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    Some species of coral might be able to adapt to a world altered by climate change, at least if countries curb their greenhouse-gas emissions1.

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    doi: https://doi.org/10.1038/d41586-022-00719-x

    ReferencesMcLachlan, R. H. et al. Sci. Rep. 12, 3712 (2022).PubMed 
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    Permafrost peat carbon approaching a climatic tipping point

    Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.This is a summary of: Fewster, R. E. et al. Imminent loss of climate space for permafrost peatlands in Europe and Western Siberia. Nat. Clim. Change https://doi.org/10.1038/s41558-022-01296-7 (2022). More

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    Imminent loss of climate space for permafrost peatlands in Europe and Western Siberia

    Hugelius, G. et al. Large stocks of peatland carbon and nitrogen are vulnerable to permafrost thaw. Proc. Natl Acad. Sci. USA 117, 20438–20446 (2020).CAS 

    Google Scholar 
    Davy, R. & Outten, S. The Arctic surface climate in CMIP6: status and developments since CMIP5. J. Clim. 33, 8047–8068 (2020).
    Google Scholar 
    Voigt, C. et al. Ecosystem carbon response of an Arctic peatland to simulated permafrost thaw. Glob. Change Biol. 25, 1746–1764 (2019).
    Google Scholar 
    Swindles, G. T. et al. The long-term fate of permafrost peatlands under rapid climate warming. Sci. Rep. 5, 17951 (2015).CAS 

    Google Scholar 
    Du, R. et al. The role of peat on permafrost thaw based on field observations. Catena 208, 105772 (2022).CAS 

    Google Scholar 
    Chaudhary, N. et al. Modelling past and future peatland carbon dynamics across the pan-Arctic. Glob. Change Biol. 26, 4119–4133 (2020).
    Google Scholar 
    Müller, J. & Joos, F. Committed and projected future changes in global peatlands—continued transient model simulations since the Last Glacial Maximum. Biogeosciences 18, 3657–3687 (2021).
    Google Scholar 
    Seppälä, M. Synthesis of studies of palsa formation underlining the importance of local environmental and physical characteristics. Quatern. Res. 75, 366–370 (2011).
    Google Scholar 
    Karjalainen, O. et al. High potential for loss of permafrost landforms in a changing climate. Environ. Res. Lett. https://doi.org/10.1088/1748-9326/abafd5 (2020).Fan, X., Duan, Q., Shen, C., Wu, Y. & Xing, C. Global surface air temperatures in CMIP6: historical performance and future changes. Environ. Res. Lett. 15, 104056 (2020).
    Google Scholar 
    Tebaldi, C. et al. Climate model projections from the Scenario Model Intercomparison Project (ScenarioMIP) of CMIP6. Earth Syst. Dyn. 12, 253–293 (2021).
    Google Scholar 
    Zoltai, S. & Tarnocai, C. Properties of a wooded palsa in northern Manitoba. Arct. Alp. Res. 3, 115–129 (1971).
    Google Scholar 
    Minke, M., Donner, N., Karpov, N. S., de Klerk, P. & Joosten, H. Distribution, diversity, development and dynamics of polygon mires: examples from Northeast Yakutia (Siberia). Peatl. Int. 1, 36–40 (2007).
    Google Scholar 
    O’Neill, H. B., Wolfe, S. A. & Duchesne, C. New ground ice maps for Canada using a paleogeographic modelling approach. Cryosphere 13, 753–773 (2019).
    Google Scholar 
    Fronzek, S., Luoto, M. & Carter, T. R. Potential effect of climate change on the distribution of palsa mires in subarctic Fennoscandia. Clim. Res. 32, 1–12 (2006).
    Google Scholar 
    Luoto, M., Fronzek, S. & Zuidhoff, F. S. Spatial modelling of palsa mires in relation to climate in northern Europe. Earth Surf. Process. Landf. 29, 1373–1387 (2004).
    Google Scholar 
    Peregon, A., Maksyutov, S., Kosykh, N. P. & Mironycheva-Tokareva, N. P. Map-based inventory of wetland biomass and net primary production in Western Siberia. J. Geophys. Res. Biogeosci. 113, G01007 (2008).
    Google Scholar 
    Terentieva, I., Lapshina, E. D., Sabrekov, A. F., Maksyutov, S. S. & Glagolev, M. V. Mapping of West Siberian wetland complexes using landsat imagery: implications for methane emissions. Biogeosciences 13, 4615–4626 (2016).CAS 

    Google Scholar 
    Zoltai, S., Siltanen, R. M. & Johnson, J. D. A Wetland Data Base for the Western Boreal, Subarctic, and Arctic Regions of Canada (Natural Resources Canada, Canadian Forest Service, 2000).Fewster, R. E. et al. Drivers of Holocene palsa distribution in North America. Quat. Sci. Rev. https://doi.org/10.1016/j.quascirev.2020.106337 (2020).Parviainen, M. & Luoto, M. Climate envelopes of mire complex types in Fennoscandia. Geogr. Ann. A 89, 137–151 (2007).
    Google Scholar 
    Aalto, J., Harrison, S. & Luoto, M. Statistical modelling predicts almost complete loss of major periglacial processes in northern Europe by 2100. Nat. Commun. 8, 515 (2017).
    Google Scholar 
    Eyring, V. et al. Overview of the Coupled Model Intercomparison Project Phase 6 (CMIP6) experimental design and organization. Geosci. Model Dev. 9, 1937–1958 (2016).
    Google Scholar 
    Brunner, L. et al. Reduced global warming from CMIP6 projections when weighting models by performance and independence. Earth Syst. Dyn. 11, 995–1012 (2020).
    Google Scholar 
    O’Neill, B. C. et al. The Scenario Model Intercomparison Project (ScenarioMIP) for CMIP6. Geosci. Model Dev. 9, 3461–3482 (2016).
    Google Scholar 
    Aalto, J., Venäläinen, A., Heikkinen, R. K. & Luoto, M. Potential for extreme loss in high‐latitude Earth surface processes due to climate change. Geophys. Res. Lett. 41, 3914–3924 (2014).
    Google Scholar 
    Halsey, L. A., Vitt, D. H. & Zoltai, S. C. Disequilibrium response of permafrost in boreal continental western Canada to climate change. Climatic Change 30, 57–73 (1995).
    Google Scholar 
    Camill, P. & Clark, J. S. Climate change disequilibrium of boreal permafrost peatlands caused by local processes. Am. Nat. 151, 207–222 (1998).CAS 

    Google Scholar 
    Borge, A. F., Westermann, S., Solheim, I. & Etzelmüller, B. Strong degradation of palsas and peat plateaus in northern Norway during the last 60 years. Cryosphere 11, 1–16 (2017).
    Google Scholar 
    Åkerman, H. J. & Johansson, M. Thawing permafrost and thicker active layers in sub‐arctic Sweden. Permafr. Periglac. Process. 19, 279–292 (2008).
    Google Scholar 
    Olvmo, M., Holmer, B., Thorsson, S., Reese, H. & Lindberg, F. Sub-arctic palsa degradation and the role of climatic drivers in the largest coherent palsa mire complex in Sweden (Vissátvuopmi), 1955–2016. Sci. Rep. 10, 8937 (2020).CAS 

    Google Scholar 
    Payette, S., Delwaide, A., Caccianiga, M. & Beauchemin, M. Accelerated thawing of subarctic peatland permafrost over the last 50 years. Geophys. Res. Lett. 31, L18208 (2004).
    Google Scholar 
    Treat, C. C. et al. Effects of permafrost aggradation on peat properties as determined from a pan‐Arctic synthesis of plant macrofossils. J. Geophys. Res. Biogeosci. 121, 78–94 (2016).CAS 

    Google Scholar 
    Dearborn, K. D., Wallace, C. A., Patankar, R. & Baltzer, J. L. Permafrost thaw in boreal peatlands is rapidly altering forest community composition. J. Ecol. 109, 1452–1467 (2021).CAS 

    Google Scholar 
    Olefeldt, D. & Roulet, N. T. Effects of permafrost and hydrology on the composition and transport of dissolved organic carbon in a subarctic peatland complex. J. Geophys. Res. Biogeosci. 117, G01005 (2012).
    Google Scholar 
    Burd, K., Estop-Aragonés, C., Tank, S. E. & Olefeldt, D. Lability of dissolved organic carbon from boreal peatlands: interactions between permafrost thaw, wildfire, and season. Can. J. Soil Sci. 100, 503–515 (2020).
    Google Scholar 
    Klaminder, J., Yoo, K., Rydberg, J. & Giesler, R. An explorative study of mercury export from a thawing palsa mire. J. Geophys. Res. Biogeosci. 113, G04034 (2008).
    Google Scholar 
    Luoto, M. & Seppälä, M. Thermokarst ponds as indicators of the former distribution of palsas in Finnish Lapland. Permafr. Periglac. Process. 14, 19–27 (2003).
    Google Scholar 
    Vitt, D. H., Halsey, L. A. & Zoltai, S. C. The changing landscape of Canada’s western boreal forest: the current dynamics of permafrost. Can. J. For. Res. 30, 283–287 (2000).
    Google Scholar 
    Turetsky, M., Wieder, R., Vitt, D., Evans, R. & Scott, K. The disappearance of relict permafrost in boreal North America: effects on peatland carbon storage and fluxes. Glob. Change Biol. 13, 1922–1934 (2007).
    Google Scholar 
    Jorgenson, M. T. et al. Resilience and vulnerability of permafrost to climate change. Can. J. For. Res. 40, 1219–1236 (2010).
    Google Scholar 
    Magnússon, R. Í. et al. Rapid vegetation succession and coupled permafrost dynamics in Arctic thaw ponds in the Siberian lowland tundra. J. Geophys. Res. Biogeosci. 125, e2019JG005618 (2020).
    Google Scholar 
    Zoltai, S. Permafrost distribution in peatlands of west-central Canada during the Holocene warm period 6000 years bp. Géogr. Phys. Quat. 49, 45–54 (1995).
    Google Scholar 
    Seppälä, M. An expermental study of the formation of palsas. In Proc. 4th Canadian Permafrost Conference (ed. French, H. M.) 36–42 (National Research Council of Canada, Ottawa, 1982).Yu, Z., Loisel, J., Brosseau, D. P., Beilman, D. W. & Hunt, S. J. Global peatland dynamics since the Last Glacial Maximum. Geophys. Res. Lett. 37, L13402 (2010).
    Google Scholar 
    Serreze, M. C. & Barry, R. G. Processes and impacts of Arctic amplification: a research synthesis. Glob. Planet. Change 77, 85–96 (2011).
    Google Scholar 
    Thurner, M. et al. Carbon stock and density of northern boreal and temperate forests. Glob. Ecol. Biogeogr. 23, 297–310 (2014).
    Google Scholar 
    Seppälä, M. The origin of palsas. Geogr. Ann. A 68, 141–147 (1986).
    Google Scholar 
    Mamet, S. D., Chun, K. P., Kershaw, G. G., Loranty, M. M. & Peter Kershaw, G. Recent increases in permafrost thaw rates and areal loss of palsas in the western Northwest Territories, Canada. Permafr. Periglac. Process. 28, 619–633 (2017).
    Google Scholar 
    Camill, P. Permafrost thaw accelerates in boreal peatlands during late-20th century climate warming. Climatic Change 68, 135–152 (2005).CAS 

    Google Scholar 
    Quinton, W. L. & Baltzer, J. The active-layer hydrology of a peat plateau with thawing permafrost (Scotty Creek, Canada). Hydrol. J. 21, 201–220 (2013).
    Google Scholar 
    Turetsky, M. R., Wieder, R. K. & Vitt, D. H. Boreal peatland C fluxes under varying permafrost regimes. Soil Biol. Biochem. 34, 907–912 (2002).CAS 

    Google Scholar 
    Schädel, C. et al. Potential carbon emissions dominated by carbon dioxide from thawed permafrost soils. Nat. Clim. Change 6, 950–953 (2016).
    Google Scholar 
    Myers‐Smith, I. H. & Hik, D. S. Climate warming as a driver of tundra shrubline advance. J. Ecol. 106, 547–560 (2018).
    Google Scholar 
    Gibson, C. M. et al. Wildfire as a major driver of recent permafrost thaw in boreal peatlands. Nat. Commun. 9, 3041 (2018).
    Google Scholar 
    Gibson, C. M., Estop-Aragonés, C., Flannigan, M., Thompson, D. K. & Olefeldt, D. Increased deep soil respiration detected despite reduced overall respiration in permafrost peat plateaus following wildfire. Environ. Res. Lett. 14, 125001 (2019).CAS 

    Google Scholar 
    Estop-Aragonés, C. et al. Respiration of aged soil carbon during fall in permafrost peatlands enhanced by active layer deepening following wildfire but limited following thermokarst. Environ. Res. Lett. 13, 085002 (2018).
    Google Scholar 
    Treat, C. C. et al. Predicted vulnerability of carbon in permafrost peatlands with future climate change and permafrost thaw in western Canada. J. Geophys. Res. Biogeosci. 126, e2020JG005872 (2021).CAS 

    Google Scholar 
    Jones, M. C. et al. Rapid carbon loss and slow recovery following permafrost thaw in boreal peatlands. Glob. Change Biol. 23, 1109–1127 (2017).
    Google Scholar 
    Turetsky, M. R. et al. Carbon release through abrupt permafrost thaw. Nat. Geosci. 13, 138–143 (2020).CAS 

    Google Scholar 
    Heffernan, L., Estop‐Aragonés, C., Knorr, K. H., Talbot, J. & Olefeldt, D. Long‐term impacts of permafrost thaw on carbon storage in peatlands: deep losses offset by surficial accumulation. J. Geophys. Res. Biogeosci. 125, e2019JG005501 (2020).CAS 

    Google Scholar 
    Gallego-Sala, A. V. et al. Latitudinal limits to the predicted increase of the peatland carbon sink with warming. Nat. Clim. Change 8, 907–913 (2018).CAS 

    Google Scholar 
    Qiu, C. et al. The role of northern peatlands in the global carbon cycle for the 21st century. Glob. Ecol. Biogeogr. 29, 956–973 (2020).
    Google Scholar 
    Harris, I., Osborn, T. J., Jones, P. & Lister, D. Version 4 of the CRU TS monthly high-resolution gridded multivariate climate dataset. Sci. Data 7, 109 (2020).
    Google Scholar 
    Hugelius, G. et al. Maps of Northern Peatland Extent, Depth, Carbon Storage and Nitrogen Storage Version 1.0 (Bolin Centre for Climate Research, 2020); https://doi.org/10.17043/hugelius-2020Brownrigg, R. mapdata: Extra Map Databases. R version 2.3.0 https://CRAN.R-project.org/package=mapdata (2018).Olefeldt, D., Turetsky, M. R., Crill, P. M. & McGuire, A. D. Environmental and physical controls on northern terrestrial methane emissions across permafrost zones. Glob. Change Biol. 19, 589–603 (2013).
    Google Scholar 
    Pissart, A. Palsas, lithalsas and remnants of these periglacial mounds: a progress report. Prog. Phys. Geog. 26, 605–621 (2002).
    Google Scholar 
    Wolfe, S. A., Stevens, C. W., Gaanderse, A. J. & Oldenborger, G. A. Lithalsa distribution, morphology and landscape associations in the Great Slave Lowland, Northwest Territories, Canada. Geomorphology 204, 302–313 (2014).
    Google Scholar 
    Lara, M. J., Nitze, I., Grosse, G. & McGuire, A. D. Tundra landform and vegetation productivity trend maps for the Arctic Coastal Plain of northern Alaska. Sci. Data 5, 180058 (2018).
    Google Scholar 
    Jorgenson, M. T. & Grunblatt, J. Landscape-Level Ecological Mapping of Northern Alaska and Field Site Photography (Arctic Landscape Conservation Cooperative, U.S. Fish & Wildlife Service, 2013).Xu, J., Morris, P. J., Liu, J. & Holden, J. PEATMAP: refining estimates of global peatland distribution based on a meta-analysis. Catena 160, 134–140 (2018).
    Google Scholar 
    ESRI. ArcMap v.10.6.1 (Environmental Systems Research Institute, 2018).Brown, J., Ferrians, O. Jr, Heginbottom, J. A. & Melnikov, E. Circum-Arctic Map of Permafrost and Ground-Ice Conditions (US Geological Survey, 1997).QGIS v.3.12 (QGIS Association, 2020); https://qgis.orgHugelius, G. et al. The Northern Circumpolar Soil Carbon Database: spatially distributed datasets of soil coverage and soil carbon storage in the northern permafrost regions. Earth Syst. Sci. Data 5, 3 (2013).
    Google Scholar 
    Everett, K. R. in Developments in Soil Science Vol. 11 (eds Wilding, L. P. et al.) 1–53 (Elsevier, 1983).Tokarska, K. B. et al. Past warming trend constrains future warming in CMIP6 models. Sci. Adv. 6, eaaz9549 (2020).CAS 

    Google Scholar 
    Forster, P. et al. in Climate Change 2021: The Physical Science Basis (eds Masson-Delmotte, V. et al.) Ch. 7 (IPCC, Cambridge Univ. Press, 2021).Flynn, C. M. & Mauritsen, T. On the climate sensitivity and historical warming evolution in recent coupled model ensembles. Atmos. Chem. Phys. 20, 7829–7842 (2020).CAS 

    Google Scholar 
    Morris, P. J. et al. Global peatland initiation driven by regionally asynchronous warming. Proc. Natl Acad. Sci. USA 115, 4851–4856 (2018).CAS 

    Google Scholar 
    Latombe, G. et al. Comparison of spatial downscaling methods of general circulation model results to study climate variability during the Last Glacial Maximum. Geosci. Model Dev. 11, 2563–2579 (2018).
    Google Scholar 
    Galar, M., Fernández, A., Barrenechea, E., Bustince, H. & Herrera, F. An overview of ensemble methods for binary classifiers in multi-class problems: experimental study on one-vs-one and one-vs-all schemes. Pattern Recognit. 44, 1761–1776 (2011).
    Google Scholar 
    Petrucci, C. J. A primer for social worker researchers on how to conduct a multinomial logistic regression. J. Soc. Serv. Res. 35, 193–205 (2009).
    Google Scholar 
    Fronzek, S. et al. Evaluating sources of uncertainty in modelling the impact of probabilistic climate change on sub-arctic palsa mires. Nat. Hazards Earth Syst. Sci. 11, 2981–2995 (2011).
    Google Scholar 
    Aalto, J. & Luoto, M. Integrating climate and local factors for geomorphological distribution models. Earth Surf. Process. Landf. 39, 1729–1740 (2014).
    Google Scholar 
    Graham, M. H. Confronting multicollinearity in ecological multiple regression. Ecology 84, 2809–2815 (2003).
    Google Scholar 
    Dormann, C. F. et al. Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36, 27–46 (2013).
    Google Scholar 
    Anisimov, O. A. & Nelson, F. E. Permafrost zonation and climate change in the northern hemisphere: results from transient general circulation models. Climatic Change 35, 241–258 (1997).
    Google Scholar 
    Armstrong, R. A. When to use the Bonferroni correction. Ophthalm. Physiol. Opt. 34, 502–508 (2014).
    Google Scholar 
    Menard, S. Standards for standardized logistic regression coefficients. Soc. Forces 89, 1409–1428 (2011).
    Google Scholar 
    Powers, D. M. Evaluation: from precision, recall and F-measure to ROC, informedness, markedness and correlation. Mach. Learn. Technol. 2, 37–63 (2011).
    Google Scholar 
    Pearce, J. & Ferrier, S. Evaluating the predictive performance of habitat models developed using logistic regression. Ecol. Model. 133, 225–245 (2000).
    Google Scholar  More

  • in

    Slaked lime improves growth, antioxidant capacity and reduces Cd accumulation of peanut (Arachis hypogaea L.) under Cd stress

    Soil pH, biomass and Cd content of peanutSoil pHFigure 1 shows that, in this study, application of slaked lime significantly increased soil pH in nearly all growth stages (p  C1200  > C900  > C600  > C300  > C0. Among the soil characteristics, soil pH is considered as an important index that impact Cd uptake by crops, since pH can obviously affect the speciation and solubility of Cd in soil liquids15. The use of slaked lime can neutralize excessive H+ concentrations in soil solutions and decrease Cd solubility33, but there were no observable differences among the different growth stages.Figure 1Effects of slaked lime application on soil pH values. The values are means (± SD) of three replicates. Bar groups with different capital letters indicate significant differences (p  More

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    Changes in trophic structure of an exploited fish community at the centennial scale are linked to fisheries and climate forces

    Kroodsma, D. A. et al. Tracking the global footprint of fisheries. Science 359, 904–908 (2018).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Luong, A. D., Dewulf, J. & De Laender, F. Quantifying the primary biotic resource use by fisheries: A global assessment. Sci. Total Environ. 719, 137352 (2020).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Pauly, D. How the global fish market contributes to human micronutrient deficiencies. Nature 574, 41–42 (2019).ADS 
    CAS 
    PubMed 

    Google Scholar 
    FAO. The State of World Fisheries and Aquaculture 2020 (FAO, 2020). https://doi.org/10.4060/ca9229en.Book 

    Google Scholar 
    Shin, Y.-J., Rochet, M.-J., Jennings, S., Field, J. G. & Gislason, H. Using size-based indicators to evaluate the ecosystem effects of fishing. ICES J. Mar. Sci. 62, 384–396 (2005).
    Google Scholar 
    Perry, A. L. Climate change and distribution shifts in marine fishes. Science 308, 1912–1915 (2005).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Novaglio, C., Smith, A. D. M., Frusher, S. & Ferretti, F. Identifying historical baseline at the onset of exploitation to improve understanding of fishing impacts. Aquat. Conserv. Mar. Freshwat. Ecosyst. 30, 475–485 (2020).
    Google Scholar 
    Nagelkerken, I. & Connell, S. D. Global alteration of ocean ecosystem functioning due to increasing human CO2 emissions. Proc. Natl. Acad. Sci. 112, 13272–13277 (2015).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Nagelkerken, I., Goldenberg, S. U., Ferreira, C. M., Ullah, H. & Connell, S. D. Trophic pyramids reorganize when food web architecture fails to adjust to ocean change. Science 832, 829–832 (2020).ADS 

    Google Scholar 
    Lemoine, N. P. & Burkepile, D. E. Temperature-induced mismatches between consumption and metabolism reduce consumer fitness. Ecology 93, 2483–2489 (2012).PubMed 

    Google Scholar 
    Scheffer, M., Carpenter, S., Foley, J. A., Folke, C. & Walker, B. Catastrophic shifts in ecosystems. Nature 413, 591–596 (2001).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Moore, J. K. et al. Sustained climate warming drives declining marine biological productivity. Science 359, 1139–1143 (2018).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Ullah, H., Nagelkerken, I., Goldenberg, S. U. & Fordham, D. A. Climate change could drive marine food web collapse through altered trophic flows and cyanobacterial proliferation. PLoS Biol. 16, e2003446 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    Wing, S. R., Durante, L. M., Connolly, A. J., Sabadel, A. J. M. & Wing, L. C. Overexploitation and decline in kelp forests inflate the bioenergetic costs of fisheries. Glob. Ecol. Biogeogr. https://doi.org/10.1111/geb.13448 (2021).Article 

    Google Scholar 
    Maureaud, A. et al. Global change in the trophic functioning of marine food webs. PLoS One 12, e0182826 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    Wernberg, T. et al. Climate-driven regime shift of a temperate marine ecosystem. Science 353, 169–172 (2016).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Pauly, D. Anecdotes and the shifting baseline syndrome of fisheries. Trends Ecol. Evol. 10, 430 (1995).CAS 
    PubMed 

    Google Scholar 
    Chown, S. L. Marine food webs destabilized. Science 369, 770–771 (2020).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Saporiti, F. et al. Longer and less overlapping food webs in anthropogenically disturbed marine ecosystems: Confirmations from the past. PLoS One 9, 1–13 (2014).
    Google Scholar 
    Gilby, B. L. et al. Human actions alter tidal marsh seascapes and the provision of ecosystem services. Estuaries Coasts https://doi.org/10.1007/s12237-020-00830-0 (2020).Article 

    Google Scholar 
    Halpern, B. S. et al. Recent pace of change in human impact on the world’s ocean. Sci. Rep. 9, 11609 (2019).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Durante, L. M., Beentjes, M. P. & Wing, S. R. Shifting trophic architecture of marine fisheries in New Zealand: Implications for guiding effective ecosystem-based management. Fish Fish. 21, 813–830 (2020).
    Google Scholar 
    Shears, N. T. & Bowen, M. M. Half a century of coastal temperature records reveal complex warming trends in western boundary currents. Sci. Rep. 7, 1–9 (2017).CAS 

    Google Scholar 
    Wing, S. R. & Wing, E. Prehistoric fisheries in the Caribbean. Coral Reefs 20, 1–8 (2001).
    Google Scholar 
    Halpern, B. S. et al. A global map of human impact on marine ecosystems. Science 319, 948–952 (2008).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Irwin, G. & Walrond, C. ‘When was New Zealand first settled?—Extinction and decline’. Te Ara—the Encyclopedia of New Zealand 8 (2016). http://www.teara.govt.nz/en/when-was-new-zealand-first-settled/page-7. Accessed 4 June 2019.Johnson, D. & Haworth, J. Hooked—The Sory of New Zealand Fishing Industry (Hazard Press, 2004).
    Google Scholar 
    Urlich, S. C. & Handley, S. J. From ‘clean and green’ to ‘brown and down’: A synthesis of historical changes to biodiversity and marine ecosystems in the Marlborough Sounds, New Zealand. Ocean Coast. Manage. 198, 105349 (2020).
    Google Scholar 
    Ramos, R. & González-Solís, J. Trace me if you can: The use of intrinsic biogeochemical markers in marine top predators. Front. Ecol. Environ. 10, 258–266 (2012).
    Google Scholar 
    Graham, D. H. Food of fishes of Otago Harbour and Adjacent Sea. R. Soc. N. Z. 20, 421–436 (1939).
    Google Scholar 
    Hanchet, S. Diet of spiny dogfish, Squalus acanthias Linnaeus, on the east coast, South Island, New Zealand. J. Fish Biol. 39, 313–323 (1991).
    Google Scholar 
    Connell, A., Dunn, M. & Forman, J. Diet and dietary variation of New Zealand hoki Macruronus novaezelandiae. NZ J. Mar. Freshw. Res. 44, 289–308 (2010).
    Google Scholar 
    Forman, J. & Dunn, M. The influence of ontogeny and environment on the diet of lookdown dory, Cyttus traversi. NZ J. Mar. Freshw. Res. 44, 329–342 (2010).
    Google Scholar 
    Horn, P. L., Forman, J. S. & Dunn, M. R. Dietary partitioning by two sympatric fish species, red cod (Pseudophycis bachus) and sea perch ( Helicolenus percoides), on Chatham Rise, New Zealand. Mar. Biol. Res. 8, 624–634 (2012).
    Google Scholar 
    Fisheries New Zealand. Fisheries Assessment Plenary, May 2020: Stock Assessments and Stock Status (2020).Ladds, M., Pinkerton, M. H., Jones, E., Durante, L. & Dunn, M. Relationship between morphometrics and trophic levels in deep-sea fishes. Mar. Ecol. Prog. Ser. 637, 225–235 (2020).ADS 

    Google Scholar 
    Durante, L. M. et al. Oceanographic transport along frontal zones forms carbon, nitrogen, and oxygen isoscapes on the east coast of New Zealand : Implications for ecological studies. Cont. Shelf Res. 216, 1–15 (2021).
    Google Scholar 
    Funes, M., Irigoyen, A. J., Trobbiani, G. A. & Galván, D. E. Stable isotopes reveal different dependencies on benthic and pelagic pathways between Munida gregaria ecotypes. Food Webs 17, 1–9 (2018).
    Google Scholar 
    Zeldis, J. R. & Jillett, J. B. Aggregation of pelagic Munida gregaria (Fabricius) (Decapoda, Anomura) by coastal fronts and internal waves. J. Plankton Res. 4, 839–857 (1982).
    Google Scholar 
    Durante, L. M., Beentjes, M. P. & Wing, S. R. Decadal changes in exploited fish communities and their relationship with temperature, fisheries exploitation, and ecological traits in New Zealand waters. NZ J. Mar. Freshw. Res. 10, 1–27 (2021).
    Google Scholar 
    Prugh, L. R. et al. The rise of the mesopredator. Bioscience 59, 779–791 (2009).
    Google Scholar 
    Chiswell, S. M. & Sutton, P. J. H. Relationships between long-term ocean warming, marine heat waves and primary production in the New Zealand region. NZ J. Mar. Freshw. Res. https://doi.org/10.1080/00288330.2020.1713181 (2020).Article 

    Google Scholar 
    Thomsen, M. S. et al. Local extinction of bull kelp (Durvillaea spp.) due to a marine heatwave. Front. Mar. Sci. 6, 1–10 (2019).
    Google Scholar 
    Pinkerton, M. H. et al. Changes to the food-web of the Hauraki Gulf during the period of human occupation: A mass-balance model approach. New Zealand Aquatic Environment and Biodiversity Report No. 160. (2015).Garrison, L. Fishing effects on spatial distribution and trophic guild structure of the fish community in the Georges Bank region. ICES J. Mar. Sci. 57, 723–730 (2000).
    Google Scholar 
    Link, J. S. & Garrison, L. P. Changes in piscivory associated with fishing induced changes to the finfish community on Georges Bank. Fish. Res. 55, 71–86 (2002).
    Google Scholar 
    Wainright, S. C., Fogarty, M. J., Greenfield, R. C. & Fry, B. Long-term changes in the Georges Bank food web: Trends in stable isotopic compositions of fish scales. Mar. Biol. 115, 481–493 (1993).
    Google Scholar 
    Udy, J. A. et al. Regional differences in supply of organic matter from kelp forests drive trophodynamics of temperate reef fish. Mar. Ecol. Prog. Ser. 621, 19–32 (2019).ADS 

    Google Scholar 
    Koenigs, C., Miller, R. & Page, H. Top predators rely on carbon derived from giant kelp Macrocystis pyrifera. Mar. Ecol. Prog. Ser. 537, 1–8 (2015).ADS 
    CAS 

    Google Scholar 
    Clark, M. R., Anderson, O. F., Chris Francis, R. I. C. & Tracey, D. M. The effects of commercial exploitation on orange roughy (Hoplostethus atlanticus) from the continental slope of the Chatham Rise, New Zealand, from 1979 to 1997. Fish. Res. 45, 217–238 (2000).
    Google Scholar 
    Fenaughty, J. M. & Bagley, N. M. WJ Scott New Zealand Trawling Survey—South Island East Coast. Technical Report 157. (1981).Brodeur, R. & Pearcy, W. Effects of environmental variability on trophic interactions and food web structure in a pelagic upwelling ecosystem. Mar. Ecol. Prog. Ser. 84, 101–119 (1992).ADS 

    Google Scholar 
    Tam, J., Purca, S., Duarte, L. O., Blaskovic, V. & Espinoza, P. Changes in the diet of hake associated with El Niño 1997–1998 in the northern Humboldt Current ecosystem. Adv. Geosci. 6, 63–67 (2006).
    Google Scholar 
    Murphy, R. J., Pinkerton, M. H., Richardson, K. M., Bradford-Grieve, J. M. & Boyd, P. W. Phytoplankton distributions around New Zealand derived from SeaWiFS remotely-sensed ocean colour data. NZ J. Mar. Freshw. Res. 35, 343–362 (2001).
    Google Scholar 
    Zeldis, J. Ecology of Munida gregaria (Decapoda, Anomura) distribution and abundance, population dynamics and fisheries. Mar. Ecol. Prog. Ser. 22, 77–99 (1985).ADS 

    Google Scholar 
    Williams, B. G. The effect of the environment on the morphology of Munida Gregaria (Fabricius) (Decapoda, Anomura). Crustaceana 24, 197–210 (1973).
    Google Scholar 
    Myers, R. A., Baum, J. K., Shepherd, T. D., Powers, S. P. & Peterson, C. H. Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 315, 1846–1850 (2007).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Udy, J. A. et al. Organic matter derived from kelp supports a large proportion of biomass in temperate rocky reef fish communities: Implications for ecosystem-based management. Aquat. Conserv. Mar. Freshw. Ecosyst. 29, 1503–1519 (2019).
    Google Scholar 
    Jackson, J. B. C. Historical overfishing and the recent collapse of coastal ecosystems. Science 293, 629–637 (2001).CAS 
    PubMed 

    Google Scholar 
    Kirby, R. R., Beaugrand, G. & Lindley, J. A. Synergistic effects of climate and fishing in a marine ecosystem. Ecosystems 12, 548–561 (2009).
    Google Scholar 
    MacGibbon, D. J., Beentjes, M. P., Lyon, W. L. & Ladroit, Y. Inshore trawl survey of Canterbury Bight and Pegasus Bay, April–June 2018 (KAH1803). New Zealand Fisheries Assessment Report 2019/03. (2019).Stevens, W. D., O’Driscoll, R. L., Ballara, S. L. & Schimel, A. C. G. Trawl survey of hoki and middle-depth species on the Chatham Rise, January 2018 (TAN1801). New Zealand Fisheries Assessment Report 2018/41. (2018).Durante, L. M., Sabadel, A. J. M., Frew, R. D., Ingram, T. & Wing, S. R. Effects of fixatives on stable isotopes of fish muscle tissue: Implications for trophic studies on preserved specimens. Ecol. Appl. 30, 1–16 (2020).
    Google Scholar 
    Post, D. M. Using stable isotopes to estimate trophic position: Models, methods, and assumptions. Ecology 83, 703–718 (2002).
    Google Scholar 
    Post, D. M. et al. Getting to the fat of the matter: Models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152, 179–189 (2007).ADS 
    PubMed 

    Google Scholar 
    Verburg, P. The need to correct for the Suess effect in the application of δ13C in sediment of autotrophic Lake Tanganyika, as a productivity proxy in the Anthropocene. J. Paleolimnol. 37, 591–602 (2007).ADS 

    Google Scholar 
    Keeling, C. D. The Suess effect: 13Carbon-14Carbon interrelations. Environ. Int. 2, 229–300 (1979).CAS 

    Google Scholar 
    Sabadel, A., Durante, L. & Wing, S. Stable isotopes of amino acids from reef fishes uncover Suess and nitrogen enrichment effects on local ecosystems. Mar. Ecol. Prog. Ser. 647, 149–160 (2020).ADS 
    CAS 

    Google Scholar 
    Eide, M., Olsen, A., Ninnemann, U. S. & Eldevik, T. A global estimate of the full oceanic 13C Suess effect since the preindustrial. Glob. Biogeochem. Cycles 31, 492–514 (2017).ADS 
    CAS 

    Google Scholar 
    McMahon, K. W. & McCarthy, M. D. Embracing variability in amino acid δ15N fractionation: Mechanisms, implications, and applications for trophic ecology. Ecosphere 7, 1–26 (2016).
    Google Scholar 
    Chikaraishi, Y. et al. Determination of aquatic food-web structure based on compound-specific nitrogen isotopic composition of amino acids. Limnol. Oceanogr. Methods 7, 740–750 (2009).CAS 

    Google Scholar 
    Whiteman, J. P., Smith, E. A. E., Besser, A. C. & Newsome, S. D. A guide to using compound-specific stable isotope analysis to study the fates of molecules in organisms and ecosystems. Diversity 11, 1–18 (2019).
    Google Scholar 
    Hilton, G. M. et al. A stable isotopic investigation into the causes of decline in a sub-Antarctic predator, the rockhopper penguin. Glob. Change Biol. 12, 611–625 (2006).ADS 

    Google Scholar 
    Lorrain, A. et al. Nitrogen and carbon isotope values of individual amino acids: A tool to study foraging ecology of penguins in the Southern Ocean. Mar. Ecol. Prog. Ser. 391, 293–306 (2009).ADS 
    CAS 

    Google Scholar 
    Quillfeldt, P. & Masello, J. F. Compound-specific stable isotope analyses in Falkland Islands seabirds reveal seasonal changes in trophic positions. BMC Ecol. 20, 1–12 (2020).
    Google Scholar 
    Sabadel, A. J. M., Woodward, E. M. S., Van Hale, R. & Frew, R. D. Compound-specific isotope analysis of amino acids: A tool to unravel complex symbiotic trophic relationships. Food Webs 6, 9–18 (2016).
    Google Scholar 
    Styring, A. K. et al. Practical considerations in the determination of compound-specific amino acid δ15N values in animal and plant tissues by gas chromatography-combustion-isotope ratio mass spectrometry, following derivatisation to their N-acetylisopropyl e. Rapid Commun. Mass Spectrom. 26, 2328–2334 (2012).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Coplen, T. B. Guidelines and recommended terms for expression of stable-isotope-ratio and gas-ratio measurement results. Rapid Commun. Mass Spectrom. 25, 2538–2560 (2011).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Phillips, D. L. & Gregg, J. W. J. W. Uncertainty in source partitioning using stable isotopes. Oecologia 127, 171–179 (2001).ADS 
    PubMed 

    Google Scholar 
    Jack, L. & Wing, S. R. Individual variability in trophic position and diet of a marine omnivore is linked to kelp bed habitat. Mar. Ecol. Prog. Ser. 443, 129–139 (2011).ADS 
    CAS 

    Google Scholar 
    McCutchan, J. H., Lewis, W. M., Kendall, C. & McGrath, C. C. Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102, 378–390 (2003).CAS 

    Google Scholar 
    Hussey, N. E. et al. Rescaling the trophic structure of marine food webs. Ecol. Lett. 17, 239–250 (2014).PubMed 

    Google Scholar 
    McMahon, K. W., Thorrold, S. R., Elsdon, T. S. & Mccarthy, M. D. Trophic discrimination of nitrogen stable isotopes in amino acids varies with diet quality in a marine fish. Limnol. Oceanogr. 60, 1076–1087 (2015).ADS 
    CAS 

    Google Scholar 
    Jackson, A. L., Inger, R., Parnell, A. C. & Bearhop, S. Comparing isotopic niche widths among and within communities: SIBER—Stable Isotope Bayesian Ellipses in R. J. Anim. Ecol. 80, 595–602 (2011).PubMed 

    Google Scholar 
    Layman, C. A., Arrington, D. A., Montaña, C. G. & Post, D. M. Can stable isotope ratios provide for community-wide measures of trophic structure?. Ecology 88, 42–48 (2007).PubMed 

    Google Scholar 
    Wold, S., Sjöström, M. & Eriksson, L. PLS-regression: A basic tool of chemometrics. Chemom. Intell. Lab. Syst. 58, 109–130 (2001).CAS 

    Google Scholar 
    Anderson, M., Gorley, R. N. & Clarke, K. R. PERMANOVA + for PRIMER: Guide to Software and Statistical Methods. 1, 1:218 (2008).Mullan, A. Influence of Southern Oscillation on New Zealand Weather. In Proceedings of Western Pacific International Meeting and Workshop on TOGA-COARE (1996).Francis, M. P., Hurst, R. J., McArdle, B. H., Bagley, N. W. & Anderson, O. F. New Zealand demersal fish assemblages. Environ. Biol. Fishes 65, 215–234 (2002).
    Google Scholar 
    Beentjes, M. P., Bull, B., Hurst, R. J. & Bagley, N. W. Demersal fish assemblages along the continental shelf and upper slope of the east coast of the South Island, New Zealand. NZ J. Mar. Freshw. Res. 36, 197–223 (2002).
    Google Scholar 
    R Core Team. R: A Language and Environment for Statistical Computing. (2020).SAS Institute. JMP. (2018).Clarke, K. R. & Gorley, R. N. PRIMER v6: User Manual/Tutorial. (PRIMER-E, 2006). More

  • in

    Mild chronic exposure to pesticides alters physiological markers of honey bee health without perturbing the core gut microbiota

    European Commission. Report from the commission to the European Parliament and the council on the implementation of the measures concerning the apiculture sector of Regulation (EU) No 1308/2013 of the European Parliament and of the Council establishing a common organisation of the markets in agricultural products. p. 1–16. https://eur-lex.europa.eu/legal-content/en/ALL/?uri=CELEX:52016DC0776 (2016).Motta, E. V. S. & Moran, N. A. Impact of glyphosate on the honey bee gut microbiota: Effects of intensity, duration, and timing of exposure. msystems 5, e00268-e1220. https://doi.org/10.1128/mSystems.00268-20 (2020).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Klein, A. M. et al. Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. B-Biol. Sci. 274, 303–313. https://doi.org/10.1098/rspb.2006.3721 (2007).Article 

    Google Scholar 
    Ollerton, J. Pollinator diversity: Distribution, ecological function, and conservation. Annu. Rev. Ecol. Evol. Syst. 48, 353–376. https://doi.org/10.1146/annurev-ecolsys-110316-022919 (2017).Article 

    Google Scholar 
    Greenleaf, S. S. & Kremen, C. Wild bees enhance honey bees’ pollination of hybrid sunflower. PNAS 103, 13890–13895. https://doi.org/10.1073/pnas.0600929103 (2006).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Williams, I. H. The dependence of crop production within the European Union on pollination by honey bees. Agric. Zool. Rev. 20, 20 (1994).
    Google Scholar 
    Potts, S. G. et al. Declines of managed honey bees and beekeepers in Europe. J. Apic. Res. 49, 15–22. https://doi.org/10.3896/ibra.1.49.1.02 (2010).Article 

    Google Scholar 
    Vanengelsdorp, D., Hayes, J., Underwood, R. M. & Pettis, J. A survey of honey bee colony losses in the US, fall 2007 to spring 2008. PLoS One 3, 6. https://doi.org/10.1371/journal.pone.0004071 (2008).CAS 
    Article 

    Google Scholar 
    Chagnon, M. Fédération Canadienne de la Faune (Bureau régional du Québec, 2008).
    Google Scholar 
    Schreinemachers, P. & Tipraqsa, P. Agricultural pesticides and land use intensification in high, middle and low income countries. Food Policy 37, 616–626. https://doi.org/10.1016/j.foodpol.2012.06.003 (2012).Article 

    Google Scholar 
    Haber, A. I., Steinhauer, N. A. & vanEngelsdorp, D. Use of chemical and nonchemical methods for the control of Varroa destructor (Acari: Varroidae) and associated winter colony losses in US beekeeping operations. J. Econ. Entomol. https://doi.org/10.1093/jee/toz088 (2019).Article 
    PubMed 

    Google Scholar 
    Le Conte, Y., Ellis, M. & Ritter, W. Varroa mites and honey bee health: Can Varroa explain part of the colony losses?. Apidologie 41, 353–363. https://doi.org/10.1051/apido/2010017 (2010).Article 

    Google Scholar 
    Ellis, J. D., Evans, J. D. & Pettis, J. Colony losses, managed colony population decline, and colony collapse disorder in the United States. J. Apic. Res. 49, 134–136. https://doi.org/10.3896/IBRA.1.49.1.30 (2010).Article 

    Google Scholar 
    Chauzat, M. P. et al. Influence of pesticide residues on honey bee (Hymenoptera: Apidae) colony health in France. Environ. Entomol 38, 514–523. https://doi.org/10.1603/022.038.0302 (2009).CAS 
    Article 
    PubMed 

    Google Scholar 
    Juan-Borras, M., Domenech, E. & Escriche, I. Mixture-risk-assessment of pesticide residues in retail polyfloral honey. Food Control 67, 127–134. https://doi.org/10.1016/j.foodcont.2016.02.051 (2016).CAS 
    Article 

    Google Scholar 
    Kasiotis, K. M., Anagnostopoulos, C., Anastasiadou, P. & Machera, K. Pesticide residues in honeybees, honey and bee pollen by LC–MS/MS screening: Reported death incidents in honeybees. Sci. Total. Environ 485–486, 633–642. https://doi.org/10.1016/j.scitotenv.2014.03.042 (2014).CAS 
    Article 
    PubMed 

    Google Scholar 
    Mullin, C. A. et al. High levels of miticides and agrochemicals in north american apiaries: Implications for honey bee health. PLoS One 5, 19. https://doi.org/10.1371/journal.pone.0009754 (2010).CAS 
    Article 

    Google Scholar 
    Brandt, A., Gorenflo, A., Siede, R., Meixner, M. & Buchler, R. The neonicotinoids thiacloprid, imidacloprid, and clothianidin affect the immunocompetence of honey bees (Apis mellifera L.). J. Insect. Physiol. 86, 40–47. https://doi.org/10.1016/j.jinsphys.2016.01.001 (2016).CAS 
    Article 
    PubMed 

    Google Scholar 
    Alptekin, S. et al. Induced thiacloprid insensitivity in honeybees (Apis mellifera L.) is associated with up-regulation of detoxification genes. Insect Mol. Biol. 25, 171–180. https://doi.org/10.1111/imb.12211 (2016).CAS 
    Article 
    PubMed 

    Google Scholar 
    Tesovnik, T. et al. Exposure of honey bee larvae to thiamethoxam and its interaction with Nosema ceranae infection in adult honey bees. Environ. Pollut. 256, 113443. https://doi.org/10.1016/j.envpol.2019.113443 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    Gregore, A. et al. Effects of coumaphos and imidacloprid on honey bee (Hymenoptera: Apidae) lifespan and antioxidant gene regulations in laboratory experiments. Sci. Rep. https://doi.org/10.1038/s41598-018-33348-4 (2018).Article 

    Google Scholar 
    Schneider, C. W., Tautz, J., Grunewald, B. & Fuchs, S. RFID tracking of sublethal effects of two neonicotinoid insecticides on the foraging behavior of Apis mellifera. PLoS One 7, 9. https://doi.org/10.1371/journal.pone.0030023 (2012).CAS 
    Article 

    Google Scholar 
    Vazquez, D. E., Ilina, N., Pagano, E. A., Zavala, J. A. & Farina, W. M. Glyphosate affects the larval development of honey bees depending on the susceptibility of colonies. PLoS One https://doi.org/10.1371/journal.pone.0205074 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Vázquez, D. E., Latorre-Estivalis, J. M., Ons, S. & Farina, W. M. Chronic exposure to glyphosate induces transcriptional changes in honey bee larva: A toxicogenomic study. Environ. Pollut. https://doi.org/10.1016/j.envpol.2020.114148 (2020).Article 
    PubMed 

    Google Scholar 
    Farina, W. M., Balbuena, M., Herbert, L. T., Mengoni Goñalons, C. & Vázquez, D. E. Effects of the herbicide glyphosate on honey bee sensory and cognitive abilities: Individual impairments with implications for the hive. Insects 10, 354. https://doi.org/10.3390/insects10100354 (2019).Article 
    PubMed Central 

    Google Scholar 
    Wang, Y. H., Zhu, Y. C. & Li, W. H. Interaction patterns and combined toxic effects of acetamiprid in combination with seven pesticides on honey bee (Apis mellifera L.). Ecotox. Environ. Safe 190, 10. https://doi.org/10.1016/j.ecoenv.2019.110100 (2020).CAS 
    Article 

    Google Scholar 
    Kretschmann, A., Gottardi, M., Dalhoff, K. & Cedergreen, N. The synergistic potential of the azole fungicides prochloraz and propiconazole toward a short α-cypermethrin pulse increases over time in Daphnia magna. Aquat. Toxicol. 162, 94–101. https://doi.org/10.1016/j.aquatox.2015.02.011 (2015).CAS 
    Article 
    PubMed 

    Google Scholar 
    Yuan, X. et al. Gut microbiota: An underestimated and unintended recipient for pesticide-induced toxicity. Chemosphere https://doi.org/10.1016/j.chemosphere.2019.04.088 (2019).Article 
    PubMed 

    Google Scholar 
    Yang, Y. et al. Effects of three common pesticides on survival, food consumption and midgut bacterial communities of adult workers Apis cerana and Apis mellifera. Environ. Pollut. 249, 860–867. https://doi.org/10.1016/j.envpol.2019.03.077 (2019).CAS 
    Article 
    PubMed 

    Google Scholar 
    Martinson, V. G. et al. A simple and distinctive microbiota associated with honey bees and bumble bees. Mol. Ecol. 20, 619–628. https://doi.org/10.1111/j.1365-294X.2010.04959.x (2011).Article 
    PubMed 

    Google Scholar 
    Corby-Harris, V., Maes, P. & Anderson, K. E. The bacterial communities associated with honey bee (Apis mellifera) foragers. PLoS One 9, 13. https://doi.org/10.1371/journal.pone.0095056 (2014).CAS 
    Article 

    Google Scholar 
    Moran, N. A., Hansen, A. K., Powell, J. E. & Sabree, Z. L. Distinctive gut microbiota of honey bees assessed using deep sampling from individual worker bees. PLoS One https://doi.org/10.1371/journal.pone.0036393 (2012).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Bonilla-Rosso, G. & Engel, P. Functional roles and metabolic niches in the honey bee gut microbiota. Curr. Opin. Microbiol. 43, 69–76. https://doi.org/10.1016/j.mib.2017.12.009 (2018).CAS 
    Article 
    PubMed 

    Google Scholar 
    Kwong, W. K. & Moran, N. A. Gut microbial communities of social bees. Nat. Rev. Microbiol. 14, 374–384. https://doi.org/10.1038/nrmicro.2016.43 (2016).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Kešnerová, L. et al. Gut microbiota structure differs between honeybees in winter and summer. ISME J. 14, 801–814. https://doi.org/10.1038/s41396-019-0568-8 (2020).Article 
    PubMed 

    Google Scholar 
    Killer, J., Dubná, S., Sedláček, I. & Švec, P. Lactobacillus apis sp. Nov., from the stomach of honeybees (Apis mellifera), having an in vitro inhibitory effect on the causative agents of American and European foulbrood. Int. J. Syst. Evol. Microbiol. 64, 152–157. https://doi.org/10.1099/ijs.0.053033-0 (2014).CAS 
    Article 
    PubMed 

    Google Scholar 
    Forsgren, E., Olofsson, T. C., Váasquez, A. & Fries, I. Novel lactic acid bacteria inhibiting Paenibacillus larvae in honey bee larvae. Apidologie 41, 99–108. https://doi.org/10.1051/apido/2009065 (2010).Article 

    Google Scholar 
    Schwarz, R. S., Huang, Q. & Evans, J. D. Hologenome theory and the honey bee pathosphere. Curr. Opin. Insect Sci. 10, 1–7. https://doi.org/10.1016/j.cois.2015.04.006 (2015).Article 
    PubMed 

    Google Scholar 
    Engel, P., Martinson, V. G. & Moran, N. A. Functional diversity within the simple gut microbiota of the honey bee. PNAS 109, 11002–11007. https://doi.org/10.1073/pnas.1202970109 (2012).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Kešnerová, L. et al. Disentangling metabolic functions of bacteria in the honey bee gut. PLoS Biol. 15, 28. https://doi.org/10.1371/journal.pbio.2003467 (2017).CAS 
    Article 

    Google Scholar 
    Kwong, W. K., Engel, P., Koch, H. & Moran, N. A. Genomics and host specialization of honey bee and bumble bee gut symbionts. PNAS 111, 11509–11514. https://doi.org/10.1073/pnas.1405838111 (2014).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Lee, F. J., Rusch, D. B., Stewart, F. J., Mattila, H. R. & Newton, I. L. G. Saccharide breakdown and fermentation by the honey bee gut microbiome. Environ. Microbiol. 17, 796–815. https://doi.org/10.1111/1462-2920.12526 (2015).CAS 
    Article 
    PubMed 

    Google Scholar 
    Motta, E. V. S., Raymann, K. & Moran, N. A. Glyphosate perturbs the gut microbiota of honey bees. PNAS 115, 10305–10310. https://doi.org/10.1073/pnas.1803880115 (2018).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Blot, N., Veillat, L., Rouze, R. & Delatte, H. Glyphosate, but not its metabolite AMPA, alters the honeybee gut microbiota. PLoS One 14, 16. https://doi.org/10.1371/journal.pone.0215466 (2019).CAS 
    Article 

    Google Scholar 
    Raymann, K. et al. Imidacloprid decreases honey bee survival rates but does not affect the gut microbiome. Appl. Environ. Microbiol. 84, 13. https://doi.org/10.1128/aem.00545-18 (2018).CAS 
    Article 

    Google Scholar 
    Rouze, R., Mone, A., Delbac, F., Belzunces, L. & Blot, N. The honeybee gut microbiota is altered after chronic exposure to different families of insecticides and infection by Nosema ceranae. Microbes Environ. 34, 226–233. https://doi.org/10.1264/jsme2.ME18169 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    DeGrandi-Hoffman, G., Corby-Harris, V., DeJong, E. W., Chambers, M. & Hidalgo, G. Honey bee gut microbial communities are robust to the fungicide PristineA (R) consumed in pollen. Apidologie 48, 340–352. https://doi.org/10.1007/s13592-016-0478-y (2017).CAS 
    Article 

    Google Scholar 
    Liu, Y. J. et al. Thiacloprid exposure perturbs the gut microbiota and reduces the survival status in honeybees. J. Hazard. Mater. 389, 11. https://doi.org/10.1016/j.jhazmat.2019.121818 (2020).CAS 
    Article 

    Google Scholar 
    Syromyatnikov, M. Y., Isuwa, M. M., Savinkova, O. V., Derevshchikova, M. I. & Popov, V. N. The effect of pesticides on the microbiome of animals. Agriculture 10, 79. https://doi.org/10.3390/agriculture10030079 (2020).CAS 
    Article 

    Google Scholar 
    Thompson, H. M. et al. Evaluating exposure and potential effects on honeybee brood (Apis mellifera) development using glyphosate as an example. Integr. Environ. Assess. Manag. 10, 463–470. https://doi.org/10.1002/ieam.1529 (2014).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Motta, E. V. S. et al. Oral and topical exposure to glyphosate in herbicide formulation impact the gut microbiota and survival rates of honey bees. Appl. Environ. Microbiol. https://doi.org/10.1128/AEM.01150-20 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Berg, C. J. et al. Glyphosate residue concentrations in honey attributed through geospatial analysis to proximity of large-scale agriculture and transfer off-site by bees. PLoS ONE 13, e0198876. https://doi.org/10.1371/journal.pone.0198876 (2018).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Rubio, F., Guo, E. & Kamp, L. Survey of glyphosate residues in honey, corn, and soy products. Abstr. Pap. Am. Chem. Soc. https://doi.org/10.4172/2161-0525.1000249 (2015).Article 

    Google Scholar 
    El Agrebi, N. et al. Honeybee and consumer’s exposure and risk characterisation to glyphosate-based herbicide (GBH) and its degradation product (AMPA): Residues in beebread, wax, and honey. Sci. Total. Environ. 704, 135312. https://doi.org/10.1016/j.scitotenv.2019.135312 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    Kubik, M. et al. Residues of captan (contact) and difenoconazole (systemic) fungicides in bee products from an apple orchard. Apidologie 31, 531–541 (2000).CAS 
    Article 

    Google Scholar 
    Lopez, S. H., Lozano, A., Sosa, A., Hernando, M. D. & Fernandez-Alba, A. R. Screening of pesticide residues in honeybee wax comb by LC-ESI-MS/MS. A pilot study. Chemosphere 163, 44–53. https://doi.org/10.1016/j.chemosphere.2016.07.008 (2016).CAS 
    Article 

    Google Scholar 
    Pettis, J. S. et al. Crop pollination exposes honey bees to pesticides which alters their susceptibility to the gut pathogen Nosema ceranae. PLoS One 8, 9. https://doi.org/10.1371/journal.pone.0070182 (2013).CAS 
    Article 

    Google Scholar 
    Abdallah, O. I., Hanafi, A., Ghani, S. B. A., Ghisoni, S. & Lucini, L. Pesticides contamination in Egyptian honey samples. J. Consum. Prot. Food Sci. 12, 317–327. https://doi.org/10.1007/s00003-017-1133-x (2017).CAS 
    Article 

    Google Scholar 
    Blaga, G. V. et al. Antifungal residues analysis in various Romanian honey samples analysis by high resolution mass spectrometry. J. Environ. Sci. Health Part B-Pestic. Contam. Agric. Wastes https://doi.org/10.1080/03601234.2020.1724016 (2020).Article 

    Google Scholar 
    Piechowicz, B., Wos, I., Podbielska, M. & Grodzicki, P. The transfer of active ingredients of insecticides and fungicides from an orchard to beehives. J. Environ. Sci. Health Part B-Pestic. Contam. Agric. Wastes 53, 18–24. https://doi.org/10.1080/03601234.2017.1369320 (2018).CAS 
    Article 

    Google Scholar 
    Almasri, H. et al. Mixtures of an insecticide, a fungicide and a herbicide induce high toxicities and systemic physiological disturbances in winter Apis mellifera honey bees. Ecotoxicol. Environ. Saf. 203, 111013. https://doi.org/10.1016/j.ecoenv.2020.111013 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    Babendreier, D., Joller, D., Romeis, J., Bigler, F. & Widmer, F. Bacterial community structures in honeybee intestines and their response to two insecticidal proteins. FEMS Microbiol. Ecol. 59, 600–610. https://doi.org/10.1111/j.1574-6941.2006.00249.x (2007).CAS 
    Article 
    PubMed 

    Google Scholar 
    Emery, O., Schmidt, K. & Engel, P. Immune system stimulation by the gut symbiont Frischella perrara in the honey bee (Apis mellifera). Mol. Ecol. 26, 2576–2590. https://doi.org/10.1111/mec.14058 (2017).CAS 
    Article 
    PubMed 

    Google Scholar 
    Yanez, O., Gauthier, L., Chantawannakul, P. & Neumann, P. Endosymbiotic bacteria in honey bees: Arsenophonus spp. are not transmitted transovarially. FEMS Microbiol. Lett. https://doi.org/10.1093/femsle/fnw147 (2016).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Tornisielo, V. L., Botelho, R. G., Alves, P. A. T., Bonfleur, E. J. & Monteiro, S. H. Pesticide tank mixes: an environmental point of view. in Herbicides-Current Research and Case Studies in Use. 473–487 (InTech, 2013).

    Google Scholar 
    Kanga, L. H., Siebert, S. C., Sheikh, M. & Legaspi, J. C. Pesticide residues in conventionally and organically managed Apiaries in South and North Florida. Curre. Investig. Agric. Curr. Res. https://doi.org/10.32474/CIACR.2019.07.000262 (2019).Article 

    Google Scholar 
    Lambert, O. et al. Widespread occurrence of chemical residues in beehive matrices from apiaries located in different landscapes of western France. PLoS One 8, 12. https://doi.org/10.1371/journal.pone.0067007 (2013).CAS 
    Article 

    Google Scholar 
    Mullins, J. W. Pest Control with Enhanced Environmental Safety, Vol 524 ACS Symposium Series, Vol. 13 183–198 (American Chemical Society, 1993).Book 

    Google Scholar 
    Nguyen, B. K. et al. Does imidacloprid seed-treated maize have an impact on honey bee mortality?. J. Econ. Entomol. 102, 616–623. https://doi.org/10.1603/029.102.0220 (2009).CAS 
    Article 
    PubMed 

    Google Scholar 
    Pollak, P. Fine chemicals–the industry and the business. Chem. Int. 29, 22. https://doi.org/10.1515/ci.2007.29.5.22b (2007).Article 

    Google Scholar 
    Amrhein, N., Deus, B., Gehrke, P. & Steinrücken, H. C. The site of the inhibition of the shikimate pathway by glyphosate. II. Interference of glyphosate with chorismate formation in vivo and in vitro. Plant. Physiol. 66, 830–834. https://doi.org/10.1104/pp.66.5.830 (1980).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Cao, G. et al. A novel 5-enolpyruvylshikimate-3-phosphate synthase shows high glyphosate tolerance in Escherichia coli and tobacco plants. PLoS One 7, e38718. https://doi.org/10.1371/journal.pone.0038718 (2012).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Hitchcock, C. A., Dickinson, K., Brown, S. B., Evans, E. G. V. & Adams, D. J. Interaction of azole antifungal antibiotics with cytochrome P-450-dependent 14α-sterol demethylase purified from Candida albicans. Biochem. J. 266, 475–480. https://doi.org/10.1042/bj2660475 (1990).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Alberoni, D., Favaro, R., Baffoni, L., Angeli, S. & Di Gioia, D. Neonicotinoids in the agroecosystem: In-field long-term assessment on honeybee colony strength and microbiome. Sci. Total Environ. https://doi.org/10.1016/j.scitotenv.2020.144116 (2021).Article 
    PubMed 

    Google Scholar 
    Xu, C. et al. Changes in gut microbiota may be early signs of liver toxicity induced by epoxiconazole in rats. Chemotherapy 60, 135–142. https://doi.org/10.1159/000371837 (2014).CAS 
    Article 
    PubMed 

    Google Scholar 
    Yang, C., Hamel, C., Vujanovic, V. & Gan, Y. Fungicide: Modes of action and possible impact on nontarget microorganisms. ISRN Ecol. https://doi.org/10.5402/2011/130289 (2011).Article 

    Google Scholar 
    Coupe, R. H., Kalkhoff, S. J., Capel, P. D. & Gregoire, C. Fate and transport of glyphosate and aminomethylphosphonic acid in surface waters of agricultural basins. Pest Manag. Sci. 68, 16–30. https://doi.org/10.1002/ps.2212 (2012).CAS 
    Article 
    PubMed 

    Google Scholar 
    Howe, C. M. et al. Toxicity of glyphosate-based pesticides to four North American frog species. Environ. Toxicol. Chem. 23, 1928–1938. https://doi.org/10.1002/etc.2268 (2004).CAS 
    Article 
    PubMed 

    Google Scholar 
    Wagner, N., Reichenbecher, W., Teichmann, H., Tappeser, B. & Lötters, S. Questions concerning the potential impact of glyphosate-based herbicides on amphibians. Environ. Toxicol. Chem. 32, 1688–1700. https://doi.org/10.1002/etc.2268 (2013).CAS 
    Article 
    PubMed 

    Google Scholar 
    Pareja, L. et al. Evaluation of glyphosate and AMPA in honey by water extraction followed by ion chromatography mass spectrometry. A pilot monitoring study. Anal. Methods 11, 2123–2128. https://doi.org/10.1039/c9ay00543a (2019).CAS 
    Article 

    Google Scholar 
    Thompson, T. S., van den Heever, J. P. & Limanowka, R. E. Determination of glyphosate, AMPA, and glufosinate in honey by online solid-phase extraction-liquid chromatography-tandem mass spectrometry.. Food. Addit. Contam. Part A Chem. Anal. Control. Expo. Risk. Assess 36, 434–446. https://doi.org/10.1080/19440049.2019.1577993 (2019).CAS 
    Article 
    PubMed 

    Google Scholar 
    Dai, P. et al. The herbicide glyphosate negatively affects midgut bacterial communities and survival of honey bee during larvae reared in vitro. J. Agric. Food Chem. 66, 7786–7793. https://doi.org/10.1021/acs.jafc.8b02212 (2018).CAS 
    Article 
    PubMed 

    Google Scholar 
    Zheng, H., Powell, J. E., Steele, M. I., Dietrich, C. & Moran, N. A. Honeybee gut microbiota promotes host weight gain via bacterial metabolism and hormonal signaling. PNAS 114, 4775–4780. https://doi.org/10.1073/pnas.1701819114 (2017).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    du Rand, E. E. et al. Detoxification mechanisms of honey bees (Apis mellifera) resulting in tolerance of dietary nicotine. Sci. Rep. https://doi.org/10.1038/srep11779 (2015).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Xiao, W. J. et al. Modulation of the pentose phosphate pathway alters phase I metabolism of testosterone and dextromethorphan in HepG2 cells. Acta Pharmacol. Sin. 36, 259–267. https://doi.org/10.1038/aps.2014.137 (2015).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Renzi, M. T. et al. Chronic toxicity and physiological changes induced in the honey bee by the exposure to fipronil and Bacillus thuringiensis spores alone or combined. Ecotox. Environ. Safe. 127, 205–213. https://doi.org/10.1016/j.ecoenv.2016.01.028 (2016).CAS 
    Article 

    Google Scholar 
    Singh, A., Gupta, V., Siddiqi, N., Tiwari, S. & Gopesh, A. Time course studies on impact of low temperature exposure on the levels of protein and enzymes in fifth instar larvae of Eri Silkworm, Philosamia ricini (Lepidoptera: satuniidae). Biochem. Anal. Biochem. 6, 6. https://doi.org/10.4172/2161-1009.1000321 (2017).CAS 
    Article 

    Google Scholar 
    Vlahović, M., Lazarević, J., Perić-Mataruga, V., Ilijin, L. & Mrdaković, M. Plastic responses of larval mass and alkaline phosphatase to cadmium in the gypsy moth larvae. Ecotox. Environ. Safe 72, 1148–1155. https://doi.org/10.1016/j.ecoenv.2008.03.012 (2009).CAS 
    Article 

    Google Scholar 
    Coleman, J. E. Structure and mechanism of alkaline-phosphatase. Annu. Rev. Biophys. Biomol. Struct. 21, 441–483. https://doi.org/10.1146/annurev.bb.21.060192.002301 (1992).CAS 
    Article 
    PubMed 

    Google Scholar 
    Bates, J. M., Akerlund, J., Mittge, E. & Guillemin, K. Intestinal alkaline phosphatase detoxifies lipopolysaccharide and prevents inflammation in zebrafish in response to the gut microbiota. Cell Host Microbe 2, 371–382. https://doi.org/10.1016/j.chom.2007.10.010 (2007).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Kanost, M. R. & Gorman, M. J. Phenoloxidases in insect immunity. Insect Immunol. 1, 69–96. https://doi.org/10.1016/B978-012373976-6.50006-9 (2008).Article 

    Google Scholar 
    Collison, E., Hird, H., Cresswell, J. & Tyler, C. Interactive effects of pesticide exposure and pathogen infection on bee health—a critical analysis. Biol. Rev. 91, 1006–1019. https://doi.org/10.1111/brv.12206 (2016).Article 
    PubMed 

    Google Scholar 
    Helmer, S. H., Kerbaol, A., Aras, P., Jumarie, C. & Boily, M. Effects of realistic doses of atrazine, metolachlor, and glyphosate on lipid peroxidation and diet-derived antioxidants in caged honey bees (Apis mellifera). Environ. Sci. Pollut. Res. 22, 8010–8021. https://doi.org/10.1007/s11356-014-2879-7 (2015).CAS 
    Article 

    Google Scholar 
    Efferth, T., Schwarzl, S. M., Smith, J. & Osieka, R. Role of glucose-6-phosphate dehydrogenase for oxidative stress and apoptosis. Cell Death Differ. 13, 527–528. https://doi.org/10.1038/sj.cdd.4401807 (2006).CAS 
    Article 
    PubMed 

    Google Scholar 
    Corona, M. & Robinson, G. E. Genes of the antioxidant system of the honey bee: Annotation and phylogeny. Insect Mol. Biol. 15, 687–701. https://doi.org/10.1111/j.1365-2583.2006.00695.x (2006).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Field, L. M., Devonshire, A. L., Ffrench-Constant, R. H. & Forde, B. G. Changes in DNA methylation are associated with loss of insecticide resistance in the peach-potato aphid Myzus persicae (Sulz.). FEBS Lett. 243, 323–327. https://doi.org/10.1016/0014-5793(89)80154-1 (1989).CAS 
    Article 

    Google Scholar 
    Ma, M. et al. Isolation of carboxylesterase (esterase FE4) from Apis cerana cerana and its role in oxidative resistance during adverse environmental stress. Biochimie 144, 85–97. https://doi.org/10.1016/j.biochi.2017.10.022 (2018).CAS 
    Article 
    PubMed 

    Google Scholar 
    Zou, F., Guo, Q., Shen, B. & Zhu, C. A cluster of CYP6 gene family associated with the major quantitative trait locus is responsible for the pyrethroid resistance in Culex pipiens pallen. Insect Mol. Biol. 28, 528–536. https://doi.org/10.1111/imb.12571 (2019).CAS 
    Article 
    PubMed 

    Google Scholar 
    Lang, M. L., Braun, C. L., Kanost, M. R. & Gorman, M. J. Multicopper oxidase-1 is a ferroxidase essential for iron homeostasis in Drosophila melanogaster. PNAS 109, 13337–13342. https://doi.org/10.1073/pnas.1208703109 (2012).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Habineza, P. et al. The promoting effect of gut microbiota on growth and development of Red Palm Weevil, Rhynchophorus ferrugineus (Olivier) (Coleoptera: Dryophthoridae) by modulating its nutritional metabolism. Front. Microbiol. https://doi.org/10.3389/fmicb.2019.01212 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Kwong, W. K., Mancenido, A. L. & Moran, N. A. Immune system stimulation by the native gut microbiota of honey bees. R. Soc. Open Sci. 4, 170003. https://doi.org/10.1098/rsos.170003 (2017).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Paradis, D., Berail, G., Bonmatin, J. M. & Belzunces, L. P. Sensitive analytical methods for 22 relevant insecticides of 3 chemical families in honey by GC-MS/MS and LC-MS/MS. Anal. Bioanal. Chem 406, 621–633. https://doi.org/10.1007/s00216-013-7483-z (2014).CAS 
    Article 
    PubMed 

    Google Scholar 
    Wiest, L. et al. Multi-residue analysis of 80 environmental contaminants in honeys, honeybees and pollens by one extraction procedure followed by liquid and gas chromatography coupled with mass spectrometric detection. J. Chromatogr. A 1218, 5743–5756. https://doi.org/10.1016/j.chroma.2011.06.079 (2011).CAS 
    Article 
    PubMed 

    Google Scholar 
    Zufelato, M. S., Lourenco, A. P., Simoes, Z. L. P., Jorge, J. A. & Bitondi, M. M. G. Phenoloxidase activity in Apis mellifera honey bee pupae, and ecdysteroid-dependent expression of the prophenoloxidase mRNA. Insect Biochem. Mol. Biol. 34, 1257–1268. https://doi.org/10.1016/j.ibmb.2004.08.005 (2004).CAS 
    Article 
    PubMed 

    Google Scholar 
    Gallup, J. M. qPCR inhibition and amplification of difficult templates. in PCR troubleshooting and optimization: the essential guide. 23–65 (Horizon Scientific Press, 2011).
    Google Scholar 
    Caporaso, J. G. et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. PNAS 108, 4516–4522. https://doi.org/10.1073/pnas.1000080107 (2011).Article 
    PubMed 

    Google Scholar 
    Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120. https://doi.org/10.1093/bioinformatics/btu170 (2014).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Callahan, B. J. et al. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583. https://doi.org/10.1038/nmeth.3869 (2016).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    McMurdie, P. J. & Holmes, S. phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8, e61217. https://doi.org/10.1371/journal.pone.0061217 (2013).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Davis, N. M., Proctor, D. M., Holmes, S. P., Relman, D. A. & Callahan, B. J. Simple statistical identification and removal of contaminant sequences in marker-gene and metagenomics data. Microbiome 6, 226. https://doi.org/10.1186/s40168-018-0605-2 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Schliep, K. P. phangorn: Phylogenetic analysis in R. Bioinformatics 27, 592–593. https://doi.org/10.1093/bioinformatics/btq706 (2011).CAS 
    Article 
    PubMed 

    Google Scholar 
    Hothorn, T., Bretz, F. & Westfall, P. Simultaneous inference in general parametric models. Biom. J. 50, 346–363. https://doi.org/10.1002/bimj.200810425 (2008).MathSciNet 
    Article 
    PubMed 
    MATH 

    Google Scholar 
    Belzunces, L. P., Theveniau, M., Masson, P. & Bounias, M. Membrane acetylcholinesterase from Apis mellifera head solubilized by phosphatidylinositol-specific phospholipase-C interacts with an anti-CRD antibody. Comp. Biochem. Physiol. B-Biochem. Mol. Biol. 95, 609–612. https://doi.org/10.1016/0305-0491(90)90029-s (1990).Article 

    Google Scholar 
    Bergmeyer, H. U. & Gawehn, K. Principles of Enzymatic Analysis (Verlag Chemie, 1978).
    Google Scholar 
    Al-Lawati, H., Kamp, G. & Bienefeld, K. Characteristics of the spermathecal contents of old and young honeybee queens. J. Insect Physiol. 55, 117–122. https://doi.org/10.1016/j.jinsphys.2008.10.010 (2009).CAS 
    Article 

    Google Scholar 
    Habig, W. H., Pabst, M. J. & Jakoby, W. B. Glutathione s-transferases—first enzymatic step in mercapturic acid formation. J. Biol. Chem. 249, 7130–7139 (1974).CAS 
    Article 

    Google Scholar 
    Bounias, M., Kruk, I., Nectoux, M. & Popeskovic, D. Toxicology of cupric salts on honeybees. V. Gluconate and sulfate action on gut alkaline and acid phosphatases. Ecotox. Envirom. Safe 35, 67–76. https://doi.org/10.1006/eesa.1996.0082 (1996).CAS 
    Article 

    Google Scholar 
    Alaux, C. et al. Interactions between Nosema microspores and a neonicotinoid weaken honeybees (Apis mellifera). Environ. Microbiol. 12, 774–782. https://doi.org/10.1111/j.1462-2920.2009.02123.x (2010).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Therneau, T. “Survival”: A Package for Survival Analysis in S. R package version 2.38. https://CRAN.R-project.org/package=survival. (2015).Kassambara, A. & Kosinski, M. “Survminer”: Drawing Survival Curves using “ggplot2”. R package version 0.4.2. https://CRAN.R-project.org/package=survminer. (2018).de Mendiburu, F. Statistical Procedures for Agricultural Research. Package “Agricolae” Version 1.44. Comprehensive R Archive Network. Institute for Statistics and Mathematics, Vienna, Austria. http://cran.r-project.org/web/packages/agricolae/agricolae.pdf (2013).Caraux, G. & Pinloche, S. PermutMatrix: A graphical environment to arrange gene expression profiles in optimal linear order. Bioinformatics 21, 1280–1281. https://doi.org/10.1093/bioinformatics/bti141 (2004).Article 
    PubMed 

    Google Scholar  More

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    Publisher Correction: Natural selection for imprecise vertical transmission in host–microbiota systems

    AffiliationsDepartment of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ, USAMarjolein Bruijning, Lucas P. Henry, Simon K. G. Forsberg, C. Jessica E. Metcalf & Julien F. AyrolesLewis-Sigler Institute for Integrative Genomics, Princeton, NJ, USALucas P. Henry, Simon K. G. Forsberg & Julien F. AyrolesAuthorsMarjolein BruijningLucas P. HenrySimon K. G. ForsbergC. Jessica E. MetcalfJulien F. AyrolesCorresponding authorCorrespondence to
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    A comprehensive catalogue of plant-pollinator interactions for Chile

    In recent years there has been an increasing concern regarding the global decline of pollinators and pollination services1,2,3. Recent studies estimate that over 87% of the flowering plant species rely on biotic pollination4. Pollination is a mutualistic interaction, and plants provide pollinators with various rewards, including nectar, oil, or excess pollen to feed upon5,6. Although bees are the most well-known pollinator group, pollination can be performed by a wide variety of species, including mammals, birds, reptiles, and other insects.Plant-pollinator interactions are among the key processes that generate and maintain biodiversity7,8. The coevolutionary processes involved in animal pollination have helped maintain the structure and function of entire communities and species’ networks. Wild plant species and natural ecosystems provide several products and services, including nutrient cycling, medicine, food, a source of pollinators for domesticated crops, and alternative food and shelter sources for agricultural pollinators9. However, the complex web of interactions and the large number of species involved (ca. 400,000 species globally) makes it challenging to estimate pollinators’ value in natural ecosystems, particularly when the life history of so many pollinator species remains little studied and understood10.Pollinators also provide highly valuable ecosystem services to crops11,12. More than 70% of the world’s crops depend directly on insect pollination, making pollination key to food security11,13. The European honeybee (Apis mellifera) is likely the most economically important pollinator of crops worldwide13,14. Honeybees are adaptable, easy to manage, and cost-efficient. However, in recent years, ‘colony collapse’ caused by several factors, including parasitic mites and the excessive use of pesticides and herbicides, have led to a decline in managed honeybee colonies in many parts of the world15,16,17. Similarly, habitat loss and fragmentation have detrimental effects on both native and commercial pollinators. In degraded habitats, pollinators struggle to find resources and nesting sites18,19,20.In Chile, pollination represents a multimillion-dollar business. Between January and October 2020, the export of Chilean fruit reached USD 4.149 million, while fresh vegetables generated USD 347 million during the same period21. Although agricultural pollinators have been well studied, native pollinators remain largely unknown. With over 460 species of native bees in Chile, approximately 70% are endemic; researchers have only begun to understand the relationships between native plants and their pollinators22,23,24. Also, managed honeybees and bumblebees introduced to Chile for crop pollination are highly invasive and easily leave croplands to forage in neighbouring native ecosystems25,26, competing directly with native pollinators for the ever-diminishing resources in native grasslands and forests posing a threat to Chile’s unique ecoregions25,27.Because of the importance of pollination in the maintenance of biodiversity and the economic benefits of agricultural crop production, there is an urgent need to understand the causes behind the current decline in pollinator species. In this sense, collating and reviewing existing information on pollinators and making this information easily accessible in the form of a user-friendly database is of immeasurable value. In this study, we compiled the information available about pollination and pollinators (sensu lato) for Chile, aiming to understand plant-pollinator interactions, identify knowledge and geographic gaps, and provide a baseline from which to carry out further studies. We aimed to make a datasheet with a format that was adaptable to different regions and other countries by allowing it to be easily understood, easy to access and find and aiming to avoid duplicity of data. This study represents the first systematic effort to compile the available information on pollination and pollinators for Chile. This pollination catalogue for Chile adds to other international efforts of systematising this information as, for example, the Catalogue of Afrotropical Bees28 and the CPC Plant Pollinators Database29. More