Ecology

1.Tilman, D., Balzer, C., Hill, J. & Befort, B. L. Global food demand and the sustainable intensification of agriculture. Proc. Natl Acad. Sci. USA 108, 20260–20264 (2011).CAS 
Article 

Google Scholar 
2.Foley, J. A. et al. Global consequences of land use. Science 309, 570–574 (2005).CAS 
Article 

Google Scholar 
3.Hansen, M. C. et al. High-resolution global maps of 21st-century forest cover change. Science 342, 850–853 (2013).CAS 
Article 

Google Scholar 
4.Song, X.-P. et al. Global land change from 1982 to 2016. Nature 560, 639–643 (2018).CAS 
Article 

Google Scholar 
5.Curtis, P. G., Slay, C. M., Harris, N. L., Tyukavina, A. & Hansen, M. C. Classifying drivers of global forest loss. Science 361, 1108–1111 (2018).CAS 
Article 

Google Scholar 
6.Pimm, S. L. et al. The biodiversity of species and their rates of extinction, distribution, and protection. Science 344, 1246752 (2014).CAS 
Article 

Google Scholar 
7.Graesser, J., Ramankutty, N. & Coomes, O. T. Increasing expansion of large-scale crop production onto deforested land in sub-Andean South America. Environ. Res. Lett. 13, 084021 (2018).Article 

Google Scholar 
8.Zalles, V. et al. Near doubling of Brazil’s intensive row crop area since 2000. Proc. Natl Acad. Sci. USA 116, 428–435 (2019).CAS 
Article 

Google Scholar 
9.FAOSTAT (FAO, 2019); http://www.fao.org/faostat10.Cassman, K. G. & Grassini, P. A global perspective on sustainable intensification research. Nat. Sustain. 3, 262–268 (2020).Article 

Google Scholar 
11.Fuchs, R. et al. Why the US–China trade war spells disaster for the Amazon. Nature 567, 451–454 (2019).CAS 
Article 

Google Scholar 
12.Lambin, E. F. et al. The role of supply-chain initiatives in reducing deforestation. Nat. Clim. Change 8, 109–116 (2018).Article 

Google Scholar 
13.Rudorff, B. F. T. et al. The soy moratorium in the Amazon biome monitored by remote sensing images. Remote Sens. 3, 185–202 (2011).Article 

Google Scholar 
14.Gibbs, H. K. et al. Brazil’s soy moratorium. Science 347, 377–378 (2015).CAS 
Article 

Google Scholar 
15.Kastens, J. H., Brown, J. C., Coutinho, A. C., Bishop, C. R. & Esquerdo, J. Soy moratorium impacts on soybean and deforestation dynamics in Mato Grosso, Brazil. PLoS ONE 12, e0176168 (2017).Article 
CAS 

Google Scholar 
16.Gollnow, F., Hissa, Ld. B. V., Rufin, P. & Lakes, T. Property-level direct and indirect deforestation for soybean production in the Amazon region of Mato Grosso, Brazil. Land Use Policy 78, 377–385 (2018).Article 

Google Scholar 
17.Rausch, L. L. et al. Soy expansion in Brazil’s Cerrado. Conserv. Lett. https://doi.org/10.1111/conl.12671 (2019).18.Spera, S. A., Galford, G. L., Coe, M. T., Macedo, M. N. & Mustard, J. F. Land-use change affects water recycling in Brazil’s last agricultural frontier. Glob. Change Biol. 22, 3405–3413 (2016).Article 

Google Scholar 
19.Noojipady, P. et al. Forest carbon emissions from cropland expansion in the Brazilian Cerrado biome. Environ. Res. Lett. 12, 025004 (2017).Article 
CAS 

Google Scholar 
20.Soterroni, A. C. et al. Expanding the soy moratorium to Brazil’s Cerrado. Sci. Adv. 5, eaav7336 (2019).Article 

Google Scholar 
21.Rajão, R. et al. The rotten apples of Brazil’s agribusiness. Science 369, 246–248 (2020).Article 
CAS 

Google Scholar 
22.Heilmayr, R., Rausch, L. L., Munger, J. & Gibbs, H. K. Brazil’s Amazon soy moratorium reduced deforestation. Nat. Food 1, 801–810 (2020).Article 

Google Scholar 
23.Cerrado Manifesto. The Future of the Cerrado in the Hands of the Market: Deforestation and Native Vegetation Conversion Must Be Stopped (2017); http://d3nehc6yl9qzo4.cloudfront.net/downloads/cerradoconversionzero_sept2017_2.pdf24.Meyfroidt, P. et al. Multiple pathways of commodity crop expansion in tropical forest landscapes. Environ. Res. Lett. 9, 074012 (2014).Article 

Google Scholar 
25.PRODES (INPE, 2019); http://www.obt.inpe.br/OBT/assuntos/programas/amazonia/prodes26.Turubanova, S., Potapov, P. V., Tyukavina, A. & Hansen, M. C. Ongoing primary forest loss in Brazil, Democratic Republic of the Congo, and Indonesia. Environ. Res. Lett. 13, 074028 (2018).Article 

Google Scholar 
27.Argentina: Oilseeds and Products Annual (USDA Foreign Agricultural Service, 2016).28.Nepstad, D. et al. Slowing Amazon deforestation through public policy and interventions in beef and soy supply chains. Science 344, 1118–1123 (2014).CAS 
Article 

Google Scholar 
29.Seymour, F. & Harris, N. L. Reducing tropical deforestation. Science 365, 756–757 (2019).CAS 
Article 

Google Scholar 
30.Richards, P. D., Walker, R. T. & Arima, E. Y. Spatially complex land change: the indirect effect of Brazil’s agricultural sector on land use in Amazonia. Glob. Environ. Change 29, 1–9 (2014).Article 

Google Scholar 
31.Gasparri, N. I. & le Polain de Waroux, Y. The coupling of South American soybean and cattle production frontiers: new challenges for conservation policy and land change science. Conserv. Lett. 8, 290–298 (2015).Article 

Google Scholar 
32.Fehlenberg, V. et al. The role of soybean production as an underlying driver of deforestation in the South American Chaco. Glob. Environ. Change 45, 24–34 (2017).Article 

Google Scholar 
33.le Polain de Waroux, Y. et al. The restructuring of South American soy and beef production and trade under changing environmental regulations. World Dev. 121, 188–202 (2019).Article 

Google Scholar 
34.Tyukavina, A. et al. Types and rates of forest disturbance in Brazilian Legal Amazon, 2000–2013. Sci. Adv. 3, e1601047 (2017).Article 

Google Scholar 
35.De Sy, V. et al. Land use patterns and related carbon losses following deforestation in South America. Environ. Res. Lett. 10, 124004 (2015).Article 

Google Scholar 
36.Fearnside, P. M. Soybean cultivation as a threat to the environment in Brazil. Environ. Conserv. 28, 23–38 (2002).Article 

Google Scholar 
37.Barona, E., Ramankutty, N., Hyman, G. & Coomes, O. T. The role of pasture and soybean in deforestation of the Brazilian Amazon. Environ. Res. Lett. https://doi.org/10.1088/1748-9326/5/2/024002 (2010).38.Macedo, M. N. et al. Decoupling of deforestation and soy production in the southern Amazon during the late 2000s. Proc. Natl Acad. Sci. USA 109, 1341–1346 (2012).CAS 
Article 

Google Scholar 
39.Alexandratos, N. & Bruinsma, J. World Agriculture Towards 2030/2050: the 2012 Revision (FAO, 2012).
Google Scholar 
40.Brandão, A. Jr et al. Estimating the potential for conservation and farming in the Amazon and Cerrado under four policy scenarios. Sustainability https://doi.org/10.3390/su12031277 (2020).41.Martini, D. Z., Moreira, M. A., Cruz de Aragão, L. E. Oe, Formaggio, A. R. & Dalla-Nora, E. L. Potential land availability for agricultural expansion in the Brazilian Amazon. Land Use Policy 49, 35–42 (2015).Article 

Google Scholar 
42.Hunke, P., Mueller, E. N., Schröder, B. & Zeilhofer, P. The Brazilian Cerrado: assessment of water and soil degradation in catchments under intensive agricultural use. Ecohydrology 8, 1154–1180 (2014).Article 

Google Scholar 
43.Nosetto, M. D., Paez, R. A., Ballesteros, S. I. & Jobbágy, E. G. Higher water-table levels and flooding risk under grain vs. livestock production systems in the subhumid plains of the Pampas. Agric. Ecosyst. Environ. 206, 60–70 (2015).Article 

Google Scholar 
44.Schulz, C. et al. Physical, ecological and human dimensions of environmental change in Brazil’s Pantanal wetland: synthesis and research agenda. Sci. Total Environ. 687, 1011–1027 (2019).CAS 
Article 

Google Scholar 
45.Weinhold, D., Killick, E. & Reis, E. J. Soybeans, poverty and inequality in the Brazilian Amazon. World Dev. 52, 132–143 (2013).Article 

Google Scholar 
46.Garrett, R. D. & Rausch, L. L. Green for gold: social and ecological tradeoffs influencing the sustainability of the Brazilian soy industry. J. Peasant Stud. 43, 461–493 (2016).Article 

Google Scholar 
47.Oliveira, G. & Hecht, S. Sacred groves, sacrifice zones and soy production: globalization, intensification and neo-nature in South America. J. Peasant Stud. 43, 251–285 (2016).Article 

Google Scholar 
48.Garrett, R. D. et al. Intensification in agriculture-forest frontiers: land use responses to development and conservation policies in Brazil. Glob. Environ. Change 53, 233–243 (2018).Article 

Google Scholar 
49.Song, X.-P. et al. National-scale soybean mapping and area estimation in the United States using medium resolution satellite imagery and field survey. Remote Sens. Environ. 190, 383–395 (2017).Article 

Google Scholar 
50.King, L. et al. A multi-resolution approach to national-scale cultivated area estimation of soybean. Remote Sens. Environ. 195, 13–29 (2017).Article 

Google Scholar 
51.Potapov, P. et al. Annual continuous fields of woody vegetation structure in the Lower Mekong region from 2000-2017 Landsat time-series. Remote Sens. Environ. 232, 111278 (2019).Article 

Google Scholar 
52.Potapov, P. et al. Landsat analysis ready data for global land cover and land cover change mapping. Remote Sens. 12, 426 (2020).Article 

Google Scholar 
53.Global Forest Resources Assessment 2015 (FAO, 2015).54.Brazil’s Submission of a Forest Reference Emission Level (FREL) for Reducing Emissions from Deforestation in the Amazonia Biome for REDD+ Results-Based Payments Under the UNFCCC from 2016 to 2020 (Ministry of Environment of Brazil, 2018); https://redd.unfccc.int/files/2018_frel_submission_brazil.pdf55.Olson, D. M. et al. Terrestrial ecoregions of the world: a new map of life on Earth. BioScience 51, 933–938 (2001).Article 

Google Scholar 
56.Morton, D. C. et al. Cropland expansion changes deforestation dynamics in the southern Brazilian Amazon. Proc. Natl Acad. Sci. USA 103, 14637–14641 (2006).CAS 
Article 

Google Scholar  More

1.Elson, C. S. The Ecology of Invasions by Animals and Plants (Springer Nature, 2020).
Google Scholar 
2.Riccardi, A. & Atkinson, S. Distinctiveness magnifies the impact of biological invaders in aquatic ecosystems. Ecol. Lett. 7, 781–784. https://doi.org/10.1111/j.1461-0248.2004.00642.x (2004).Article 

Google Scholar 
3.Ricciardi, A. & Ryan, R. The exponential growth of invasive species denialism. Biol. Invasions 20, 549–553. https://doi.org/10.1007/s10530-017-1561-7 (2018).Article 

Google Scholar 
4.Anton, A. et al. Global ecological impacts of marine exotic species. Nat. Ecol. Evol. 3, 787–800. https://doi.org/10.1038/s41559-019-0851-0 (2019).Article 
PubMed 
PubMed Central 

Google Scholar 
5.Davis, M. A. et al. Don’t judge species on their origins. Nature 474, 153–154. https://doi.org/10.1038/474153a (2011).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
6.Sakai, A. K. et al. The population biology of invasive species. Annu. Rev. Ecol. Syst. 32, 305–332. https://doi.org/10.1146/annurev.ecolsys.32.081501.114037 (2001).Article 

Google Scholar 
7.Hutchings, J. A. Unintentional selection, unanticipated insights: Introductions, stocking and the evolutionary ecology of fishes. J. Fish Biol. 85, 1907–1926 (2014).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
8.Frenot, Y. et al. Biological invasions in the Antarctic: Extent, impacts and implications. Biol. Rev. 80, 45–72 (2005).PubMed 
Article 
PubMed Central 

Google Scholar 
9.MacCrimmon, H. R. & Marshall, T. World distribution of brown trout, Salmo trutta. J. Fish. Board Can. 25, 2527–2548 (1968).Article 

Google Scholar 
10.Labonne, J. et al. Invasion dynamics of a fish-free landscape by brown trout (Salmo trutta). PLoS ONE 8, 1–7 (2013).Article 
CAS 

Google Scholar 
11.Lecomte, F., Beall, E., Chat, J., Davaine, P. & Gaudin, P. The complete history of salmonid introductions in the Kerguelen Islands, Southern Ocean. Polar Biol. 36, 457–475. https://doi.org/10.1007/s00300-012-1281-5 (2013).Article 

Google Scholar 
12.de Leaniz, C. G., Gajardo, G. & Consuergra, S. From Best to Pest: changing perspectives on the impact of exotic salmonids in the Southern Hemisphere. Syst. Biodivers. 8, 447–459 (2010).Article 

Google Scholar 
13.Lésel, R. & Derenne, P. Introducing animals to Iles Kerguelen. Polar Rec. 17, 485–494 (1975).Article 

Google Scholar 
14.Monzón-Argüello, C. et al. Contrasting patterns of genetic and phenotypic differentiation in two invasive salmonids in the southern hemisphere. Evol. Appl. 71, 921–936. https://doi.org/10.1111/eva.12188 (2014).Article 

Google Scholar 
15.Stewart, L. A history of migratory salmon acclimatization experiments in parts of the Southern Hemisphere and the possible effects of oceanic currents and gyres upon their outcome. Adv. Mar. Biol. 17, 397–466. https://doi.org/10.1016/S0065-2881(08)60305-3 (1980).Article 

Google Scholar 
16.Grobbelaar, J. U. The lentic and lotic freshwater types of Marion Island (sub-Antarctic): A limnological study. Verhandlungen Inte. Vereinigung Limnol. 19, 949–951. https://doi.org/10.1080/03680770.1974.11896202 (1975).Article 

Google Scholar 
17.Grobbelaar, J. U. Factors limiting the algal growth on the sub-Antarctic island Marion. Verhandlungen Int. Vereinigung Limnol. 20, 1159–1164. https://doi.org/10.1080/03680770.1977.11896666 (1978).Article 

Google Scholar 
18.Lèsel, R., Therezien, Y. & Vibert, R. Introduction de salmonide´s aux Iˆles Kerguelen: Premiers re´sultats et observations pre´liminaires. Ann. d’Hydrobiol. 2, 275–304 (1971).
Google Scholar 
19.Wojtenka, J. & van Steenberghe, F. Variations nycthe´me´rales et saisonnie`res de la faune en place et en de´rive, strate´gie alimentaire de la truite (Salmo trutta L.) dans une petite rivie`re des ıˆles Kerguelen. Com. Natl. Franç. Rech. Antarct. 51, 413–442 (1981).
Google Scholar 
20.Cooper, J., Crafford, J. E. & Hecht, T. Introduction and extinction of brown trout (Salmo trutta L.) in an impoverished subantarctic stream. Antarct. Sci. 4, 9–14 (1992).ADS 
Article 

Google Scholar 
21.Jonsson, B. & Jonsson, N. Ecology of Atlantic Salmon and Brown Trout: Habitat as a Template for Life Histories (Springer, 2011).Book 

Google Scholar 
22.Boel, M. et al. The physiological basis of the migration continuum in brown trout (Salmo trutta). Physiol. Biochem. Zool. 87, 334–345 (2014).PubMed 
Article 
PubMed Central 

Google Scholar 
23.Cucherousset, J., Ombredane, D., Charles, K., Marchand, F. & Bagliniere, J.-L. A continuum of life history tactics in a brown trout Salmo trutta population. Can. J. Fish. Aquat. Sci. 62, 1600–1610 (2005).Article 

Google Scholar 
24.del Villar-Guerra, D., Aarestrup, K., Skov, C. & Koed, A. Marine migrations in anadromous brown trout (Salmo trutta): Fjord residency as a possible alternative in the continuum of migration to the open sea. Ecol. Freshw. Fish 23, 594–693. https://doi.org/10.1111/eff.12110 (2014).Article 

Google Scholar 
25.Eldøy, S. H. et al. Marine migration and habitat use of anadromous brown trout Salmo trutta. Can. J. Fish. Aquat. Sci. 72, 1366–1378. https://doi.org/10.1139/cjfas-2014-0560 (2015).Article 

Google Scholar 
26.Flaten, A. C. et al. The first months at sea: Migration and habitat use of sea trout Salmo trutta post-smolts. J. Fish Biol. 89, 1624–1640. https://doi.org/10.1111/jfb.13065 (2016).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
27.Bordeleau, X. et al. Nutritional correlates of spatio-temporal variations in the marine habitat use of brown trout, Salmo trutta, veteran migrants. Can. J. Fish. Aquat. Sci. 75, 1744–1754. https://doi.org/10.1139/cjfas-2017-0350 (2018).Article 

Google Scholar 
28.Eldøy, S. H. et al. The effects of nutritional state, sex and body size on the marine migration behaviour of sea trout. Mar. Ecol. Prog. Ser. 665, 185–200 (2021).ADS 
Article 

Google Scholar 
29.McDowall, R. M., Allibone, R. M. & Chadderton, W. L. Issues for the conservation and management of Falkland Islands freshwater fishes. Aquat. Conserv. Mar. Freshw. Ecosyst. 11, 473–486. https://doi.org/10.1002/aqc.499 (2001).Article 

Google Scholar 
30.Dartnall, H. J. G. The freshwater fauna of the souht polar region: A 140-year review. Pap. Proc. R. Soc. Tasman. 15, 19–57 (2017).
Google Scholar 
31.Berthier, E., Le Bris, R., Mabileau, L., Testut, L. & Rémy, F. Ice wastage on the Kerguelen Islands (49°S, 69°E) between 1963 and 2006. J. Geophys. Res. 114, 1–14. https://doi.org/10.1029/2008JF001192 (2009).Article 

Google Scholar 
32.Frenot, Y., Gloaguen, J. C., Picot, G., Bougere, J. & Benjamin, D. Azorella selago Hook. used to estimate glacier fluctuations and climatic history in the Kerguelen Islands over the last two centuries. Oecologia 95, 140–144 (1993).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
33.Delettre, Y. Biologie et écologie de Limnophyes pusillus Eaton, 1875 (Diptera, Chironomidae) aux Iles Kerguelen 1- Présentation générale et étude des populations larvaires. Rev. d’Ecol. Biol. Sol 15, 475–486 (1978).
Google Scholar 
34.Gay, C. Ecologie du zooplancton d’eau douce des Iles Kerguelen: 1- Caractéristiques du milieu et inventaire des entomostracés. Com. Natl. Franç. Rech. Antarct. 47, 43–57 (1981).
Google Scholar 
35.Wojtenka, J. & Van Steenberghe, F. Variations nycthémérales et saisonnières de la faune en place et en derive, stratégie alimentaire de la truite (Salmo trutta L.) dans une petite rivière des Iles Kerguelen. Com. Natl. Franç. Rech. Antarct. 51, 413–423 (1982).
Google Scholar 
36.Davidsen, J. G. et al. (Portail Data INRAE, 2020).37.Labonne, J. et al. From the bare minimum: Genetics and selection in populations founded by only a few parents. Evol. Ecol. Res. 17, 21–34 (2016).
Google Scholar 
38.Frenot, Y., Gloaguen, J. C. & Trehen, P. in Antarctic Communities: Species, Structure and Survival, Vol. 358–366 (eds B. Battaglia, J. Valencia, & D.W.H. Walton) (Cambridge University Press, 1997).39.Huston, A. H. in Methods for Fish Biology (eds C.B. Schreck & P.B. Moyle) 273–343 (American Fisheries Society, 1990).40.Davidsen, J. G. et al. Can sea trout Salmo trutta compromise successful eradication of Gyrodactylus salaris by hiding from CFT Legumin (rotenone) treatments?. J. Fish Biol. 82, 1411–1418. https://doi.org/10.1111/jfb.12065 (2013).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
41.Gauthey, Z. et al. The concentration of plasma metabolites varies throughout reproduction and affects offspring number in wild brown trout (Salmo trutta). Comp. Biochem. Physiol. A 184, 90–96 (2015).CAS 
Article 

Google Scholar 
42.Quéméré, E. et al. An improved PCR-based method for faster sex determination in brown trout (Salmo trutta) and Atlantic salmon (Salmo salar). Conserv. Genet. Resour. 6, 825–827. https://doi.org/10.1007/s12686-014-0259-8 (2014).Article 

Google Scholar 
43.Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254 (1976).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
44.Kruger, N. J. in The Protein Protocols Handbook (ed J.M. Walker) 17–24 (Humana Press, 2009).45.Davidsen, J. G. et al. Marine trophic niche-use and life history diversity among Arctic charr Salvelinus alpinus in southwestern Greenland. J. Fish Biol. 96, 681–692 (2020).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
46.Eldøy, S. H., Davidsen, J. G., Vignon, M. & Power, M. The biology and feeding ecology of Arctic charr in the Kerguelen Islands. J. Fish Biol. 98, 526–536. https://doi.org/10.1111/jfb.14596 (2020).Article 
PubMed 
PubMed Central 

Google Scholar 
47.Craig, H. Isotopic standards for carbon and oxygen and correction factors for mass spectrometric analysis of carbon dioxide. Geochim. Cosmochim. Acta 12, 133–149 (1957).ADS 
CAS 
Article 

Google Scholar 
48.Mariotti, A. Atmospheric nitrogen is a reliable standard for natural 15N abundance measurements. Nature 303, 685–687 (1983).ADS 
CAS 
Article 

Google Scholar 
49.Jardine, T. D. et al. Carbon from periphyton supports fish biomass in waterholes of a wet-dry tropical river. River Res. Appl. 29, 560–573 (2013).Article 

Google Scholar 
50.Hyslop, E. J. Stomach contents analysis: A review of methods and their application. J. Fish Biol. 17, 411–429. https://doi.org/10.1111/j.1095-8649.1980.tb02775.x (1980).Article 

Google Scholar 
51.Závorka, L., Slavík, O. & Horký, P. Validation of scale-reading estimates of age and growth in a brown trout Salmo trutta population. Biologia 69, 691–695. https://doi.org/10.2478/s11756-014-0356-x (2014).Article 

Google Scholar 
52.Pincock, D. G. False Detections: What they are and how to remove them from detection data. Vemco Appl. Note 1, 1–11 (2012).
Google Scholar 
53.France, R. L. & Peters, R. H. Ecosystem differences in the trophic enrichment of 13C in aquatic food webs. Can. J. Fish. Aquat. Sci. 54, 1255–1258 (1997).Article 

Google Scholar 
54.Fry, B. Conservative mixing of stable isotopes across estuarine salinity gradients: A conceptual framework for monitoring watershed influences on downstream fisheries production. Estuaries 25, 264–271 (2002).Article 

Google Scholar 
55.Wissel, B. & Fry, B. Tracing Mississippi River influences in estuarine food webs of coastal Louisiana. Oecologi 144, 659–672. https://doi.org/10.1007/s00442-005-0119-z (2005).ADS 
Article 

Google Scholar 
56.Kline, T. T., Wilson, W. J. & Goering, J. J. Natural isotope indicators of fish migration at Prudhoe Bay, Alaska. Can. J. Aquat. Sci. 55, 1494–1502 (1998).Article 

Google Scholar 
57.Phillips, D. L. Converting isotope values to diet composition: the use of mixing models. J. Mammal. 93, 342–352 (2012).Article 

Google Scholar 
58.Schawarcz, H. P. Some theoretical aspects of isotope paleodiet studies. J. Archaeol. Sci. 18, 261–275 (1991).Article 

Google Scholar 
59.Post, D. M. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83, 703–718 (2002).Article 

Google Scholar 
60.Saucède, T. et al. in The Kerguelen Plateau: Marine Ecosystem and Fisheries. Proceedings of the Second Symposium (eds D. Welsford, J. Dell, & G. Duhamel) 95–116 (Australian Antarctic Division, 2019).61.Batschelet, E. Circular Statistics in Biology. (Academic Press, 1981).62.Zar, J. H. Bisostatistical Analysis. 5th edn, (Prentice-Hall/Pearson, 2010).63.Cherel, Y., Ducatez, S., Fontaine, C., Richard, P. & Guinet, C. Stable isotopes reveal the trophic position and mesopelagic fish diet of female southern elephant seals breeding on the Kerguelen Islands. Mar. Ecol. Prog. Ser. 370, 239–247 (2008).ADS 
Article 

Google Scholar 
64.Guerreiro, M. et al. Habitat and trophic ecology of Southern Ocean cephalopods from stable isotope analyses. Mar. Ecol. Prog. Ser. 530, 119–134 (2015).ADS 
CAS 
Article 

Google Scholar 
65.Ciancio, J., Beauchamp, D. A. & Pascuala, M. Marine effect of introduced salmonids: Prey consumption by exotic steelhead and anadromous brown trout in the Patagonian Continental Shelf. Limnol. Oceanogr. 55, 2181–2192 (2010).ADS 
Article 

Google Scholar 
66.Thorstad, E. B. et al. Marine life of the sea trout. Mar. Biol. 163(47), 1–19. https://doi.org/10.1007/s00227-016-2820-3 (2016).Article 

Google Scholar 
67.Závorka, L., Koeck, B., Killen, S. S. & Kainz, M. J. Aquatic predators influence flux of essential micronutrients. Trends Ecol. Evol. 34, 880–881 (2019).PubMed 
Article 
PubMed Central 

Google Scholar 
68.Colombo, S. M., Wacker, A., Parrish, C. C., Kainz, M. J. & Arts, M. T. A fundamental dichotomy in long-chain polyunsaturated fatty acid abundance between and within marine and terrestrial ecosystems. Environ. Rev. 25, 163–174. https://doi.org/10.1139/er-2016-0062 (2017).CAS 
Article 

Google Scholar 
69.Jarry, M. et al. Sea trout (Salmo trutta) growth patterns during early steps of invasion in the Kerguelen Islands. Polar Biol. 41, 925–934 (2018).Article 

Google Scholar 
70.O’Neal, A. L. & Stanford, J. A. Partial migration in a robust brown trout population of a Patagonian river. Trans. Am. Fish. Soc. 140, 623–635 (2011).Article 

Google Scholar 
71.Gross, M. R., Coleman, R. M. & McDowall, R. M. Aquatic productivity and the evolution of diadromous fish migration. Science 239, 1291–1293 (1988).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
72.Jonsson, B. & Jonsson, N. Partial migration: niche shift versus sexual maturation in fishes. Rev. Fish Biol. Fish. 3, 348–365 (1993).Article 

Google Scholar 
73.Newton, C. The Trouts Tale. The Fish that Followed an Empire. 218 (The Medlar Press, 2013).74.Davidsen, J. G. et al. Does reduced feeding prior to release improve the marine migration of hatchery brown trout Salmo trutta L. smolts?. J. Fish Biol. 85, 1992–2002 (2014).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
75.Westley, P. A. H. & Fleming, I. A. Landscape factors that shape a slow and persistent aquatic invasion: Brown trout in Newfoundland 1883–2010. Biodivers. Res. 17, 566–579 (2011).
Google Scholar 
76.Larsson, S. Thermal preference of Arctic charr, Salvelinus alpinus, and brown trout, Salmo trutta: Implications for their niche segregation. Environ. Biol. Fishes 73, 89–96 (2005).Article 

Google Scholar 
77.Elliot, J. M. Daily energy intake and growth of piscivorous brown trout, Salmo trutta. Freshwat. Biol. 44, 237–245 (2000).Article 

Google Scholar 
78.Elliot, J. M. & Hurley, M. A. Optimum energy intake and gross efficiency of energy conversion for brown trout, Salmo trutta, feeding on invertebrates or fish. Freshwat. Biol. 44, 605–615 (2000).Article 

Google Scholar 
79.Jensen, J. L. A. et al. Water temperatures influence the marine area use of Salvelinus alpinus and Salmo trutta. J. Fish Biol. 84, 1640–1653. https://doi.org/10.1111/jfb.12366 (2014).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
80.Rikardsen, A. H. et al. The marine temperature and depth preferences of Arctic charr and sea trout, as recorded by data storage tags. Fish. Oceanogr. 16, 436–447. https://doi.org/10.1111/j.1365-2419.2007.00445.x (2007).Article 

Google Scholar 
81.Chernitsky, A. G., Zabruskov, G. V., Ermolaev, V. V. & Shkurko, D. S. Life history of trout, Salmo trutta L., in the Varsina River estuary, (The Barents Sea). Nord. J. Freshw. Res. 71, 183–189 (1995).
Google Scholar 
82.Honkanen, H. M. et al. Summer survival and activity patterns of estuary feeding anadromous Salmo trutta. Ecol. Freshwat. Fish 29, 31–39 (2020).Article 

Google Scholar 
83.Thomas, T., Davaine, P. & Beall, E. Dynamique de la migration et reproduction de la truite de mer, Salmo trutta L., dans la Rivière Norvégienne Iles Kerguelen. Com. Natl. Franç. Rech. Antarct. 47, 5–42 (1981).
Google Scholar 
84.Beall, E. & Davaine, P. Analyse scalimetrique de la truite de mer (Salmo trutta L.): formation des anneaux et criteres d’identification chez les individus sedentaires et migrateurs d’une meme population acclimatee aux iles Kerguelen (TAAF). Aquat. Living Resour. 1, 3–16 (1988).Article 

Google Scholar 
85.Ciancio, J. E., Pascual, M. A., Botto, F., Frere, E. & Iribarne, O. Trophic relationships of exotic anadromous salmonids in the southern Patagonian Shelf as inferred from stable isotopes. Limnol. Oceanogr. 53, 788–798 (2008).ADS 
Article 

Google Scholar 
86.Davidsen, J. G. et al. Trophic niche variation among sea trout Salmo trutta in Central Norway investigated by three different time-integrated trophic tracers. J. Aquat. Biol. 26, 217–227. https://doi.org/10.3354/ab00689 (2017).Article 

Google Scholar 
87.Elliott, J. A. Stomach contents of adult sea trout caught in six English rivers. J. Fish Biol. 50, 1129–1132 (1997).
Google Scholar 
88.Knutsen, J. A., Knutsen, H., Gjøsæter, J. & Jonsson, B. Food of anadromous brown trout at sea. J. Fish Biol. 59, 533–543 (2001).Article 

Google Scholar 
89.Rikardsen, A. H. et al. Temporal variability in marine feeding of sympatric Arctic charr and sea trout. J. Fish Biol. 70, 837–847 (2007).Article 

Google Scholar 
90.Grønvik, S. & Klemetsen, A. Marine food and diet overlap of Co-occuring Arctic charr (Salvelinus alpinus L.), brown trout (Salmo trutta L.) and Atlantic salmon (S. salar L.) off Senja, N. Norway. Polar Biol. 7, 173–177 (1987).Article 

Google Scholar 
91.Aulus-Giacosa, L. Spatio-temporal evolution of life history traits related to dispersal. Brown trout (Salmo trutta L.) colonization of the sub-Antarctic Kerguelen Islands PhD thesis, Université de Pau et des Pays de l’Adour (2021).92.Cherel, Y., Fontaine, C., Richard, P., Labat, J. P. Isotopic niches and trophic levels of myctophid fishes and their predators in the Southern Ocean. Limnol. Oceanogr. 55, 324–332. (2010). More

1.Moore, T. R. & Knowles, R. Can. J. Soil Sci. 69, 33–38 (1989).CAS 
Article 

Google Scholar 
2.Swindles, G. T. et al. Nat. Geosci. 12, 922–928 (2019).CAS 
Article 

Google Scholar 
3.Huang, Y. et al. Nat. Clim. Change https://doi.org/10.1038/s41558-021-01059-w (2021).4.Yu, Z. C., Loisel, J., Brosseau, D. P., Beilman, D. W. & Hunt, S. J. Geophys. Res. Lett. 37, L13402 (2010).
Google Scholar 
5.Roulet, N. T., Lafleur, P. M., Richard, P. J. H., Moore, T. R., Humphreys, E. R. & Bubier, J. Glob. Change Biol. 13, 397–411 (2007).Article 

Google Scholar 
6.Turetsky, M. R. et al. Glob. Change Biol. 20, 2183–2197 (2014).Article 

Google Scholar 
7.Loisel, J. et al. Nat. Clim. Change 11, 70–77 (2021).Article 

Google Scholar 
8.Evans, C. D. et al. Nature https://doi.org/10.1038/s41586-021-03523-1 (2021).9.Hugelius, G. et al. Proc. Natl Acad. Sci. USA 117, 20438–20446 (2020).CAS 
Article 

Google Scholar 
10.Voigt, C. et al. Glob. Change Biol. 25, 1746–1764 (2019).Article 

Google Scholar 
11.Leifeld, J. & Menichetti, L. Nat. Commun. 9, 1071 (2018).CAS 
Article 

Google Scholar 
12.Hatano, R., Toma, Y., Hamada, Y., Arai, H., Susilawati, H. L. & Inubushi, K. in Tropical Peatland Ecosystems (eds Osaki, M. & Tsuji, N.) 339–351 (Springer, 2016). More

BOOK REVIEW
07 June 2021

It takes a wood to raise a tree: a memoir

An ecologist traces forests’ support networks — and finds parallels in her own life.

Emma Marris

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Emma Marris

Emma Marris is an environmental writer who lives in Klamath Falls, Oregon.

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Douglas firs in British Columbia, Canada: ‘mother trees’ help seedlings all around to flourish.Credit: Getty

Finding the Mother Tree: Discovering the Wisdom of the Forest Suzanne Simard Knopf (2021)Growing up in the rainforests of the Pacific Northwest, I often grieved that their beauty — sky-high Douglas firs, rustling alders, sword ferns draped across the slopes — was born of a brutal battle for light, water and nutrients. So I thought.In 1997, ecologist Suzanne Simard made the cover of Nature with the discovery of a subterranean lace of tree roots and fungal filaments, or hyphae, in British Columbia (S. Simard et al. Nature 388, 579–582; 1997). It was “a network as brilliant as a Persian rug”, she recalls in her memoir Finding the Mother Tree — a network through which multiple tree species were exchanging carbon. The trees were cooperating.The discovery of this fungal network, or ‘wood wide web’, as it came to be known, upended a dominant scientific narrative — that competition is the primary force shaping forests. Forest ecology is instead a much more nuanced dance, in which species sometimes fight and sometimes get along. This calls into question the way that most foresters manage trees. Clear-cutting, weeding and planting single species in well-spaced rows makes sense only if trees do best when they have all the resources they need to themselves.
Rediscovering the bush telegraph
Throughout her career, Simard has shown that, in fact, it takes a whole ‘village’ to raise a tree. Alders fix atmospheric nitrogen, which can then be used by pines and other tree species. Older, deeper-rooted trees bring up water from lower in the soil to shallow-rooted plants. Carbon, water, nutrients and information about threats and conditions are shared across the fungal-root network. When Douglas firs are infested with western spruce budworm (Choristoneura occidentalis), they alert pines to which they are connected through the wood wide web, and these respond by producing defence enzymes. In the middle of all this activity are the mother trees. The oldest, largest and most experienced, they subsidize the growth and flourishing of seedlings all around.Simard creates her own complex network in this memoir, by weaving the story of these discoveries with vignettes from her past. The themes of her research — cooperation, the legacies that one generation leaves for the next, the ways in which organisms react to and recover from stress and disease — are also themes in her own life. The network of friends, family and colleagues who support Simard, as a scientist and as a woman, is visible throughout: as central to the story as a forest’s web of fungal filaments and delicate rootlets.Simard’s life story is, of course, unique, yet it has a striking universality. After working for a logging company, she moved into government service and then into academia, trying in each job to untangle the subterranean mysteries of the forest. She fought to have her ideas taken seriously in a male-dominated field. (There are shades of Lab Girl, by US geobiologist Hope Jahren, in her clear-eyed depictions of what she has to deal with behind the scenes — from being passed over for jobs for which she was the best candidate, to being called “Miss Birch” behind her back, a sound-alike for a much harsher epithet.) Simard found love, lost it, and found it again. She struggled, like so many scientists, to balance her research and her roles as a wife and mother. She faced mortality when diagnosed with cancer.

The thread-like roots of fungi are an essential element of a forest’s ‘wood wide web’, through which trees exchange carbon, water, nutrients and information.Credit: Claire Welsh

Moving through life’s highs and lows with her is rewarding because of these resonances, and because she comes across as the kind of person who usually doesn’t write memoirs — shy and occasionally fearful, always earnest. It feels like a privilege to be let into her life.The muddy, stressful and occasionally exhilarating experience of fieldwork shines through. “Jittery with adrenaline”, while labelling seedlings in one field experiment, she describes feeling “as if I were about to parachute out of a plane, maybe land on Easter Island”. Simard got her first morsel of proof for her theory in 1993, while kneeling on the forest floor holding a Geiger counter to detect the radioactive carbon-14 that she used to track carbon flows through plants and fungi. “I was enraptured, focused, immersed, and the breeze sifting through the crowns of my little birches and firs and cedars seemed to lift me clear up,” she writes.After publishing her Nature paper, Simard showed that trees direct more resources to their offspring than they do to unrelated seedlings. The finding suggests that trees maintain a level of control through the network that one might call intelligence. As she argues, plants seem to have agency. They perceive, relate and communicate, make decisions, learn and remember, she writes: “qualities we normally ascribe to sentience, wisdom”. For Simard, that implies that they are due a certain respect.
The community of trees
She does not spell out the ethical implications, but the ideas raise fascinating moral questions. What responsibilities do we owe plants? Is logging or farming crops, to harvest and eat, cruel? What kinds of legal right might a tree have if we base our theories of rights on whether individuals, such as humans and chimpanzees, have intelligence or sentience?It is tempting to ascribe the dominance of the ‘brutal competition’ narrative to the fact that ecology was dominated by men, and to find poetic power in the idea that a woman saw cooperation when her male colleagues couldn’t. But Simard tells a more complex tale. She struggled to see the truth in the soil and in her heart — and got there only because she was determined and intuitive.Simard writes that big old trees are “mothering their children” by sending them, through the forest network, sugars, water, nutrients and information about threats. Reading this on page 5, I was sceptical. By the end I was convinced. The beauty of the forests of my youth turns out to be shaped, in a sense, by love.

Nature 594, 171-172 (2021)
doi: https://doi.org/10.1038/d41586-021-01512-y

Competing Interests
The author declares no competing interests.

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Results of chemical analysisThe results of the study showed that the concentrations of Cd and Pb among all analyzed fruit samples (n = 242) were below the associated LOQs in only 87 and 96 samples, respectively. Similarly, in vegetable samples (n = 128) we found that Cd and Pb concentrations were below the LOQ in 31 and 69 samples, respectively. The levels of the Cd and Pb in the analyzed food samples were compared and contrasted with the maximum levels in foodstuffs regulated by legal acts: Commission Regulation (EU) No 488/2014 of 12 May 2014 amending Regulation (EC) No 1881/2006 as regards maximum levels of cadmium in foodstuffs and Commission Regulation (EU) 2015/1005 of 25 June 2015 amending Regulation (EC) No 1881/2006 as regards maximum levels of lead in certain foodstuffs3,4. It was found that in 12 food samples, the Cd content exceeded the maximum acceptable level. Among the fruit samples, this result was observed in: frozen raspberries (n = 1; 122% of maximum level) and frozen strawberries (n = 1; 114% of maximum level). In the case of vegetables, this result was observed in: fresh beetroots (n = 2; 203% and 670% of maximum level), frozen carrot (n = 1; 113% of maximum level), fresh celery (n = 4; 130%, 150%, 345%, 356% of maximum level) and processed tomatoes (n = 3; 102%, 112%, 134% of maximum level). The maximum permissible Pb level was exceeded in 3 analyzed food samples: fresh beetroot (n = 1; 135% of maximum level), frozen carrot (n = 1; 117% of maximum level) and 1 sample of frozen tomatoes in which the Pb concentration was up to 1074% of the acceptable limit (Table 5).Table 5 The number and type of food samples in which the maximum level of Cd or Pb has been exceeded.Full size tableTables 6 and 7 present the mean and SD, as well as the minimum and maximum values for the Cd and Pb contents in each of the analyzed fruits (Table 6) and vegetables (Table 7). Heavy metals concentrations were reported in mg/kg f.m. (fresh mass) in the fresh, frozen and processed products, while the content of Cd and Pb in dried products were presented in mg/kg d.w. (dry weight). Lack of a value in the tables means that the Cd or Pb value was below the LOQ for that particular sample.Table 6 The mean value, standard deviation, minimum and maximum values ​​of Cd and Pb concentrations in particular types of fruit samples.Full size tableTable 7 The mean value, standard deviation, minimum and maximum values of Cd and Pb concentrations in particular types of vegetable samples.Full size tableThe analysis of Cd and Pb contents in all food products is necessary due to the possibility of assessing the health risks associated with consumption of contaminated ready-to-eat different types of food. A review of the scientific literature showed that the issue of food contamination with heavy metals is discussed by several researchers. However, they mostly include only fresh fruits and vegetables. Additionally, there is a little data concerning the level of heavy metals contamination of vegetables and fruits cultivated in other European countries in the available literature. Consequently, the results presented in this paper may form the basis for further research on the scale of food contamination with heavy metals such as Pb and Cd.Among fruits such as apples, pears, raspberries and strawberries, the highest average values of both Cd and Pb were observed in dried products (Cd: 0.023, 0.015, 0.116, 0.131 mg/kg d.w., respectively; Pb: 0.127, 0.036, 0.111, 0.161 mg/kg d.w., respectively). In cranberry samples, the highest levels of Cd were determined in fresh fruits (0.008 mg/kg f.m.), while Pb—in processed products (0.01 mg/kg f.m.). In the case of grape samples, the same average Cd concentration was recorded in both dried and fresh products (0.001 mg/kg), while the highest Pb content was observed in processed products (0.07 mg/kg f.m.). In most fruit samples the lowest average Cd concentrations were determined in processed products (grapes, pears, raspberries and strawberries—0.0004, 0.0008, 0.009, 0.003 mg/kg f.m., respectively), while Pb—in fresh fruits (cranberries, grapes, pears—0.004, 0.005, 0.008 mg/kg f.m.) or processed (raspberries and strawberries—0.011 and 0.006 mg/kg f.m.). In apple samples, the same average Pb value was recorded in both fresh fruit and processed products (0.009 mg/kg f.m.).The content of Cd and Pb in fruits, in the results available in the literature, is very diverse. The demonstrated average Cd content in apples (0.001 mg/kg f.m.) is lower compared to studies from other regions of the world, including Great Britain (0.002 mg/kg f.m.)23. The amounts of Cd in raspberries and strawberries tested in Poland were higher compared to those investigated by Norton et al. (2015) (0.002 mg/kg f.m. vs 0.011 mg/kg f.m. and 0.002 mg/kg f.m. vs 0.018 mg/kg f.m.)23. Additionally, in samples collected in Turkey and Serbia, the Cd content in the analyzed products was below the LOQ24,25.Our results of Pb values in fruit samples are similar to those reported by some researchers and the range of values presented for this element in other analyses were very wide. However, as in the case of Cd content in apples purchased in Poland, Pb concentrations in these fruits (0.009 mg/kg f.m.) were also lower than other studies—minimum of 200%23. The average Pb content in grapes (0.009 mg/kg f.m.) was comparable to that obtained by Bağdatlıoğlu et al. (2010) (0.006 mg/kg f.m.)24. The results of author’s research regarding the content of Pb in raspberries (0.012 mg/kg f.m.) exceeded 2.5 times those published by Norton et al. (2015)23. Pb concentrations in strawberries (0.009 mg/kg f.m.) compared to other studies are in their lower range (0.010 mg/kg–0.027 mg/kg f.m.)23,24.The highest average concentrations of Cd were determined in fresh vegetables (beetroot and celery—0.235 and 0.152 mg/kg f.m., respectively) and dried—carrots and tomatoes (0.2 and 0.103 mg/kg d.w.), while Pb—in frozen vegetables (beetroots and tomatoes—0.173 and 0.294 mg/kg f.m.), as well as dried (carrots and celery—0.206 and 0.259 mg/kg d.w.). For most samples, the lowest average Cd and Pb levels were observed in processed products (beetroots, carrots, celery). Exceptions were samples of tomatoes—the lowest average Cd and Pb concentration values were observed in fresh foodstuffs (0.003 and 0.016 mg/kg f.m., respectively).Analyses conducted by other scientists indicate lower average Cd content in fresh beetroots (0.018–0.09 mg/kg f.m.)23,26 and higher by almost 600% in the case of Pb (0.58 mg/kg f.m.)26 compared to our research (Cd—0.235 mg/kg f.m.; Pb—0.095 mg/kg f.m.). Only the British study has shown lower Pb content (0.033 mg/kg f.m.)23. Our results—concentration of Cd (0.041 mg/kg f.m.) and Pb (0.027 mg/kg f.m.) in fresh carrot samples were similar to those obtained by other authors from the same territory in Poland, but also those from Great Britain, China or Brazil—Cd values ranged from 0.014 mg/kg f.m. to 0.03 mg/kg f.m., while Pb from 0.023 mg/kg f.m. to 0.971 mg/kg f.m.23,26,27,28. In the scientific literature we found only individual articles regarding celery heavy metal contamination. Guerra et al. (2012) showed 3 times lower Cd content in this vegetable—0.05 mg/kg f.m.26. The concentration of Pb in Brazilian research indicates higher content (0.47 mg/kg f.m.) than those obtained in this study (0.031 mg/kg f.m.)26. Tomatoes are the most frequently analyzed products, probably due to the easiness and simplicity of processing. Our analysis showed relatively low concentration of Cd and Pb in fresh tomatoes (Cd—0.003 mg/kg f.m.; Pb—0.016 mg/kg f.m.). In the most available scientific data Cd levels were in the range of 0.028 mg/kg f.m. to 0.033 mg/kg f.m., and Pb from 0.078 mg/kg f.m. to 0.18 mg/kg f.m.26,28. Only Norton et al. (2015) and Bagdatlioglu et al. (2010) noted lower or equal Cd and Pb values in the corresponding product23,24.Massadeh et al. (2018) in Jordan determined Pb and Cd of various canned fruits and canned vegetables including canned juice (pineapple), canned tomato sauce, canned whole carrots and canned green beans. They showed metal concentration levels in the samples were in the range of 0.50–0.60 mg/kg f.m. for Cd and 2.6–3.0 mg/kg f.m. for Pb29. These results significantly exceed the values shown in present study, as well as the results presented by Domagała-Świątkiewicz and Gąstoł (2012) in the analysis of vegetable juices (beetroot, carrot, celery)30.The high contamination found in vegetables might be closely related to the pollutants in irrigation water, farm soil, fertilizers and also industrial and low pollution household emissions. Differences in levels of contamination between fruits and vegetables may result from the specificity of the geographical area from which they are collected, their diverse capacity to accumulate heavy metals, as well as the way they are processed. It should be pointed out that in polluted environments (soil, water, and air), the presence of toxic metals in elevated concentrations is not uncommon. Due to the structure of consumption of various groups of food products both in Poland and other countries, a significant risk of exposure to heavy metals is associated with the consumption of fruits and vegetables, which are one of the main elements of the diet. Unfortunately, complete elimination of elements such as Cd or Pb from these products is impossible, and the technological processes used in food production can only remove a small part of the impurities from selected products or even contribute to their increased contamination. Thus, there is a need for regular monitoring of heavy metals on every kind of foodstuff, not only in fresh products, in order to estimate the health risk from heavy metals in the human food chain.Statistical analysisANOVAFor the purpose of ANOVA carried out to detect significant differences in the heavy metal concentrations of the four types of food (fresh, dried, frozen, and processed), samples with concentration value below the LOQ were removed from the analysis. In the case of Cd concentration, the value of F statistic was 11.15 for fruits and 4.049 for vegetables, leading to significant results with p-values below 0.001 and 0.01 respectively. For the of Pb concentration, the ANOVA results were even more extreme with F values of 56.59 for fruits and 7.13 for vegetables with associated p-values being below 0.001 in both cases. These results show that there is strong evidence to believe that mean Cd and Pb contents in the four types of fruits and vegetables are not equal (Table 8).Table 8 Analysis of variance (ANOVA) for variates in four groups.Full size tableOutlier analysisThe boxplots depicted in Fig. 1 were used to illustrate the outlier analysis for Cd and Pb. Each plot shows the median of the observations along with the lower quartile (Q1) and the upper quartile (Q3). The highest and the lowest observations are shown by the whiskers. From Fig. 1a, there appears to be two outliers in the dried fruits with values 0.277 and 0.210. From Fig. 1b, there seems to be six outliers in the fresh vegetables with values of 0.203, 0.670, 0.260, 0.690, 0.300 and 0.712. In Fig. 1c, we see two outliers in the processed fruits with values of 0.127 and 0.047. Finally, Fig. 1d shows that there is one one outlier in the frozen vegetable category with the value of 0.537.Figure 1Outlier analysis in case: Cd concentration in: (a) fruits, (b) vegetables, and Pb concentration in: (c) fruits, (d) vegetables.Full size imageOutliers associated with high Cd and Pb values in fruit and vegetable samples may be the result of sample contamination during technological processes or vegetables/fruits cultivation in a polluted agricultural area.Post-hoc multiple comparisonSince the ANOA results indicated significant differences among the mean concentrations of Cd and Pb both in fruits and vegetables, to further detect the specific different means, the Tukey HSD test22 was applied. The results are presented in Fig. 2. For the Cd concentration, comparison of all pairs of means indicated that the content of Cd in dried fruits is significantly different from mean concentrations of other types of food namely fresh, frozen, and processed fruits, see Fig. 2a. In the case of vegetables, the mean Cd contents of fresh and processed vegetables are different, see Fig. 2b, although mean Cd content of frozen and fresh vegetables are also significantly different if a significance level of 10% is used. Upon analyzing the mean concentrations of Pb in fruits, we found that the mean content of dried fruits was significantly different from the other three types, namely fresh, frozen and processed, see Fig. 2c. For the Pb concentrations in vegetables, a highly significant difference was detected between the means of processed and dried vegetables. In addition, mean Pb concentrations of fresh versus dried and processed versus frozen vegetables were significantly different, see Fig. 2d.Figure 2Post-hoc Multiple Comparison Tukey-Test of Cd and Pb in all samples of fruits and vegetables; differences in Cd mean concentration of: (a) fruits, (b) vegetables; differences in Pb mean concentration of: (c) fruits, (d) vegetables.Full size image More

1.Stearns, S.C. The Evolution of Life Histories. https://doi.org/10.1046/j.1420-9101.1993.6020304.x (Oxford University Press/Wiley, 1992).2.Dingle, H. The evolution of life histories. in Population Biology (Wöhrmann K., Jain S.K. eds.). https://doi.org/10.1007/978-3-642-74474-7_9 (Springer, 1990).3.Yang, L., Walck, J. L. & El-Kassaby, Yousry, A. Roles of the environment in plant life-history tradeoffs. in Advances in Seed Biology (Jimenez-Lopez, J.C. ed.) 674. https://doi.org/10.5772/intechopen.70312.4.Hamrick, J. L. & Godt, M. J. W. Effects of life history traits on genetic diversity in plant species. Philos. Trans. R. Soc. Lond.. Ser. B Biol. Sci. 351, 1291–1298 (1996).5.Hobbs, R. J., Higgs, E. & Harris, J. A. Novel ecosystems: Implications for conservation and restoration. Trends Ecol. Evol. 24, 599–605 (2006).Article 

Google Scholar 
6.Prozherina, N., Freiwald, V., Rousi, M. & Oksanen, E. Interactive effect of springtime frost and elevated ozone on early growth, foliar injuries and leaf structure of birch (Betula pendula). New Phytol. 159, 623–636 (2003).CAS 
Article 

Google Scholar 
7.Zvereva, Elena, L., Roitto, M. & Kozlov, M. V. Growth and reproduction of vascular plants in polluted environments: A synthesis of existing knowledge. Environ. Rev. 18, 355–367 (2010).8.Niinemets, Ü. Responses of forest trees to single and multiple environmental stresses from seedlings to mature plants: Past stress history, stress interactions, tolerance and acclimation. For. Ecol. Manag. 260, 1623–1639 (2010).Article 

Google Scholar 
9.Possen, B. J. H. M. et al. Adaptability of birch (Betula pendula Roth) and aspen (Populus tremula L.) genotypes to different soil moisture conditions. For. Ecol. Manag. 262, 1387–1399 (2011).10.Řehounková, K. & Prach, K. Life-history traits and habitat preferences of colonizing plant species in long-term spontaneous succession in abandoned gravel–sand pits. Basic Appl. Ecol. 11, 45–53 (2010).Article 

Google Scholar 
11.Franiel, I. The Biology and Ecology of Betula pendula Roth on Post-Industrial Waste Dumping Grounds: The Variability Range of Life History Traits (Silesia University, 2012).
Google Scholar 
12.Kompała-Ba̧ba, A. & Ba̧ba, W. Participation of grasses (Poaceae) in the communities, which developed on iron smelter affected lands in the Silesian Uplands. Fragm. Florist. Geobot. Pol. 20, 267–284 (2013).13.Kompała-Bąba, A. & Bąba, W. The spontaneous succession in a sand-pit—The role of life history traits and species habitat preferences. Polish J. Ecol. 61, 13–22 (2013).
Google Scholar 
14.Darbah, J. N. T. et al. Impacts of elevated atmospheric CO2 and O3 on paper birch (Betula papyrifera): Reproductive fitness. Sci. World J. 7, 240–246 (2007).Article 

Google Scholar 
15.Alvarez-Cansino, L., Zunzunegui, M., Díaz Barradas, M. C. & Esquivias, M. P. Gender-specific costs of reproduction on vegetative growth and physiological performance in the dioecious shrub Corema album. Ann. Bot. 106, 989–998 (2010).16.Zvereva, E. L., Roitto, M. & Kozlov, M. V. Growth and reproduction of vascular plants in polluted environments: A synthesis of existing knowledge. Environ. Rev. 18, 355–367 (2010).CAS 
Article 

Google Scholar 
17.Franiel, I. & Babczyńska, A. The growth and reproductive effort of Betula pendula Roth in a heavy-metals polluted area. Polish J. Environ. Stud. 20, 1097–1101 (2011).CAS 

Google Scholar 
18.Lancaster, L. T., Morrison, G. & Fitt, R. N. Life history trade-offs, the intensity of competition, and coexistence in novel and evolving communities under climate change. Philos. Trans. R. Soc. B Biol. Sci. 372, (2017).19.Obeso, J. R. Costs of reproduction in ilex aquifolium: Effects at tree, branch and leaf levels. J. Ecol. 85, 159–166 (1997).Article 

Google Scholar 
20.Obeso, J. R. The costs of reproduction in plants. New Phytol. 155, 321–348 (2002).Article 

Google Scholar 
21.Cipollini, M. L. & Stiles, E. W. Costs of reproduction in Nyssa sylvatica: Sexual dimorphism in reproductive frequency and nutrient flux. Oecologia 86, 585–593 (1991).ADS 
Article 

Google Scholar 
22.Seidling, W., Starfinger, U. & Stöcklin, J. Plant population ecology. Prog. Bot. 55, 345–370 (1994).Article 

Google Scholar 
23.Possen, B. J. H. M. et al. Variation in 13 leaf morphological and physiological traits within a silver birch ( Betula pendula ) stand and their relation to growth. Can. J. For. Res. 44, 657–665 (2014).Article 

Google Scholar 
24.Körner, C. Limitation and stress—Always or never?. J. Veg. Sci. 14, 141–143 (2003).
Google Scholar 
25.Giuliani, C., Lazzaro, L., Mariotti Lippi, M., Calamassi, R. & Foggi, B. Temperature-related effects on the germination capacity of black locust (Robinia pseudoacacia L., Fabaceae) seeds. Folia Geobot. 50, 275–282 (2015).26.Wolkovich, E. M. et al. Warming experiments underpredict plant phenological responses to climate change. Nature https://doi.org/10.1038/nature11014 (2012).Article 
PubMed 

Google Scholar 
27.Koski, V. & Rousi, M. A review of the promises and constraints of breeding silver birch (Betula pendula Roth) in Finland. For. Int. J. For. Res. 78, 187–198 (2005).
Google Scholar 
28.Marguí, E., Queralt, I., Carvalho, M. L. & Hidalgo, M. Assessment of metal availability to vegetation (Betula pendula) in Pb–Zn ore concentrate residues with different features. Environ. Pollut. 145, 179–184 (2007).Article 

Google Scholar 
29.Hynynen, J. et al. Silviculture of birch (Betula pendula Roth and Betula pubescens Ehrh.) in northern Europe. Forestry 83, 103–119 (2010).30.Frouz, J. et al. Development of canopy cover and woody vegetation biomass on reclaimed and unreclaimed post-mining sites. Ecol. Eng. 84, 233–239 (2015).Article 

Google Scholar 
31.Řehounková, K., Lencová, K. & Prach, K. Spontaneous establishment of woodland during succession in a variety of central European disturbed sites. Ecol. Eng. 111, 94–99 (2018).Article 

Google Scholar 
32.Franiel, I. & Więski, K. Leaf features of silver birch (Betula pendula Roth). Variability within and between two populations (uncontaminated vs Pb-contaminated and Zn-contaminated site). Trees 19, 81–88 (2005).33.Kozlov, M. V. & Zvereva, E. L. Industrial barrens: Extreme habitats created by non-ferrous metallurgy. Rev. Environ. Sci. Bio/Technol. 6, 231–259 (2007).CAS 
Article 

Google Scholar 
34.Zvereva, E. L. & Kozlov, M. V. Growth and reproduction of dwarf shrubs, Vaccinium myrtillus and V. vitis-idaea, in a severely polluted area. Basic Appl. Ecol. https://doi.org/10.1016/j.baae.2004.11.003 (2005).35.Kozlov, M. V. Pollution resistance of mountain birch, Betula pubescens subsp. czerepanovii, near the copper–nickel smelter: Natural selection or phenotypic acclimation? Chemosphere 59, 189–197 (2005).36.Kondracki, J. Geografia fizyczna Polski. (Physical Geography of Poland). (PWN (in Polish), 2001).37.Pełka-Gościniak, J. Environmental aspects of relief transformation (Silesian Upland, Southern Poland). Environ. Socio-Econ. Stud. 2, 13–20.38.Tomusiak, R. et al. Age tables for silver birch (Betula pendula Roth) trees for early succession stands on abandoned agricultural lands. Sylwan 158, 579–589 (2014).
Google Scholar 
39.Szymkiewicz, B. Tablice Zasobności i Przyrostu Drzewostanów Ważniejszych Gatunków Drzew Leśnych. (Państwowe Wydawnictwo Rolnicze i Leśne, 2001).40.Dubois, H., Verkasalo, E. & Claessens, H. Potential of Birch (Betula pendula Roth and B. pubescens Ehrh.) for forestry and forest-based industry sector within the changing climatic and socio-economic context of Western Europe. Forests 11, 336 (2020).41.Ostrowska, A., Gawliński, S. & Szczubiałka, Z. Metody Analizy i Oceny Właściwości Gleb i Roślin. Katalog (Methods for Analysis and Assessment of Soil and Plant Properties) Catalog. (Instytut Ochrony Środowiska, 1991).42.Baskin, C. C. & Baskin, J. M. Seeds : Ecology, Biogeography, and Evolution of Dormancy and Germination. (Elsevier, 2014).43.Soltani, E., Ghaderi-Far, F., Baskin, C. C. & Baskin, J. M. Problems with using mean germination time to calculate rate of seed germination. Aust. J. Bot. 63, 631–635 (2015).Article 

Google Scholar 
44.Flores, P., Poggi, D., García, S. M., Catraro, M. & Gariglio, N. Effects of pre-stratification storage conditions on black walnut seed post-stratification germination capacity. Int. J. Fruit Sci. 17, 29–40 (2017).Article 

Google Scholar 
45.Ranal, M. A., de Santana, D. G., Ferreira, W. R. & Mendes-Rodrigues, C. Calculating germination measurements and organizing spreadsheets. Rev. Bras. Botân. 32, 849–855 (2009).Article 

Google Scholar 
46.Matthews, S. & Khajeh Hosseini, M. Mean germination time as an indicator of emergence performance in soil of seed lots of maize (Zea mays). Seed Sci. Technol. 34, 339–347 (2006).47.Ter Braak, C. J. F. & Šmilauer, P. Canoco Reference Manual and User’s Guide: Software for Ordination, Version 5.0. (Microcomputer Power, 2012).48.Inc., D. Dell Statistica (Data Analysis Software System, Version 13). (2016).49.Team, R. D. C. R: A Language and Environment for Statistical Computing. (R Foundation for Statistical Computing, 2008).50.Nicotra, A. B. et al. Plant phenotypic plasticity in a changing climate. Trends Plant Sci. 15, 684–692 (2010).CAS 
Article 

Google Scholar 
51.Gray, S. B. & Brady, S. M. Plant developmental responses to climate change. Dev. Biol. 419, 64–77 (2016).CAS 
Article 

Google Scholar 
52.Dahl, Å. E. & Fredrikson, M. The timetable for development of maternal tissues sets the stage for male genomic selection in Betula pendula (Betilaceae). Am. J. Bot. 83, 895–902 (1996).Article 

Google Scholar 
53.Kozlov, M. V. & Zvereva, E. L. Reproduction of mountain birch along a strong pollution gradient near Monchegorsk, Northwestern Russia. Environ. Pollut. 132, 443–451 (2004).CAS 
Article 

Google Scholar 
54.Sultan, S. E. Phenotypic plasticity in plants: A case study in ecological development. Evol. Dev. 5, 25–33 (2003).Article 

Google Scholar 
55.Zvereva, E. L. & Kozlov, M. V. Effects of pollution-induced habitat disturbance on the response of willows to simulated herbivory. J. Ecol. 89, 21–30 (2001).Article 

Google Scholar 
56.Eränen, J. K. Local adaptation of mountain birch to heavy metals in subarctic industrial barrens. For. Snow Landsc. Res. 80, 161–167 (2006).
Google Scholar 
57.Neuvonen, S., Nyyssonen, T., Ranta, H. & Kiilunen, S. Simulated acid rain and the reproduction of mountain birch [Betula pubescens ssp. tortuosa (Ledeb.) Nyman]: A cautionary tale. New Phytol. 118, 111–117 (1991).58.Cuinica, L. G., Abreu, I., Gomes, C. R. & Esteves da Silva, J. C. G. Exposure of Betula pendula Roth pollen to atmospheric pollutants CO, O3 and SO2. Grana 52, 299–304 (2013).59.Pasonen, H.-L., Pulkkinen, P. & Kärkkäinen, K. Genotype-environment interactions in pollen competitive ability in an anemophilous tree, Betula pendula Roth. Theor. Appl. Genet. 105, 465–473 (2002).Article 

Google Scholar 
60.Sarvas, R. On the flowering of birch and the quality of seed crop. Commun. Inst. For. Fenn. 1–38 (1952).61.Midmore, E., McCartan, S., Jinks, R. & Cahalan, C. Using thermal time models to predict germination of five provenances of silver birch (Betula pendula Roth) in southern England. Silva Fenn. 49, 1–12 (2015).62.Bojarczuk, K. et al. Effect of polluted soil and fertilisation on growth and physiology of Silver Birch (Betula pendula Roth.) seedlings. Polish J. Environ. Stud. 11, 483–492 (2002).63.Wierzbicka, M. & Rostański, A. Microevolutionary changes in ecotypes of calamine waste heap vegetation near Olkusz, Poland: A review. Acta Bot. Cracoviensia 44, 7–10 (2002).
Google Scholar 
64.Mahdi, T. & Whittaker, J. B. Do birch trees (Betula pendula) grow better if foraged by wood ants?. J. Anim. Ecol. 62, 101–116 (1993).Article 

Google Scholar 
65.Barantal, S. et al. Contrasting effects of tree species and genetic diversity on the leaf—Miner communities associated with silver birch. Oecologia 189, 687–697 (2019).ADS 
Article 

Google Scholar 
66.Santamour, Frank, S. & Greene, A. European hornet damage to ash and birch trees. J. Arboric. 12, 273–279 (1986).67.Klingeman, B., Oliver, J. & F., H. Who’s doin’ all that chewin’? The European hornet. Tenn. Green Times 2, 34–36 (2001).68.Ylioja, T., Roininen, H., Heinonen, J. & Rousi, M. Susceptibility of Betula pendula clones to Phytobia betulae, a dipteran miner of birch stems. Can. J. For. Res. 30, 1824–1829 (2000).Article 

Google Scholar 
69.Franiel, I. Development of Betula pendula seedlings growing on the Silesia Steelworks dumping grounds in Katowice. Acta Agrophys. 51, 51–55 (2001).
Google Scholar  More

1.Díaz et al. Summary for Policymakers of the Global Assessment.pdf.2.Kehoe, L. et al. Biodiversity at risk under future cropland expansion and intensification. Nat. Ecol. Evolut. 1, 1129–1135 (2017).Article 

Google Scholar 
3.Hendershot, J. N. et al. Intensive farming drives long-term shifts in avian community composition. Nature 579, 393–396 (2020).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
4.Bommarco, R., Kleijn, D. & Potts, S. G. Ecological intensification: Harnessing ecosystem services for food security. Trends Ecol. Evol. 28, 230–238 (2013).PubMed 
Article 
PubMed Central 

Google Scholar 
5.Michael, D. R., Wood, J. T., O’Loughlin, T. & Lindenmayer, D. B. Influence of land sharing and land sparing strategies on patterns of vegetation and terrestrial vertebrate richness and occurrence in Australian endangered eucalypt woodlands. Agr. Ecosyst. Environ. 227, 24–32 (2016).Article 

Google Scholar 
6.Tittonell, P. Ecological intensification of agriculture—Sustainable by nature. Curr. Opin. Environ. Sustain. 8, 53–61 (2014).Article 

Google Scholar 
7.Willer, E. H., Schlatter, B., Trávní, J., Kemper, L. & Lernoud, J. The World of Organic Agriculture Statistics and Emerging Trends 2020. 337.8.Reganold, J. P. & Wachter, J. M. Organic agriculture in the twenty-first century. Nat. Plants 2 (2016).9.Connor, D. J. Organic agriculture cannot feed the world. Field Crop Res. 106, 187–190 (2008).Article 

Google Scholar 
10.Seufert, V. & Ramankutty, N. Many shades of gray—The context-dependent performance of organic agriculture. Sci. Adv. 3, e1602638 (2017).11.Smith, O. M. et al. Landscape context affects the sustainability of organic farming systems. Proc. Natl. Acad. Sci. 117, 2870–2878 (2020).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
12.Bengtsson, J., Ahnström, J. & Weibull, A.-C. The effects of organic agriculture on biodiversity and abundance: A meta-analysis: Organic agriculture, biodiversity and abundance. J. Appl. Ecol. 42, 261–269 (2005).Article 

Google Scholar 
13.Tuck, S. L. et al. Land-use intensity and the effects of organic farming on biodiversity: A hierarchical meta-analysis. J. Appl. Ecol. 51, 746–755 (2014).PubMed 
PubMed Central 
Article 

Google Scholar 
14.Lichtenberg, E. M. et al. A global synthesis of the effects of diversified farming systems on arthropod diversity within fields and across agricultural landscapes. Glob. Change Biol. 23, 4946–4957 (2017).ADS 
Article 

Google Scholar 
15.Lori, M., Symnaczik, S., Mäder, P., De Deyn, G. & Gattinger, A. Organic farming enhances soil microbial abundance and activity—A meta-analysis and meta-regression. PLOS ONE 12, e0180442 (2017).16.Kleijn, D., Rundlöf, M., Scheper, J., Smith, H. G. & Tscharntke, T. Does conservation on farmland contribute to halting the biodiversity decline?. Trends Ecol. Evol. 26, 474–481 (2011).PubMed 
Article 
PubMed Central 

Google Scholar 
17.Birkhofer, K., Ekroos, J., Corlett, E. B. & Smith, H. G. Winners and losers of organic cereal farming in animal communities across Central and Northern Europe. Biol. Cons. 175, 25–33 (2014).Article 

Google Scholar 
18.Mackie, K. A., Müller, T., Zikeli, S. & Kandeler, E. Long-term copper application in an organic vineyard modifies spatial distribution of soil micro-organisms. Soil Biol. Biochem. 65, 245–253 (2013).CAS 
Article 

Google Scholar 
19.Buchholz, J. et al. Soil biota in vineyards are more influenced by plants and soil quality than by tillage intensity or the surrounding landscape. Sci. Rep. 7 (2017).20.Hole, D. G. et al. Does organic farming benefit biodiversity?. Biol. Cons. 122, 113–130 (2005).Article 

Google Scholar 
21.Power, A. G. Ecosystem services and agriculture: Tradeoffs and synergies. Philos. Trans. R. Soc. B Biol. Sci. 365, 2959–2971 (2010).Article 

Google Scholar 
22.Peigné, J. et al. Earthworm populations under different tillage systems in organic farming. Soil Tillage Res. 104, 207–214 (2009).Article 

Google Scholar 
23.Biondi, A., Desneux, N., Siscaro, G. & Zappalà, L. Using organic-certified rather than synthetic pesticides may not be safer for biological control agents: Selectivity and side effects of 14 pesticides on the predator Orius laevigatus. Chemosphere 87, 803–812 (2012).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
24.Mehrabi, Z., Seufert, V., Ramankutty, N. The conventional versus alternative agricultural divide: A response to Garibaldi et al. Trends Ecol. Evolut. 32, 720–721 (2017).25.Tscharntke, T., Klein, A. M., Kruess, A., Steffan-Dewenter, I. & Thies, C. Landscape perspectives on agricultural intensification and biodiversity – ecosystem service management. Ecol. Lett. 8, 857–874 (2005).Article 

Google Scholar 
26.Gámez-Virués, S. et al. Landscape simplification filters species traits and drives biotic homogenization. Nat. Commun. 6 (2015).27.Holzschuh, A., Steffan-Dewenter, I. & Tscharntke, T. Agricultural landscapes with organic crops support higher pollinator diversity. Oikos 117, 354–361 (2008).Article 

Google Scholar 
28.Muneret, L., Auriol, A., Thiéry, D. & Rusch, A. Organic farming at local and landscape scales fosters biological pest control in vineyards. Ecol. Appl. 29, e01818 (2019).29.Gabriel, D. et al. Scale matters: The impact of organic farming on biodiversity at different spatial scales: Scale matters in organic farming. Ecol. Lett. 13, 858–869 (2010).PubMed 
Article 
PubMed Central 

Google Scholar 
30.Agreste. Pratiques Phytosanitaires en Viticulture. Campagne 2016. (2020)31.Agreste. La Viticulture Bio en Nouvelle-Aquitaine: Un Dynamisme à Tous les Stades de la Filière. (2020).32.Gruber, S. & Claupein, W. Effect of tillage intensity on weed infestation in organic farming. Soil Tillage Res. 105, 104–111 (2009).Article 

Google Scholar 
33.Pfingstmann, A. et al. Contrasting effects of tillage and landscape structure on spiders and springtails in vineyards. Sustainability 11, 2095 (2019).Article 

Google Scholar 
34.Dittmer, S. & Schrader, S. Longterm effects of soil compaction and tillage on Collembola and straw decomposition in arable soil. Pedobiologia 44, 527–538 (2000).Article 

Google Scholar 
35.Kolb, S., Uzman, D., Leyer, I., Reineke, A. & Entling, M. H. Differential effects of semi-natural habitats and organic management on spiders in viticultural landscapes. Agric. Ecosyst. Environ. 287, 106695 (2020).36.Birkhofer, K. et al. Relationships between multiple biodiversity components and ecosystem services along a landscape complexity gradient. Biol. Cons. 218, 247–253 (2018).Article 

Google Scholar 
37.Kratschmer, S. et al. Tillage intensity or landscape features: What matters most for wild bee diversity in vineyards?. Agric. Ecosyst. Environ. 266, 142–152 (2018).Article 

Google Scholar 
38.Ullmann, K. S., Meisner, M. H. & Williams, N. M. Impact of tillage on the crop pollinating, ground-nesting bee, Peponapis pruinosa in California. Agric. Ecosyst. Environ. 232, 240–246 (2016).Article 

Google Scholar 
39.Jiang, X., Wright, A. L., Wang, X. & Liang, F. Tillage-induced changes in fungal and bacterial biomass associated with soil aggregates: A long-term field study in a subtropical rice soil in China. Appl. Soil. Ecol. 48, 168–173 (2011).Article 

Google Scholar 
40.Zuber, S. M. & Villamil, M. B. Meta-analysis approach to assess effect of tillage on microbial biomass and enzyme activities. Soil Biol. Biochem. 97, 176–187 (2016).CAS 
Article 

Google Scholar 
41.Luff, M. L. The biology of the ground beetle Harpalus rufipes in a strawberry field in Northumberland. Ann. Appl. Biol. 94, 153–164 (1980).Article 

Google Scholar 
42.Shearin, A. F., Reberg-Horton, S. C. & Gallandt, E. R. Direct effects of tillage on the activity density of ground beetle (Coleoptera: Carabidae) weed seed predators. Environ. Entomol. 36, 1140–1146 (2007).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
43.Rundlöf, M. et al. Seed coating with a neonicotinoid insecticide negatively affects wild bees. Nature 521, 77–80 (2015).ADS 
PubMed 
Article 
CAS 
PubMed Central 

Google Scholar 
44.Martin, E. A. et al. The interplay of landscape composition and configuration: new pathways to manage functional biodiversity and agroecosystem services across Europe. Ecol. Lett. 22, 1083–1094 (2019).PubMed 
Article 
PubMed Central 

Google Scholar 
45.Goded, S., Ekroos, J., Azcárate, J. G., Guitián, J. A. & Smith, H. G. Effects of organic farming on plant and butterfly functional diversity in mosaic landscapes. Agric. Ecosyst. Environ. 284, 106600 (2019).46.Rusch, A., Valantin-Morison, M., Sarthou, J.-P. & Roger-Estrade, J. Multi-scale effects of landscape complexity and crop management on pollen beetle parasitism rate. Landsc. Ecol. 26, 473–486 (2011).Article 

Google Scholar 
47.Tamburini, G., De Simone, S., Sigura, M., Boscutti, F. & Marini, L. Conservation tillage mitigates the negative effect of landscape simplification on biological control. J. Appl. Ecol. 53, 233–241 (2016).Article 

Google Scholar 
48.Le Féon, V. et al. Intensification of agriculture, landscape composition and wild bee communities: A large scale study in four European countries. Agric. Ecosyst. Environ. 137, 143–150 (2010).Article 

Google Scholar 
49.Sousa, J. P. et al. Changes in Collembola richness and diversity along a gradient of land-use intensity: A pan European study. Pedobiologia 50, 147–156 (2006).Article 

Google Scholar 
50.Vanbergen, A. J. et al. Scale-specific correlations between habitat heterogeneity and soil fauna diversity along a landscape structure gradient. Oecologia 153, 713–725 (2007).ADS 
PubMed 
Article 
PubMed Central 

Google Scholar 
51.Lehmitz, R., Russell, D., Hohberg, K., Christian, A. & Xylander, W. E. R. Active dispersal of oribatid mites into young soils. Appl. Soil. Ecol. 55, 10–19 (2012).Article 

Google Scholar 
52.Concepción, E. D., Díaz, M. & Baquero, R. A. Effects of landscape complexity on the ecological effectiveness of agri-environment schemes. Landsc. Ecol. 23, 135–148 (2008).Article 

Google Scholar 
53.Tscharntke, T. et al. Landscape moderation of biodiversity patterns and processes – Eight hypotheses. Biol. Rev. 87, 661–685 (2012).PubMed 
Article 
PubMed Central 

Google Scholar 
54.Desneux, N., Decourtye, A. & Delpuech, J.-M. The sublethal effects of pesticides on beneficial arthropods. Annu. Rev. Entomol. 52, 81–106 (2007).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
55.Naveed, M. et al. Simultaneous loss of soil biodiversity and functions along a copper contamination gradient: When soil goes to sleep. Soil Sci. Soc. Am. J. 78, 1239–1250 (2014).ADS 
Article 
CAS 

Google Scholar 
56.Eijsackers, H., Beneke, P., Maboeta, M., Louw, J. P. E. & Reinecke, A. J. The implications of copper fungicide usage in vineyards for earthworm activity and resulting sustainable soil quality. Ecotoxicol. Environ. Saf. 62, 99–111 (2005).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
57.Le Provost, G. et al. Land-use history impacts functional diversity across multiple trophic groups. Proc. Natl. Acad. Sci. 117, 1573–1579 (2020).PubMed 
Article 
CAS 
PubMed Central 

Google Scholar 
58.Muneret, L. et al. Organic farming expansion drives natural enemy abundance but not diversity in vineyard-dominated landscapes. Ecol. Evol. https://doi.org/10.1002/ece3.5810 (2019).Article 
PubMed 
PubMed Central 

Google Scholar 
59.Lechenet, M., Dessaint, F., Py, G., Makowski, D. & Munier-Jolain, N. Reducing pesticide use while preserving crop productivity and profitability on arable farms. Nat. Plants 3 (2017).60.Le Féon, V. et al. Solitary bee abundance and species richness in dynamic agricultural landscapes. Agric. Ecosyst. Environ. 166, 94–101 (2013).Article 

Google Scholar 
61.McCravy, K. & Ruholl, J. Bee (Hymenoptera: Apoidea) diversity and sampling methodology in a midwestern USA deciduous forest. Insects 8, 81 (2017).PubMed Central 
Article 

Google Scholar 
62.Bano, R. & Roy, S. Extraction of Soil Microarthropods: A Low Cost Berlese-Tullgren Funnels Extractor. 4.63.Grueber, C. E., Nakagawa, S., Laws, R. J. & Jamieson, I. G. Multimodel inference in ecology and evolution: Challenges and solutions: Multimodel inference. J. Evol. Biol. 24, 699–711 (2011).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
64.Burnham, K. P. & Anderson, D. R. Multimodel inference: Understanding AIC and BIC in model selection. Sociol. Methods Res. 33, 261–304 (2004).MathSciNet 
Article 

Google Scholar 
65.Bartoń, K. MuMIn: Multi-Model Inference. R Package Version 1.43.17. https://CRAN.R-project.org/package=MuMIn (2020).66.R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ (2020).67.Hartig, F. DHARMa: Residual Diagnostics for Hierarchical (Multi-Level/Mixed) Regression Models (2020). R Package Version 0.3.3.0. https://CRAN.R-project.org/package=DHARMa68.Bates, D., Maechler, M., Bolker, B., Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67(1), 1–48. https://doi.org/10.18637/jss.v067.i01 (2015). More

1.Mutreja, A. et al. Evidence for several waves of global transmission in the seventh cholera pandemic. Nature 477, 462–465 (2011).CAS 
Article 

Google Scholar 
2.Ali, M., Nelson, A. R., Lopez, A. L. & Sack, D. A. Updated global burden of cholera in endemic countries. PLoS Negl. Trop. Dis. 9, e0003832 (2015).Article 

Google Scholar 
3.Bompangue, D. N. et al. Lakes as source of cholera outbreaks, Democratic Republic of Congo. Emerg. Infect. Dis. 14, 798–800 (2008).Article 

Google Scholar 
4.Weill, F. X. et al. Genomic history of the seventh pandemic of cholera in Africa. Science 358, 785–789 (2017).CAS 
Article 

Google Scholar 
5.Hounmanou, Y. M. G. et al. Genomic insights into Vibrio cholerae O1 responsible for cholera epidemics in Tanzania between 1993 and 2017. PLoS Neglect Trop. D. 13, e0007934 (2019).Article 

Google Scholar 
6.Colwell, R. R. Global climate and infectious disease: the cholera paradigm. Science 274, 2025–2031 (1996).CAS 
Article 

Google Scholar 
7.Singleton, F., Attwell, R., Jangi, M. & Colwell, R. Influence of salinity and organic nutrient concentration on survival and growth of Vibrio choleraein aquatic microcosms. Appl. Environ. Microbiol. 43, 1080–1085 (1982).CAS 
Article 

Google Scholar 
8.Kirschner, A. K. T. et al. Rapid growth of planktonic Vibrio cholerae non-O1/non-O139 strains in a large alkaline lake in Austria: Dependence on temperature and dissolved organic carbon quality. Appl. Environ. Microb. 74, 2004–2015 (2008).CAS 
Article 

Google Scholar 
9.Reid, P. C. et al. The continuous plankton recorder: concepts and history, from Plankton Indicator to undulating recorders. Prog. Oceanogr. 57, 117–173 (2003).Article 

Google Scholar 
10.Vezzulli, L. et al. Climate influence on Vibrio and associated human diseases during the past half-century in the coastal North Atlantic. Proc. Natl. Acad. Sci. USA. 113, E5062–E5071 (2016).CAS 
Article 

Google Scholar 
11.Huq, A. et al. Detection, isolation, and identification of Vibrio cholerae from the environment. Curr. Protoc. Microbiol. https://doi.org/10.1002/9780471729259.mc06a05s26 (2012).12.Thompson, F. L. et al. Phylogeny and molecular identification of vibrios on the basis of multilocus sequence analysis. Appl. Environ. Microb. 71, 5107–5115 (2005).CAS 
Article 

Google Scholar 
13.Vezzulli, L. et al. GbpA as a novel qPCR target for the species-specific detection of Vibrio cholerae O1, O139, Non-O1/Non-O139 in environmental, stool, and historical continuous plankton recorder samples. s. PLoS ONE 10, e0123983 (2015).Article 

Google Scholar 
14.Alam, M. et al. Toxigenic Vibrio cholerae in the aquatic environment of Mathbaria, Bangladesh. Appl. Environ. Microb. 72, 2849–2855 (2006).CAS 
Article 

Google Scholar 
15.Senoh, M. et al. Isolation of viable but nonculturable Vibrio cholerae O1 from environmental water samples in Kolkata, India, in a culturable state. Microbiol. Open 3, 239–246 (2014).CAS 
Article 

Google Scholar 
16.Vezzulli, L. et al. Whole-genome enrichment provides deep insights into vibrio cholerae metagenome from an African river. Microb. Ecol. 73, 734–738 (2017).CAS 
Article 

Google Scholar 
17.Kaboré, S. et al. Occurrence of Vibrio cholerae in water reservoirs of Burkina Faso. Res Microbiol 169, 1–10 (2018).Article 

Google Scholar 
18.Bwire, G. et al. Environmental surveillance of Vibrio cholerae O1/O139 in the five African Great Lakes and other major surface water sources in Uganda. Front. Microbiol. 9, 1560 (2018).Article 

Google Scholar 
19.Vezzulli, L., Baker-Austin, C., Kirschner, A., Pruzzo, C. & Martinez-Urtaza, J. Global emergence of environmental non-O1/O139 Vibrio cholerae infections linked with climate change: a neglected research field? Environ. Microbiol. 22, 4342–4355 (2020).CAS 
Article 

Google Scholar  More