas, H. Fungal siderophore metabolism with a focus on Aspergillus fumigatus. Nat. Prod. Rep. 31(10), 1266–1276. https://doi.org/10.1039/c4np00071d (2014).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
67.Griffin, A. S., West, S. A. & Buckling, A. Cooperation and competition in pathogenic bacteria. Nature 430(7003), 1024–1027. https://doi.org/10.1038/nature02744 (2004).ADS 
CAS 
Article 
PubMed 

Google Scholar 
68.Wu, D. et al. Tissue metabolic responses to salt stress in wild and cultivated barley. PLoS ONE 8(1), e55431. https://doi.org/10.1371/journal.pone.0055431 (2013).ADS 
CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
69.Widodo, Patterson, J. H.; Newbigin, E. et al.. Metabolic responses to salt stress of Barley (Hordeum Vulgare L.) cultivars, sahara and clipper, which differ in salinity tolerance. J. Exp. Bot. 60(14), 4089–4103 (2009). https://doi.org/10.1093/jxb/erp243CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
70.Yang, C.-W. et al. Comparative effects of salt-stress and alkali-stress on the growth, photosynthesis, solute accumulation, and ion balance of Barley plants. Phytosynthetica 47, 79–86 (2009).CAS 
Article 

Google Scholar  More