Ecology

1.
Nazaries, L. et al. Evidence of microbial regulation of biogeochemical cycles from a study on methane flux and land use change. Appl. Environ. Microbiol. 79, 4031–4040. https://doi.org/10.1128/aem.00095-13 (2013).
CAS  Article  PubMed  PubMed Central  Google Scholar 
2.
Offre, P., Spang, A. & Schleper, C. Archaea in biogeochemical cycles. Annu. Rev. Microbiol. 67(67), 437–457. https://doi.org/10.1146/annurev-micro-092412-155614 (2013).
CAS  Article  PubMed  Google Scholar 

3.
Rousk, J. & Bengtson, P. Microbial regulation of global biogeochemical cycles. Front. Microbiol. https://doi.org/10.3389/fmicb.2014.00103 (2014).
Article  PubMed  PubMed Central  Google Scholar 

4.
IPCC. Climate Change 2013: The physical science basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change 1535 pp (Cambridge, United Kingdom and New York, NY, USA, 2013).

5.
Shade, A. et al. Fundamentals of microbial community resistance and resilience. Front. Microbiol. https://doi.org/10.3389/fmicb.2012.00417 (2012).
Article  PubMed  PubMed Central  Google Scholar 

6.
Allison, S. D. & Martiny, J. B. H. Resistance, resilience, and redundancy in microbial communities. Proc. Natl. Acad. Sci. USA 105, 11512–11519. https://doi.org/10.1073/pnas.0801925105 (2008).
ADS  Article  PubMed  Google Scholar 

7.
Griffiths, B. S. & Philippot, L. Insights into the resistance and resilience of the soil microbial community. FEMS Microbiol. Rev. 37, 112–129. https://doi.org/10.1111/j.1574-6976.2012.00343.x (2013).
CAS  Article  PubMed  Google Scholar 

8.
Lindh, M. V. & Pinhassi, J. Sensitivity of bacterioplankton to environmental disturbance: a review of Baltic Sea field studies and experiments. Front. Mar. Sci. https://doi.org/10.3389/fmars.2018.00361 (2018).
Article  Google Scholar 

9.
Free, A., McDonald, M. A. & Pagaling, E. Diversity-function relationships in natural, applied, and engineered microbial ecosystems. Adv. Appl. Microbiol. 105(105), 131–189. https://doi.org/10.1016/bs.aambs.2018.07.002 (2018).
CAS  Article  PubMed  Google Scholar 

10.
Hillebrand, H. et al. Decomposing multiple dimensions of stability in global change experiments. Ecol. Lett. 21, 21–30. https://doi.org/10.1111/ele.12867 (2018).
Article  PubMed  Google Scholar 

11.
Griffiths, B. S. et al. Ecosystem response of pasture soil communities to fumigation-induced microbial diversity reductions: an examination of the biodiversity-ecosystem function relationship. Oikos 90, 279–294. https://doi.org/10.1034/j.1600-0706.2000.900208.x (2000).
Article  Google Scholar 

12.
Baho, D. L., Peter, H. & Tranvik, L. J. Resistance and resilience of microbial communities-temporal and spatial insurance against perturbations. Environ. Microbiol. 14, 2283–2292. https://doi.org/10.1111/j.1462-2920.2012.02754.x (2012).
Article  PubMed  Google Scholar 

13.
Berga, M., Székely, A. J. & Langenheder, S. Effects of disturbance intensity and frequency on bacterial community composition and function. PLoS ONE 7, e36959 (2012).
ADS  CAS  Article  Google Scholar 

14.
Ager, D., Evans, S., Li, H., Lilley, A. K. & van der Gast, C. J. Anthropogenic disturbance affects the structure of bacterial communities. Environ. Microbiol. 12, 670–678. https://doi.org/10.1111/j.1462-2920.2009.02107.x (2010).
Article  PubMed  Google Scholar 

15.
Sjöstedt, J. et al. Reduced diversity and changed bacterioplankton community composition do not affect utilization of dissolved organic matter in the Adriatic Sea. Aquat. Microb. Ecol. 71, 15–24 (2013).
Article  Google Scholar 

16.
Vaquer-Sunyer, R. et al. Dissolved organic nitrogen inputs from wastewater treatment plant effluents increase responses of planktonic metabolic rates to warming. Environ. Sci. Technol. 49, 11411–11420. https://doi.org/10.1021/acs.est.5b00674 (2015).
ADS  CAS  Article  PubMed  Google Scholar 

17.
Bergen, B. et al. Acidification and warming affect prominent bacteria in two seasonal phytoplankton bloom mesocosms. Environ. Microbiol. 18, 4579–4595. https://doi.org/10.1111/1462-2920.13549 (2016).
CAS  Article  PubMed  Google Scholar 

18.
Salis, R. K., Bruder, A., Piggott, J. J., Summerfield, T. C. & Matthaei, C. D. High-throughput amplicon sequencing and stream benthic bacteria: identifying the best taxonomic level for multiplestressor research. Sci. Rep. 7, 12. https://doi.org/10.1038/srep44657 (2017).
CAS  Article  Google Scholar 

19.
Sjöstedt, J., Langenheder, S., Kritzberg, E., Karlsson, C. M. G. & Lindstrom, E. S. Repeated disturbances affect functional but not compositional resistance and resilience in an aquatic bacterioplankton community. Environ. Microbiol. Rep. 10, 493–500. https://doi.org/10.1111/1758-2229.12656 (2018).
CAS  Article  PubMed  Google Scholar 

20.
Odum, E. P. in Stress effects on natural ecosystems (eds G. W. Barrett & R. Rosenberg) 43–47 (Wiley, London 1981).

21.
Herren, C. M., Webert, K. C. & McMahon, K. D. Environmental disturbances decrease the variability of microbial populations within periphyton. mSystems 1, 14. https://doi.org/10.1128/mSystems.00013-16 (2016).
Article  Google Scholar 

22.
Tobor-Kaplon, M. A., Bloem, J. & de Ruiter, P. C. Functional stability of microbial communites from long-term stressed soils to additional disturbances. Environ. Toxicol. Chem. 25, 1993–1999 (2006).
CAS  Article  Google Scholar 

23.
Tolkkinen, M. et al. Multi-stressor impacts on fungal diversity and ecosystem functions in streams: natural vs. anthropogenic stress. Ecology 96, 672–683. https://doi.org/10.1890/14-0743.1 (2015).
CAS  Article  PubMed  Google Scholar 

24.
Müller, A. K., Westergaard, K., Christensen, S. & Sørensen, S. J. The diversity and function of soil microbial communities exposed to different disturbances. Microb. Ecol. 44, 49–58 (2002).
Article  Google Scholar 

25.
Leyer, G. J. & Johnson, E. A. Acid adaptation induces cross-protection against environmental stresses in salmonella-typhimurium. Appl. Environ. Microbiol. 59, 1842–1847. https://doi.org/10.1128/aem.59.6.1842-1847.1993 (1993).
CAS  Article  PubMed  PubMed Central  Google Scholar 

26.
Rillig, M. C., Rolff, J., Tietjen, B., Wehner, J. & Andrade-Linares, D. R. Community priming-effects of sequential stressors on microbial assemblages. FEMS Microbiol. Ecol. https://doi.org/10.1093/femsec/fiv040 (2015).
Article  PubMed  Google Scholar 

27.
Andrade-Linares, D. R., Lehmann, A. & Rillig, M. C. Microbial stress priming—a meta-analysis. Environ. Microbiol. https://doi.org/10.1111/1462-2920.13223 (2016).
Article  PubMed  Google Scholar 

28.
Cebrian, G., Sagarzazu, N., Pagan, R., Condon, S. & Manas, P. Development of stress resistance in Staphylococcus aureus after exposure to sublethal environmental conditions. Int. J. Food Microbiol. 140, 26–33. https://doi.org/10.1016/j.ijfoodmicro.2010.02.017 (2010).
CAS  Article  PubMed  Google Scholar 

29.
Vinebrooke, R. D. et al. Impacts of multiple stressors on biodiversity and ecosystem functioning: the role of species co-tolerance. Oikos 104, 451–457 (2004).
Article  Google Scholar 

30.
Mills, A. L. & Mallory, L. M. The community structure of sessile heterotrophic bacteria stressed by acid mine drainage. Microb. Ecol. 14, 219–232 (1987).
CAS  Article  Google Scholar 

31.
Atlas, R. M., Horowitz, A., Krichevsky, M. & Bej, A. K. Response of microbial populations to environmental disturbance. Microb. Ecol. 22, 249–256 (1991).
CAS  Article  Google Scholar 

32.
Berga, M., Zha, Y. H., Szekely, A. J. & Langenheder, S. Functional and compositional stability of bacterial metacommunities in response to salinity changes. Front. Microbiol. 8, 11. https://doi.org/10.3389/fmicb.2017.00948 (2017).
Article  Google Scholar 

33.
Allison, G. The influence of species diversity and stress intensity on community resistance and resilience. Ecol. Monogr. 74, 117–134. https://doi.org/10.1890/02-0681 (2004).
Article  Google Scholar 

34.
Downing, A. L. & Leibold, M. A. Species richness facilitates ecosystem resilience in aquatic food webs. Freshwat. Biol. 55, 2123–2137. https://doi.org/10.1111/j.1365-2427.2010.02472.x (2010).
Article  Google Scholar 

35.
Kim, M., Heo, E., Kang, H. & Adams, J. Changes in soil bacterial community structure with increasing disturbance frequency. Microb. Ecol. 66, 171–181. https://doi.org/10.1007/s00248-013-0237-9 (2013).
Article  PubMed  Google Scholar 

36.
Gibbons, S. M. et al. Disturbance regimes predictably alter diversity in an ecologically complex bacterial system. mBio https://doi.org/10.1128/mBio.01372-16 (2016).
Article  PubMed  PubMed Central  Google Scholar 

37.
Devictor, V., Julliard, R. & Jiguet, F. Distribution of specialist and generalist species along spatial gradients of habitat disturbance and fragmentation. Oikos 117, 507–514. https://doi.org/10.1111/j.2008.0030-1299.16215.x (2008).
Article  Google Scholar 

38.
Futuyma, D. J. & Moreno, G. The evolution of ecological specialization. Annu. Rev. Ecol. Syst. 19, 207–233. https://doi.org/10.1146/annurev.es.19.110188.001231 (1988).
Article  Google Scholar 

39.
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. https://doi.org/10.1890/08-0851.1 (2009).
Article  PubMed  Google Scholar 

40.
Blanck, H. A critical review of procedures and approaches used for assessing pollution-induced community tolerance (PICT) in biotic communities. Hum. Ecol. Risk Assess. 8, 1003–1034. https://doi.org/10.1080/1080-700291905792 (2002).
Article  Google Scholar 

41.
Li, J. et al. Initial copper stress strengthens the resistance of soil microorganisms to a subsequent copper stress. Microb. Ecol. 67, 931–941. https://doi.org/10.1007/s00248-014-0391-8 (2014).
CAS  Article  PubMed  Google Scholar 

42.
Girvan, M. S., Campbell, C. D., Killham, K., Prosser, J. I. & Glover, L. A. Bacterial diversity promotes community stability and functional resilience after perturbation. Environ. Microbiol. 7, 301–313 (2005).
CAS  Article  Google Scholar 

43.
Azarbad, H. et al. Resilience of soil microbial communities to metals and additional stressors: DNA-based approaches for assessing “stress-on-stress” responses. Int. J. Mol. Sci. 17, 1–21 (2016).
Article  Google Scholar 

44.
Calow, P. Physiological costs of combating chemical toxicants: ecological implications. Comp. Biochem. Physiol. Part C Comp. Pharmacol. 100, 3–6 (1991).
CAS  Article  Google Scholar 

45.
Kuperman, R. G. & Carreiro, M. M. Soil heavy metal concentrations, microbial biomass and enzyme activities in contaminated grassland ecosytem. Soil Biol. Biochem. 29, 179–190 (1997).
CAS  Article  Google Scholar 

46.
Mulder, C. P. H., Uliassi, D. D. & Doak, D. F. Physical stress and diversity-productivity relationships: the role of positive interactions. Proc. Natl. Acad. Sci. USA 98, 6704–6708. https://doi.org/10.1073/pnas.111055298 (2001).
ADS  CAS  Article  PubMed  Google Scholar 

47.
Grman, E., Lau, J. A., Schoolmaster, D. R. & Gross, K. L. Mechanisms contributing to stability in ecosystem function depend on the environmental context. Ecol. Lett. 13, 1400–1410. https://doi.org/10.1111/j.1461-0248.2010.01533.x (2010).
Article  PubMed  Google Scholar 

48.
Philippot, L. et al. Effect of primary mild stress on resilience and resistance of the nitrate reducer community to a subsequent severe stress. FEMS Microbiol. Lett. 285, 51–57 (2008).
CAS  Article  Google Scholar 

49.
Kassen, B. & Bell, G. Experimental evolution in Chlamydomonas. IV. Selection in environments that vary through time at different scales. Heredity 80, 732–741 (1998).
Article  Google Scholar 

50.
Venail, P. A., Kaltz, O., Olivieri, I., Pommier, T. & Mouquet, N. Diversification in temporally heterogeneous environments: effect of the grain in experimental bacterial populations. J. Evol. Biol. 24, 2485–2495. https://doi.org/10.1111/j.1420-9101.2011.02376.x (2011).
CAS  Article  PubMed  Google Scholar 

51.
Nezhad, M. H., Hussain, M. A. & Britz, M. L. Stress responses in probiotic Lactobacillus casei. Crit. Rev. Food Sci. Nutr. 55, 740–749. https://doi.org/10.1080/10408398.2012.675601 (2015).
CAS  Article  Google Scholar 

52.
Zhai, Z. Y. et al. Proteomic characterization of the acid tolerance response in Lactobacillus delbrueckii subsp bulgaricusCAUH1 and functional identification of a novel acid stress-related transcriptional regulator Ldb0677. Environ. Microbiol. 16, 1524–1537. https://doi.org/10.1111/1462-2920.12280 (2014).
CAS  Article  PubMed  Google Scholar 

53.
Morita, R. Y. Psychrophilic bacteria. Bacteriol. Rev. 39, 144–167 (1975).
CAS  Article  Google Scholar 

54.
Persson, I., Pirard, J., Larsson, A., Holm, C. & Lousa-Alvin, A. Kväveafskiljningens effekt på Ekoln. Report No. 2012-12, 72 (Svenskt Vatten Utveckling, 2012).

55.
Baath, E. & Kritzberg, E. pH tolerance in freshwater bacterioplankton: trait variation of the community as measured by leucine incorporation. Appl. Environ. Microbiol. 81, 7411–7419. https://doi.org/10.1128/aem.02236-15 (2015).
Article  PubMed  PubMed Central  Google Scholar 

56.
Sinclair, L., Osman, O. A., Bertilsson, S. & Eiler, A. Microbial community composition and diversity via 16S rRNA gene amplicons: evaluating the illumina platform. PLoS ONE https://doi.org/10.1371/journal.pone.0116955 (2015).
Article  PubMed  PubMed Central  Google Scholar 

57.
Edgar, R. C. UPARSE highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10, 996+ (2013).
CAS  Article  Google Scholar 

58.
Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461 (2010).
CAS  Article  Google Scholar 

59.
Apprill, A., McNally, S., Parsons, R. & Weber, L. Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton. Aquat. Microb. Ecol. 75, 129–137. https://doi.org/10.3354/ame01753 (2015).
Article  Google Scholar 

60.
Oksanen, J. et al. vegan: Community Ecology Package. https://CRAN.R-project.org/package=vegan (2015).

61.
del Giorgio, P., Bird, D. F., Prairie, Y. T. & Planas, D. Flow cytometric determination of bacterial abundance in lake plankton with the green nucleic acid stain SYTO 13. Limnol. Oceanogr. 41, 783–789 (1996).
ADS  Article  Google Scholar 

62.
Smith, D. C. & Azam, F. A simple, economical method for measuring bacterial protein synthesis rates in seawater using 3H-Leucine. Mar. Microbial. Food Webs 6, 107–114 (1992).
Google Scholar 

63.
Kirchman, D. L. in Handbook of methods in aquatic microbial ecology (eds P. F. Kemp, E. B. Sherr, B. F. Sherr, & J. J. Cole) (Lewis Publishers, London, 1993).

64.
Ylla, I., Peter, H., Romani, A. M. & Tranvik, L. J. Different diversity-functioning relationship in lake and stream bacterial communities. FEMS Microbiol. Ecol. 85, 95–103. https://doi.org/10.1111/1574-6941.12101 (2013).
Article  PubMed  Google Scholar 

65.
Maxwell, S. E., Delaney, H. D. & Kelly, K. Designing Experiments and Analyzing Data: A Model Comparison Perspective (3, Routledge, London, 2018).
Google Scholar  More

1.
Brunetti, R. et al. Morphological evidence that the molecularly determined Ciona intestinalis type A and type B are different species: Ciona robusta and Ciona intestinalis. J. Zool. Syst. Evol. Res. 53, 186–193. https://doi.org/10.1111/jzs.12101 (2015).
Article  Google Scholar 
2.
Lambert, C. C. Historical introduction, overview, and reproductive biology of the protochordates. Can. J. Zool. 83, 1–7. https://doi.org/10.1139/z04-160 (2005).
Article  Google Scholar 

3.
Dybern, B. I. The distribution and salinity tolerance of Ciona intestinalis (L.) F. typica with special reference to the waters around Southern Scandinavia. Ophelia 4, 207–226. https://doi.org/10.1080/00785326.1967.10409621 (1967).
Article  Google Scholar 

4.
Lambert, C. C. & Lambert, G. Persistence and differential distribution of nonindigenous ascidians in harbors of the Southern California Bight. Mar. Ecol. Progr. Ser. https://doi.org/10.3354/meps259145 (2003).
Article  Google Scholar 

5.
Lambert, C. C. & Lambert, G. Non-indigenous ascidians in southern California harbors and marinas. Mar. Biol. 130, 675–688. https://doi.org/10.1007/s002270050289 (1998).
Article  Google Scholar 

6.
Lundälv, T. & Christie, H. Comparative trends and ecological patterns of rocky subtidal communities in the Swedish and Norwegian Skagerrak area. Hydrobiologia 142, 71–80. https://doi.org/10.1007/BF00026748 (1987).
Article  Google Scholar 

7.
Hoshino, Z. & Nishikawa, T. Taxonomic studies of Ciona intestinalis (L.) and its allies. Seto Mar. Biol. Lab. Pubbl. 30, 61–79 (1985).
Article  Google Scholar 

8.
Mazzola, A. & Riggio, S. Fouling of Palermo harbour. 2nd contribution. Mem. Biol. Mar. Oceanogr. 6, 41–43 (1977).
Google Scholar 

9.
Havenhand, J. N. & Svane, I. Roles of hydrodynamics and larval behaviour in determining spatial aggregation in the tunicate Ciona intestinalis. Mar. Ecol. Progr. Ser. 68, 271–276. https://doi.org/10.3354/meps068271 (1991).
ADS  Article  Google Scholar 

10.
Koechlin, N. Settlement of epifauna of Spirographis spallanzani, Sycon ciliatum and Ciona intestinalis in the harbor of Lezardrieux. Cah. Biol. Mar. 18, 325–337 (1977).
Google Scholar 

11.
Zupo, V., Buia, M. C., Gambi, M. C., Lorenti, M. & Procaccini, G. Temporal variations in the spatial distribution of shoot density in a Posidonia oceanica meadow and patterns of genetic diversity. Mar. Ecol. 27, 328–338. https://doi.org/10.1111/j.1439-0485.2006.00133.x (2006).
ADS  Article  Google Scholar 

12.
Keough, M. J. Patterns of recruitment of sessile invertebrates in two subtidal habitats. J. Exp. Mar. Biol. Ecol. 66, 213–245. https://doi.org/10.1016/0022-0981(83)90162-4 (1983).
Article  Google Scholar 

13.
Cayer, D., MacNeil, M. & Bagnall, A. G. Tunicate fouling in Nova Scotia aquaculture: a new development. J. Shellfish Res. 18, 327 (1999).
Google Scholar 

14.
de Oliveira Marins, F., da Silva Oliveira, C., Maciel, N. M. V. & Skinner, L. F. Reinclusion of Ciona intestinalis (Ascidiacea: Cionidae) in Brazil—a methodological view. Mar. Biodivers. Rec. https://doi.org/10.1017/S175526720900116X (2009).
Article  Google Scholar 

15.
Svane, I. & Lundälv, T. Reproductive patterns and population dynamics of Ascidia mentula O.F. Müller on the Swedish west coast. J. Exp. Mar. Biol. Ecol. 50, 163–182. https://doi.org/10.1016/0022-0981(81)90048-4 (1981).
Article  Google Scholar 

16.
Svane, I. & Lundalv, T. Persistence stability in ascidian populations: long-term population dynamics and reproductive pattern of Pyura tessellata (forbes) in gullmarfjorden on the swedish west coast. Sarsia 67, 249–257. https://doi.org/10.1016/0022-0981(81)90048-4 (1982).
Article  Google Scholar 

17.
Svane, I. Ascidian reproductive patterns related to long-term population dynamics. Sarsia 68, 249–255. https://doi.org/10.1080/00364827.1982.10421339 (1983).
Article  Google Scholar 

18.
Lambert, G. The general ecology and growth of a solitary ascidian, Corella willmeriana. Biol. Bull. 135, 296–307. https://doi.org/10.2307/1539783 (1968).
Article  PubMed  Google Scholar 

19.
Goodbody, I. The biology of Ascidia nigra (Savigny). 11. The development and survival of young ascidians. Biol. Bull. 124, 31–44. https://doi.org/10.2307/1539566 (1963).
Article  Google Scholar 

20.
Goodbody, I. The Biology of Ascidia nigra (Savigny). I. Survival and mortality in an adult population. Biol. Bull. 122, 40–51. https://doi.org/10.2307/1539320 (1962).
Article  Google Scholar 

21.
Sato, A., Satoh, N. & Bishop, J. D. D. Field identification of ‘types’ A and B of the ascidian Ciona intestinalis in a region of sympatry. Mar. Biol. 159, 1611–1619. https://doi.org/10.1007/s00227-012-1898-5 (2012).
Article  Google Scholar 

22.
Harada, Y. et al. Mechanism of self-sterility in a hermaphroditic chordate. Science 320, 548–550. https://doi.org/10.1126/science.1152488 (2008).
ADS  CAS  Article  PubMed  Google Scholar 

23.
Sawada, H., Morita, M. & Iwano, M. Self/non-self recognition mechanisms in sexual reproduction: New insight into the self-incompatibility system shared by flowering plants and hermaphroditic animals. Biochem. Biophys. Res. Commun. 450, 1142–1148. https://doi.org/10.1016/j.bbrc.2014.05.099 (2014).
CAS  Article  PubMed  Google Scholar 

24.
Dehal, P. et al. The draft genome of Ciona intestinalis: Insights into chordate and vertebrate origins. Science 298, 2157–2167. https://doi.org/10.1126/science.1080049 (2002).
ADS  CAS  Article  PubMed  Google Scholar 

25.
Sasaki, A., Miyamoto, Y., Satou, Y., Satoh, N. & Ogasawara, M. Novel endostyle-specific genes in the ascidian Ciona intestinalis. Zool. Sci. 20, 1025–1030. https://doi.org/10.2108/zsj.20.1025 (2003).
CAS  Article  PubMed  Google Scholar 

26.
Joly, J. S. et al. Culture of Ciona intestinalis in closed systems. Dev. Dyn. 236, 1832–1840. https://doi.org/10.1002/dvdy.21124 (2007).
Article  PubMed  Google Scholar 

27.
Gallo, A. & Tosti, E. Adverse effect of antifouling compounds on the reproductive mechanisms of the ascidian Ciona intestinalis. Mar. Drugs 11, 3554–3568. https://doi.org/10.3390/md11093554 (2013).
CAS  Article  PubMed  PubMed Central  Google Scholar 

28.
Corbo, J. C., Di Gregorio, A. & Levine, M. The Ascidian as a model organism in developmental and evolutionary biology. Cell 106, 535–538. https://doi.org/10.1016/s0092-8674(01)00481-0 (2001).
CAS  Article  PubMed  Google Scholar 

29.
Stolfi, A. & Christiaen, L. Genetic and genomic toolbox of the chordate Ciona intestinalis. Genetics 192(1), 55–66. https://doi.org/10.1534/genetics.112.140590 (2012).
CAS  Article  PubMed  PubMed Central  Google Scholar 

30.
Dahlberg, C. et al. Refining the Ciona intestinalis model of central nervous system regeneration. PLoS ONE 4(2), e4458. https://doi.org/10.1371/journal.pone.0004458 (2009).
ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

31.
Bollner, T., Beesley, P. W. & Thorndyke, M. C. Distribution of GABA-like immunoreactivity during post-metamorphic development and regeneration of the central nervous system in the ascidian Ciona intestinalis. Cell Tissue Res. 272, 553–561. https://doi.org/10.1007/BF00318562 (1993).
CAS  Article  Google Scholar 

32.
Ando, R., Hama, H., Yamamoto-Hino, M., Mizuno, H. & Miyawaki, A. An optical marker based on the UV-induced green-to-red photoconversion of a fluorescent protein. Proc. Natl. Acad. Sci. USA 99, 12651–12656. https://doi.org/10.1073/pnas.202320599 (2002).
ADS  CAS  Article  PubMed  Google Scholar 

33.
Carver, C. E., Mallet, A. L. & Vercaemer, B. Biological synopsis of the solitary tunicate Ciona intestinalis. Can. Man. Rep. Fish. Aquat. Sci. 2746 (2006).

34.
Fiala-Médioni, A. Filter-feeding ethology of benthic invertebrates (ascidians). IV. Pumping rate, filtration rate, filtration efficiency. Mar. Biol. 48, 243–249. https://doi.org/10.1007/BF00397151 (1978).
Article  Google Scholar 

35.
Hoxha, T. et al. Comparative feeding rates of native and invasive ascidians. Mar. Pollut. Bull. 135, 1067–1071. https://doi.org/10.1016/j.marpolbul.2018.08.039 (2018).
CAS  Article  PubMed  Google Scholar 

36.
Petersen, J. K., Mayer, S. & Knudsen, M. Å. Beat frequency of cilia in the branchial basket of the ascidian Ciona intestinalis in relation to temperature and algal cell concentration. Mar. Biol. 133, 185–192. https://doi.org/10.1007/s002270050457 (1999).
Article  Google Scholar 

37.
Millar, R. H. The biology of ascidians. Adv. Mar. Biol. 9, 1–100 (1971).
ADS  Article  Google Scholar 

38.
Thomas, N. W. Mucus-secreting cells from the alimentary canal of Ciona intestinalis. J. Mar. Biol. Assoc. U. K. 50, 429–438. https://doi.org/10.1017/S0025315400004628 (1970).
Article  Google Scholar 

39.
Flood, P. R. & Fiala-Medioni, A. Ultrastructure and histochemistry of the food trapping mucous film in benthic filter-feeders (Ascidians). Acta Zool. 62, 53–65. https://doi.org/10.1111/j.1463-6395.1981.tb00616.x (1981).
Article  Google Scholar 

40.
Randløv, A. & Riisgard, H. U. Efficiency of particle retention and filtration rate in four species of ascidians. Mar. Ecol. Progr. Ser. 11, 89–103 (1979).
Google Scholar 

41.
Petersen, J. K. & Riisgard, H. U. Filtration capacity of the ascidian Ciona intestinalis and its grazing impact in a shallow fjord. Mar. Ecol. Prog. Ser. 88, 9–17 (1992).
ADS  Article  Google Scholar 

42.
Lumare, F., Di Muro, P., Tenderini, L. & Zupo, V. Experimental intensive culture of Penaeus monodon in the cold-temperate climate of the North-East coast of Italy (a fishery ‘valle’ of the River Po Delta). Aquaculture 113, 231–241. https://doi.org/10.1016/0044-8486(93)90476-F (1993).
Article  Google Scholar 

43.
Mutalipassi, M., Di Natale, M., Mazzella, V. & Zupo, V. Automated culture of aquatic model organisms: shrimp larvae husbandry for the needs of research and aquaculture. Animal 12, 155–163. https://doi.org/10.1017/S1751731117000908 (2018).
CAS  Article  PubMed  Google Scholar 

44.
Armsworthy, S. L., MacDonald, B. A. & Ward, J. E. Feeding activity, absorption efficiency and suspension feeding processes in the ascidian, Halocynthia pyriformis (Stolidobranchia: Ascidiacea): responses to variations in diet quantity and quality. J. Exp. Mar. Biol. Ecol. 260, 41–69. https://doi.org/10.1016/S0022-0981(01)00238-6 (2001).
Article  PubMed  Google Scholar 

45.
Coughlan, J. The estimation of filtering rate from the clearance of suspensions. Mar. Biol. 2, 356–358. https://doi.org/10.1007/BF00355716 (1969).
Article  Google Scholar 

46.
Pascoe, P. L., Parry, H. E. & Hawkins, A. J. S. Dynamic filter-feeding responses in fouling organisms. Aquat. Biol. 1, 177–185. https://doi.org/10.3354/ab00022 (2007).
CAS  Article  Google Scholar 

47.
Petersen, J. K. Ascidian suspension feeding. J. Exp. Mar. Biol. Ecol. 342, 127–137. https://doi.org/10.1016/j.jembe.2006.10.023 (2007).
Article  Google Scholar 

48.
Robbins, I. J. The effects of body size, temperature, and suspension density on the filtration and ingestion of inorganic particulate suspensions by ascidians. J. Exp. Mar. Biol. Ecol. 70, 65–78. https://doi.org/10.1016/0022-0981(83)90149-1 (1983).
Article  Google Scholar 

49.
Varrella, S. et al. Toxic diatom aldehydes affect defence gene networks in sea urchins. PLoS ONE 11, e0149734. https://doi.org/10.1371/journal.pone.0149734 (2016).
CAS  Article  PubMed  PubMed Central  Google Scholar 

50.
Varrella, S. et al. First morphological and molecular evidence of the negative impact of diatom-derived hydroxyacids on the sea urchin Paracentrotus lividus. Toxicol. Sci. 151, 419–433. https://doi.org/10.1093/toxsci/kfw053 (2016).
CAS  Article  PubMed  PubMed Central  Google Scholar 

51.
Jacobi, Y., Yahel, G. & Shenkar, N. Efficient filtration of micron and submicron particles by ascidians from oligotrophic waters. Limnol. Oceanogr. 63, S267–S279. https://doi.org/10.1002/lno.10736 (2018).
ADS  CAS  Article  Google Scholar 

52.
Robbins, I. J. The regulation of ingestion rate, at high suspended particulate concentrations, by some phleobranchiate ascidians. J. Exp. Mar. Biol. Ecol. 82, 1–10. https://doi.org/10.1016/0022-0981(84)90135-7 (1984).
Article  Google Scholar 

53.
Ogasawara, M. et al. Gene expression profiles in young adult Ciona intestinalis. Dev. Genes Evol. 212, 173–185. https://doi.org/10.1007/s00427-002-0230-7 (2002).
Article  PubMed  Google Scholar 

54.
Hendrickson, C. et al. Culture of adult ascidians and ascidian genetics. Methods Cell Biol. 143–170, 2004. https://doi.org/10.1016/S0091-679X(04)74007-8 (2004).
Article  Google Scholar 

55.
Petersen, S. Feeding response to fish feed diets in Ciona intestinalis: implications for IMTA. IMTA. MSc thesis. University of Bergen (2016).

56.
Knuckey, R. M., Brown, M. R., Robert, R. & Frampton, D. M. F. Production of microalgal concentrates by flocculation and their assessment as aquaculture feeds. Aquacult. Eng. 35, 300–313. https://doi.org/10.1016/j.aquaeng.2006.04.001 (2006).
Article  Google Scholar 

57.
Raniello, R., Iannicelli, M. M., Nappo, M., Avila, C. & Zupo, V. Production of Cocconeis neothumensis (Bacillariophyceae) biomass in batch cultures and bioreactors for biotechnological applications: light and nutrient requirements. J. Appl. Phycol. 19, 383–391. https://doi.org/10.1007/s10811-006-9145-4 (2007).
CAS  Article  Google Scholar 

58.
Nappo, M. et al. Metabolite profiling of the benthic diatom Cocconeis scutellum by GC-MS. J. Appl. Phycol. 21, 295–306. https://doi.org/10.1007/s10811-008-9367-8 (2009).
CAS  Article  Google Scholar 

59.
Ruocco, N. et al. Diatom-derived oxylipins induce cell death in sea urchin embryos activating caspase-8 and caspase 3/7. Aquat. Toxicol. 176, 128–140 (2016).
CAS  Article  Google Scholar 

60.
Ruocco, N., Costantini, M. & Santella, L. New insights into negative effects of lithium on sea urchin Paracentrotus lividus embryos. Sci. Rep. 6, 1–12. https://doi.org/10.1038/srep32157 (2016).
CAS  Article  Google Scholar 

61.
Sigsgaard, S. J., Petersen, J. K. & Iversen, J. J. L. Relationship between specific dynamic action and food quality in the solitary ascidian Ciona intestinalis. Mar. Biol. 143, 1143–1149. https://doi.org/10.1007/s00227-003-1164-y (2003).
Article  Google Scholar 

62.
Liu, L. et al. Ciona intestinalis as an emerging model organism: its regeneration under controlled conditions and methodology for egg dechorionation. J. Zhejiang Univ. Sci. B 7, 467–474. https://doi.org/10.1631/jzus.2006.B0467 (2006).
Article  PubMed  PubMed Central  Google Scholar 

63.
Costantini, S. et al. Evaluating the effects of an organic extract from the mediterranean sponge Geodia cydonium on human breast cancer cell lines. Int. J. Mol. Sci. https://doi.org/10.3390/ijms18102112 (2017).
Article  PubMed  PubMed Central  Google Scholar 

64.
Costantini, S. et al. Anti-inflammatory effects of a methanol extract from the marine sponge Geodia cydonium on the human breast cancer MCF-7 cell line. Mediators Inflamm. https://doi.org/10.1155/2015/204975 (2015).
Article  PubMed  PubMed Central  Google Scholar 

65.
Ruocco, N. et al. High-quality RNA extraction from the sea urchin Paracentrotus lividus embryos. PLoS ONE 12, e0172171. https://doi.org/10.1371/journal.pone.0172171 (2017).
CAS  Article  PubMed  PubMed Central  Google Scholar 

66.
Fujikawa, T., Munakata, T., Kondo, S. I., Satoh, N. & Wada, S. Stress response in the ascidian Ciona intestinalis: transcriptional profiling of genes for the heat shock protein 70 chaperone system under heat stress and endoplasmic reticulum stress. Cell Stress Chaperones 15, 193–204. https://doi.org/10.1007/s12192-009-0133-x (2010).
CAS  Article  PubMed  Google Scholar 

67.
Pfaffl, M. W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, 45e–445. https://doi.org/10.1093/nar/29.9.e45 (2001).
Article  Google Scholar 

68.
Pfaffl, M. W. Relative expression software tool (REST(C)) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30, 36e–336. https://doi.org/10.1093/nar/30.9.e36 (2002).
Article  Google Scholar 

69.
Ginzburg, L. R. The theory of population dynamics: I. Back to first principles. J. Theor. Biol. 122, 385–399. https://doi.org/10.1016/S0022-5193(86)80180-1 (1986).
MathSciNet  Article  Google Scholar 

70.
Turchin, P. Does population ecology have general laws?. Oikos 94, 17–26. https://doi.org/10.1034/j.1600-0706.2001.11310.x (2001).
Article  Google Scholar  More

1.
Wikelski, M. Evolution of body size in Galapagos marine iguanas. Proc. R. Soc. B 272, 1985–1993 (2005).
PubMed  Google Scholar 
2.
Reidenberg, J. S. Anatomical adaptations of aquatic mammals. Anat. Rec. 290, 507–513 (2007).
Google Scholar 

3.
Aubret, F., Bonnet, X. & Shine, R. The role of adaptive plasticity in a major evolutionary transition: early aquatic experience affects locomotor performance of terrestrial snakes. Funct. Ecol. 21, 1154–1161 (2007).
Google Scholar 

4.
Palmer, J. D. The biological rhythms and clocks of intertidal animals (Oxford University Press, Oxford, 1995).
Google Scholar 

5.
Hindle, A. G., Rosen, D. A. & Trites, A. W. Swimming depth and ocean currents affect transit costs in Steller sea lions Eumetopias jubatus. Aquat. Biol. 10, 139–148 (2010).
Google Scholar 

6.
Frazer, N. B. Effect of tidal cycles on loggerhead sea turtles (Caretta caretta) emerging from the sea. Copeia 1983, 516–519 (1983).
Google Scholar 

7.
Hay, D. E. Tidal influence on spawning time of Pacific Herring (Clupea harengus pallasi). Can. J. Fish. Aquat. Sci. 47, 2390–2401 (1990).
Google Scholar 

8.
Gibson, R. N. Tidally-synchronised behaviour in marine fishes. In Rhythms in fishes (ed. Ali, M. A.) 63–81 (Springer, Berlin, 1992).
Google Scholar 

9.
Bernard, I. et al. In situ spawning in a marine broadcast spawner, the Pacific oyster Crassostrea gigas: timing and environmental triggers. Limnol. Oceanogr. 61, 635–647 (2016).
ADS  Google Scholar 

10.
Leite-Castro, L. V. et al. Reproductive biology of the sea cucumber Holothuria grisea in Brazil: importance of social and environmental factors in breeding coordination. Mar. Biol. 163, 67 (2016).
Google Scholar 

11.
Collin, R., Kerr, K., Contolini, G. & Ochoa, I. Reproductive cycles in tropical intertidal gastropods are timed around tidal amplitude cycles. Ecol. Evol. 7, 5977–5991 (2017).
PubMed  PubMed Central  Google Scholar 

12.
Reinert, H. K. Habitat variation within sympatric snake populations. Ecology 65, 1673–1682 (1984).
Google Scholar 

13.
Reinert, H. K. & Zappalorti, R. T. Timber rattlesnakes (Crotalus horridus) of the Pine Barrens: their movement patterns and habitat preference. Copeia 1988, 964–978 (1988).
Google Scholar 

14.
Bauder, J. M. et al. Multi-level, multi-scale habitat selection by a wide-ranging, federally threatened snake. Landsc. Ecol. 33, 743–763 (2018).
Google Scholar 

15.
Cook, T. R., Bonnet, X., Fauvel, T., Shine, R. & Brischoux, F. Foraging behaviour and energy budgets of sea snakes from New Caledonia: insights from implanted data-loggers. J. Zool. 298, 82–93 (2016).
Google Scholar 

16.
Udyawer, V., Read, M., Hamann, M., Simpfendorfer, C. A. & Heupel, M. R. Effects of environmental variables on the movement and space use of coastal sea snakes over multiple temporal scales. J. Exp. Mar. Biol. Ecol. 473, 26–34 (2015).
Google Scholar 

17.
Udyawer, V., Simpfendorfer, C. A. & Heupel, M. R. Diel patterns in three-dimensional use of space by sea snakes. Anim. Biotelemetry 3, 29 (2015).
Google Scholar 

18.
Udyawer, V., Simpfendorfer, C. A., Read, M., Hamann, M. & Heupel, M. R. Exploring habitat selection in sea snakes using passive acoustic monitoring and Bayesian hierarchical models. Mar. Ecol. Prog. Ser. 546, 249–262 (2016).
ADS  Google Scholar 

19.
Udyawer, V., Read, M., Hamann, M., Heupel, M. R. & Simpfendorfer, C. A. Importance of shallow tidal habitats as refugia from trawl fishing for sea snakes. J. Herpetol. 50, 527–533 (2016).
Google Scholar 

20.
Udyawer, V., Simpfendorfer, C. A., Heupel, M. R. & Clark, T. D. Temporal and spatial activity-associated energy partitioning in free-swimming sea snakes. Funct. Ecol. 31, 1739–1749 (2017).
Google Scholar 

21.
Kerford, M. R., Wirsing, A. J., Heithaus, M. R. & Dill, L. M. Danger on the rise: diurnal tidal state mediates an exchange of food for safety by the bar-bellied sea snake Hydrophis elegans. Mar. Ecol. Prog. Ser. 358, 289–294 (2008).
ADS  Google Scholar 

22.
Wirsing, A. J. & Heithaus, M. R. Olive-headed sea snakes Disteria major shift seagrass microhabitats to avoid shark predation. Mar. Ecol. Prog. Ser. 387, 287–293 (2009).
ADS  Google Scholar 

23.
Shetty, S. & Shine, R. Activity patterns of yellow-lipped sea kraits (Laticauda colubrina) on a Fijian island. Copeia 2002, 77–85 (2002).
Google Scholar 

24.
Goiran, C., Dubey, S. & Shine, R. Effects of season, sex and body size on the feeding ecology of turtle-headed sea snakes (Emydocephalus annulatus) on IndoPacific inshore coral reefs. Coral Reefs 32, 527–538 (2013).
ADS  Google Scholar 

25.
Shine, R. All at sea: aquatic life modifies mate-recognition modalities in sea snakes (Emydocephalus annulatus, Hydrophiidae). Behav. Ecol. Sociobiol. 57, 591–598 (2005).
Google Scholar 

26.
Shine, R., Shine, T. & Shine, B. Intraspecific habitat partitioning by the sea snake Emydocephalus annulatus (Serpentes, Hydrophiidae): the effects of sex, body size, and colour pattern. Biol. J. Linn. Soc. 80, 1–10 (2003).
Google Scholar 

27.
Rezaie-Atagholipour, M., Riyahi-Bakhtiari, A. & Sajjadi, M. Feeding habits of the annulated sea snake, Hydrophis cyanocinctus, in the Persian Gulf. J. Herpetol. 47, 328–330 (2013).
Google Scholar 

28.
Shine, R., Brischoux, F. & Pile, A. A seasnake’s colour affects its susceptibility to algal fouling. Proc. R. Soc. B 277, 2459–2464 (2010).
CAS  PubMed  Google Scholar 

29.
Shine, R., Goiran, C., Shine, T., Fauvel, T. & Brischoux, F. Phenotypic divergence between seasnake (Emydocephalus annulatus) populations from adjacent bays of the New Caledonian Lagoon. Biol. J. Linn. Soc. 107, 824–832 (2012).
Google Scholar 

30.
Lukoschek, V. & Shine, R. Sea snakes rarely venture far from home. Ecol. Evol. 2, 1113–1121 (2012).
PubMed  PubMed Central  Google Scholar 

31.
Heatwole, H. Sea snakes. Australian natural history series 2nd edn. (University of New South Wales Press, Randwick, 1999).
Google Scholar 

32.
Lukoschek, V., Beger, M., Ceccarelli, D., Richards, Z. & Pratchett, M. Enigmatic declines of Australia’s sea snakes from a biodiversity hotspot. Biol. Conserv. 166, 191–202 (2013).
Google Scholar 

33.
Goiran, C. & Shine, R. Decline in sea snake abundance on a protected coral reef system in the New Caledonian Lagoon. Coral Reefs 32, 281–284 (2013).
ADS  Google Scholar 

34.
Udyawer, V. et al. Future directions in marine snake research and management. Front. Mar. Sci. 5, 399 (2018).
Google Scholar 

35.
Harrison, H. B. et al. Back-to-back coral bleaching events on isolated atolls in the Coral Sea. Coral Reefs 38, 713–719 (2019).
ADS  Google Scholar 

36.
Richardson, L. E., Graham, N. A., Pratchett, M. S., Eurich, J. G. & Hoey, A. S. Mass coral bleaching causes biotic homogenization of reef fish assemblages. Glob. Change Biol. 24, 3117–3129 (2018).
ADS  Google Scholar 

37.
Mitrovich, M. J., Diffendorfer, J. E., Brehme, C. S. & Fisher, R. N. Effects of urbanization and habitat composition on site occupancy of two snake species using regional monitoring data from southern California. Glob. Ecol. Conserv. 15, e00427 (2018).
Google Scholar 

38.
Ineich, I. The sea snakes of New Caledonia (Elapidae, Hydrophiinae). In Compendium of marine species from New Caledonia (eds Payri, C. & Richer de Forges, B.) 403–410 (Institut de Recherche pour le Développement, Marseille, 2007).
Google Scholar 

39.
Goiran, C., Bustamante, P. & Shine, R. Industrial melanism in the seasnake Emydocephalus annulatus. Curr. Biol. 27, 2510–2513 (2017).
CAS  PubMed  Google Scholar 

40.
Shine, R., Bonnet, X., Elphick, M. & Barrott, E. A novel foraging mode in snakes: browsing by the sea snake Emydocephalus annulatus (Serpentes, Hydrophiidae). Funct. Ecol. 18, 16–24 (2004).
Google Scholar 

41.
Avolio, C., Shine, R. & Pile, A. J. The adaptive significance of sexually dimorphic scale rugosity in sea snakes. Am. Nat. 167, 728–738 (2006).
PubMed  Google Scholar 

42.
Goiran, C., Brown, G. P. & Shine, R. Niche partitioning within a population of seasnakes is constrained by ambient thermal homogeneity and small prey size. Biol. J. Linn. Soc. 129, 644–651 (2020).
Article  Google Scholar  More

1.
Berdalet, E. et al. Harmful algal blooms in benthic systems: recent progress and future research. Oceanography 30, 36–45 (2017).
Google Scholar 
2.
Yasumoto, T., Inoue, A., Bagnis, R. & Garcon, M. Ecological survey on a dinoflagellate possibly responsible for the induction of ciguatera. Bull. Jpn. Soc. Sci. Fish. 45, 395–399 (1979).
Google Scholar 

3.
Shimizu, Y. et al. Gambierdiscus toxicus, a ciguatera-causing dinoflagellate from Hawaii. Bull. Jpn. Soc. Sci. Fish. 48, 811–813 (1982).
Google Scholar 

4.
Chinain, M., Germain, M., Deparis, X., Pauillac, S. & Legrand, A.-M. Seasonal abundance and toxicity of the dinoflagellate Gambierdiscus spp. (Dinophyceae), the causative agent of ciguatera in Tahiti, French Polynesia. Mar. Biol. 135, 259–267 (1999).
Google Scholar 

5.
Litaker, R. W. et al. Ciguatoxicity of Gambierdiscus and Fukuyoa species from the Caribbean and Gulf of Mexico. PLoS ONE 12(10), e0185776 (2017).
PubMed  PubMed Central  Google Scholar 

6.
Yasumoto, T. et al. Environmental studies on a toxic dinoflagellate responsible for ciguatera. Nippon Suisan Gakkaishi 46, 1397–1404 (1980).
CAS  Google Scholar 

7.
Roué, M. et al. Evidence of the bioaccumulation of ciguatoxins in giant clams (Tridacna maxima) exposed to Gambierdiscus spp. cells. Harmful Algae 57, 78–87 (2016).
PubMed  Google Scholar 

8.
Darius, H. T. et al. Tectus niloticus (Tegulidae, Gastropod) as a novel vector of ciguatera poisoning: detection of Pacific ciguatoxins in toxic samples from Nuku Hiva Island (French Polynesia). Toxins 10, 2. https://doi.org/10.3390/toxins10010002 (2018).
CAS  Article  Google Scholar 

9.
Darius, H. T. et al. Toxicological investigations on the sea urchin Tripneustes gratilla (Toxopneustidae, Echinoid) from Anaho Bay (Nuku Hiva, French Polynesia): evidence for the presence of Pacific ciguatoxins. Mar. Drugs 16(4), 122. https://doi.org/10.3390/md16040122 (2018).
CAS  Article  PubMed Central  Google Scholar 

10.
Friedman, M. et al. An updated review of Ciguatera Fish Poisoning: clinical, epidemiological, environmental, and public health management. Mar. Drugs 15(3), 72 (2017).
PubMed Central  Google Scholar 

11.
Lehane, L. & Lewis, R. J. Ciguatera: recent advances but the risk remains. Int. J. Food Microbiol. 61, 91–125 (2000).
CAS  PubMed  Google Scholar 

12.
Lewis, R. J. The changing face of ciguatera. Toxicon 39, 97–106 (2001).
CAS  PubMed  Google Scholar 

13.
Ciminiello, P. et al. The Genoa 2005 outbreak. Determination of putative palytoxin in Mediterranean Ostreopsis ovata by a new liquid chromatography tandem mass spectrometry method. Anal. Chem. 78, 6153–6159 (2006).
CAS  PubMed  Google Scholar 

14.
Ciminiello, P. et al. Putative palytoxin and its new analogue, ovatoxin-a, in Ostreopsis ovata collected along the Ligurian coasts during the 2006 toxic outbreak. J. Am. Soc. Mass Spectrom. 19, 111–120 (2008).
CAS  PubMed  Google Scholar 

15.
Ciminiello, P. et al. Complex palytoxin-like profile of Ostreopsis ovate. identification of four new ovatoxins by high-resolution liquid chromatography/mass spectrometry. Rapid Commun. Mass Spectrom. 24, 2735–2744 (2010).
ADS  CAS  PubMed  Google Scholar 

16.
Vila, M., Abós-Herràndiz, R., Isern-Fontanet, J., Àlvarez, J. & Berdalet, E. Establishing the link between Ostreopsis cf. ovata blooms and human health impacts using ecology and epidemiology. Sci. Mar. 80(S1), 107–115 (2016).
CAS  Google Scholar 

17.
Durando, P. et al. Ostreopsis ovata and human health: epidemiological and clinical features of respiratory syndrome outbreaks from a two-year syndromic surveillance, 2005–06, in north-west Italy. Eurosurveillance 12(6), E070607 (2007).
PubMed  Google Scholar 

18.
Onuma, Y. et al. Identification of putative palytoxin as the cause of clupeotoxism. Toxicon 37, 55–65 (1999).
CAS  PubMed  Google Scholar 

19.
Aligizaki, K., Katikou, P., Milandri, A. & Diogène, J. Occurrence of palytoxin-group toxins in seafood and future strategies to complement the present state of the art. Toxicon 57, 390–399 (2011).
CAS  PubMed  Google Scholar 

20.
Alcala, A. C., Alcala, L. C., Garth, J. S., Yasumura, D. & Yasumoto, T. Human fatality due to ingestion of the crab Demania reynaudii that contained a palytoxin-like toxin. Toxicon 26, 105–107 (1988).
CAS  PubMed  Google Scholar 

21.
Taniyama, S. The occurrence of palytoxin-like poisoning and ciguatera in parts of the mainland of Japan. Nippon Suisan Gakkaishi 74, 917–918 (2008).
CAS  Google Scholar 

22.
Ramos, V. & Vasconcelos, V. Palytoxin and analogs: biological and ecological effects. Mar. Drugs 8, 2021–2037 (2010).
CAS  PubMed  PubMed Central  Google Scholar 

23.
Faimali, M. et al. Toxic effects of harmful benthic dinoflagellate Ostreopsis ovata on invertebrate and vertebrate marine organisms. Mar. Environ. Res. 76, 97–107 (2012).
CAS  PubMed  Google Scholar 

24.
Simonini, R., Orlandi, M. & Abbate, M. Is the toxic dinoflagellate Ostreopsis cf. ovata harmful to Mediterranean benthic invertebrates? Evidences from ecotoxicological tests with the polychaete Dinophilus gyrociliatus. Mar. Environ. Res. 72, 230–233 (2011).
CAS  PubMed  Google Scholar 

25.
Privitera, D. et al. Toxic effects of Ostreopsis ovata on larvae and juveniles of Paracentrotus lividus. Harmful Algae 18, 16–23 (2012).
Google Scholar 

26.
Neves, R. A., Contins, M. & Nascimento, S. M. Effects of the toxic benthic dinoflagellate Ostreopsis cf. ovata on fertilization and early development of the sea urchin Lytechinus variegatus. Mar. Environ. Res. 135, 11–17 (2018).
CAS  PubMed  Google Scholar 

27.
Gorbi, S. et al. Effects of harmful dinoflagellate Ostreopsis cf. ovata exposure on immunological, histological and oxidative responses of mussels Mytilus galloprovincialis. Fish Shellfish Immunol. 35, 941–950 (2013).
CAS  PubMed  Google Scholar 

28.
Vale, C. & Ares, I. R. Biochemistry of palytoxins and ostreocins. In Phycotoxins: Chemistry and Biochemistry (ed. Botana, L.) 95–118 (Blackwell Publishing, Oxford, 2007).
Google Scholar 

29.
Shears, N. T. & Ross, P. M. Blooms of benthic dinoflagellates of the genus Ostreopsis; an increasing and ecologically important phenomenon on temperate reefs in New Zealand and worldwide. Harmful Algae 8, 916–925 (2009).
Google Scholar 

30.
Totti, C., Accoroni, S., Cerino, F., Cucchiari, E. & Romagnoli, T. Ostreopsis ovata bloom along the Conero Riviera (northern Adriatic Sea): relationships with environmental conditions and substrata. Harmful Algae 9, 233–239 (2010).
Google Scholar 

31.
Murakami, Y., Oshima, Y. & Yasumoto, T. Identification of okadaic acid as a toxic component of a marine dinoflagellate Prorocentrum lima. Bull. Jpn. Soc. Sci. Fish. 48, 69–72 (1982).
CAS  Google Scholar 

32.
Yasumoto, T., Murata, M., Oshima, Y., Matsumoto, G. & Clardy, J. Diarrhetic shellfish poisoning . In Seafood Toxins (ed. Ragelis, E. P.) 207–214 (American Chemical Society, Washington, 1984).
Google Scholar 

33.
Morton, S. L. & Bomber, J. W. Maximizing okadaic acid content from Prorocentrum hoffmannianum Faust. J. Appl. Phycol. 6, 41–44 (1994).
CAS  Google Scholar 

34.
Ten-Hage, L. et al. Okadaic acid production from the marine benthic dinoflagellate Prorocentrum arenarium Faust (Dinophyceae) isolated from Europa Island coral reef ecosystem (SW Indian Ocean). Toxicon 38, 1043–1054 (2000).
CAS  PubMed  Google Scholar 

35.
Faust, M. A., Vandersea, M. W., Kibler, S. R., Tester, P. A. & Litaker, R. W. Prorocentrum levis, a new benthic species (Dinophyceae) from a mangrove island, Twin Cays, Belize. J. Phycol. 44, 232–240 (2008).
CAS  PubMed  Google Scholar 

36.
An, T., Winshell, J., Scorzetti, G., Fell, J. W. & Rein, K. S. Identification of okadaic acid production in the marine dinoflagellate Prorocentrum rhathymum from Florida Bay. Toxicon 55, 653–657 (2010).
CAS  PubMed  Google Scholar 

37.
Luo, Z. et al. Morphology, molecular phylogeny and okadaic acid production of epibenthic Prorocentrum (Dinophyceae) species from the northern South China Sea. Algal Res. 22, 14–30 (2017).
Google Scholar 

38.
Lim, Z. F. et al. Taxonomy and toxicity of Prorocentrum from Perhentian Islands (Malaysia), with a description of a non-toxigenic species Prorocentrum malayense sp. Nov. (Dinophyceae). Harmful Algae 83, 95–108 (2019).
CAS  PubMed  Google Scholar 

39.
Lawrence, J. E., Grant, J., Quilliam, M. A., Bauder, A. G. & Cembella, A. D. Colonization and growth of the toxic dinoflagellate Prorocentrum lima and associated fouling macroalgae on mussels in suspended culture. Mar. Ecol. Prog. Ser. 201, 147–154 (2000).
ADS  Google Scholar 

40.
Levasseur, M. et al. Pelagic and epiphytic summer distributions of Prorocentrum lima and P. mexicanum at two mussel farms in the Gulf of St. Lawrence, Canada. Aquat. Microb. Ecol. 30, 283–293 (2003).
Google Scholar 

41.
Foden, J., Purdie, D. A., Morris, S. & Nascimento, S. Epiphytic abundance and toxicity of Prorocentrum lima populations in the Fleet Lagoon, UK. Harmful Algae 4, 1063–1074 (2005).
CAS  Google Scholar 

42.
Kobayashi, J. et al. Amphidinolide C: the first twenty-five membered macrocyclic lactone with potent antineoplastic activity from the cultured dinoflagellate Amphidinium sp. J. Am. Chem. Soc. 110, 490–494 (1988).
CAS  Google Scholar 

43.
Holmes, M. J., Lewis, R. J., Jones, A. & Hoy, A. W. W. Cooliatoxin, the first toxin from Coolia monotis (Dinophyceae). Nat. Toxins 3, 355–362 (1995).
CAS  PubMed  Google Scholar 

44.
Kobayashi, J. I. & Kubota, T. Bioactive macrolides and polyketides from marine dinoflagellates of the genus Amphidinium. J. Nat. Prod. 70, 451–460 (2007).
CAS  PubMed  Google Scholar 

45.
Kobayashi, J. I. Amphidinolides and its related macrolides from marine dinoflagellates. J. Antibiot. 61, 271–284 (2008).
CAS  PubMed  Google Scholar 

46.
Pagliara, P. & Caroppo, C. Toxicity assessment of Amphidinium carterae, Coolia cfr. monotis and Ostreopsis cfr. ovata (Dinophyta) isolated from the northern Ionian Sea (Mediterranean Sea). Toxicon 60, 1203–1214 (2012).
CAS  PubMed  Google Scholar 

47.
Wakeman, K. C., Yamaguchi, A., Roy, M. C. & Jenke-Kodama, H. Morphology, phylogeny and novel chemical compounds from Coolia malayensis (Dinophyceae) from Okinawa, Japan. Harmful Algae 44, 8–19 (2015).
CAS  Google Scholar 

48.
Karafas, S., Teng, S. T., Leaw, C. P. & Alves-de-Souza, C. An evaluation of the genus Amphidinium (Dinophyceae) combining evidence from morphology, phylogenetics, and toxin production, with the introduction of six novel species. Harmful Algae 68, 128–151 (2017).
PubMed  Google Scholar 

49.
Ballantine, D. L., Tosteson, T. R. & Bardales, A. T. Population dynamics and toxicity of natural populations of benthic dinoflagellates in southwestern Puerto Rico. J. Exp. Mar. Biol. Ecol. 119, 201–212 (1988).
Google Scholar 

50.
Bomber, J. W. & Aikman, K. E. The ciguatera dinoflagellates. Biol. Oceanogr. 6, 291–311 (1989).
Google Scholar 

51.
Bomber, J. W., Rubio, M. G. & Norris, D. R. Epiphytism of dinoflagellates associated with the disease ciguatera: substrate specificity and nutrition. Phycologia 28, 360–368 (1989).
Google Scholar 

52.
Faust, M. A. Observation of sand-dwelling toxic dinoflagellates (Dinophyceae) from widely differing sites, including two new species. J. Phycol. 31, 996–1003 (1995).
Google Scholar 

53.
Tindall, D. R. & Morton, S. L. Community dynamics and physiology of epiphytic/benthic dinoflagellates associated with ciguatera. In Physiological Ecology of Harmful Algal Blooms (eds Anderson, D. M. et al.) 293–314 (Springer, Berlin, 1998).
Google Scholar 

54.
Kibler, S. R., Litaker, R. W., Holland, W. C., Vandersea, M. W. & Tester, P. A. Growth of eight Gambierdiscus (Dinophyceae) species: effects of temperature, salinity and irradiance. Harmful Algae 19, 1–14 (2012).
Google Scholar 

55.
Kibler, S. R., Tester, P. A., Kunkel, K. E., Moore, S. K. & Litaker, R. W. Effects of ocean warming on growth and distribution of dinoflagellates associated with ciguatera fish poisoning in the Caribbean. Ecol. Model. 136, 194–210 (2015).
Google Scholar 

56.
Kibler, S. R. et al. Gambierdiscus and Fukuyoa species in the greater Caribbean: regional growth projections for ciguatera-associated dinoflagellates. Ecol. Model. 360, 201–218 (2017).
Google Scholar 

57.
Xu, Y. et al. Influence of environmental variables on Gambierdiscus spp. (Dinophyceae) growth and distribution. PLoS ONE 11(4), e0153197 (2016).
PubMed  PubMed Central  Google Scholar 

58.
David, H., Kromkamp, J. C. & Orive, E. Relationship between strains of Coolia monotis (Dinophyceae) from the Atlantic Iberian Peninsula and their sampling sites. J. Exp. Mar. Biol. Ecol. 487, 59–67 (2017).
Google Scholar 

59.
David, H., Laza-Martínez, A., Kromkamp, J. C. & Orive, E. Pysiological response of Prorocentrum lima (Dinophyceae) to varying light intensities. FEMS Microbiol. Ecol. https://doi.org/10.1093/femsec/fix166 (2018).
Article  PubMed  Google Scholar 

60.
Larsson, M. E., Smith, K. F. & Doblin, M. A. First description of the environmental niche of the epibenthic dinoflagellate species Coolia palmyrensis, C. malayensis, and C. tropicalis (Dinophyceae) from eastern Australia. J. Phycol. 55, 565–577 (2019).
CAS  PubMed  Google Scholar 

61.
Richlen, M. L. & Lobel, P. S. Effects of depth, habitat, and water motion on the abundance and distribution of ciguatera dinoflagellates at Johnston Atoll, Pacific Ocean. Mar. Ecol. Prog. Ser. 421, 51–66 (2011).
ADS  Google Scholar 

62.
Meroni, L., Chiantore, M., Petrillo, M. & Asnaghi, V. Habitat effects on Ostreopsis cf. ovata bloom dynamics. Harmful Algae 80, 64–71 (2018).
CAS  PubMed  Google Scholar 

63.
Yong, H. L. et al. Habitat complexity affects benthic harmful dinoflagellate assemblages in the fringing reef of Rawa Island, Malaysia. Harmful Algae 78, 56–86 (2018).
PubMed  Google Scholar 

64.
Tester, P. A., Litaker, R. W. & Berdalet, E. Climate change and harmful benthic microalgae. Harmful Algae https://doi.org/10.1016/j.hal.2019.101655 (2020).
Article  PubMed  Google Scholar 

65.
Randall, J. E. A review of ciguatera, tropical fish poisoning, with a tentative explanation of its cause. Bull. Mar. Sci. 8, 236–267 (1958).
Google Scholar 

66.
Chateau-Degat, M. L. et al. Seawater temperature, Gambierdiscus spp. variability and incidence of ciguatera poisoning in French Polynesia. Harmful Algae 4, 1053–1062 (2005).
CAS  Google Scholar 

67.
Rongo, T. & van Woesik, R. Ciguatera poisoning in Rarotonga, southern Cook islands. Harmful Algae 10, 345–355 (2011).
Google Scholar 

68.
Rongo, T. & van Woesik, R. The effects of natural disturbances, reef state, and herbivorous fish densities on ciguatera poisoning in Rarotonga, southern Cook Islands. Toxicon 64, 87–95 (2013).
CAS  PubMed  Google Scholar 

69.
Chinain, M., Darius, H. T., Gatti, C. M. & Roué, M. Update on ciguatera research in French Polynesia. SPC Fish. Newsl. 150, 43–51 (2016).
Google Scholar 

70.
Tester, P. A. et al. Sampling harmful benthic dinoflagellates: comparison of artificial and natural substrate methods. Harmful Algae 39, 8–25 (2014).
Google Scholar 

71.
Jauzein, C., Fricke, A., Mangialajo, L. & Lemée, R. Sampling of Ostreopsis cf. ovata using artificial substrates: optimization of methods for the monitoring of benthic harmful algal blooms. Mar. Poll. Bull. 107(1), 300–304 (2016).
CAS  Google Scholar 

72.
Jauzein, C. et al. Optimization of sampling, cell collection and counting for the monitoring of benthic harmful algal blooms: application to Ostreopsis spp. blooms in the Mediterranean Sea. Ecol. Indic. 91, 116–127 (2018).
Google Scholar 

73.
Beijbom, O. et al. Towards automated annotation of benthic survey images: variability of human experts and operational modes of automation. PLoS ONE 10(7), e0130312 (2015).
PubMed  PubMed Central  Google Scholar 

74.
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 

75.
Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, New York, 2009).
Google Scholar 

76.
Oksanen, J. et al. vegan: Community Ecology Package, version 2.4.2 ed. R Package (2017).

77.
Core Team, R. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, 2019).
Google Scholar 

78.
Clarke, K. R. Non-parametric multivariate analyses of changes in community structure. Aust. J. Ecol. 18(1), 117–143 (1993).
Google Scholar 

79.
Ploner, A. Heatplus: Heatmaps with Row and/or Column Covariates and Colored Clusters, 2.20.0 ed. R package (2015).

80.
Tan, T. H., Lim, P. T., Mujahid, A., Usup, G. & Leaw, C. P. Benthic harmful dinoflagellate assemblages in a fringing reef of Sampadi Island, Sarawak, Malaysia. Mar. Res. Indon. 38(2), 77–87 (2015).
Google Scholar 

81.
Fernández-Zabala, J., Tuya, F., Amorim, A. & Soler Onís, E. Benthic dinoflagellates: testing the reliability of the artificial substrate method in the Macaronesian region. Harmful Algae 87, 101634. https://doi.org/10.1016/j.hal.2019.101634 (2019).
Article  PubMed  Google Scholar 

82.
Vila, M., Garcés, E. & Masó, M. Potentially toxic epiphytic dinoflagellate assemblages on macroalgae in the NW Mediterranean. Aquat. Microb. Ecol. 26, 51–60 (2001).
Google Scholar 

83.
Parsons, M. L. & Preskitt, L. B. A survey of epiphytic dinoflagellates from the coastal waters of the island of Hawai‘i. Harmful Algae 6, 658–669 (2007).
CAS  Google Scholar 

84.
Aligizaki, K. & Nikolaidis, G. The presence of the potentially toxic genera Ostreopsis and Coolia (Dinophyceae) in the North Aegean Sea, Greece. Harmful Algae 5, 717–730 (2006).
Google Scholar 

85.
Accoroni, S. et al. Ostreopsis cf. ovata bloom in the northern Adriatic Sea during summer 2009: ecology, molecular characterization and toxin profile. Mar. Poll. Bull. 62, 2512–2519 (2011).
CAS  Google Scholar 

86.
Accoroni, S. & Totti, C. The toxic benthic dinoflagellates of the genus Ostreopsis in temperate areas: a review. Adv. Oceanogr. Limnol. https://doi.org/10.4081/aiol.2016.5591 (2016).
Article  Google Scholar 

87.
Mangialajo, L. et al. Trends in Ostreopsis proliferation along the Northern Mediterranean coasts. Toxicon 57, 408–420 (2011).
CAS  PubMed  Google Scholar 

88.
Blanfuné, A., Boudouresque, C. F., Grossel, H. & Thibaut, T. Distribution and abundance of Ostreopsis spp. and associated species (Dinophyceae) in the northwestern Mediterranean: the region and the macroalgal substrate matter. Environ. Sci. Pollut. Res. 22, 12332–12346 (2015).
Google Scholar 

89.
Mangialajo, L. et al. Benthic Dinoflagellate Integrator (BEDI): a new method for the quantification of benthic harmful algal blooms. Harmful Algae 64, 1–10 (2017).
PubMed  Google Scholar 

90.
Parsons, M. L., Settlemier, C. J. & Bienfang, P. K. A simple model capable of simulating the population dynamics of Gambierdiscus, the benthic dinoflagellate responsible for ciguatera fish poisoning. Harmful Algae 10, 71–80 (2010).
Google Scholar 

91.
Lobel, P. S., Anderson, D. M. & Durand-Clement, M. Assessment of Ciguatera dinoflagellate populations: sample variability and algal substrate selection. Biol. Bull. 175, 94–101 (1988).
Google Scholar 

92.
Gregg, W. W. & Rose, F. L. The effects of aquatic macrophytes on the stream microenvironment. Aquat. Bot. 14, 309–324 (1982).
Google Scholar 

93.
Kovalenko, K. E., Thomaz, S. M. & Warfe, D. M. Habitat complexity: approaches and future directions. Hydrobiologia 685, 1–17 (2012).
Google Scholar 

94.
Loeffler, C. R., Richlen, M. L., Brandt, M. E. & Smith, T. B. Effects of grazing, nutrients, and depth on the ciguatera-causing dinoflagellate Gambierdiscus in the US Virgin Islands. Mar. Ecol. Prog. Ser. 531, 91–104 (2015).
ADS  CAS  Google Scholar 

95.
Fraga, S., Rodríguez, F., Bravo, I., Zapata, M. & Marañón, E. Review of the main ecological features affecting benthic dinoflagellate blooms. Cryptogam. Algol. 33, 171–179 (2012).
Google Scholar 

96.
Nakahara, H., Sakami, T., Chinain, M. & Ishida, Y. The role of macroalgae in epiphytism of the toxic dinoflagellate Gambierdiscus toxicus (Dinophyceae). Phycol. Res. 44, 113–117 (1996).
Google Scholar 

97.
Villareal, T. A. & Morton, S. L. Use of cell-specific PAM-fluorometry to characterize host shading in the epiphytic dinoflagellate Gambierdiscus toxicus. Mar. Ecol. 23, 127–140 (2002).
ADS  Google Scholar 

98.
Monti, M. & Cecchin, E. Comparative growth of three strains of Ostreopsis ovata at different light intensities with focus on inter-specific allelopathic interactions. Cryptogam. Algol. 33, 113–119 (2012).
Google Scholar 

99.
Zapata, M., Fraga, S., Rodríguez, F. & Garrido, J. L. Pigment-based chloroplast types in dinoflagellates. Mar. Ecol. Prog. Ser. 465, 33–52 (2012).
ADS  CAS  Google Scholar 

100.
Yamaguchi, H., Tomori, Y., Tanimoto, Y., Oku, O. & Adachi, M. Evaluation of the effects of light intensity on growth of the benthic dinoflagellate Ostreopsis sp. 1 using a newly developed photoirradiation-culture system and a novel regression analytical method. Harmful Algae 39, 48–54 (2014).
Google Scholar  More

1.
Stockmann, U. et al. The knowns, known unknowns and unknowns of sequestration of soil organic carbon. Agric. Ecosyst. Environ. 164, 80–99 (2013).
CAS  Google Scholar 
2.
Cox, P. M. et al. Sensitivity of tropical carbon to climate change constrained by carbon dioxide variability. Nature 494, 341 (2013).
ADS  CAS  PubMed  PubMed Central  Google Scholar 

3.
Six, J., Conant, R. T., Paul, E. A. & Paustian, K. Stabilization mechanisms of soil organic matter: Implications for C-saturation of soils. Plant Soil 241, 155–176 (2002).
CAS  Google Scholar 

4.
Haynes, R. Labile organic matter fractions as central components of the quality of agricultural soils: An overview. Adv. Agron. 85, 221–268 (2005).
CAS  Google Scholar 

5.
Banger, K., Toor, G., Biswas, A., Sidhu, S. & Sudhir, K. Soil organic carbon fractions after 16 years of applications of fertilizers and organic manure in a Typic Rhodalfs in semi-arid tropics. Nutr. Cycl. Agroecosyst. 86, 391–399 (2010).
Google Scholar 

6.
Blair, G. J., Lefroy, R. D. & Lisle, L. Soil carbon fractions based on their degree of oxidation, and the development of a carbon management index for agricultural systems. Aust. J. Agric. Res. 46, 1459–1466 (1995).
Google Scholar 

7.
Kumar, K., Goh, K. Crop residues and management practices: Effects on soil quality, soil nitrogen dynamics, crop yield, and nitrogen recovery. In Advances in Agronomy, Vol. 68, 197–319 (Elsevier , Amsterdam, 1999).

8.
Jiang, D., Zhuang, D. & Huang, Y. Crop residues as an energy feedstock: Availability and sustainability. In Sustainable Bioenergy Production, 236–249 (CRC Press, Boca Raton, 2014).

9.
Rengel, Z. The role of crop residues in improving soil fertility. In Nutrient Cycling in Terrestrial Ecosystems, 183–214 (Springer, Berlin, 2007).

10.
Kalbitz, K., Solinger, S., Park, J.-H., Michalzik, B. & Matzner, E. Controls on the dynamics of dissolved organic matter in soils: A review. Soil Sci. 165, 277–304 (2000).
ADS  CAS  Google Scholar 

11.
Xiao, Y., Huang, Z. & Lu, X. Changes of soil labile organic carbon fractions and their relation to soil microbial characteristics in four typical wetlands of Sanjiang Plain, Northeast China. Ecol. Eng. 82, 381–389 (2015).
Google Scholar 

12.
Li, S. et al. Dynamics of soil labile organic carbon fractions and C-cycle enzyme activities under straw mulch in Chengdu Plain. Soil Till. Res. 155, 289–297 (2016).
Google Scholar 

13.
Allison, S. D., Czimczik, C. I. & Treseder, K. K. Microbial activity and soil respiration under nitrogen addition in Alaskan boreal forest. Glob. Change Biol. 14, 1156–1168 (2008).
ADS  Google Scholar 

14.
Chen, J. et al. Costimulation of soil glycosidase activity and soil respiration by nitrogen addition. Glob. Change Biol. 23, 1328–1337 (2017).
ADS  Google Scholar 

15.
Allison, S. D., Gartner, T. B., Mack, M. C., McGuire, K. & Treseder, K. Nitrogen alters carbon dynamics during early succession in boreal forest. Soil Biol. Biochem. 42, 1157–1164 (2010).
CAS  Google Scholar 

16.
Jian, S. et al. Soil extracellular enzyme activities, soil carbon and nitrogen storage under nitrogen fertilization: A meta-analysis. Soil Biol. Biochem. 101, 32–43 (2016).
CAS  Google Scholar 

17.
Veres, Z. et al. Soil extracellular enzyme activities are sensitive indicators of detrital inputs and carbon availability. Appl. Soil Ecol. 92, 18–23 (2015).
Google Scholar 

18.
Burns, R. G. et al. Soil enzymes in a changing environment: Current knowledge and future directions. Soil Biol. Biochem. 58, 216–234 (2013).
CAS  Google Scholar 

19.
Sinsabaugh, R. L. Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biol. Biochem. 42, 391–404 (2010).
CAS  Google Scholar 

20.
Sinsabaugh, R. L., Carreiro, M. M. & Alvarez, S. Enzyme and microbial dynamics of litter decomposition. In Enzymes in the Environment, Activity, Ecology, and Applications, 249–265 (Marcel Dekker, New York, 2002).

21.
Raju, M. N., Golla, N. & Vengatampalli, R. Soil cellulase. In Soil Enzymes, 25–30 (Springer, Berlin, 2017).

22.
Deng, S. & Tabatabai, M. Cellulase activity of soils. Soil Biol. Biochem. 26, 1347–1354 (2002).
Google Scholar 

23.
Raiesi, F. & Beheshti, A. Soil specific enzyme activity shows more clearly soil responses to paddy rice cultivation than absolute enzyme activity in primary forests of northwest Iran. Appl. Soil Ecol. 75, 63–70 (2014).
Google Scholar 

24.
Reeves, D. The role of soil organic matter in maintaining soil quality in continuous cropping systems. Soil Till. Res. 43, 131–167 (1997).
ADS  Google Scholar 

25.
Chen, X. et al. Carbon and nitrogen forms in soil organic matter influenced by incorporated wheat and corn residues. Soil Sci. Plant Nutr. 63, 377–387 (2017).
CAS  Google Scholar 

26.
Zhao, S. et al. Changes in soil microbial community, enzyme activities and organic matter fractions under long-term straw return in north-central China. Agric. Ecosyst. Environ. 216, 82–88 (2016).
CAS  Google Scholar 

27.
Zhu, L. et al. Short-term responses of soil organic carbon and carbon pool management index to different annual straw return rates in a rice–wheat cropping system. CATENA 135, 283–289 (2015).
CAS  Google Scholar 

28.
Malhi, S. S. & Gill, K. S. Fertilizer N and P effects on root mass of bromegrass, alfalfa and barley. J. Sustain. Agric. 19, 51–63 (2002).
Google Scholar 

29.
Campbell, C., Selles, F., Lafond, G. & Zentner, R. Adopting zero tillage management: Impact on soil C and N under long-term crop rotations in a thin Black Chernozem. Can. J. Soil Sci. 81, 139–148 (2001).
CAS  Google Scholar 

30.
Rasmussen, P. E. & Collins, H. P. Long-term impacts of tillage, fertilizer, and crop residue on soil organic matter in temperate semiarid regions. In Advances in Agronomy, Vol. 45, 93–134 (Elsevier, Amsterdam, 1991).

31.
Xu, M. et al. Soil organic carbon active fractions as early indicators for total carbon change under straw incorporation. Biol. Fertil. Soils 47, 745 (2011).
CAS  Google Scholar 

32.
Janzen, H., Campbell, C., Brandt, S. A., Lafond, G. & Townley-Smith, L. Light-fraction organic matter in soils from long-term crop rotations. Soil Sci. Soc. Am. J. 56, 1799–1806 (1992).
ADS  Google Scholar 

33.
Wang, W., Lai, D., Wang, C., Pan, T. & Zeng, C. Effects of rice straw incorporation on active soil organic carbon pools in a subtropical paddy field. Soil Till. Res. 152, 8–16 (2015).
Google Scholar 

34.
Chen, H. L., Zhou, J. M. & Xiao, B. H. Characterization of dissolved organic matter derived from rice straw at different stages of decay. J. Soils Sediments 10, 915–922 (2010).
CAS  Google Scholar 

35.
Tirol-Padre, A., Tsuchiya, K., Inubushi, K. & Ladha, J. K. Enhancing soil quality through residue management in a rice-wheat system in Fukuoka, Japan. Soil Sci. Plant Nutr. 51, 849–860 (2005).
CAS  Google Scholar 

36.
De Troyer, I., Amery, F., Van Moorleghem, C., Smolders, E. & Merckx, R. Tracing the source and fate of dissolved organic matter in soil after incorporation of a 13C labelled residue: A batch incubation study. Soil Biol. Biochem. 43, 513–519 (2011).
Google Scholar 

37.
Treseder, K. K. Nitrogen additions and microbial biomass: A meta-analysis of ecosystem studies. Ecol. Lett. 11, 1111–1120 (2008).
PubMed  PubMed Central  Google Scholar 

38.
Du, Y. et al. Different types of nitrogen deposition show variable effects on the soil carbon cycle process of temperate forests. Glob. Chang. Boil. 20, 3222–3228 (2014).
ADS  Google Scholar 

39.
Mergel, A., Timchenko, A. & Kudeyarov, V. Role of plant root exudates in soil carbon and nitrogen transformation. In Root Demographics and Their Efficiencies in Sustainable Agriculture, Grasslands and Forest Ecosystems. Developments in Plant and Soil Sciences, Vol. 82 (eds Box J.E.) (Springer, Dordrecht, 1998).

40.
Matocha, C. J., Haszler, G. R. & Grove, J. H. Nitrogen fertilization suppresses soil phenol oxidase enzyme activity in no-tillage systems. Soil Sci. 169, 708–714 (2004).
ADS  CAS  Google Scholar 

41.
Dell, E. A., Carley, D. S., Rufty, T. & Shi, W. Heat stress and N fertilization affect soil microbial and enzyme activities in the creeping bentgrass (Agrostis stolonifera L.) rhizosphere. Appl. Soil Ecol. 56, 19–26 (2012).
Google Scholar 

42.
Freeman, C., Ostle, N., Fenner, N. & Kang, H. A regulatory role for phenol oxidase during decomposition in peatlands. Soil Biol. Biochem. 36, 1663–1667 (2004).
CAS  Google Scholar 

43.
IUSS Working Group, W. World reference base for soil resources. World Soil Resources Report 103 (2006).

44.
Jones, D. & Willett, V. Experimental evaluation of methods to quantify dissolved organic nitrogen (DON) and dissolved organic carbon (DOC) in soil. Soil Biol. Biochem. 38, 991–999 (2006).
CAS  Google Scholar 

45.
Vance, E. D., Brookes, P. C. & Jenkinson, D. S. An extraction method for measuring soil microbial biomass C. Soil Biol. Biochem. 19, 703–707 (1987).
CAS  Google Scholar 

46.
Wu, J., Joergensen, R. G., Pommerening, B., Chaussod, R. & Brookes, P. C. Measurement of soil microbial biomass C by fumigation-extraction—an automated procedure. Soil Biol. Biochem. 22, 1167–1169 (1990).
CAS  Google Scholar 

47.
Gregorich, E. & Ellert, B. Light fraction and macroorganic matter in mineral soils. In Soil Sampling and Methods of Analysis, 397–407 (1993).

48.
Sinegani, A. A. S. & Sinegani, M. S. The effects of carbonates removal on adsorption, immobilization and activity of cellulase in a calcareous soil. Geoderma 173, 145–151 (2012).
ADS  Google Scholar 

49.
Dick, W. A., Thavamani, B., Conley, S., Blaisdell, R. & Sengupta, A. Prediction of β-glucosidase and β-glucosaminidase activities, soil organic C, and amino sugar N in a diverse population of soils using near infrared reflectance spectroscopy. Soil Biol. Biochem. 56, 99–104 (2013).
CAS  Google Scholar 

50.
Yang, Q. et al. Identification of three important amino acid residues of xylanase AfxynA from Aspergillus fumigatus for enzyme activity and formation of xylobiose as the major product. Process Biochem. 50, 571–581 (2015).
CAS  Google Scholar 

51.
Vepsäläinen, M., Kukkonen, S., Vestberg, M., Sirviö, H. & Niemi, R. M. Application of soil enzyme activity test kit in a field experiment. Soil Biol. Biochem. 33, 1665–1672 (2001).
Google Scholar 

52.
Yadav, M., Singh, S. & Yadava, S. Purification, characterisation and coal depolymerisation activity of lignin peroxidase from Lenzitus betulina MTCC-1183. Appl Biochem. Micro. 48, 583–589 (2012).
CAS  Google Scholar 

53.
Anderson, A. J., Kwon, S.-I., Carnicero, A. & Falcón, M. A. Two isolates of Fusarium proliferatum from different habitats and global locations have similar abilities to degrade lignin. FEMS Microbiol. Lett. 249, 149–155 (2005).
CAS  PubMed  PubMed Central  Google Scholar 

54.
Camarero, S., Sarkar, S., Ruiz-Dueñas, F.J., Martı́nez, M.A.J. & Martı́nez, A.T. Description of a versatile peroxidase involved in the natural degradation of lignin that has both manganese peroxidase and lignin peroxidase substrate interaction sites. J. Biol. Chem. 274, 10324–10330 (1999).
CAS  PubMed  PubMed Central  Google Scholar 

55.
Feng, S. et al. Laccase activity is proportional to the abundance of bacterial laccase-like genes in soil from subtropical arable land. World J. Microb. Biotechnol. 31, 2039–2045 (2015).
CAS  Google Scholar  More

1.
Rezapour, S., Atashpaz, B., Moghaddam, S. S. & Damalas, C. A. Heavy metal bioavailability and accumulation in winter wheat (Triticum aestivum L.) irrigated with treated wastewater in calcareous soils. Sci. Total Environ. 656, 261–269. https://doi.org/10.1016/j.scitotenv.2018.11.288 (2019).
ADS  CAS  Article  PubMed  Google Scholar 
2.
Wang, S., Wu, W., Liu, F., Liao, R. & Hu, Y. Accumulation of heavy metals in soil–crop systems: a review for wheat and corn. Environ. Sci. Pollut. Res. 24, 15209–15225. https://doi.org/10.1007/s11356-017-8909-5 (2017).
CAS  Article  Google Scholar 

3.
Rezapour, S., Kouhinezhad, P., Samadi, A. & Rezapour, M. Level, pattern, and risk assessment of the selected soil trace metals in the calcareous cultivated Vertisols. Chem. Ecol. 8, 692–706. https://doi.org/10.1080/02757540.2013.810728 (2015).
CAS  Article  Google Scholar 

4.
Zhang, Y. et al. Heavy metal accumulation and health risk assessment in soil-wheat system under different nitrogen levels. Sci. Total Environ. 622–623, 1499–1508. https://doi.org/10.1016/j.scitotenv.2017.09.317 (2018).
ADS  CAS  Article  PubMed  Google Scholar 

5.
Gill, R. A. et al. Reduced glutathione mediates pheno-ultrastructure kinome and transportome in chromium-induced Brassica napus L.. Front. Plant Sci. 8, 2037. https://doi.org/10.3389/fpls.2017.02037 (2017).
Article  PubMed  PubMed Central  Google Scholar 

6.
Khan, M. U., Malik, R. N. & Muhammad, S. Human health risk from heavy metal via food crops consumption with wastewater irrigation practices in Pakistan. Chemosphere 93, 2230–2238. https://doi.org/10.1016/j.chemosphere.2013.07.067 (2013).
ADS  CAS  Article  PubMed  Google Scholar 

7.
Zajac, L. et al. Probabilistic estimates of prenatal lead exposure at toxic hotspots in low- and middle-income countries. Environ. Res. 183, 109251. https://doi.org/10.1016/j.envres.2020.109251 (2020).
CAS  Article  PubMed  Google Scholar 

8.
Odongo, A. O., Moturi, W. N. & Mbuthia, E. K. Heavy metals and parasitic geo helminths toxicity among geophagous pregnant women: a case study of Nakuru Municipality, Kenya. Environ. Geochem. Health 38, 123–131. https://doi.org/10.1007/s10653-015-9690-3 (2015).
CAS  Article  PubMed  Google Scholar 

9.
Vergara, C., María, C., Judith, L. P. & Rodriguez, H. Effects of co-cropping on soybean growth and stress response in lead-polluted soils. Chemosphere 246, 125833. https://doi.org/10.1016/j.chemosphere.2020.125833 (2020).
ADS  CAS  Article  Google Scholar 

10.
Shekar, C. C., Sammaiah, D., Shasthree, T. & Reddy, K. J. Effect of mercury on tomato growth and yield attributes. Int. J. Pharm. Biol. Sci. 2, B358–B364. https://doi.org/10.1007/s11356-018-1498-0 (2011).
CAS  Article  Google Scholar 

11.
Tiwari, K., Singh, N. K. & Rai, U. N. Chromium phytotoxicity in radish (Raphanus sativus): effects on metabolism and nutrient uptake. Bull. Environ. Contam. Toxicol. 91, 339–344. https://doi.org/10.1007/s00128-013-1047-y (2013).
CAS  Article  PubMed  Google Scholar 

12.
Bergqvist, C., Herbert, R., Persson, I. & Greger, M. Plants influence on arsenic availability and speciation in the rhizosphere, roots and shoots of three different vegetables. Environ. Pollut. 184, 540–546. https://doi.org/10.1016/j.envpol.2013.10.003 (2014).
CAS  Article  PubMed  Google Scholar 

13.
Rizwan, M. et al. A critical review on effects, tolerance mechanisms and management of cadmium in vegetables. Chemosphere 182, 90–105. https://doi.org/10.1016/j.chemosphere.2017.05.013 (2017).
ADS  CAS  Article  PubMed  Google Scholar 

14.
Rafaqat, A. G. et al. Chromium-induced physio-chemical and ultrastructural changes in four cultivars of Brassica napus L.. Chemosphere 120, 154–164. https://doi.org/10.1016/j.chemosphere.2014.06.029 (2015).
ADS  CAS  Article  Google Scholar 

15.
Ali, B. et al. Regulation of cadmium-induced proteomic and metabolic changes by 5-aminolevulinic acid in leaves of Brassica napus L.. PLoS ONE 10(4), e0123328. https://doi.org/10.1371/journal.pone.0123328 (2015) (eCollection).
CAS  Article  PubMed  PubMed Central  Google Scholar 

16.
Basharat, A. et al. Promotive role of 5-aminolevulinic acid on mineral nutrients and antioxidative defense system under lead toxicity in Brassica napus. Ind. Crops Prod. 52, 617–626. https://doi.org/10.1016/j.indcrop.2013.11.033 (2014).
CAS  Article  Google Scholar 

17.
Gill, R. A. et al. Genotypic variation of the responses to chromium toxicity in four oilseed rape cultivars. Biol. Plant. 58, 539–550. https://doi.org/10.1007/s10535-014-0430-9 (2014).
CAS  Article  Google Scholar 

18.
Tandon, V., Gupta, B. M. & Tandon, R. Free radicals/reactive oxygen species. JK Pract. Nurs. Res. Pract. 12, 143–148. https://doi.org/10.1155/2011/260482 (2005).
Article  Google Scholar 

19.
Yang, Y., Liu, H., Xiang, X. H. & Liu, F. Y. Outline of occupational chromium poisoning in China. Bull Environ. Contam. Toxicol. 90, 742–749. https://doi.org/10.1007/s00128-013-0998-3 (2013).
CAS  Article  PubMed  Google Scholar 

20.
Vaiserman, A. M. Aging-modulating treatments: from reductionism to a system oriented perspective. Front. Genet. 5, 1–3. https://doi.org/10.3389/fgene.2014.00446 (2016).
CAS  Article  Google Scholar 

21.
Bewley, J.D. & Black, M. Biochemistry of germination and growth. In: Physiology and Biochemistry of seeds in relation to germination. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-66668-1_5 (1978).

22.
Zadoks, J. C., Chang, T. T. & Konzak, C. T. A decimal code for the growth stages of cereals. Weed Res. 14, 415–421. https://doi.org/10.1111/j.1365-3180.1974.tb01084.x (1974).
Article  Google Scholar 

23.
Vernay, P. et al. Effect of chromium species on phytochemical and physiological parameters in Datura innoxia. Chemosphere 72, 763–771. https://doi.org/10.1016/j.chemosphere.2008.03.018 (2008).
ADS  CAS  Article  PubMed  Google Scholar 

24.
Arnon, D. T. Copper enzymes in isolated chloroplasts: polyphenol oxidase in Beta vulgaris. J. Plant Physiol. 24, 1–15. https://doi.org/10.1104/pp.24.1.1 (1949).
CAS  Article  Google Scholar 

25.
Zofia, L., Kmiecik, W. & Korus, A. Content of vitamin C, carotinoids, chlorophylls and polyphenols in green parts of dill (Anethum graveolens L.) depending on plant height. J. Food Compos. Anal. 19, 134–140. https://doi.org/10.1016/j.jfca.2005.04.009 (2006).
CAS  Article  Google Scholar 

26.
Ryan, J., Estfan, G. & Rashid, A. Soil and Plant Analysis Laboratory Manual. 2nd ed., pp. 87–89. ISBN 9788172337650 (2001).

27.
Panichev, N., Mandiwana, K., Kataeva, M. & Siebert, S. Determination of Cr (VI) in plants by electrothermal atomic absorption spectrometry after leaching with sodium carbonate. Spectrochim. Acta Part B 60, 699–703. https://doi.org/10.1016/j.sab.2005.02.018 (2005).
ADS  CAS  Article  Google Scholar 

28.
Chandra, R., Kumar, P. K. & Singh, J. Impact of an aerobically treated and untreated (raw) distillery effluent irrigation on soil micro flora, growth, total chlorophyll and protein contents of Phaseolus aureus L.. J. Environ. Biol. 25, 381–385 (2004).
PubMed  Google Scholar 

29.
Velthof, G., Van-Beusichem, M. & Raijmakers, W. Relationship between availability indices and plant uptake of nitrogen and phosphorus from organic products. Plant Soil 200, 215. https://doi.org/10.1023/A:1004336903214 (1998).
CAS  Article  Google Scholar 

30.
Steel, R. G. D. & Torrie, J. H. Principles and Procedures of Statistics 172–177 (McGraw Hill Book Crop., Inc., Singapore, 1984).
Google Scholar 

31.
Chun, X. L. et al. Effects of arsenic on seed germination and physiological activities of wheat seedlings. J. Environ. Sci. 19, 725–732. https://doi.org/10.1016/S1001-0742(07)60121-1 (2007).
Article  Google Scholar 

32.
Alghobar, M. A. & Suresha, A. Evaluation of metal accumulation in soil and tomatoes irrigated with sewage water from Mysore city, Karnataka India. J. Saudi Soc. Agric. Sci. 16, 49–59. https://doi.org/10.1016/j.jssas.2015.02.002 (2017).
Article  Google Scholar 

33.
Yourtchi, M. S. & Bayat, H. Y. Effect of cadmium toxicity on growth, cadmium accumulation and macronutrient content of durum wheat (Dena CV). Int. J. Agric. Crop Sci. 6, 1099–1103 (2013).
CAS  Google Scholar 

34.
Barberon, M. & Geldner, N. Radial transport of nutrients: the plant root as a polarized epithelium. Plant Physiol. 166, 528–537. https://doi.org/10.1104/pp.114.246124 (2014).
CAS  Article  PubMed  PubMed Central  Google Scholar 

35.
Shahid, M. et al. Heavy-metal-induced reactive oxygen species: phytotoxicity and physicochemical changes in plants. Rev. Environ. Contam. Toxicol. 232, 1–44. https://doi.org/10.1007/978-3-319-06746-9_1 (2014).
CAS  Article  PubMed  Google Scholar 

36.
Yadav, K. K. et al. Mechanistic understanding and holistic approach of phytoremediation: a review on application and future prospects. Ecol. Eng. 120, 274–298. https://doi.org/10.1016/j.ecoleng.2018.05.039 (2018).
Article  Google Scholar 

37.
Gopal, R. & Rizvi, A. H. Excess lead alters growth, metabolism and translocation of certain nutrients in radish. Chemosphere 70, 1539–1544. https://doi.org/10.1016/j.chemosphere.2007.08.043 (2008).
ADS  CAS  Article  PubMed  Google Scholar 

38.
Antoniadis, V. et al. Trace elements in the soil-plant interface: phytoavailability, translocation, and phytoremediation—a review. Earth Sci. Rev. 172, 621–645. https://doi.org/10.1016/j.earscirev.2017.06.005 (2017).
ADS  CAS  Article  Google Scholar 

39.
Hamid, N., Bukhari, N. & Jawaid, F. Physiological responses of phaseolus vulgaris to different lead concentrations. Pak. J. Bot. 42, 239–246 (2010).
CAS  Google Scholar 

40.
Osma, M., Serin, Z. & Leblebici, A. Heavy metals accumulation in some vegetables and soils in Istanbul. Ekoloji. 21, 1–8. https://doi.org/10.5053/ekoloji.2011.821 (2012).
CAS  Article  Google Scholar 

41.
Singh, S., Parihar, P., Singh, R., Singh, V. P. & Prasad, S. M. Heavy metal tolerance in plants: role of transcriptomics, proteomics, metabolomics, and ionomics. Front. Plant Sci. 6, 1143–1148. https://doi.org/10.3389/fpls.2015.01143 (2015).
Article  PubMed  Google Scholar 

42.
Zeng, L. S., Liao, M., Chen, C. L. & Huang, C. Y. Effects of lead contamination on soil microbial activity and physiological indices in soil-Pb-rice (Oryza sativa L.) system. Chemosphere 65, 567–574. https://doi.org/10.1016/j.chemosphere.2006.02.039 (2006).
ADS  CAS  Article  PubMed  Google Scholar 

43.
Qadir, S., Qureshi, M. I., Javed, S. & Abdin, M. Z. Genotypic variation in phytoremediation potential of Brassica juncea cultivars exposed to Cd stress. Plant Sci. 167, 1171–1181. https://doi.org/10.1016/j.plantsci.2004.06.018 (2004).
CAS  Article  Google Scholar 

44.
Xiong, T. T. et al. Foliar uptake and metal(loid) bioaccessibility in vegetables exposed to particulate matter. Environ. Geochem. Health 36, 897–909. https://doi.org/10.1007/s10653-014-9607-6 (2014).
CAS  Article  PubMed  Google Scholar 

45.
Zheljazkov, V. D. & Nielsen, N. E. Effect of heavy metals on peppermint and cornmint. Plant Soil 178, 59–66. https://doi.org/10.1007/BF00011163 (1996).
CAS  Article  Google Scholar 

46.
Lavado, R. S., Porcelli, C. A. & Alvarez, R. Nutrient and heavy metal concentration and distribution in corn, soybean and wheat as affected by different tillage systems in Argentine Pampas. Soil Tillage Res. 62, 55–60. https://doi.org/10.1016/S0167-1987(01)00216-1 (2001).
Article  Google Scholar 

47.
Gupta, N. et al. Trace elements in soil-vegetables interface: translocation, bioaccumulation, toxicity and amelioration—a review. Sci. Total Environ. 651, 2927–2942. https://doi.org/10.1016/j.scitotenv.2018.10.047 (2019).
ADS  CAS  Article  PubMed  Google Scholar 

48.
Ho, W. M., Ang, L. H. & Lee, D. K. Assessment of Pb uptake, translocation in Kenaf (Hibiscus cannabinus L.) for phytoremediation of sand tailings. J. Evniron. Sci. 20, 1341–47. https://doi.org/10.1016/S1001-0742(08)62231-7 (2008).
CAS  Article  Google Scholar 

49.
Vogel-Mikus, K., Drobne, D. & Regvar, M. Zn, Cd and Pb accumulation and arbuscular mycorrhizal colonization of pennycress Thlaspi praecox Wulf (Brassicaceae) from the vicinity of a lead mine and smelter in Slovenia. Environ. Pollut. 133, 233–242. https://doi.org/10.1016/j.envpol.2004.06.021 (2005).
CAS  Article  PubMed  Google Scholar 

50.
Liu, J. G., Li, K. Q., Xu, J. K. & Zhang, Z. J. Lead toxicity, uptake and translocation in different rice cultivars. Plant Sci. 165, 793–802. https://doi.org/10.1016/S0168-9452(03)00273-5 (2003).
CAS  Article  Google Scholar 

51.
Zhang, M. K., Liu, Z. Y. & Wang, H. Use of single extraction methods to predict bioavailability of heavy metals in polluted soils to rice. Commun. Soil Sci. Plant Anal. 41, 820–831. https://doi.org/10.1080/00103621003592341 (2010).
CAS  Article  Google Scholar 

52.
Shahid, M. et al. Foliar heavy metal uptake, toxicity and detoxification in plants: a comparison of foliar and root metal uptake. J. Hazard. Mater. 325, 36–58. https://doi.org/10.1016/j.jhazmat.2016.11.063 (2016).
CAS  Article  PubMed  Google Scholar 

53.
Sharma, R. K., Agrawal, M., Bhushan, S. & Agrawal, S. B. Physiological and biochemical responses resulting from cadmium and zinc accumulation in carrot plants. J. Plant Nutr. 33, 1066–1079. https://doi.org/10.1080/01904161003729774 (2010).
CAS  Article  Google Scholar 

54.
McBride, M. B., Shayler, H. A., Russell-Anelli, J. M., Spliethoff, H. M. & Marquez, L. G. Arsenic and lead uptake by vegetable crops grown on an old Orchard site amended with compost. Water Air Soil Pollut. 226, 265–272. https://doi.org/10.1007/s11270-015-2529-9 (2015).
ADS  CAS  Article  PubMed  PubMed Central  Google Scholar  More

1.
Ward, J. V & Stanford, J. A. Serial discontinuity concept of lotic ecosystems. In Dynamics of Lotic Systems, Ann Arbor Science, Ann Arbor 29–42 (1983).
2.
Bouwman, A. F. et al. Nutrient dynamics, transfer and retention along the aquatic continuum from land to ocean: towards integration of ecological and biogeochemical models. Biogeosciences 10, 1–22 (2013).
ADS  Google Scholar 

3.
Proia, L. et al. Microbial carbon processing along a river discontinuum. Freshw. Sci. 35, 1133–1147 (2016).
Google Scholar 

4.
Casas-Ruiz, J. P. et al. A tale of pipes and reactors: Controls on the in-stream dynamics of dissolved organic matter in rivers. Limnol. Oceanogr. 62, S85–S94 (2017).
CAS  Google Scholar 

5.
Artigas, J. et al. Phosphorus use by planktonic communities in a large regulated Mediterranean river. Sci. Total Environ. 426, 180–187 (2012).
ADS  CAS  PubMed  Google Scholar 

6.
Gómez-Gener, L., Gubau, M., von Schiller, D., Marcé, R. & Obrador, B. Effect of small water retention structures on diffusive CO2 and CH4 emissions along a highly impounded river. Inl. Waters 8, 449–460 (2018).
Google Scholar 

7.
Irriberri, J., Unanue, M., Barcina, I. & Egea, L. Seasonal variation in population density and heterotrophic activity of attached and free-living bacteria in coastal waters. Appl. Environ. Microbiol. 53, 2308–2314 (1987).
Google Scholar 

8.
Grossart, H. & Simon, M. Bacterial colonization and microbial decomposition of limnetic organic aggregates (lake snow). Aquat. Microb. Ecol. 15, 1127–1140 (1998).
Google Scholar 

9.
Simon, M., Grossart, H. P., Schweitzer, B. & Ploug, H. Microbial ecology of organic aggregates in aquatic ecosystems. Aquat. Microb. Ecol. 28, 175–211 (2002).
Google Scholar 

10.
Wilczek, S., Wörner, U., Pusch, M. T. & Fischer, H. Role of suspended particles for extracellular enzyme activity and biotic control of pelagic bacterial populations in the large lowland river Elbe. Fundam. Appl. Limnol./Arch. für Hydrobiol. 169, 153–168 (2007).
Google Scholar 

11.
Rieck, A., Herlemann, D. P. R., Jürgens, K. & Grossart, H. P. Particle-associated differ from free-living bacteria in surface waters of the baltic sea. Front. Microbiol. 6, 1297 (2015).
PubMed  PubMed Central  Google Scholar 

12.
Ruiz-González, C., Proia, L., Ferrera, I., Gasol, J. M. & Sabater, S. Effects of large river dam regulation on bacterioplankton community structure. FEMS Microbiol. Ecol. 84, 316–331 (2013).
PubMed  Google Scholar 

13.
Salazar, G. et al. Particle-association lifestyle is a phylogenetically conserved trait in bathypelagic prokaryotes. Mol. Ecol. 24, 5692–5706 (2015).
PubMed  Google Scholar 

14.
López-Pérez, M., Kimes, N. E., Haro-Moreno, J. M. & Rodriguez-Valera, F. Not all particles are equal: The selective enrichment of particle-associated bacteria from the mediterranean sea. Front. Microbiol. 7, 996 (2016).
PubMed  PubMed Central  Google Scholar 

15.
Mestre, M., Borrull, E., Sala, M. & Gasol, J. M. Patterns of bacterial diversity in the marine planktonic particulate matter continuum. ISME J. 11, 999–1010 (2017).
PubMed  PubMed Central  Google Scholar 

16.
Zeglin, L. H. Stream microbial diversity in response to environmental changes: Review and synthesis of existing research. Front. Microbiol. 6, 1–15 (2015).
Google Scholar 

17.
Galand, P. E., Lovejoy, C., Pouliot, J. & Vincent, W. F. Heterogeneous archaeal communities in the particle-rich environment of an arctic shelf ecosystem. J. Mar. Syst. 74, 774–782 (2008).
Google Scholar 

18.
Orsi, W. D. et al. Ecophysiology of uncultivated marine euryarchaea is linked to particulate organic matter. ISME J. 9, 1747–1763 (2015).
PubMed  PubMed Central  Google Scholar 

19.
Crump, B. C. & Baross, J. A. Archaeaplankton in the Columbia River, its estuary and the adjacent coastal ocean, USA. FEMS Microbiol. Ecol. 31, 231–239 (2000).
CAS  PubMed  Google Scholar 

20.
Dumestre, J., Casamayor, E. O., Massana, R. & Pedrós-alió, C. Changes in bacterial and archaeal assemblages in an equatorial river induced by the water eutrophication of Petit Saut dam reservoir (French Guiana). Aquat. Microb. Ecol. 26, 209–221 (2001).
Google Scholar 

21.
Galand, P. E., Lovejoy, C. & Vincent, W. F. Remarkably diverse and contrasting archaeal communities in a large arctic river and the coastal Arctic Ocean. Aquat. Microb. Ecol. 44, 115–126 (2006).
Google Scholar 

22.
Leibold, M. A. & Chase, J. M. Metacommunity Ecology (Princeton University Press, Princeton, 2018).
Google Scholar 

23.
Lindström, E. S. & Langenheder, S. Local and regional factors influencing bacterial community assembly. Environ. Microbiol. Rep. 4, 1–9 (2012).
PubMed  Google Scholar 

24.
Staley, C. et al. Species sorting and seasonal dynamics primarily shape bacterial communities in the Upper Mississippi River. Sci. Total Environ. 505, 435–445 (2015).
ADS  CAS  PubMed  Google Scholar 

25.
Ruiz-González, C. et al. Weak coherence in abundance patterns between bacterial classes and their constituent OTUs along a regulated river. Front. Microbiol. 6, 1–13 (2015).
Google Scholar 

26.
Grossart, H. P. Ecological consequences of bacterioplankton lifestyles: Changes in concepts are needed. Environ. Microbiol. Rep. 2, 706–714 (2010).
PubMed  Google Scholar 

27.
Azam, F. & Malfatti, F. Microbial structuring of marine ecosystems. Nat. Rev. Microbiol. 5, 782–791 (2007).
CAS  PubMed  Google Scholar 

28.
Böckelmann, U., Manz, W., Neu, T. R. & Szewzyk, U. Characterization of the microbial community of lotic organic aggregates (‘river snow’) in the Elbe River of Germany by cultivation and molecular methods. FEMS Microbiol. Ecol. 33, 157–170 (2000).
Google Scholar 

29.
Ghiglione, J. F. et al. Diel and seasonal variations in abundance, activity, and community structure of particle-attached and free-living bacteria in NW Mediterranean Sea. Microb. Ecol. 54, 217–231 (2007).
CAS  PubMed  PubMed Central  Google Scholar 

30.
Rösel, S. & Grossart, H. P. Contrasting dynamics in activity and community composition of free-living and particle-associated bacteria in spring. Aquat. Microb. Ecol. 66, 169–181 (2012).
Google Scholar 

31.
Crespo, B. G., Pommier, T., Fernández-Gómez, B. & Pedrós-Alió, C. Taxonomic composition of the particle-attached and free-living bacterial assemblages in the Northwest Mediterranean Sea analyzed by pyrosequencing of the 16S rRNA. Microbiologyopen 2, 541–552 (2013).
CAS  PubMed  PubMed Central  Google Scholar 

32.
Ortega-Retuerta, E., Joux, F., Jeffrey, W. H. & Ghiglione, J. F. Spatial variability of particle-attached and free-living bacterial diversity in surface waters from the Mackenzie River to the Beaufort Sea (Canadian Arctic). Biogeosciences 10, 2747–2759 (2013).
ADS  Google Scholar 

33.
Hollibaughl, J. T., Wongl, P. S. & Michael, C. Similarity of particle-associated and free-living bacterial communities in northern San Francisco. Water 21, 103–114 (2000).
Google Scholar 

34.
Moeseneder, M. M., Winter, C. & Herndl, G. J. Horizontal and vertical complexity of attached and free-living bacteria of the eastern Mediterranean Sea, determined by 16S rDNA and 16S rRNA fingerprints. Limnol. Oceanogr. 46, 95–107 (2001).
ADS  CAS  Google Scholar 

35.
Eloe, E. A. et al. Compositional differences in particle-associated and free-living microbial assemblages from an extreme deep-ocean environment. Environ. Microbiol. Rep. 3, 449–458 (2011).
PubMed  Google Scholar 

36.
Zhang, R., Liu, B., Lau, S., Ki, J.-S. & Qian, P.-Y. Particle-attached and free-living bacterial communities in a contrasting marine environment: Victoria Harbor, Hong Kong. FEMS Microbiol. Ecol. 61, 496–508 (2007).
CAS  PubMed  Google Scholar 

37.
Mestre, M. et al. Spatial variability of marine bacterial and archaeal communities along the particulate matter continuum. Mol. Ecol. 26, 6827–6840 (2017).
CAS  PubMed  Google Scholar 

38.
Ivars-Martinez, E. et al. Comparative genomics of two ecotypes of the marine planktonic copiotroph Alteromonas macleodii suggests alternative lifestyles associated with different kinds of particulate organic matter. ISME J. 2, 1194–1212 (2008).
CAS  PubMed  Google Scholar 

39.
Fernández-Gómez, B. et al. Ecology of marine Bacteroidetes: A comparative genomics approach. ISME J. 7, 1026–1037 (2013).
PubMed  PubMed Central  Google Scholar 

40.
Newton, R. J., Jones, S. E., Eiler, A., McMahon, K. D. & Bertilsson, S. A guide to the natural history of freshwater lake bacteria. Microbiol. Mol. Biol. Rev. 75, 14–49 (2011).
CAS  PubMed  PubMed Central  Google Scholar 

41.
Kasalický, V., Jezbera, J., Hahn, M. W. & Šimek, K. The diversity of the Limnohabitans genus, an important group of freshwater bacterioplankton, by characterization of 35 isolated strains. PLoS ONE 8, e58209 (2013).
ADS  PubMed  PubMed Central  Google Scholar 

42.
Simek, K. et al. Broad habitat range of the phylogenetically narrow R-BT065 cluster, representing a core group of the Betaproteobacterial genus Limnohabitans. Appl. Environ. Microbiol. 76, 631–639 (2010).
CAS  PubMed  Google Scholar 

43.
Jezberová, J., Šimek, K., Hahn, M. W., Jezbera, J. & Kasalický, V. Patterns of Limnohabitans microdiversity across a large set of freshwater habitats as revealed by reverse line blot hybridization. PLoS ONE 8, e58527 (2013).
ADS  PubMed  PubMed Central  Google Scholar 

44.
Shade, A. et al. Conditionally rare taxa disproportionately contribute to temporal changes in microbial diversity. MBio 5, 1–9 (2014).
Google Scholar 

45.
Castelle, C. J. et al. Genomic expansion of domain archaea highlights roles for organisms from new phyla in anaerobic carbon cycling. Curr. Biol. 25, 690–701 (2015).
CAS  PubMed  Google Scholar 

46.
Stahl, D. A. & de la Torre, J. R. Physiology and diversity of ammonia-oxidizing archaea. Annu. Rev. Microbiol. 66, 83–101 (2012).
CAS  PubMed  Google Scholar 

47.
Liu, X. et al. Insights into the ecology, evolution, and metabolism of the widespread Woesearchaeotal lineages. Microbiome 6, 1–16 (2018).
Google Scholar 

48.
Ortiz-Alvarez, R. & Casamayor, E. O. High occurrence of Pacearchaeota and Woesearchaeota (Archaea superphylum DPANN) in the surface waters of oligotrophic high-altitude lakes. Environ. Microbiol. Rep. 8, 210–217 (2016).
CAS  PubMed  Google Scholar 

49.
Fillol, M., Auguet, J.-C., Casamayor, E. O. & Borrego, C. M. Insights in the ecology and evolutionary history of the Miscellaneous Crenarchaeotic Group lineage. ISME J. 10, 653–677 (2016).
Google Scholar 

50.
Durbin, A. M. & Teske, A. Archaea in organic-lean and organic-rich marine subsurface sediments: an environmental gradient reflected in distinct phylogenetic lineages. Front. Microbiol. 3, 168 (2012).
PubMed  PubMed Central  Google Scholar 

51.
Fillol, M., Sànchez-Melsió, A., Gich, F. & Borrego, M. C. Diversity of Miscellaneous Crenarchaeotic Group archaea in freshwater karstic lakes and their segregation between planktonic and sediment habitats. FEMS Microbiol. Ecol. 91, fiv20 (2015).
Google Scholar 

52.
Compte-Port, S. et al. Abundance and Co-Distribution of Widespread Marine Archaeal Lineages in Surface Sediments of Freshwater Water Bodies across the Iberian Peninsula. Microb. Ecol. 74, 776–787 (2017).
PubMed  Google Scholar 

53.
Allgaier, M. & Grossart, H. Diversity and seasonal dynamics of actinobacteria populations in four lakes in Northeastern Germany. Appl. Environ. Microbiol. 72, 3489–3497 (2006).
CAS  PubMed  PubMed Central  Google Scholar 

54.
Grasshoff, K., Kremling, K. & Ehrhardt, M. Methods of Seawater Analysis (Wiley-VCH Verlag Gmbh, Weinheim, 1999).
Google Scholar 

55.
Dowd, S. E. et al. Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiol. 8, 125 (2008).
PubMed  PubMed Central  Google Scholar 

56.
Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335–336 (2010).
CAS  PubMed  PubMed Central  Google Scholar 

57.
Desantis, T. Z. et al. Gene database and workbench compatible with ARB. (California Institute of Technology, accessed 2 October 2 2014);http://aem.asm.org/.

58.
Desantis, T. Z. et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72, 5069–5072 (2006).
CAS  PubMed  PubMed Central  Google Scholar 

59.
Caporaso, J. G. et al. PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26, 266–267 (2010).
CAS  PubMed  Google Scholar 

60.
Quast, C. et al. The SILVA ribosomal RNA gene database project : improved data processing and web-based tools. Nucleic Acids Res. 41, 590–596 (2013).
Google Scholar 

61.
Parks, D. H. et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat. Biotechnol. 36, 996 (2018).
CAS  PubMed  Google Scholar 

62.
Lozupone, C. & Knight, R. UniFrac : A new phylogenetic method for comparing microbial communitiess. Appl. Environ. Microbiol. 71, 8228–8235 (2005).
CAS  PubMed  PubMed Central  Google Scholar 

63.
Andersen, S. K., Kirkegaard, R. H., Karst, S. M. & Albertsen, M. ampvis2: An R package to analyse and visualise 16S rRNA amplicon data. BioRxiv https://doi.org/10.1101/299537 (2018).
Article  Google Scholar 

64.
R Development Core Team. R: A language and environment for statistical computing. ISBN: 3-900051-07-0 (2011).

65.
Dufrene, M. & Legendre, P. Species assemblages and indicator species: The need for flexible asymmetrical approach. Ecol. Monogr. 67, 345–366 (1997).
Google Scholar 

66.
De Cáceres, M. & Legendre, P. Associations between species and groups of sites: Indices and statistical inference. Ecology 90, 3566–3574 (2009).
PubMed  Google Scholar 

67.
Aßhauer, K. P., Wemheuer, B., Daniel, R. & Meinicke, P. Tax4Fun: Predicting functional profiles from metagenomic 16S rRNA data. Bioinformatics 31, 2882–2884 (2015).
PubMed  PubMed Central  Google Scholar 

68.
Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Stat. Soc. 57, 289–300 (1995).
MathSciNet  MATH  Google Scholar 

69.
Wickham, H. ggplot2. Elegant Grsaphics for Data Analysis (Springer, New York , 2009). https://doi.org/10.1007/978-0-387-98141-3.
Google Scholar  More

Study sites and sampling
Three soil types were selected (Table 2). The first was an Andisol31 (Volcanic–allophanic) formed from recent Volcanic ash deposited in the Andes. This was collected from a native temperate rainforest dominated by old growth Nothofagus betuloides (Mirb.) located in Puyehue National Park, where mean annual precipitation is typically  > 8,000 mm year−112. The soils are derived from basaltic scoria with high levels of allophane, imogolite, and ferrihydrite material32. The second soil type was an Ultisol (Metamorphic) sampled in Alerce Costero National Park in the coastal range. It is derived from Metamorphic-schist with high levels of illite-kaolinite33. Finally, an Inceptisol (Granitic) was selected from an ancient Araucaria araucana and Nothofagus pumilio forest in Nahuelbuta National Park. This soil type originates from intrusive Granitic rock parent materials. Mean annual precipitation in this ancient forest reaches  > 1,491 mm and mean annual temperatures reach 13.3 °C34 (Table 2). From each soil sample, four composite soil samples were taken from the Ah mineral horizon (5–10 cm) after removing litter and organic horizons. The samples were then transported to a laboratory under cold conditions. All soils were homogenized and sieved ( More