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    Strategic planning to mitigate mining impacts on protected areas in the Brazilian Amazon

    Adams, V. M., Iacona, G. D. & Possingham, H. P. Weighing the benefits of expanding protected areas versus managing existing ones. Nat. Sustain. 2, 404–411 (2019).Article 

    Google Scholar 
    Blicharska, M. et al. Biodiversity’s contributions to sustainable development. Nat. Sustain. 2, 1083–1093 (2019).Article 

    Google Scholar 
    Hanson, J. O. et al. Global conservation of species’ niches. Nature 580, 232–234 (2020).CAS 
    Article 

    Google Scholar 
    Sonter, L. J., Barrett, D. J., Soares-filho, B. S. & Moran, C. J. Global demand for steel drives extensive land-use change in Brazil’ s Iron Quadrangle. Glob. Environ. Change 26, 63–72 (2014).Article 

    Google Scholar 
    Siqueira-Gay, J., Soares-Filho, B., Sánchez, L. E., Oviedo, A. & Sonter, L. J. Proposed legislation to mine Brazil’s Indigenous lands will threaten Amazon forests and their valuable ecosystem services. One Earth 3, 356–362 (2020).Article 

    Google Scholar 
    El Bizri, H. R., Macedo, J. C. B. M., Plaglia, A. P. & Morcatty, T. Q. Mining undermining Brazil’s environment. Science 353, 2–3 (2016).Article 

    Google Scholar 
    Ferreira, J. et al. Brazil’s environmental leadership at risk. Science 346, 706–707 (2014).CAS 
    Article 

    Google Scholar 
    Rudke, A. P. et al. Impact of mining activities on areas of environmental protection in the southwest of the Amazon: a GIS- and remote sensing-based assessment. J. Environ. Manage. 263, 110392 (2020).Article 

    Google Scholar 
    Naughton-Treves, L. & Holland, M. B. Losing ground in protected areas? Science 364, 832–833 (2019).CAS 
    Article 

    Google Scholar 
    Kroner, R. E. G. et al. The uncertain future of protected lands and waters. Science 364, 881–886 (2019).Article 
    CAS 

    Google Scholar 
    Pack, S. M. et al. Protected area downgrading, downsizing, and degazettement (PADDD) in the Amazon. Biol. Conserv. 197, 32–39 (2016).Article 

    Google Scholar 
    PADDDtracker.org Data Release Version 2.0 (Conservation International and World Wildlife Fund, 2019); https://doi.org/10.5281/zenodo.3371733Bebbington, A. J., Humphreys, D., Aileen, L., Rogan, J. & Agrawal, S. Resource extraction and infrastructure threaten forest cover and community rights. Proc. Natl Acad. Sci. USA 115, 13164–13173 (2018).CAS 
    Article 

    Google Scholar 
    Paiva, P. F. P. R. et al. Deforestation in protect areas in the Amazon: a threat to biodiversity. Biodivers. Conserv. 29, 19–38 (2020).Article 

    Google Scholar 
    Boldy, R., Santini, T., Annandale, M., Erskine, P. D. & Sonter, L. J. Understanding the impacts of mining on ecosystem services through a systematic review. Extr. Ind. Soc. https://doi.org/10.1016/j.exis.2020.12.005 (2020).Murguía, D. I., Bringezu, S. & Schaldach, R. Global direct pressures on biodiversity by large-scale metal mining: spatial distribution and implications for conservation. J. Environ. Manage. 180, 409–420 (2016).Article 

    Google Scholar 
    Kobayashi, H., Watando, H. & Kakimoto, M. A global extent site-level analysis of land cover and protected area overlap with mining activities as an indicator of biodiversity pressure. J. Clean. Prod. 84, 459–468 (2014).Article 

    Google Scholar 
    Craig, M. D., White, D. A., Stokes, V. L. & Prince, J. Can postmining revegetation create habitat for a threatened mammal? Ecol. Manage. Restor. 18, 149–155 (2017).Article 

    Google Scholar 
    Sonter, L. J. et al. Mining drives extensive deforestation in the Brazilian Amazon. Nat. Commun. 8, 1013 (2017).Article 
    CAS 

    Google Scholar 
    Siqueira-Gay, J., Sonter, L. J. & Sánchez, L. E. Exploring potential impacts of mining on forest loss and fragmentation within a biodiverse region of Brazil’s northeastern Amazon. Resour. Policy 67, 101662 (2020).Article 

    Google Scholar 
    Siqueira-Gay, J. & Sánchez, L. E. Keep the Amazon niobium in the ground. Environ. Sci. Policy 111, 1–6 (2020).CAS 
    Article 

    Google Scholar 
    Mascia, M. B. & Pailler, S. Protected area downgrading, downsizing, and degazettement (PADDD) and its conservation implications. Conserv. Lett. 4, 9–20 (2011).Article 

    Google Scholar 
    Raiter, K. G., Possingham, H. P., Prober, S. M. & Hobbs, R. J. Under the radar: mitigating enigmatic ecological impacts. Trends Ecol. Evol. 29, 635–644 (2014).Article 

    Google Scholar 
    Whitehead, A. L., Kujala, H. & Wintle, B. A. Dealing with cumulative biodiversity impacts in strategic environmental assessment: a new frontier for conservation planning. Conserv. Lett. 10, 195–204 (2017).Article 

    Google Scholar 
    Jenner, N. Making Mining ‘Forest-Smart’: Executive Summary Report (World Bank, 2019); http://documents.worldbank.org/curated/en/369711560319906622/Making-Mining-Forest-Smart-Executive-Summary-ReportRenca: Situação legal dos direitos minerários da reserva nacional do cobre (WWF, 2017).Soares-Filho, B. S., Cerqueira, G. C. & Pennachin, C. L. DINAMICA—a stochastic cellular automata model designed to simulate the landscape dynamics in an Amazonian colonization frontier. Ecol. Modell. 154, 217–235 (2002).Article 

    Google Scholar 
    Strand, J. et al. Spatially explicit valuation of the Brazilian Amazon forest’s ecosystem services. Nat. Sustain. 1, 657–664 (2018).Article 

    Google Scholar 
    Barber, C. P., Cochrane, M. A., Souza, C. M. & Laurance, W. F. Roads, deforestation, and the mitigating effect of protected areas in the Amazon. Biol. Conserv. 177, 203–209 (2014).Article 

    Google Scholar 
    Rorato, A. C. et al. Brazilian Amazon Indigenous peoples threatened by mining bill. Environ. Res. Lett. 15, 1040a3 (2020).Article 

    Google Scholar 
    Villén-Pérez, S., Anaya-Valenzuela, L., Conrado da Cruz, D. & Fearnside, P. M. Mining threatens isolated Indigenous peoples in the Brazilian Amazon. Glob. Environ. Change 72, (2022).Siqueira-Gay, J. & Sánchez, L. E. The outbreak of illegal gold mining in the Brazilian Amazon boosts deforestation. Reg. Environ. Change 21, 28 (2021).Article 

    Google Scholar 
    Sonter, L. J., Dade, M. C., Watson, J. E. M. & Valenta, R. K. Renewable energy production will exacerbate mining threats to biodiversity. Nat. Commun. 11, 4174 (2020).CAS 
    Article 

    Google Scholar 
    Tallis, H., Kennedy, C. M., Ruckelshaus, M., Goldstein, J. & Kiesecker, J. M. Mitigation for one & all: an integrated framework for mitigation of development impacts on biodiversity and ecosystem services. Environ. Impact Assess. Rev. 55, 21–34 (2015).Article 

    Google Scholar 
    Bull, J. W. et al. Quantifying the “avoided” biodiversity impacts associated with economic development. Front. Ecol. Environ. https://doi.org/10.1002/fee.2496 (2022).Gastauer, M. et al. Mine land rehabilitation: modern ecological approaches for more sustainable mining. J. Clean. Prod. 172, 1409–1422 (2018).Article 

    Google Scholar 
    Souza, B. A., Rosa, J. C. S., Siqueira-Gay, J. & Sánchez, L. E. Mitigating impacts on ecosystem services requires more than biodiversity offsets. Land Use Policy 105, 105393 (2021).Article 

    Google Scholar 
    Ritter, C. D. et al. Environmental impact assessment in Brazilian Amazonia: challenges and prospects to assess biodiversity. Biol. Conserv. 206, 161–168 (2017).Article 

    Google Scholar 
    Good Practice Handbook: Cumulative Impact Assessment and Management, Guidance for the Private Sector in Emerging Markets (IFC, 2013).Gunn, J. H. & Noble, B. F. Integrating cumulative effects in regional strategic environmental assessment frameworks: lessons from practice. J. Environ. Assess. Policy Manage. 11, 267–290 (2009).Article 

    Google Scholar 
    Ferrante, L. & Fearnside, P. M. The Amazon’ s road to deforestation. Science 20, 20–22 (2020).
    Google Scholar 
    Runge, C. A., Tulloch, A. I. T., Gordon, A. & Rhodes, J. R. Quantifying the conservation gains from shared access to linear infrastructure. Conserv. Biol. 31, 1428–1438 (2017).Article 

    Google Scholar 
    Kiesecker, J. M., Copeland, H., Pocewicz, A. & McKenney, B. Development by design: blending landscape-level planning with the mitigation hierarchy. Front. Ecol. Environ. 8, 261–266 (2010).Article 

    Google Scholar 
    Heiner, M. et al. Moving from reactive to proactive development planning to conserve Indigenous community and biodiversity values. Environ. Impact Assess. Rev. 74, 1–13 (2019).Article 

    Google Scholar 
    Pfaff, A., Robalino, J., Herrera, D. & Sandoval, C. Protected areas’ impacts on Brazilian Amazon deforestation: examining conservation–development interactions to inform planning. PLoS ONE 10, 1–17 (2015).Article 
    CAS 

    Google Scholar 
    Almeida, C. A. et al. High spatial resolution land use and land cover mapping of the Brazilian Legal Amazon in 2008 using Landsat-5 / TM and MODIS data. Acta Amazon. 46, 291–302 (2008).Article 

    Google Scholar 
    Asner, G. P. & Tupayachi, R. Accelerated losses of protected forests from gold mining in the Peruvian Amazon. Environ. Res. Lett. 12, 094004 (2016).Article 

    Google Scholar 
    Boham-Carter, G. F. Geographic Information Systems for Geoscientists: Modelling with GIS (Elsevier, 1994).Soares-Filho, B., Rodrigues, H. & Follador, M. A hybrid analytical–heuristic method for calibrating land-use change models. Environ. Model. Softw. 43, 80–87 (2013).Article 

    Google Scholar 
    INPE. TerraClass https://www.terraclass.gov.br/geoportal-aml/ (2021).INPE. Slope http://www.dsr.inpe.br/topodata/acesso.php (2020).Ministério do Meio Ambiente (MMA). Conservation units http://mapas.mma.gov.br/i3geo/datadownload.htm (2022).Fundação Nacional do Índio (FUNAI). Indigenous lands http://www.funai.gov.br/index.php/shape (2021).Leite-Filho, A., Soares-filho, B. S., Davis, J. & Rodrigues, H. Dinamica EGO Guidebook (Centro de Sensoriamento Remoto, UFMG, 2020).Serviço Geológico do Brasil. Mineral deposits https://geosgb.cprm.gov.br/ (2020).Soares-Filho, B. et al. Simulating the response of land-cover changes to road paving and governance along a major Amazon highway: the Santarém-Cuiabá corridor. Glob. Change Biol. 10, 745–764 (2004).Article 

    Google Scholar 
    Centro de Sensoriamento Remoto. Biodiversity https://csr.ufmg.br/amazones/biodiversity/ (2021).Fahrig, L. Ecological responses to habitat fragmentation per se. Annu. Rev. Ecol. Evol. Syst. 48, 1–23 (2017).Pardini, R., de Bueno, A. A., Gardner, T. A., Prado, P. I. & Metzger, J. P. Beyond the fragmentation threshold hypothesis: regime shifts in biodiversity across fragmented landscapes. PLoS ONE 5, e13666 (2010).Montibeller, B., Kmoch, A., Virro, H., Mander, Ü. & Uuemaa, E. Increasing fragmentation of forest cover in Brazil’s Legal Amazon from 2001 to 2017. Sci. Rep. 10, 5803 (2020).CAS 
    Article 

    Google Scholar 
    Cabral, A. I. R., Saito, C., Pereira, H. & Laques, A. E. Deforestation pattern dynamics in protected areas of the Brazilian Legal Amazon using remote sensing data. Appl. Geogr. 100, 101–115 (2018).Article 

    Google Scholar 
    Colson, F., Bogaert, J. & Ceulemans, R. Fragmentation in the Legal Amazon, Brazil: can landscape metrics indicate agricultural policy differences? Ecol. Indic. 11, 1467–1471 (2011).Article 

    Google Scholar 
    Monmonier, M. S. Measures of pattern complexity for choroplethic maps. Am. Cartogr. 1, 159–169 (1974).Article 

    Google Scholar 
    Werner, T. T. et al. Global-scale remote sensing of mine areas and analysis of factors explaining their extent. Glob. Environ. Change 60, 102007 (2020).Article 

    Google Scholar 
    Soares-Filho, B. et al. Roads, http://maps.csr.ufmg.br/ (2016). More

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    Reply to: Fire activity as measured by burned area reveals weak effects of ENSO in China

    Resco de Dios et al. claim that the modulation of ENSO on fire in China is weak. They base their claim on the insignificant correlations they find between gridded area and ENSO indices on individual grid points in China. Unlike their analysis of individual grid points, our analyses were based on the covariance of data on these grid points. Combining all grid points, our correlation analysis increases the degree of freedom, raises the likelihood of a significance test, and therefore is reliable and robust. Fire in individual grid points can be noisy on a local scale, while climate plays a more critical role in modulating large-scale fires.Many previous studies revealed the dominant impacts of ENSO in different regions of China7, 8. Resco de Dios et al. stated that the ENSO could only influence the ignitions and thus has little effect on fire activity. In fact, fuel availability and flammability are also key factors in fire occurrence, particularly for large-scale fires9. This is evidenced by the strong correlations between fire occurrence and interannual climate variability.China’s fire policy not only suppresses existing fires but also prevents human-ignited fire occurrences. As revealed in previous studies, the fire suppression policy since 1987 decreased not only burnt areas but also fire occurrences10.The study by Resco de Dios et al. was based on MODIS-derived annual area burned, which differs from our ground-truthed WFAC fire occurrence dataset. The MODIS cannot sufficiently distinguish the wildfire from the frequent crop fires and thus vastly misinterrupt the crop fires as wildfire, especially over the northern plains where forests are rare. Here, we show that the EOF analyses of the WFAC can also reveal the dipole fire pattern between southwestern and southeastern China. We highlight that the dipole fire pattern and ENSO modulation are on large scales. The fire control policy not only suppresses existing fires but also prevents human-ignited fire occurrences, and thus plays an effective role in reducing five activities in China. More

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    Rewetting global wetlands effectively reduces major greenhouse gas emissions

    Lindgren, A., Hugelius, G. & Kuhry, P. Extensive loss of past permafrost carbon but a net accumulation into present-day soils. Nature 560, 219–222 (2018).Article 

    Google Scholar 
    Nichols, J. E. & Peteet, D. M. Rapid expansion of northern peatlands and doubled estimate of carbon storage. Nat. Geosci. 12, 917–921 (2019).Article 

    Google Scholar 
    Bridgham, S. D. et al. The carbon balance of North American wetlands. Wetlands 26, 889–916 (2006).Article 

    Google Scholar 
    Dixon, M. J. R. et al. Tracking global change in ecosystem area: the wetland extent trends index. Biol. Conserv. 193, 27–35 (2016).Article 

    Google Scholar 
    Darrah, S. E. et al. Improvements to the Wetland Extent Trends (WET) index as a tool for monitoring natural and human-made wetlands. Ecol. Indic. 99, 294–298 (2019).Article 

    Google Scholar 
    Asselen, S. et al. Drivers of wetland conversion: a global meta-analysis. PLoS ONE 8, e81292 (2013).Article 

    Google Scholar 
    Davidson, N. C. How much wetland has the world lost? Long-term and recent trends in global wetland area. Mar. Freshw. Res. 65, 934–941 (2014).Article 

    Google Scholar 
    Galatowitsch, S. M. in The Wetland Book II: Distribution, Description, and Conservation (eds Finlayson, C.M. et al.) 359–367 (Springer, 2018).Limpert, K. E. et al. Reducing emissions from degraded floodplain wetlands. Front. Environ. Sci. 8, 8 (2020); https://doi.org/10.3389/fenvs.2020.00008Laine, J. et al. Effect of water-level drawdown on global climatic warming: northern peatlands. AMBIO 25, 179–184 (1996).
    Google Scholar 
    Ise, T. et al. High sensitivity of peat decomposition to climate change through water-table feedback. Nat. Geosci. 1, 763–766 (2008).Article 

    Google Scholar 
    Saunois, M. et al. The global methane budget 2000–2017. Earth. Syst. Sci. Data 12, 1561–1623 (2020).Article 

    Google Scholar 
    Leifeld, J. et al. Intact and managed peatland soils as a source and sink of GHGs from 1850 to 2100. Nat. Clim. Change 9, 945–947 (2019).Article 

    Google Scholar 
    Günther, A. et al. Prompt rewetting of drained peatlands reduces climate warming despite methane emissions. Nat. Commun. 11, 1644 (2020).Article 

    Google Scholar 
    Hooijer, A. et al. Subsidence and carbon loss in drained tropical peatlands. Biogeoscience 9, 1053–1071 (2012).Article 

    Google Scholar 
    Prananto, J. A. et al. Drainage increases CO2 and N2O emissions from tropical peat soils. Glob. Change Biol. 26, 4583–4600 (2020).Article 

    Google Scholar 
    Jauhiainen, J. et al. Carbon dioxide and methane fluxes in drained tropical peat before and after hydrological restoration. Ecology 89, 3503–3514 (2008).Article 

    Google Scholar 
    Bridgham, S. D. et al. Methane emissions from wetlands: biogeochemical, microbial, and modeling perspectives from local to global scales. Glob. Change Biol. 19, 1325–1346 (2013).Article 

    Google Scholar 
    Schuldt, R. et al. Modelling Holocene carbon accumulation and methane emissions of boreal wetlands—an Earth system model approach. Biogeosciences 10, 1659–1674 (2012).Article 

    Google Scholar 
    McNicol, G. et al. Effects of seasonality, transport pathway, and spatial structure on greenhouse gas fluxes in a restored wetland. Glob. Change Biol. 23, 2768–2782 (2017).Article 

    Google Scholar 
    Yu, K. et al. Redox window with minimum global warming potential contribution from rice soils. Soil Sci. Soc. Am. J. 68, 2086–2091 (2004).Article 

    Google Scholar 
    Huang, Y. et al. Tradeoff of CO2 and CH4 emissions from global peatlands under water-table drawdown. Nat. Clim. Change 11, 618–622 (2021).Article 

    Google Scholar 
    Ojanen, P. & Minkkinen, K. Rewetting offers rapid climate benefits for tropical and agricultural peatlands but not for forestry‐drained peatlands. Glob. Biogeochem. Cycles 34, e2019GB006503 (2020).Article 

    Google Scholar 
    Evans, C. D. et al. Overriding water table control on managed peatland greenhouse gas emissions. Nature 593, 548–552 (2021).
    Google Scholar 
    Strack, M., Keith, A. M. & Xu, B. Growing season carbon dioxide and methane exchange at a restored peatland on the Western Boreal Plain. Ecol. Eng. 64, 231–239 (2014).Article 

    Google Scholar 
    Karki, S. et al. Carbon balance of rewetted and drained peat soils used for biomass production: a mesocosm study. Glob. Change Biol. Bioenergy 8, 969–980 (2016).Article 

    Google Scholar 
    Whiting, G. J. & Chanton, J. P. Greenhouse carbon balance of wetlands: methane emission versus carbon sequestration. Tellus B 53, 521–528 (2001).
    Google Scholar 
    Moore, T. R. et al. A multi-year record of methane flux at the Mer Bleue Bog, Southern Canada. Ecosystems 14, 646–657 (2011).Article 

    Google Scholar 
    Zhu, X. et al. Ammonia oxidation pathways and nitrifier denitrification are significant sources of N2O and NO under low oxygen availability. Proc. Natl Acad. Sci. USA 110, 6328–6333 (2013).Article 

    Google Scholar 
    Cole, J. J. et al. Plumbing the global carbon cycle: integrating inland waters into the terrestrial carbon budget. Ecosystems 10, 171–184 (2007).Article 

    Google Scholar 
    Holgerson, M. A. & Raymond, P. A. Large contribution to inland water CO2 and CH4 emissions from very small ponds. Nat. Geosci. 9, 222–226 (2016).Article 

    Google Scholar 
    Raymond, P. A. et al. Global carbon dioxide emissions from inland waters. Nature 503, 355–359 (2013).Article 

    Google Scholar 
    Rosentreter, J. A. et al. Half of global methane emissions come from highly variable aquatic ecosystem sources. Nat. Geosci. 14, 225–230 (2021).Article 

    Google Scholar 
    Lehner, B. & Döll, P. Development and validation of a global database of lakes, reservoirs and wetlands. J. Hydrol. 296, 1–22 (2004).Article 

    Google Scholar 
    Schuur, E. A. et al. The effect of permafrost thaw on old carbon release and net carbon exchange from tundra. Nature 459, 556–559 (2009).Article 

    Google Scholar 
    Delgado-Baquerizo, M. et al. Climate legacies drive global soil carbon stocks in terrestrial ecosystems. Sci. Adv. 3, e1602008 (2017).Article 

    Google Scholar 
    Hengl, T. et al. SoilGrids250m: global gridded soil information based on machine learning. PLoS ONE 12, e0169748 (2017).Article 

    Google Scholar 
    Walker, X. J. et al. Increasing wildfires threaten historic carbon sink of boreal forest soils. Nature 572, 520–523 (2019).Article 

    Google Scholar 
    Baird, A. J. et al. Validity of managing peatlands with fire. Nat. Geosci. 12, 884–885 (2019).Article 

    Google Scholar 
    Ritchie, H., Roser, M. & Rosado, P. CO2 and GHG Emissions: Atmospheric Concentrations (Our World in Data, 2020); https://ourworldindata.org/atmospheric-concentrations#citationFriedlingstein, P. et al. Global carbon budget 2019. Earth Syst. Sci. Data 11, 1783–1838 (2019).Article 

    Google Scholar 
    Tian, H. et al. A comprehensive quantification of global nitrous oxide sources and sinks. Nature 586, 248–256 (2020).Article 

    Google Scholar 
    Cook-Patton, S. C. et al. Mapping carbon accumulation potential from global natural forest regrowth. Nature 585, 545–550 (2020).Article 

    Google Scholar 
    Jaenicke, J. et al. Planning hydrological restoration of peatlands in Indonesia to mitigate carbon dioxide emissions. Mitig. Adapt. Strateg. Glob. Change 15, 223–239 (2010).Article 

    Google Scholar 
    Wohl, E. Landscape-scale carbon storage associated with beaver dams. Geophys. Res. Lett. 40, 3631–3636 (2013).Article 

    Google Scholar 
    Law, A. et al. Using ecosystem engineers as tools in habitat restoration and rewilding: beaver and wetlands. Sci. Total Environ. 605–606, 1021–1030 (2017).Article 

    Google Scholar 
    Brown, L. E. et al. Macroinvertebrate community assembly in pools created during peatland restoration. Sci. Total Environ. 569, 361–372 (2016).Article 

    Google Scholar 
    Finlayson, C. M. & Rea, N. Reasons for the loss and degradation of Australian wetlands. Wetl. Ecol. Manage. 7, 1–11 (1999).Article 

    Google Scholar 
    Liu, J. et al. Water conservancy projects in China: achievements, challenges and way forward. Glob. Environ. Change 23, 633–643 (2013).Article 

    Google Scholar 
    Rogelj, J. et al. in Special Report on Global Warming of 1.5 °C (eds Masson-Delmotte, V. et al.) Ch. 2 (IPCC, WMO, 2018).Svensson, B. H. & Rosswall, T. In situ methane production from acid peat in plant communities with different moisture regimes in a subarctic mire. Oikos 43, 341–350 (1984).Article 

    Google Scholar 
    Waddington, J. M. & Roulet, N. T. Atmosphere–wetland carbon exchanges: scale dependency of CO2 and CH4 exchange on the developmental topography of a peatland. Glob. Biogeochem. Cycles 10, 233–245 (1996).Article 

    Google Scholar 
    Kling, G. W. et al. The flux of CO2 and CH4 from lakes and rivers in Arctic Alaska. Hydrobiologia 240, 23–36 (1992).Article 

    Google Scholar 
    Humphreys, E. R. et al. Two bogs in the Canadian Hudson Bay lowlands and a temperate bog reveal similar annual net ecosystem exchange of CO2. Arct. Antarct. Alp. Res. 46, 103–113 (2014).Article 

    Google Scholar 
    Caffrey, J. M. Factors controlling net ecosystem metabolism in US estuaries. Estuaries 27, 90–101 (2004).Article 

    Google Scholar 
    Roberts, B. J. et al. Multiple scales of temporal variability in ecosystem metabolism rates: results from 2 years of continuous monitoring in a forested headwater stream. Ecosystems 10, 588–606 (2007).Article 

    Google Scholar 
    Myhre, G. et al. in Climate Change 2013: The Physical Science Basis (eds Stocker, T.F. et al.) 710–714 (Cambridge Univ. Press, 2013).Glenn, A. J. et al. Comparison of net ecosystem CO2 exchange in two peatlands in western Canada with contrasting dominant vegetation, Sphagnum and Carex. Agric. For. Meteorol. 140, 115–135 (2006).Article 

    Google Scholar 
    Bond-Lamberty, B. & Thomson, A. Temperature-associated increases in the global soil respiration record. Nature 464, 579–582 (2010).Article 

    Google Scholar 
    Zhao, J. et al. Intensified inundation shifts a freshwater wetland from a CO2 sink to a source. Glob. Change Biol. 25, 3319–3333 (2019).Article 

    Google Scholar 
    Peichl, M. et al. A 12-year record reveals pre-growing season temperature and water table level threshold effects on the net carbon dioxide exchange in a boreal fen. Environ. Res. Lett. 9, 55006 (2014).Article 

    Google Scholar 
    Peng, Z. & Peng, G. Suitability mapping of global wetland areas and validation with remotely sensed data. Sci. China Earth Sci. 57, 2883–2892 (2014).
    Google Scholar 
    Zhang, B. et al. Methane emissions from global wetlands: an assessment of the uncertainty associated with various wetland extent data sets. Atmos. Environ. 165, 310–321 (2017).Article 

    Google Scholar 
    Gumbricht, T. et al. An expert system model for mapping tropical wetlands and peatlands reveals South America as the largest contributor. Glob. Change Biol. 23, 3581–3599 (2017).Article 

    Google Scholar 
    ERA5 Monthly Averaged Data on Pressure Levels from 1979 to Present (ECMWF, 2020); https://doi.org/10.24381/cds.6860a573FAOSTAT Emissions Database (FAO, 2020); http://www.fao.org/faostat/en/#data/GTQiu, C. et al. Large historical carbon emissions from cultivated northern peatlands. Sci. Adv. 7, eabf1332 (2021).Article 

    Google Scholar 
    Frolking, S., Roulet, N. & Fuglestvedt, J. How northern peatlands influence the Earth’s radiative budget: sustained methane emission versus sustained carbon sequestration. J. Geophys. Res. Biogeosci. 111, G01008 (2006).
    Google Scholar 
    Neubauer, S. C. & Megonigal, J. P. Moving beyond global warming potentials to quantify the climatic role of ecosystems. Ecosystems 18, 1000–1013 (2015).Article 

    Google Scholar 
    Matthews, E. & Fung, I. Methane emission from natural wetlands: global distribution, area, and environmental characteristics of sources. Glob. Biogeochem. Cycles 1, 61–86 (1987).Article 

    Google Scholar 
    Melton, J. R. et al. Present state of global wetland extent and wetland methane modelling: conclusions from a model inter-comparison project (WETCHIMP). Biogeosciences 10, 753–788 (2013).Article 

    Google Scholar 
    Papa, F. et al. Interannual variability of surface water extent at the global scale, 1993–2004. J. Geophys. Res. Atmos. 115, D12111 (2010).Article 

    Google Scholar 
    Junk, W. J. et al. Current state of knowledge regarding the world’s wetlands and their future under global climate change: a synthesis. Aquat. Sci. 75, 151–167 (2013).Article 

    Google Scholar 
    Schroeder, R. et al. Development and evaluation of a multi-year fractional surface water data set derived from active/passive microwave remote sensing data. Remote Sens. 7, 16688–16732 (2015).Article 

    Google Scholar 
    Vanessa, R. et al. A global assessment of inland wetland conservation status. Bioscience 6, 523–533 (2017).
    Google Scholar 
    Davidson, N. et al. Global extent and distribution of wetlands: trends and issues. Mar. Freshw. Res. 69, 620–627 (2018).Article 

    Google Scholar 
    ArcWorld 1:3 M. Continental Coverage (ESRI, 1992); http://www.oceansatlas.org/subtopic/en/c/593/Digital Chart of the World 1:1 M (ESRI, 1993); https://www.ngdc.noaa.gov/mgg/topo/report/s5/s5Avii.htmlGlobal Wetlands (UNEP-WCMC, 1993); https://www.arcgis.com/home/item.html?id=105a402642e146eaa665315279a322d1Moreno-Mateos, D. et al. Structural and functional loss in restored wetland ecosystems. PLoS Biol. 10, e1001247 (2012).Article 

    Google Scholar 
    Ramsar COP12 DOC.8 Report of the Secretary General to COP12 on the Implementation of the Convention (Ramsar Convention Secretariat, 2015).Page, S. E. et al. Peatlands and global change: response and resilience. Annu. Rev. Environ. Resour. 41, 35–57 (2016).Article 

    Google Scholar 
    Swindles, G. T. et al. Widespread drying of European peatlands in recent centuries. Nat. Geosci. 12, 922–928 (2019).Article 

    Google Scholar  More

  • in

    Weak effects on growth and cannibalism under fluctuating temperatures in damselfly larvae

    Vázquez, D. P., Gianoli, E., Morris, W. F. & Bozinovic, F. Ecological and evolutionary impacts of changing climatic variability. Biol. Rev. 92, 22–42. https://doi.org/10.1111/brv.12216 (2017).Article 
    PubMed 

    Google Scholar 
    Marshall, K. E. & Sinclair, B. J. The impacts of repeated cold exposure on insects. J. Exp. Biol. 215, 1607–1613. https://doi.org/10.1242/jeb.059956 (2012).Article 
    PubMed 

    Google Scholar 
    Bale, J. & Hayward, S. Insect overwintering in a changing climate. J. Exp. Biol. 213, 980–994 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    Kingsolver, J. G. Feeding, growth, and the thermal environment of cabbage white caterpillars, Pieris rapae L. Physiol. Biochem. Zool. 73, 621–628 (2000).CAS 
    PubMed 
    Article 

    Google Scholar 
    Stange, E. E. & Ayres, M. P. Climate change impacts: Insects (JohnWiley & Sons, 2010).
    Google Scholar 
    Chapman, A. D. Numbers of Living Species in Australia and the World: Report for the Department of the Environment and Heritage Canberra, Australia (Department of the Environment and Heritage, 2006).
    Google Scholar 
    Colinet, H., Sinclair, B. J., Vernon, P. & Renault, D. Insects in fluctuating thermal environments. Annu. Rev. Entomol. 60, 123–140. https://doi.org/10.1146/annurev-ento-010814-021017 (2015).CAS 
    Article 
    PubMed 

    Google Scholar 
    Hickling, R., Roy, D. B., Hill, J. K. & Thomas, C. D. A northward shift of range margins in British Odonata. Glob. Change Biol. 11, 502–506. https://doi.org/10.1111/j.1365-2486.2005.00904.x (2005).ADS 
    Article 

    Google Scholar 
    Rumpf, S. B., Hülber, K., Zimmermann, N. E. & Dullinger, S. Elevational rear edges shifted at least as much as leading edges over the last century. Glob. Ecol. Biogeogr. 28, 533–543. https://doi.org/10.1111/geb.12865 (2019).Article 

    Google Scholar 
    Halsch, C. A. et al. Insects and recent climate change. Proc. Natl. Acad. Sci. 118, e2002543117. https://doi.org/10.1073/pnas.2002543117 (2021).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    McCain, C. M. & Garfinkel, C. F. Climate change and elevational range shifts in insects. Curr. Opin. Insect Sci. 47, 111–118. https://doi.org/10.1016/j.cois.2021.06.003 (2021).Article 
    PubMed 

    Google Scholar 
    Angilletta, M. J. Jr. & Angilletta, M. J. Thermal Adaptation: A Theoretical and Empirical Synthesis (Oxford University Press, 2009).Book 

    Google Scholar 
    Angilletta, M. J. & Dunham, A. E. The temperature-size rule in ectotherms: Simple evolutionary explanations may not be general. Am. Nat. 162, 332–342. https://doi.org/10.1086/377187 (2003).Article 
    PubMed 

    Google Scholar 
    Jensen, J. L. W. V. Sur les fonctions convexes et les inégalités entre les valeurs moyennes. Acta Math. 30, 175–193 (1906).MathSciNet 
    MATH 
    Article 

    Google Scholar 
    Ruel, J. J. & Ayres, M. P. Jensen’s inequality predicts effects of environmental variation. Trends Ecol. Evol. 14, 361–366 (1999).CAS 
    PubMed 
    Article 

    Google Scholar 
    Kingsolver, J. G. & Woods, H. A. Thermal sensitivity of growth and feeding in Manduca sexta Caterpillars. Physiol. Zool. 70, 631–638. https://doi.org/10.1086/515872 (1997).CAS 
    Article 
    PubMed 

    Google Scholar 
    Gillooly, J. F., Brown, J. H., West, G. B., Savage, V. M. & Charnov, E. L. Effects of size and temperature on metabolic rate. Science 293, 2248–2251 (2001).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Bale, J. S. et al. Herbivory in global climate change research: Direct effects of rising temperature on insect herbivores. Glob. Change Biol. 8, 1–16 (2002).ADS 
    Article 

    Google Scholar 
    Robinet, C. & Roques, A. Direct impacts of recent climate warming on insect populations. Integr. Zool. 5, 132–142 (2010).PubMed 
    Article 

    Google Scholar 
    García-Robledo, C., Kuprewicz, E. K., Staines, C. L., Erwin, T. L. & Kress, W. J. Limited tolerance by insects to high temperatures across tropical elevational gradients and the implications of global warming for extinction. Proc. Natl. Acad. Sci. 113, 680–685. https://doi.org/10.1073/pnas.1507681113 (2016).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Vasseur, D. A. et al. Increased temperature variation poses a greater risk to species than climate warming. Proc. R. Soc. B Biol. Sci. 281, 20132612 (2014).Article 

    Google Scholar 
    Sandehson, D. E. The relation of temperature to the growth of insects. J. Econ. Entomol. 3, 113–140 (1910).Article 

    Google Scholar 
    Cook, W. C. Some Effects of Alternating Temperatures on the Growth and Metabolism of Cutworm Larvae (Oxford University Press, 1927).
    Google Scholar 
    Kingsolver, J. G., Ragland, G. J. & Diamond, S. E. Evolution in a constant environment: Thermal fluctuations and thermal sensitivity of laboratory and field populations of Manduca sexta. Evolution 63, 537–541. https://doi.org/10.1111/j.1558-5646.2008.00568.x (2009).Article 
    PubMed 

    Google Scholar 
    Eldridge, W. H., Sweeney, B. W. & Law, J. M. Fish growth, physiological stress, and tissue condition in response to rate of temperature change during cool or warm diel thermal cycles. Can. J. Fish. Aquat. Sci. 72, 1527–1537 (2015).CAS 
    Article 

    Google Scholar 
    Bernhardt, J. R., Sunday, J. M., Thompson, P. L. & O’Connor, M. I. Nonlinear averaging of thermal experience predicts population growth rates in a thermally variable environment. Proc. R. Soc. B Biol. Sci. 285, 20181076. https://doi.org/10.1098/rspb.2018.1076 (2018).Article 

    Google Scholar 
    Morissette, J., Swart, S., Maccormack, T. J., Currie, S. & Morash, A. J. Thermal variation near the thermal optimum does not affect the growth, metabolism or swimming performance in wild Atlantic salmon Salmo salar. J. Fish Biol. 98, 1585–1589. https://doi.org/10.1111/jfb.14348 (2021).CAS 
    Article 
    PubMed 

    Google Scholar 
    Bozinovic, F. et al. The mean and variance of environmental temperature interact to determine physiological tolerance and fitness. Physiol. Biochem. Zool. 84, 543–552 (2011).PubMed 
    Article 

    Google Scholar 
    Boggs, C. L. The fingerprints of global climate change on insect populations. Curr. Opin. Insect Sci. 17, 69–73. https://doi.org/10.1016/j.cois.2016.07.004 (2016).Article 
    PubMed 

    Google Scholar 
    Lemoine, N. P., Drews, W. A., Burkepile, D. E. & Parker, J. D. Increased temperature alters feeding behavior of a generalist herbivore. Oikos 122, 1669–1678. https://doi.org/10.1111/j.1600-0706.2013.00457.x (2013).Article 

    Google Scholar 
    Vangansbeke, D. et al. Prey consumption by phytoseiid spider mite predators as affected by diurnal temperature variations. Biocontrol 60, 595–603 (2015).Article 

    Google Scholar 
    Davies, C., Coetzee, M. & Lyons, C. L. Effect of stable and fluctuating temperatures on the life history traits of Anopheles arabiensis and An. quadriannulatus under conditions of inter-and intra-specific competition. Parasit. Vectors 9, 1–9 (2016).Article 

    Google Scholar 
    Delava, E., Fleury, F. & Gibert, P. Effects of daily fluctuating temperatures on the Drosophila-Leptopilina boulardi parasitoid association. J. Therm. Biol. 60, 95–102 (2016).PubMed 
    Article 

    Google Scholar 
    Amarasekare, P. & Coutinho, R. M. Effects of temperature on intraspecific competition in ectotherms. Am. Nat. 184, E50–E65. https://doi.org/10.1086/677386 (2014).Article 
    PubMed 

    Google Scholar 
    Jiang, L. & Morin, P. J. Temperature-dependent interactions explain unexpected responses to environmental warming in communities of competitors. J. Anim. Ecol. 73, 569–576 (2004).Article 

    Google Scholar 
    Novich, R. A., Erickson, E. K., Kalinoski, R. M. & DeLong, J. P. The temperature independence of interaction strength in a sit-and-wait predator. Ecosphere 5, 1–9 (2014).Article 

    Google Scholar 
    Fox, L. R. Cannibalism in natural populations. Annu. Rev. Ecol. Syst. 6, 87–106 (1975).Article 

    Google Scholar 
    Polis, G. A. The evolution and dynamics of intraspecific predation. Annu. Rev. Ecol. Syst. 12, 225–251 (1981).Article 

    Google Scholar 
    Nishimura, K. & Isoda, Y. Evolution of cannibalism: Referring to costs of cannibalism. J. Theor. Biol. 226, 293–302. https://doi.org/10.1016/j.jtbi.2003.09.007 (2004).ADS 
    MathSciNet 
    Article 
    PubMed 
    MATH 

    Google Scholar 
    Crumrine, P. W. Body size, temperature, and seasonal differences in size structure influence the occurrence of cannibalism in larvae of the migratory dragonfly, Anax junius. Aquat. Ecol. 44, 761–770 (2010).Article 

    Google Scholar 
    Reglero, P., Urtizberea, A., Torres, A. P., Alemany, F. & Fiksen, Ø. Cannibalism among size classes of larvae may be a substantial mortality component in tuna. Mar. Ecol. Prog. Ser. 433, 205–219 (2011).ADS 
    Article 

    Google Scholar 
    Nilsson-Örtman, V., Stoks, R. & Johansson, F. Competitive interactions modify the temperature dependence of damselfly growth rates. Ecology 95, 1394–1406. https://doi.org/10.1890/13-0875.1 (2014).Article 
    PubMed 

    Google Scholar 
    Pritchard, G. & Leggott, M. Temperature, incubation rates and the origins of dragonflies. Adv. Odonatol. 3, 121–126 (1987).
    Google Scholar 
    Hassall, C. & Thompson, D. J. The effects of environmental warming on Odonata: A review. Int. J. Odonatol. 11, 131–153 (2008).Article 

    Google Scholar 
    Johansson, F. & Crowley, P. H. Larval cannibalism and population dynamics of dragonflies. In Aquatic Insects: Challenges to Populations 36–54 (CABI, 2008).Rudolf, V. H. W. & Rasmussen, N. L. Ontogenetic functional diversity: Size structure of a keystone predator drives functioning of a complex ecosystem. Ecology 94, 1046–1056 (2013).PubMed 
    Article 

    Google Scholar 
    Hyeun-Ji, L. & Johansson, F. Compensating for a bad start: Compensatory growth across life stages in an organism with a complex life cycle. Can. J. Zool. 94, 41–47 (2016).Article 

    Google Scholar 
    Sokolovska, N., Rowe, L. & Johansson, F. Fitness and body size in mature odonates. Ecol. Entomol. 25, 239–248. https://doi.org/10.1046/j.1365-2311.2000.00251.x (2000).Article 

    Google Scholar 
    Karl, T. R. Modern global climate change. Science 302, 1719–1723. https://doi.org/10.1126/science.1090228 (2003).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Meehl, G. A. et al. Climate Change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (Cambridge University Press, 2007).
    Google Scholar 
    Meehl, G. A. More intense, more frequent, and longer lasting heat waves in the 21st century. Science 305, 994–997. https://doi.org/10.1126/science.1098704 (2004).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Khelifa, R. Spatiotemporal Pattern of Phenology Across Geographic Gradients in Insects, in Chapter 1 (Geographic Gradients in Climate Change Response Explained by Non-linear Thermal-Performance Curves) (University of Zurich, 2017).
    Google Scholar 
    Boudot, J. P. & Kalkman, V. Atlas of the European Dragonflies and Damselflies (KNNV Publishing, 2015).
    Google Scholar 
    Norling, U. Growth, winter preparations and timing of emergence in temperate zone Odonata: Control by a succession of larval response patterns. Int. J. Odonatol. 24, 1–36 (2021).Article 

    Google Scholar 
    Sniegula, S. & Johansson, F. Photoperiod affects compensating developmental rate across latitudes in the damselfly Lestes sponsa. Ecol. Entomol. 35, 149–157. https://doi.org/10.1111/j.1365-2311.2009.01164.x (2010).Article 

    Google Scholar 
    Sniegula, S., Golab, M. J. & Johansson, F. Size-mediated priority and temperature effects on intra-cohort competition and cannibalism in a damselfly. J. Anim. Ecol. 88, 637–648. https://doi.org/10.1111/1365-2656.12947 (2019).Article 
    PubMed 

    Google Scholar 
    Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675. https://doi.org/10.1038/nmeth.2089 (2012).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Benke, A. C. A method for comparing individual growth rates of aquatic insects with special reference to the Odonata. Ecology 51, 328–331 (1970).Article 

    Google Scholar 
    Nilsson-Örtman, V., Stoks, R., De Block, M. & Johansson, F. Generalists and specialists along a latitudinal transect: Patterns of thermal adaptation in six species of damselflies. Ecology 93, 1340–1352. https://doi.org/10.1890/11-1910.1 (2012).Article 
    PubMed 

    Google Scholar 
    Eklund, A. et al. Sveriges Framtida Klimat: Underlag Till Dricksvattenutredningen (SMHI, 2015).
    Google Scholar 
    McPeek, M. A. Determination of species composition in the Enallagma damselfly assemblages of permanent lakes. Ecology 71, 83–98. https://doi.org/10.2307/1940249 (1990).Article 

    Google Scholar 
    Kirillin, G. et al. FLake-global: Online lake model with worldwide coverage. Environ. Model. Softw. 26, 683–684. https://doi.org/10.1016/j.envsoft.2010.12.004 (2011).Article 

    Google Scholar 
    SMHI. Advanced Climate Change Scenario Service. https://www.smhi.se.R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2019).Suhling, F., Suhling, I. & Richter, O. Temperature response of growth of larval dragonflies–An overview. Int. J. Odonatol. 18, 15–30 (2015).Article 

    Google Scholar 
    Padfield, D., O’Sullivan, H. & Pawar, S. rTPC and nls.multstart: A new pipeline to fit thermal performance curves in R. Methods Ecol. Evol. 1, 1. https://doi.org/10.1111/2041-210X.13585 (2021).Article 

    Google Scholar 
    Kleiber, M. Body size and metabolism. Hilgardia 6, 315–353 (1932).CAS 
    Article 

    Google Scholar 
    Hemmingsen, A. Reports of the Steno Memorial Hospital and Nordisk Insulin Laboratorium. Energy Metab. Relat. Body Size Respir. Surf. Evol. 9, 6–110 (1960).
    Google Scholar 
    Dell, A. I., Pawar, S. & Savage, V. M. Systematic variation in the temperature dependence of physiological and ecological traits. Proc. Natl. Acad. Sci. 108, 10591–10596 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Logan, J. D., Wolesensky, W. & Joern, A. Temperature-dependent phenology and predation in arthropod systems. Ecol. Model. 196, 471–482. https://doi.org/10.1016/j.ecolmodel.2006.02.034 (2006).Article 

    Google Scholar 
    Pink, M. & Abrahams, M. V. Temperature and its impact on predation risk within aquatic ecosystems. Can. J. Fish. Aquat. Sci. 73, 869–876. https://doi.org/10.1139/cjfas-2015-0302 (2016).Article 

    Google Scholar 
    DeAngelis, D., Cox, D. & Coutant, C. Cannibalism and size dispersal in young-of-the-year largemouth bass: Experiment and model. Ecol. Model. 8, 133–148 (1980).Article 

    Google Scholar 
    Fagan, W. F. & Odell, G. M. Size-dependent cannibalism in praying mantids: Using biomass flux to model size-structured populations. Am. Nat. 147, 230–268 (1996).Article 

    Google Scholar 
    Dong, Q. & Deangelis, D. L. Consequences of cannibalism and competition for food in a smallmouth bass population: An individual-based modeling study. Trans. Am. Fish. Soc. 127, 174–191 (1998).Article 

    Google Scholar 
    Verheyen, J. & Stoks, R. Temperature variation makes an ectotherm more sensitive to global warming unless thermal evolution occurs. J. Anim. Ecol. 88, 624–636. https://doi.org/10.1111/1365-2656.12946 (2019).Article 
    PubMed 

    Google Scholar 
    Starr, S. M. & McIntyre, N. E. Effects of water temperature under projected climate change on the development and survival of Enallagma civile (Odonata: Coenagrionidae). Environ. Entomol. 49, 230–237. https://doi.org/10.1093/ee/nvz138 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    Culler, L. E., McPeek, M. A. & Ayres, M. P. Predation risk shapes thermal physiology of a predaceous damselfly. Oecologia 176, 653–660. https://doi.org/10.1007/s00442-014-3058-8 (2014).ADS 
    Article 
    PubMed 

    Google Scholar 
    Dokulil, M. T. et al. Increasing maximum lake surface temperature under climate change. Clim. Change https://doi.org/10.1007/s10584-021-03085-1 (2021).Article 

    Google Scholar 
    Merritt, R. W. & Cummins, K. W. An Introduction to the Aquatic Insects of North America 2nd edn. (Kendall/Hunt Publishing Company, 1984).
    Google Scholar 
    Verdonschot, R. & Peeters, E. T. Preference of larvae of Enallagma cyathigerum (Odonata: Coenagrionidae) for habitats of varying structural complexity. Eur. J. Entomol. 109, 229–234 (2012).Article 

    Google Scholar 
    McCarty, J. P., Wolfenbarger, L. L. & Wilson, J. A. eLS 1–13 (Wiley, 2017).Book 

    Google Scholar 
    Holzmann, K. L. Challenges in a Changing Climate: The Effect of Temperature Variation on Growth and Competition in Damselflies Independent thesis Advanced level (degree of Master (Two Years) thesis, Uppsala University. http://urn.kb.se/resolve?urn=urn:nbn:se:uu:diva-467582 (2022). More

  • in

    Modeling the spatial distribution of Culicoides species (Diptera: Ceratopogonidae) as vectors of animal diseases in Ethiopia

    MacLachlan, N. J. & Guthrie, A. J. Re-emergence of bluetongue, African horse sickness, and other Orbivirus diseases. Vet. Res. https://doi.org/10.1051/vetres/2010007 (2010).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Koenraadt, C. J. M. et al. Bluetongue, Schmallenberg—What is next? Culicoides-borne viral diseases in the 21st Century. BMC Res. Notes 10, 77 (2014).
    Google Scholar 
    Dennis, S. J., Meyers, A. E., Hitzeroth, I. I. & Rybicki, E. P. African horse sickness: A review of current understanding and vaccine development in the. Viruses 11, 844 (2019).CAS 
    PubMed Central 
    Article 

    Google Scholar 
    Collins, Á. B., Doherty, M. L., Barrett, D. J. & Mee, J. F. Schmallenberg virus: A systematic international literature review (2011–2019) from an Irish perspective. Ir. Vet. J. 72, 1–22 (2019).Article 

    Google Scholar 
    Tkuwet, G. & Firesbhat, A. A review on African horse sickness. Eur. J. Appl. Sci. 7, 213–219 (2015).CAS 

    Google Scholar 
    Mellor, P. S. & Hamblin, C. African horse sickness. Vet. Res. 35, 445–466 (2004).PubMed 
    Article 

    Google Scholar 
    Coetzee, P., Stokstad, M., Venter, E. H., Myrmel, M. & Van Vuuren, M. Bluetongue: A historical and epidemiological perspective with the emphasis on South Africa. Virol. J. 9, 198 (2012).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Cagienard, A., Griot, C., Mellor, P. S., Denison, E. & Stärk, K. D. Bluetongue vector species of Culicoides in Switzerland. Med. Vet. Entomol. 20, 239–247 (2006).CAS 
    PubMed 
    Article 

    Google Scholar 
    Oluwayelu, D., Adebiyi, A. & Tomori, O. Endemic and emerging arboviral diseases of livestock in Nigeria: A review. Parasit. Vectors 11, 1–12 (2018).Article 

    Google Scholar 
    Sibhat, B., Ayelet, G., Gebremedhin, E. Z., Skjerve, E. & Asmare, K. Seroprevalence of Schmallenberg virus in dairy cattle in Ethiopia. Acta Trop. 178, 61–67 (2018).PubMed 
    Article 

    Google Scholar 
    Aklilu, N. et al. African horse sickness outbreaks caused by multiple virus types in Ethiopia. Transbound. Emerg. Dis. 61, 185–192 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    Rojas, J. M., Rodríguez-Martín, D., Martín, V. & Sevilla, N. Diagnosing bluetongue virus in domestic ruminants: Current perspectives. Vet. Med. Res. Rep. 10, 17 (2019).
    Google Scholar 
    Gizaw, D., Sibhat, D., Ayalew, B. & Sehal, M. Sero-prevalence study of bluetongue infection in sheep and goats in selected areas of Ethiopia. Ethiop. Vet. J. 20, 105 (2016).Article 

    Google Scholar 
    Abera, T. et al. Bluetongue disease in small ruminants in south western Ethiopia: Cross-sectional sero-epidemiological study. BMC Res. Notes 11, 112 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Mellor, P. S., Boorman, J. & Baylis, M. Culicoides biting midges: Their role as arbovirus vectors. Annu. Rev. Entomol. 45, 307–340 (2000).CAS 
    PubMed 
    Article 

    Google Scholar 
    Carpenter, S., Groschup, M. H., Garros, C., Felippe-Bauer, M. L. & Purse, B. V. Culicoides biting midges, arboviruses and public health in Europe. Antivir. Res. 100, 102–113 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    Sick, F., Beer, M., Kampen, H. & Wernike, K. Culicoides biting midges—Underestimated vectors for arboviruses of public health and veterinary importance. Viruses 11, 376 (2019).CAS 
    PubMed Central 
    Article 

    Google Scholar 
    Blanda, V. et al. Geo-statistical analysis of Culicoides spp. distribution and abundance in Sicily, Italy. Parasit. Vectors 11, 78 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Vasić, A. et al. Species diversity, host preference and arbovirus detection of Culicoides (Diptera: Ceratopogonidae) in south-eastern Serbia. Parasit. Vectors 12, 1–9 (2019).Article 

    Google Scholar 
    Martin, E. et al. Culicoides species community composition and infection status with parasites in an urban environment of east central Texas, USA. Parasit. Vectors 12, 1–10 (2019).Article 

    Google Scholar 
    Gusmão, G. M. C., Brito, G. A., Moraes, L. S., Bandeira, M. D. C. A. & Rebêlo, J. M. M. Temporal variation in species abundance and richness of Culicoides (Diptera: Ceratopogonidae) in a tropical equatorial area. J. Med. Entomol. https://doi.org/10.1093/jme/tjz015 (2019).Article 
    PubMed 

    Google Scholar 
    Sghaier, S. et al. New species of the genus Culicoides (Diptera Ceratopogonidae) for Tunisia, with detection of Bluetongue viruses in vectors. Vet. Ital. 53, 357–366 (2017).PubMed 

    Google Scholar 
    Gordon, S. J. G. et al. The occurrence of Culicoides species, the vectors of arboviruses, at selected trap sites in Zimbabwe. Onderstepoort J. Vet. Res. 82, e1–e8 (2015).PubMed 
    Article 
    CAS 

    Google Scholar 
    Villard, P. et al. Modeling Culicoides abundance in mainland France: Implications for surveillance. Parasit. Vectors 12, 1–10 (2019).Article 

    Google Scholar 
    Diarra, M. et al. Spatial distribution modelling of Culicoides (Diptera: Ceratopogonidae) biting midges, potential vectors of African horse sickness and bluetongue viruses in Senegal. Parasit. Vectors 11, 341 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Calvete, C. et al. Spatial distribution of Culicoides imicola, the main vector of bluetongue virus, Spain. Vet. Rec. 158, 130–131 (2006).CAS 
    PubMed 
    Article 

    Google Scholar 
    Purse, B. V. et al. Modelling the distributions of Culicoides bluetongue virus vectors in Sicily in relation to satellite-derived climate variables. Med. Vet. Entomol. 18, 90–101 (2004).CAS 
    PubMed 
    Article 

    Google Scholar 
    Purse, B. V. et al. Spatial and temporal distribution of bluetongue and its Culicoides vectors in Bulgaria. Med. Vet. Entomol. 20, 335–344 (2006).CAS 
    PubMed 
    Article 

    Google Scholar 
    Leta, S. et al. Modeling the global distribution of Culicoides imicola: An ensemble approach. Sci. Rep. 9, 1–9 (2019).ADS 
    CAS 
    Article 

    Google Scholar 
    Mulatu, T. & Hailu, A. The occurrence and identification of Culicoides species in the Western Ethiopia. Acad. J. Entomol. 12, 40–43 (2019).
    Google Scholar 
    Khamala, C. P. M. & Kettle, D. S. The Culicoides Latreille (Diptera: Ceratopogonidae) of East Africa. Trans. R. Entomol. Soc. Lond. 123, 1–95 (1971).Article 

    Google Scholar 
    Venter, G. J. Specie di Culicoides (Diptera: Ceratopogonidae) vettori del virus della Bluetongue in Sud Africa. Vet. Ital. 51, 325–333 (2015).PubMed 

    Google Scholar 
    Mathieu, B. et al. Development and validation of IIKC: An interactive identification key for Culicoides (Diptera: Ceratopogonidae) females from the Western Palaearctic region. Parasit. Vectors 5, 137 (2012).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Thuiller, W., Lafourcade, B., Engler, R. & Araújo, M. B. BIOMOD—A platform for ensemble forecasting of species distributions. Ecography (Cop.) 32, 369–373 (2009).Article 

    Google Scholar 
    Baylis, M., Bouayoune, H., Touti, J. & El Hasnaoui, H. Use of climatic data and satellite imagery to model the abundance of Culicoides imicola, the vector of African horse sickness virus, in Morocco. Med. Vet. Entomol. 12, 255–266 (1998).CAS 
    PubMed 
    Article 

    Google Scholar 
    Diarra, M. et al. Modelling the abundances of two major culicoides (Diptera: Ceratopogonidae) species in the Niayes area of Senegal. PLoS One 10, e0131021 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Ramilo, D. W., Nunes, T., Madeira, S., Boinas, F. & da Fonseca, I. P. Geographical distribution of Culicoides (DIPTERA: CERATOPOGONIDAE) in mainland Portugal: Presence/absence modelling of vector and potential vector species. PLoS One 12, e0180606 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Ben Rais Lasram, F. et al. The Mediterranean Sea as a ‘cul-de-sac’ for endemic fishes facing climate change. Glob. Chang. Biol. 16, 3233–3245 (2010).ADS 
    Article 

    Google Scholar 
    Tiffin, P. & Ross-Ibarra, J. Goal-oriented evaluation of species distribution models accuracy and precision: True Skill Statistic profile and uncertainty maps. PeerJ PrePints https://doi.org/10.7287/peerj.preprints.488v1 (2014).Article 

    Google Scholar 
    Graham, M. H. Confronting multicollinearity in ecological multiple regression. Ecology 84, 2809–2815 (2003).Article 

    Google Scholar 
    Demissie, G. H. Seroepidemiological study of African horse sickness in southern Ethiopia. Open Sci. Repos. Vet. Med. 10, e70081919 (2013).
    Google Scholar 
    Zeleke, A., Sori, T., Powel, K., Gebre-Ab, F. & Endebu, B. Isolation and identification of circulating serotypes of African horse sickness virus in Ethiopia. J. Appl. Res. Vet. Med. 3, 40–43 (2005).
    Google Scholar 
    Ayelet, G. et al. Outbreak investigation and molecular characterization of African horse sickness virus circulating in selected areas of Ethiopia. Acta Trop. 127, 91–96 (2013).PubMed 
    Article 

    Google Scholar 
    Gulima, D. Seroepidemiological study of bluetongue in indigenous sheep in selected districts of Amhara National Regional State, north western Ethiopia. Ethiop. Vet. J. 13, 1–15 (2009).
    Google Scholar 
    Borkent, A. & Dominiak, P. Catalog of the biting midges of the world (Diptera: Ceratopogonidae). Zootaxa 4787, 1–377 (2020).Article 

    Google Scholar 
    Borkent, A. & Wirth, W. W. World species of biting midges (Diptera: Ceratopogonidae). Bull. Am. Museum Nat. Hist. 233, 5–195 (1997).
    Google Scholar 
    Guichard, S. et al. Worldwide niche and future potential distribution of Culicoides imicola, a major vector of bluetongue and African horse sickness viruses. PLoS One 9, e112491 (2014).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Becker, E. E. E., Venter, G. J., Labuschagne, K., Greyling, T. & van Hamburg, H. Occurrence of Culicoides species Diptera: Ceratopogonidae) in the Khomas region of Namibia during the winter months. Vet. Ital. 48, 45–54 (2012).PubMed 

    Google Scholar 
    Capela, R. et al. Spatial distribution of Culicoides species in Portugal in relation to the transmission of African horse sickness and bluetongue viruses. Med. Vet. Entomol. 17, 165–177 (2003).CAS 
    PubMed 
    Article 

    Google Scholar 
    Calvete, C. et al. Modelling the distributions and spatial coincidence of bluetongue vectors Culicoides imicola and the Culicoides obsoletus group throughout the Iberian peninsula. Med. Vet. Entomol. 22, 124–134 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    Riddin, M. A., Venter, G. J., Labuschagne, K. & Villet, M. H. Culicoides species as potential vectors of African horse sickness virus in the southern regions of South Africa. Med. Vet. Entomol. 33, 498–511 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Foxi, C. et al. Role of different Culicoides vectors (Diptera: Ceratopogonidae) in bluetongue virus transmission and overwintering in Sardinia (Italy). Parasit. Vectors 9, 440 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Musuka, G. N., Mellor, P. S., Meiswinkel, R., Baylis, M. & Kelly, P. J. Prevalence of Culicoides imicola and other species (Diptera: Ceratopogonidae) ateight sites in Zimbabwe: To the editor. J. S. Afr. Vet. Assoc. 72, 62–63 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    Meiswinkel, R. The 1996 outbreak of African horse sickness in South Africa—the entomological perspective. Arch. Virol. Suppl. 14, 69–83 (1998).CAS 
    PubMed 

    Google Scholar 
    Jean Pierre, T. et al. Characteristics, classification and genesis of vertisols under seasonally contrasted climate in the Lake Chad Basin, Central Africa. J. Afr. Earth Sci. 150, 176–193 (2019).ADS 
    CAS 
    Article 

    Google Scholar 
    Elias, E. Characteristics of Nitisol profiles as affected by land use type and slope class in some Ethiopian highlands. Environ. Syst. Res. 6, 1–15 (2017).Article 

    Google Scholar 
    Nachtergaele, F. The classification of leptosols in the world reference base for soil resources.Veronesi, E., Venter, G. J., Labuschagne, K., Mellor, P. S. & Carpenter, S. Life-history parameters of Culicoides (Avaritia) imicola Kieffer in the laboratory at different rearing temperatures. Vet. Parasitol. 163, 370–373 (2009).CAS 
    PubMed 
    Article 

    Google Scholar 
    Verhoef, F. A. A., Venter, G. J. & Weldon, C. W. Thermal limits of two biting midges, Culicoides imicola Kieffer and C. bolitinos Meiswinkel (Diptera: Ceratopogonidae). Parasites Vectors 7, 384 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Conte, A., Goffredo, M., Ippoliti, C. & Meiswinkel, R. Influence of biotic and abiotic factors on the distribution and abundance of Culicoides imicola and the Obsoletus Complex in Italy. Vet. Parasitol. 150, 333–344 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    Martinez-de la Puente, J., Navarro, J., Ferraguti, M., Soriguer, R. & Figuerola, J. First molecular identification of the vertebrate hosts of Culicoides imicola in Europe and a review of its blood-feeding patterns worldwide: Implications for the transmission of bluetongue disease and African horse sickness. Med. Vet. Entomol. 31, 333–339 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    Purse, B. V. et al. Impacts of climate, host and landscape factors on Culicoides species in Scotland. Med. Vet. Entomol. 26, 168–177 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    Leta, S. et al. Updating the global occurrence of Culicoides imicola, a vector for emerging viral diseases. Sci. Data 6, 1–8 (2019).CAS 
    Article 

    Google Scholar  More

  • in

    Warming response of peatland CO2 sink is sensitive to seasonality in warming trends

    Xia, J. et al. Terrestrial carbon cycle affected by non-uniform climate warming. Nat. Geosci. 7, 173–180 (2014).CAS 
    Article 

    Google Scholar 
    Tang, R. et al. Increasing terrestrial ecosystem carbon release in response to autumn cooling and warming. Nat. Clim. Change 12, 380–385 (2022).CAS 
    Article 

    Google Scholar 
    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 
    Article 

    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 
    Article 

    Google Scholar 
    Treat, C. C. et al. Widespread global peatland establishment and persistence over the last 130,000 y. Proc. Natl Acad. Sci. USA 116, 4822–4827 (2019).CAS 
    Article 

    Google Scholar 
    Frolking, S., Roulet, N. & Fuglestvedt, J. How northern peatlands influence the Earth’s radiative budget: sustained methane emission versus sustained carbon sequestration. J. Geophys. Res. Biogeosci. 111, G01008 (2006).
    Google Scholar 
    Loisel, J. et al. Expert assessment of future vulnerability of the global peatland carbon sink. Nat. Clim. Change 11, 70–77 (2021).Article 

    Google Scholar 
    Helbig, M. et al. Direct and indirect climate change effects on carbon dioxide fluxes in a thawing boreal forest–wetland landscape. Glob. Change Biol. 23, 3231–3248 (2017).Article 

    Google Scholar 
    Koebsch, F. et al. Refining the role of phenology in regulating gross ecosystem productivity across European peatlands. Glob. Change Biol. 26, 876–887 (2020).Article 

    Google Scholar 
    Huang, Y. et al. Tradeoff of CO2 and CH4 emissions from global peatlands under water-table drawdown. Nat. Clim. Change 11, 618–622 (2021).CAS 
    Article 

    Google Scholar 
    Evans, C. D. et al. Overriding water table control on managed peatland greenhouse gas emissions. Nature 593, 548–552 (2021).CAS 

    Google Scholar 
    Helfter, C. et al. Drivers of long-term variability in CO2 net ecosystem exchange in a temperate peatland. Biogeosciences 12, 1799–1811 (2015).Article 

    Google Scholar 
    Järveoja, J., Nilsson, M. B., Gažovič, M., Crill, P. M. & Peichl, M. Partitioning of the net CO2 exchange using an automated chamber system reveals plant phenology as key control of production and respiration fluxes in a boreal peatland. Glob. Change Biol. 24, 3436–3451 (2018).Article 

    Google Scholar 
    Mäkiranta, P. et al. Responses of phenology and biomass production of boreal fens to climate warming under different water-table level regimes. Glob. Change Biol. 24, 944–956 (2018).Article 

    Google Scholar 
    Li, Q. et al. Abiotic and biotic drivers of microbial respiration in peat and its sensitivity to temperature change. Soil Biol. Biochem. 153, 108077 (2021).CAS 
    Article 

    Google Scholar 
    Moore, T. R. et al. Spring photosynthesis in a cool temperate bog. Glob. Change Biol. 12, 2323–2335 (2006).Article 

    Google Scholar 
    Korrensalo, A. et al. Species-specific temporal variation in photosynthesis as a moderator of peatland carbon sequestration. Biogeosciences 14, 257–269 (2017).CAS 
    Article 

    Google Scholar 
    Weltzin, J. F. et al. Response of bog and fen plant communities to warming and water-table manipulations. Ecology 81, 3464–3478 (2000).Article 

    Google Scholar 
    Dimitrov, D. D., Grant, R. F., Lafleur, P. M. & Humphreys, E. R. Modeling the effects of hydrology on gross primary productivity and net ecosystem productivity at Mer Bleue bog. J. Geophys. Res. Biogeosci. 116, G04010 (2011).Article 
    CAS 

    Google Scholar 
    Bubier, J., Crill, P., Mosedale, A., Frolking, S. & Linder, E. Peatland responses to varying interannual moisture conditions as measured by automatic CO2 chambers. Glob. Biogeochem. Cycles 17, 1066 (2003).Article 
    CAS 

    Google Scholar 
    Moore, T. R. & Knowles, R. The influence of water table levels on methane and carbon dioxide emissions from peatland soils. Can. J. Soil Sci. 69, 33–38 (1989).CAS 
    Article 

    Google Scholar 
    Nichols, D. S. Temperature of upland and peatland soils in a north central Minnesota forest. Can. J. Soil Sci. 78, 493–509 (1998).Article 

    Google Scholar 
    Bellisario, L. M., Moore, T. R. & Bubier, J. L. Net ecosystem CO2 exchange in a boreal peatland, northern Manitoba. Écoscience 5, 534–541 (1998).Article 

    Google Scholar 
    Yu, Z. et al. Peatlands and their role in the global carbon cycle. Eos 92, 97–98 (2011).Article 

    Google Scholar 
    Hanson, P. J. et al. Rapid net carbon loss from a whole-ecosystem warmed peatland. AGU Adv. 1, e2020AV000163 (2020).Article 

    Google Scholar 
    Vincent, L. A. et al. Observed trends in Canada’s climate and influence of low-frequency variability modes. J. Clim. 28, 4545–4560 (2015).Article 

    Google Scholar 
    Templer, P. H. et al. Climate Change Across Seasons Experiment (CCASE): a new method for simulating future climate in seasonally snow-covered ecosystems. PLoS ONE 12, e0171928 (2017).Article 
    CAS 

    Google Scholar 
    Peichl, M. et al. A 12-year record reveals pre-growing season temperature and water table level threshold effects on the net carbon dioxide exchange in a boreal fen. Environ. Res. Lett. 9, 055006 (2014).Article 

    Google Scholar 
    Helbig, M., Humphreys, E. R. & Todd, A. Contrasting temperature sensitivity of CO2 exchange in peatlands of the Hudson Bay Lowlands, Canada. J. Geophys. Res. Biogeosci. 124, 2126–2143 (2019).CAS 
    Article 

    Google Scholar 
    Griffis, T. J., Rouse, W. R. & Waddington, J. M. Interannual variability of net ecosystem CO2 exchange at a subarctic fen. Glob. Biogeochem. Cycles 14, 1109–1121 (2000).CAS 
    Article 

    Google Scholar 
    Bubier, J. L., Crill, P. M., Moore, T. R., Savage, K. & Varner, R. K. Seasonal patterns and controls on net ecosystem CO2 exchange in a boreal peatland complex. Glob. Biogeochem. Cycles 12, 703–714 (1998).CAS 
    Article 

    Google Scholar 
    Park, S.-B. et al. Temperature control of spring CO2 fluxes at a coniferous forest and a peat bog in Central Siberia. Atmosphere 12, 984 (2021).CAS 
    Article 

    Google Scholar 
    Adkinson, A. C., Syed, K. H. & Flanagan, L. B. Contrasting responses of growing season ecosystem CO2 exchange to variation in temperature and water table depth in two peatlands in northern Alberta, Canada. J. Geophys. Res. Biogeosci. 116, G01004 (2011).Article 
    CAS 

    Google Scholar 
    Heiskanen, L. et al. Carbon dioxide and methane exchange of a patterned subarctic fen during two contrasting growing seasons. Biogeosciences 18, 873–896 (2021).CAS 
    Article 

    Google Scholar 
    Lafleur, P. M., Roulet, N. T., Bubier, J. L., Frolking, S. & Moore, T. R. Interannual variability in the peatland-atmosphere carbon dioxide exchange at an ombrotrophic bog. Glob. Biogeochem. Cycles 17, 1036 (2003).Article 
    CAS 

    Google Scholar 
    Joiner, D. W., Lafleur, P. M., McCaughey, J. H. & Bartlett, P. A. Interannual variability in carbon dioxide exchanges at a boreal wetland in the BOREAS northern study area. J. Geophys. Res. Atmos. 104, 27663–27672 (1999).CAS 
    Article 

    Google Scholar 
    McVeigh, P., Sottocornola, M., Foley, N., Leahy, P. & Kiely, G. Meteorological and functional response partitioning to explain interannual variability of CO2 exchange at an Irish Atlantic blanket bog. Agric. For. Meteorol. 194, 8–19 (2014).Article 

    Google Scholar 
    Helbig, M. et al. Increasing contribution of peatlands to boreal evapotranspiration in a warming climate. Nat. Clim. Change 10, 555–560 (2020).CAS 
    Article 

    Google Scholar 
    Bourgault, M.-A., Larocque, M. & Garneau, M. How do hydrogeological setting and meteorological conditions influence water table depth and fluctuations in ombrotrophic peatlands? J. Hydrol. X 4, 100032 (2019).Article 

    Google Scholar 
    Yurova, A., Wolf, A., Sagerfors, J. & Nilsson, M. Variations in net ecosystem exchange of carbon dioxide in a boreal mire: modeling mechanisms linked to water table position. J. Geophys. Res. Biogeosci. 112, G02025 (2007).Article 
    CAS 

    Google Scholar 
    Laine, A. M. et al. Warming impacts on boreal fen CO2 exchange under wet and dry conditions. Glob. Change Biol. 25, 1995–2008 (2019).Article 

    Google Scholar 
    Chivers, M. R., Turetsky, M. R., Waddington, J. M., Harden, J. W. & McGuire, A. D. Effects of experimental water table and temperature manipulations on ecosystem CO2 fluxes in an Alaskan rich fen. Ecosystems 12, 1329–1342 (2009).CAS 
    Article 

    Google Scholar 
    Juszczak, R. et al. Ecosystem respiration in a heterogeneous temperate peatland and its sensitivity to peat temperature and water table depth. Plant Soil 366, 505–520 (2013).CAS 
    Article 

    Google Scholar 
    Hao, D. et al. Estimating hourly land surface downward shortwave and photosynthetically active radiation from DSCOVR/EPIC observations. Remote Sens. Environ. 232, 111320 (2019).Article 

    Google Scholar 
    O’Donnell, J. A., Romanovsky, V. E., Harden, J. W. & McGuire, A. D. The effect of moisture content on the thermal conductivity of moss and organic soil horizons from black spruce ecosystems in interior Alaska. Soil Sci. 174, 646–651 (2009).Article 
    CAS 

    Google Scholar 
    Nijp, J. J. et al. Rain events decrease boreal peatland net CO2 uptake through reduced light availability. Glob. Change Biol. 21, 2309–2320 (2015).Article 

    Google Scholar 
    Zhang, Y., Commane, R., Zhou, S., Williams, A. P. & Gentine, P. Light limitation regulates the response of autumn terrestrial carbon uptake to warming. Nat. Clim. Change 10, 739–743 (2020).CAS 
    Article 

    Google Scholar 
    Samson, M. et al. The impact of experimental temperature and water level manipulation on carbon dioxide release in a poor fen in northern Poland. Wetlands 38, 551–563 (2018).Article 

    Google Scholar 
    Drever, C. R. et al. Natural climate solutions for Canada. Sci. Adv. 7, eabd6034 (2021).CAS 
    Article 

    Google Scholar 
    Hemes, K. S., Runkle, B. R. K., Novick, K. A., Baldocchi, D. D. & Field, C. B. An ecosystem-scale flux measurement strategy to assess natural climate solutions. Environ. Sci. Technol. 55, 3494–3504 (2021).CAS 
    Article 

    Google Scholar 
    Walker, T. W. N. et al. A systemic overreaction to years versus decades of warming in a subarctic grassland ecosystem. Nat. Ecol. Evol. 4, 101–108 (2020).Article 

    Google Scholar 
    Xu, B. et al. Seasonal variability of forest sensitivity to heat and drought stresses: a synthesis based on carbon fluxes from North American forest ecosystems. Glob. Change Biol. 26, 901–918 (2020).Article 

    Google Scholar 
    Piao, S. et al. Net carbon dioxide losses of northern ecosystems in response to autumn warming. Nature 451, 49–52 (2008).CAS 
    Article 

    Google Scholar 
    Joyce, P. et al. How robust Is the apparent break-down of northern high-latitude temperature control on spring carbon uptake? Geophys. Res. Lett. 48, e2020GL091601 (2021).Article 

    Google Scholar 
    Grant, R. F. et al. Changes in net ecosystem productivity of boreal black spruce stands in response to changes in temperature at diurnal and seasonal time scales. Tree Physiol. 29, 1–17 (2009).CAS 
    Article 

    Google Scholar 
    Kwon, M. J. et al. Siberian 2020 heatwave increased spring CO2 uptake but not annual CO2 uptake. Environ. Res. Lett. 16, 124030 (2021).CAS 
    Article 

    Google Scholar 
    Yu, Z., Griffis, T. J. & Baker, J. M. Warming temperatures lead to reduced summer carbon sequestration in the U.S. Corn Belt. Commun. Earth Environ. 2, 53 (2021).Article 

    Google Scholar 
    Wang, S. et al. Warmer spring alleviated the impacts of 2018 European summer heatwave and drought on vegetation photosynthesis. Agric. For. Meteorol. 295, 108195 (2020).Article 

    Google Scholar 
    Wang, T. et al. Emerging negative impact of warming on summer carbon uptake in northern ecosystems. Nat. Commun. 9, 5391 (2018).CAS 
    Article 

    Google Scholar 
    Lin, X. et al. Siberian and temperate ecosystems shape Northern Hemisphere atmospheric CO2 seasonal amplification. Proc. Natl Acad. Sci. USA 117, 21079–21087 (2020).CAS 
    Article 

    Google Scholar 
    Helbig, M. et al. Warming response of peatland CO2 sink is sensitive to seasonality in warming trends. Zenodo https://doi.org/10.5281/zenodo.6685222 (2022).Didan, K. MOD13Q1 MODIS/Terra Vegetation Indices 16-Day L3 Global 250 m SIN Grid V006 [Data set]. NASA EOSDIS Land Processes DAAC (2015); https://doi.org/10.5067/MODIS/MOD13Q1.006Harris, 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).Article 

    Google Scholar 
    Lees, K. J. et al. Using spectral indices to estimate water content and GPP in Sphagnum moss and other peatland vegetation. IEEE Trans. Geosci. Remote Sens. 58, 4547–4557 (2020).Article 

    Google Scholar 
    Bennett, A. C., McDowell, N. G., Allen, C. D. & Anderson-Teixeira, K. J. Larger trees suffer most during drought in forests worldwide. Nat. Plants 1, 15139 (2015).Article 

    Google Scholar 
    Page, S. E. & Baird, A. J. Peatlands and global change: response and resilience. Annu. Rev. Environ. Resour. 41, 35–57 (2016).Article 

    Google Scholar 
    Juottonen, H. et al. Integrating decomposers, methane-cycling microbes and ecosystem carbon fluxes along a peatland successional gradient in a land uplift region. Ecosystems https://doi.org/10.1007/s10021-021-00713-w (2021). More

  • in

    Post-foraging in-colony behaviour of a central-place foraging seabird

    Naef-Daenzer, B. Patch time allocation and patch sampling by foraging great and blue tits. Anim. Behav. 59, 989–999 (2000).CAS 
    PubMed 
    Article 

    Google Scholar 
    Kotler, B. P., Brown, J. S. & Bouskila, A. Apprehension and time allocation in gerbils: The effects of predatory risk and energetic state. Ecology 85, 917–922 (2004).Article 

    Google Scholar 
    Wajnberg, E., Bernhard, P., Hamelin, F. & Boivin, G. Optimal patch time allocation for time-limited foragers. Behav. Ecol. Sociobiol. 60, 1–10 (2006).Article 

    Google Scholar 
    Embar, K., Kotler, B. P. & Mukherjee, S. Risk management in optimal foragers: The effect of sightlines and predator type on patch use, time allocation, and vigilance in gerbils. Oikos 120, 1657–1666 (2011).Article 

    Google Scholar 
    Lima, S. L. & Bednekoff, P. A. Temporal variation in danger drives antipredator behavior: The predation risk allocation hypothesis. Am. Nat. 153, 649–659 (1999).PubMed 
    Article 

    Google Scholar 
    Beauchamp, G. & Ruxton, G. D. A reassessment of the predation risk allocation hypothesis: A comment on Lima and Bednekoff. Am. Nat. 177, 143–146 (2011).PubMed 
    Article 

    Google Scholar 
    Ferrari, M. C. O., Sih, A. & Chivers, D. P. The paradox of risk allocation: A review and prospectus. Anim. Behav. 78, 579–585 (2009).Article 

    Google Scholar 
    Wolf, L. L. & Hainsworth, F. R. Foraging efficiencies and time budgets in nectar-feeding birds. Ecology 56, 117–128 (1975).Article 

    Google Scholar 
    Litzow, M. A. & Piatt, J. F. Variance in prey abundance influences time budgets of breeding seabirds: Evidence from pigeon guillemots Cepphus columba. J. Avian Biol. 34, 54–64 (2003).Article 

    Google Scholar 
    Rishworth, G. M., Tremblay, Y. & Green, D. B. Drivers of time-activity budget variability during breeding in a pelagic seabird. PLoS One 9, e116544 (2014).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Stephens, D. W., Brown, J. S. & Ydenberg, R. C. Foraging: Behavior and Ecology. (The University of Chicago Press, 2007).Orians, G. & Pearson, N. On the theory of central place foraging. In Analysis of Ecological Systems (eds. Horn, D., Mitchell, R. & Stairs, G.) 154–177 (The Ohio State University Press, 1979).Chaurand, T. & Weimerskirch, H. The regular alternation of short and long foraging trips in the blue petrel Halobaena caerulea: A previously undescribed strategy of food provisioning in a pelagic seabird. J. Anim. Ecol. 63, 275–282 (1994).Article 

    Google Scholar 
    Weimerskirch, H. et al. Alternate long and short foraging trips in pelagic seabird parents. Anim. Behav. 47, 472–476 (1994).Article 

    Google Scholar 
    Welcker, J., Beiersdorf, A., Varpe, Ø. & Steen, H. Mass fluctuations suggest different functions of bimodal foraging trips in a central-place forager. Behav. Ecol. 23, 1372–1378 (2012).Article 

    Google Scholar 
    Welcker, J. et al. Flexibility in the bimodal foraging strategy of a high Arctic alcid, the little auk Alle alle. J. Avian Biol. 40, 388–399 (2009).Article 

    Google Scholar 
    Jakubas, D., Wojczulanis-Jakubas, K., Iliszko, L. M. & Kidawa, D. Flexibility of little auks foraging in various oceanographic features in a changing Arctic. Sci. Rep. https://doi.org/10.1038/s41598-020-65210-x (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Shoji, A. et al. Dual foraging and pair coordination during chick provisioning by Manx shearwaters: Empirical evidence supported by a simple model. J. Exp. Biol. 218, 2116–2123 (2015).PubMed 
    PubMed Central 

    Google Scholar 
    Phillips, R. A., Wakefield, E. D., Croxall, J. P., Fukuda, A. & Higuchi, H. Albatross foraging behaviour: No evidence for dual foraging, and limited support for anticipatory regulation of provisioning at South Georgia. Mar. Ecol. Prog. Ser. 391, 279–292 (2009).ADS 
    Article 

    Google Scholar 
    Brown, Z. W., Welcker, J., Harding, A. M. A., Walkusz, W. & Karnovsky, N. J. Divergent diving behavior during short and long trips of a bimodal forager, the little auk Alle alle. J. Avian Biol. 43, 215–226 (2012).Article 

    Google Scholar 
    Baduini, C. L. & Hyrenbach, K. D. Biogeography of procellariiform foraging strategies: Does ocean productivity influence provisioning?. Mar. Ornithol. 31, 101–112 (2003).
    Google Scholar 
    Navarro, J. & González-Solís, J. Environmental determinants of foraging strategies in Cory’s shearwaters Calonectris diomedea. Mar. Ecol. Prog. Ser. 378, 259–267 (2009).ADS 
    CAS 
    Article 

    Google Scholar 
    Ochi, D., Oka, N. & Watanuki, Y. Foraging trip decisions by the streaked shearwater Calonectris leucomelas depend on both parental and chick state. J. Ethol. 28, 313–321 (2010).Article 

    Google Scholar 
    Congdon, B. C., Krockenberger, A. K. & Smithers, B. V. Dual-foraging and co-ordinated provisioning in a tropical Procellariiform, the wedge-tailed shearwater. Mar. Ecol. Prog. Ser. 301, 293–301 (2005).ADS 
    Article 

    Google Scholar 
    Peck, D. R. & Congdon, B. C. Colony-specific foraging behaviour and co-ordinated divergence of chick development in the wedge-tailed shearwater Puffinus pacificus. Mar. Ecol. Prog. Ser. 299, 289–296 (2005).ADS 
    Article 

    Google Scholar 
    Weimerskirch, H. How can a pelagic seabird provision its chick when relying on a distant food resource? Cyclic attendance at the colony, foraging decision and body condition in sooty shearwaters. J. Anim. Ecol. 67, 99–109 (1998).Article 

    Google Scholar 
    Stempniewicz, L. BWP update. Little Auk (Alle alle). J. Birds West. Palearct. 3, 175–201 (2001).
    Google Scholar 
    Wojczulanis-Jakubas, K. & Jakubas, D. When and why does my mother leave me? The question of brood desertion in the Dovekie (Alle Alle). Auk 129, 632–637 (2012).Article 

    Google Scholar 
    Harding, A. M. A., Van Pelt, T. I., Lifjeld, J. T. & Mehlum, F. Sex differences in little auk Alle alle parental care: Transition from biparental to paternal-only care. Ibis (Lond. 1859). 146, 642–651 (2004).Article 

    Google Scholar 
    Wojczulanis-Jakubas, K. et al. Duration of female parental care and their survival in the little auk Alle alle—Are these two traits linked ?. Behav. Ecol. Sociobiol. 74, 1–11 (2020).Article 

    Google Scholar 
    Wojczulanis, K., Dariusz, J. & Lech, S. The Little Auk Alle alle: An ecological indicator of a changing Arctic and a model organism. Polar Biol. https://doi.org/10.1007/s00300-021-02981-7 (2021).Article 

    Google Scholar 
    Steen, H., Vogedes, D., Broms, F., Falk-Petersen, S. & Berge, J. Little auks (Alle alle) breeding in a High Arctic fjord system: Bimodal foraging strategies as a response to poor food quality?. Polar Res. 26, 118–125 (2007).Article 

    Google Scholar 
    Wojczulanis-Jakubas, K., Jakubas, D., Karnovsky, N. J. & Walkusz, W. Foraging strategy of little auks under divergent conditions on feeding grounds. Polar Res. 29, 22–29 (2010).Article 

    Google Scholar 
    Jakubas, D., Wojczulanis-Jakubas, K., Iliszko, L., Darecki, M. & Stempniewicz, L. Foraging strategy of the little auk Alle alle throughout breeding season—switch from unimodal to bimodal pattern. J. Avian Biol. 45, 551–560 (2014).Article 

    Google Scholar 
    Jakubas, D., Iliszko, L., Wojczulanis-Jakubas, K. & Stempniewicz, L. Foraging by little auks in the distant marginal sea ice zone during the chick-rearing period. Polar Biol. 35, 73–81 (2012).Article 

    Google Scholar 
    Jakubas, D. et al. Intra-seasonal variation in zooplankton availability, chick diet and breeding performance of a high Arctic planktivorous seabird. Polar Biol. 391, 1547–1561 (2016).Article 

    Google Scholar 
    Jakubas, D. et al. Foraging closer to the colony leads to faster growth in little auks. Mar. Ecol. Prog. Ser. 489, 263–278 (2013).ADS 
    Article 

    Google Scholar 
    Stempniewicz, L. Predator-prey interactions between Glaucous Gull Larus hyperboreus and Little Auk Alle alle in Spitsbergen. Acta Ornithol. 29, 155–170 (1995).
    Google Scholar 
    Wojczulanis-Jakubas, K., Jakubas, D. & Stempniewicz, L. Changes in the glaucous gull predatory pressure on little auks in Southwest Spitsbergen. Waterbirds 28, 430–435 (2005).Article 

    Google Scholar 
    Kharitonov, S. Methods and Theoretical Aspects of Seabird Studies. (Proc 5 All-Russian Mar Biol School, Marine Biological Institute, 2007).Wojczulanis-Jakubas, K., Jakubas, D. & Stempniewicz, L. Avifauna of Hornsund area, SW Spitsbergen: Present state and recent changes. Polish Polar Res. 29, 187–197 (2008).
    Google Scholar 
    Keslinka, K. L., Wojczulanis-Jakubas, K., Jakubas, D. & Neubauer, G. Determinants of the little auk (Alle alle) breeding colony location and size in W and NW coast of Spitsbergen. PLoS One 14, 1–20 (2019).
    Google Scholar 
    Kidawa, D., Barcikowski, M. & Palme, R. Parent-offspring interactions in a long-lived seabird, the Little Auk (Alle alle): Begging and provisioning under simulated stress. J. Ornithol. 158, 145–157 (2017).Article 

    Google Scholar 
    Welcker, J., Beiersdorf, A., Varpe, Ø. & Steen, H. Mass fluctuations suggest different functions of bimodal foraging trips in a central-place forager. Behav. Ecol. https://doi.org/10.1093/beheco/ars131 (2012).Article 

    Google Scholar 
    Jakubas, D. & Wojczulanis, K. Predicting the sex of Dovekies by discriminant analysis. Waterbirds 30, 92–96 (2007).Article 

    Google Scholar 
    Grissot, A. et al. Parental coordination of chick provisioning in a planktivorous arctic seabird under divergent conditions on foraging grounds. Front. Ecol. Evol. 7, 349 (2019).Article 

    Google Scholar 
    Stoffel, M. A., Nakagawa, S. & Schielzeth, H. rptR: Repeatability estimation and variance decomposition by generalized linear mixed-effects models. Methods Ecol. Evol. 8, 1639–1644 (2017).Article 

    Google Scholar 
    R Core Team. R: A Language and Environment for Statistical Computing. R. (2019).Wojczulanis-Jakubas, K., Jakubas, D. & Stempniewicz, L. Sex-specific parental care by incubating Little Auks (Alle alle). Ornis Fenn. 86, 140–148 (2009).
    Google Scholar 
    Welcker, J., Steen, H., Harding, A. M. A. & Gabrielsen, G. W. Sex-specific provisioning behaviour in a monomorphic seabird with a bimodal foraging strategy. Ibis (Lond. 1859). 151, 502–513 (2009).Article 

    Google Scholar 
    Kidawa, D. et al. Parental efforts of an Arctic seabird, the little auk Alle alle under variable foraging conditions. Mar. Biol. Res. 11, 349–360 (2015).Article 

    Google Scholar 
    Wickham, H. Hadley Wickham. Media 35, 211 (2009).
    Google Scholar 
    Karnovsky, N. J. et al. Inter-colony comparison of diving behavior of an Arctic top predator: Implications for warming in the Greenland Sea. Mar. Ecol. Prog. Ser. 440, 229–240 (2011).ADS 
    Article 

    Google Scholar 
    Karnovsky, N. et al. Foraging distributions of little auks Alle alle across the Greenland Sea: Implications of present and future Arctic climate change. Mar. Ecol. Prog. Ser. 415, 283–293 (2010).ADS 
    Article 

    Google Scholar 
    Gremillet, D. et al. Little auks buffer the impact of current Arctic climate change. Mar. Ecol. Prog. Ser. 454, 197–206 (2012).ADS 
    Article 

    Google Scholar 
    Harding, A. M. A. et al. Flexibility in the parental effort of an Arctic-breeding seabird. Funct. Ecol. 23, 348–358 (2009).Article 

    Google Scholar 
    Jakubas, D. et al. Foraging effort does not influence body condition and stress level in little auks. Mar. Ecol. Prog. Ser. 432, 277–290 (2011).ADS 
    Article 

    Google Scholar 
    Jakubas, D., Wojczulanis-Jakubas, K., Iliszko, L. M., Strøm, H. & Stempniewicz, L. Habitat foraging niche of a High Arctic zooplanktivorous seabird in a changing environment. Sci. Rep. 7, 1–14 (2017).CAS 
    Article 

    Google Scholar  More

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    Increased incompatibility of heterologous algal symbionts under thermal stress in the cnidarian-dinoflagellate model Aiptasia

    Sylvan, J. How to protect a coral reef: the public trust doctrine and the law of the sea recommended citation. Sustain. Dev. Law Policy 7, 12 (2006).
    Google Scholar 
    LaJeunesse, T. C. et al. Systematic revision of symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr. Biol. 28, 2570–2580.e6 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    Kopp, C. et al. Highly dynamic cellular-level response of symbiotic coral to a sudden increase in environmental nitrogen. mBio 4, e00052–13 (2013).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Muscatine, L. The role of symbiotic algae in carbon and energy flux in reef corals. Coral Reef. 25, 75–87 (1990).
    Google Scholar 
    Dubinsky, Z. & Stambler, N. Coral reefs: an ecosystem in transition. (Springer, 2011).Wiedenmann, J. et al. Nutrient enrichment can increase the susceptibility of reef corals to bleaching. https://doi.org/10.1038/NCLIMATE1661 (2012).Suggett, D. J., Warner, M. E. & Leggat, W. Symbiotic dinoflagellate functional diversity mediates coral survival under ecological crisis. Trends Ecol. Evolution 32, 735–745 (2017).Article 

    Google Scholar 
    Morris, L. A., Voolstra, C. R., Quigley, K. M., Bourne, D. G. & Bay, L. K. Nutrient availability and metabolism affect the stability of coral–symbiodiniaceae symbioses. Trends Microbiol. 27, 678–689 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Lehnert, E. M. et al. Extensive differences in gene expression between symbiotic and aposymbiotic cnidarians. G3 (Bethesda) 4, 277–95 (2014).CAS 
    Article 

    Google Scholar 
    Dubinsky, Z. & Berman-Frank, I. Uncoupling primary production from population growth in photosynthesizing organisms in aquatic ecosystems. in. Aquat. Sci. 63, 4–17 (2001).CAS 
    Article 

    Google Scholar 
    Burriesci, M. S., Raab, T. K. & Pringle, J. R. Evidence that glucose is the major transferred metabolite in dinoflagellate–cnidarian symbiosis. J. Exp. Biol. 215, 3467–3477 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Davy, S. K., Allemand, D. & Weis, V. M. Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol. Mol. Biol. Rev. 76, 229–61 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Rädecker, N., Pogoreutz, C., Voolstra, C. R., Wiedenmann, J. & Wild, C. Nitrogen cycling in corals: the key to understanding holobiont functioning? Trends Microbiol. 23, 490–497 (2015).PubMed 
    Article 
    CAS 

    Google Scholar 
    Cui, G. et al. Host-dependent nitrogen recycling as a mechanism of symbiont control in Aiptasia. PLOS Genet. 15, e1008189 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Rädecker, N. et al. Heat stress destabilizes symbiotic nutrient cycling in corals. Proc. Natl Acad. Sci. USA 118, https://doi.org/10.1073/pnas.2022653118 (2021).Weis, V. M. Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis. J. Exp. Biol. 211, 3059–3066 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    Wooldridge, S. A. Breakdown of the coral-algae symbiosis: towards formalising a linkage between warm-water bleaching thresholds and the growth rate of the intracellular zooxanthellae. Biogeosciences Discuss. 9, 8111–8139 (2012).
    Google Scholar 
    Cziesielski, M. J., Schmidt‐Roach, S. & Aranda, M. The past, present, and future of coral heat stress studies. Ecol. Evol. https://doi.org/10.1002/ece3.5576 (2019).Leggat, W. et al. Differential responses of the coral host and their algal symbiont to thermal stress. PLoS ONE 6, e26687 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Pinzón, J. H. et al. Whole transcriptome analysis reveals changes in expression of immune-related genes during and after bleaching in a reef-building coral. R. Soc. Open Sci. 2, 140214 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Ziegler, M., Seneca, F. O., Yum, L. K., Palumbi, S. R. & Voolstra, C. R. Bacterial community dynamics are linked to patterns of coral heat tolerance. Nat. Commun. 8, 14213 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bang, C. et al. Metaorganisms in extreme environments: do microbes play a role in organismal adaptation? Zoology 127, 1–19 (2018).PubMed 
    Article 

    Google Scholar 
    Berkelmans, R. & van Oppen, M. J. H. The role of zooxanthellae in the thermal tolerance of corals: a “nugget of hope” for coral reefs in an era of climate change. Proc. Biol. Sci./R. Soc. 273, 2305–12 (2006).
    Google Scholar 
    Sampayo, E. M., Ridgway, T., Bongaerts, P. & Hoegh-Guldberg, O. Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type. Proc. Natl Acad. Sci. 105, 10444–10449 (2008).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Howells, E. J. et al. Coral thermal tolerance shaped by local adaptation of photosymbionts. Nat. Clim. Change https://doi.org/10.1038/nclimate1330 (2011).Cziesielski, M. J. et al. Multi-omics analysis of thermal stress response in a zooxanthellate cnidarian reveals the importance of associating with thermotolerant symbionts. Proc. Biol. Sci. 285, 20172654 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    Baker, A. C., Starger, C. J., McClanahan, T. R. & Glynn, P. W. Corals’ adaptive response to climate change. Nature 430, 741–741 (2004).CAS 
    PubMed 
    Article 

    Google Scholar 
    Thornhill, D. J., LaJeunesse, T. C., Kemp, D. W., Fitt, W. K. & Schmidt, G. W. Multi-year, seasonal genotypic surveys of coral-algal symbioses reveal prevalent stability or post-bleaching reversion. Mar. Biol. 148, 711–722 (2006).Article 

    Google Scholar 
    Palumbi, S. R., Barshis, D. J., Traylor-Knowles, N. & Bay, R. A. Mechanisms of reef coral resistance to environmental stress,making its relative ability to acclimate or adapt extremely important to the to future climate change. Science 344, 895–898 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    Herrera, M. et al. Temperature transcends partner specificity in the symbiosis establishment of a cnidarian. ISME J. 15, 141–153 (2021).CAS 
    PubMed 
    Article 

    Google Scholar 
    Howells, E. J. et al. Corals in the hottest reefs in the world exhibit symbiont fidelity not flexibility. Mol. Ecol. 29, 899–911 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Hume, B. C. C., Mejia-Restrepo, A., Voolstra, C. R. & Berumen, M. L. Fine-scale delineation of Symbiodiniaceae genotypes on a previously bleached central Red Sea reef system demonstrates a prevalence of coral host-specific associations. Coral Reefs 1–19 https://doi.org/10.1007/s00338-020-01917-7 (2020).Perez, S. F., Cook, C. B. & Brooks, W. R. The role of symbiotic dinoflagellates in the temperature-induced bleaching response of the subtropical sea anemone Aiptasia pallida. J. Exp. Mar. Biol. Ecol. 256, 1–14 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    Mieog, J. C. et al. The roles and interactions of symbiont, host and environment in defining coral fitness. PLoS ONE 4, e6364 (2009).Cantin, N. E., van Oppen, M. J. H., Willis, B. L., Mieog, J. C. & Negri, A. P. Juvenile corals can acquire more carbon from high-performance algal symbionts. Coral Reefs 28, 405–414 (2009).Article 

    Google Scholar 
    Herrera, M. et al. Unfamiliar partnerships limit cnidarian holobiont acclimation to warming. Glob. Change Biol. 26, 5539–5553 (2020).Article 

    Google Scholar 
    LaJeunesse, T. et al. Closely related Symbiodinium spp. differ in relative dominance in coral reef host communities across environmental, latitudinal and biogeographic gradients. Mar. Ecol. Prog. Ser. 284, 147–161 (2004).Article 

    Google Scholar 
    Parkinson, J. E. & Baums, I. B. The extended phenotypes of marine symbioses: ecological and evolutionary consequences of intraspecific genetic diversity in coral-algal associations. Front. Microbiol. 5, 445 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Coffroth, M. A., Poland, D. M., Petrou, E. L., Brazeau, D. A. & Holmberg, J. C. Environmental symbiont acquisition may not be the solution to warming seas for reef-building corals. PLoS ONE 5, e13258 (2010).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Bellantuono, A. J., Granados-Cifuentes, C., Miller, D. J., Hoegh-Guldberg, O. & Rodriguez-Lanetty, M. Coral thermal tolerance: tuning gene expression to resist thermal stress. PLoS ONE 7, e50685 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Sunagawa, S. et al. Generation and analysis of transcriptomic resources for a model system on the rise: the sea anemone Aiptasia pallida and its dinoflagellate endosymbiont. BMC Genomics 10, 258 (2009).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Baumgarten, S. et al. The genome of Aiptasia, a sea anemone model for coral symbiosis. Proc. Natl Acad. Sci. 112, 201513318 (2015).
    Google Scholar 
    Matthews, J. L. et al. Menthol-induced bleaching rapidly and effectively provides experimental aposymbiotic sea anemones (Aiptasia sp.) for symbiosis investigations. J. Exp. Biol. jeb.128934 https://doi.org/10.1242/JEB.128934 (2015).Kenkel, C. D. et al. Evidence for a host role in thermotolerance divergence between populations of the mustard hill coral (Porites astreoides) from different reef environments. Mol. Ecol. 22, 4335–4348 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    Polato, N. R., Altman, N. S. & Baums, I. B. Variation in the transcriptional response of threatened coral larvae to elevated temperatures. Mol. Ecol. 22, 1366–1382 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    DeSalvo, M., Sunagawa, S., Voolstra, C. R. & Medina, M. Transcriptomic resonses to heat stress and bleaching in the elkhorn coral Acropora palmata. Mar. Ecol. Prog. Ser. 402, 97–113 (2010).CAS 
    Article 

    Google Scholar 
    Maor-Landaw, K. & Levy, O. Gene expression profiles during short-term heat stress; branching vs. massive Scleractinian corals of the Red Sea. PeerJ 4, e1814 (2016).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Yamamoto, K. et al. Control of the heat stress-induced alternative splicing of a subset of genes by hnRNP K. Genes Cells 21, 1006–1014 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    Seneca, F. O. & Palumbi, S. R. The role of transcriptome resilience in resistance of corals to bleaching. Mol. Ecol. 24, 1467–1484 (2015).PubMed 
    Article 

    Google Scholar 
    Meyer, E. & Weis, V. M. Study of cnidarian-algal symbiosis in the “omics” age. Biol. Bull. 223, 44–65 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    Oakley, C. A. et al. Thermal shock induces host proteostasis disruption and endoplasmic reticulum stress in the model symbiotic Cnidarian Aiptasia. J. Proteome Res. 16, 2121–2134 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    Robbart, M. L., Peckol, P., Scordilis, S. P., Curran, H. A. & Brown-Saracino, J. Population recovery and differential heat shock protein expression for the corals Agaricia agaricites and A-tenuifolia in Belize. Mar. Ecol. Prog. Ser. 283, 151–160 (2004).Article 

    Google Scholar 
    Barshis, D. J. et al. Genomic basis for coral resilience to climate change. Proc. Natl Acad. Sci. 110, 1387–1392 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Traylor-Knowles, N., Rose, N. H. & Palumbi, S. R. The cell specificity of gene expression in the response to heat stress in corals. J. Exp. Biol. 220, 1837–1845 (2017).PubMed 

    Google Scholar 
    Benchimol, S. p53-dependent pathways of apoptosis. Cell Death Differ. 8, 1049–1051 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    Moya, A. et al. Functional conservation of the apoptotic machinery from coral to man: The diverse and complex Bcl-2 and caspase repertoires of Acropora millepora. BMC Genomics 17, 62 (2016).Elmore, S. Apoptosis: a review of programmed cell death. Toxicol. Pathol. 35, 495–516 (2007).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Karim, W., Nakaema, S. & Hidaka, M. Temperature effects on the growth rates and photosynthetic activities of symbiodinium cells. J. Mar. Sci. Eng. 3, 368–381 (2015).Article 

    Google Scholar 
    Cunning, R. & Baker, A. C. Excess algal symbionts increase the susceptibility of reef corals to bleaching. Nat. Clim. Change 3, 259–262 (2013).Article 

    Google Scholar 
    Rehman, A. U. et al. Symbiodinium sp. cells produce light-induced intra- and extracellular singlet oxygen, which mediates photodamage of the photosynthetic apparatus and has the potential to interact with the animal host in coral symbiosis. N. Phytologist 212, 472–484 (2016).CAS 
    Article 

    Google Scholar 
    Lesser, K. B. & Garcia, F. A. Association between polycystic ovary syndrome and glucose intolerance during pregnancy. J. Matern. Fetal Med. 6, 303–307 (1997).CAS 
    PubMed 
    Article 

    Google Scholar 
    Dunn, S. R., Schnitzler, C. E. & Weis, V. M. Apoptosis and autophagy as mechanisms of dinoflagellate symbiont release during cnidarian bleaching: every which way you lose. Proc. R. Soc. Lond. B: Biol. Sci. 274, 3079–3085 (2007).
    Google Scholar 
    DeSalvo, M. K. et al. Coral host transcriptomic states are correlated with Symbiodinium genotypes. Mol. Ecol. 19, 1174–1186 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    Levin, R. A. et al. Engineering strategies to decode and enhance the genomes of coral symbionts. Front. Microbiol. https://doi.org/10.3389/fmicb.2017.01220 (2017).Yuyama, I., Ishikawa, M., Nozawa, M., Yoshida, M. & Ikeo, K. Transcriptomic changes with increasing algal symbiont reveal the detailed process underlying establishment of coral-algal symbiosis. Sci. Rep. 8, 16802 (2018).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Sproles, A. E. et al. Sub-cellular imaging shows reduced photosynthetic carbon and increased nitrogen assimilation by the non-native endosymbiont Durusdinium trenchii in the model cnidarian Aiptasia. Environ. Microbiol. 22, 3741–3753 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Rädecker, N. et al. Using Aiptasia as a model to study metabolic interactions in Cnidarian-Symbiodinium symbioses. Front. Physiol. 9, 214 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Falkowski, P. G., Dubinsky, Z., Muscatine, L. & McCloskey, L. Population control in symbiotic corals. BioScience 43, 606–611 (1993).Article 

    Google Scholar 
    Wang & Douglas. Nitrogen recycling or nitrogen conservation in an alga-invertebrate symbiosis? J. Exp. Biol. 201, 2445–53 (1998).Loram, J. E., Trapido-Rosenthal, H. G. & Douglas, A. E. Functional significance of genetically different symbiotic algae Symbiodinium in a coral reef symbiosis. Mol. Ecol. 16, 4849–4857 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    Karako-Lampert, S. et al. Transcriptome analysis of the scleractinian coral Stylophora pistillata. PLoS One 9, e88615 (2014).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Hillyer, K. E., Tumanov, S., Villas-Bôas, S. & Davy, S. K. Metabolite profiling of symbiont and host during thermal stress and bleaching in a model cnidarian-dinoflagellate symbiosis. J. Exp. Biol. 219, 516–27 (2016).PubMed 

    Google Scholar 
    Bertucci, A., Forêt, S., Ball, E. E. & Miller, D. J. Transcriptomic differences between day and night in Acropora millepora provide new insights into metabolite exchange and light-enhanced calcification in corals. Mol. Ecol. 24, 4489–4504 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    Matthews, J. L. et al. Optimal nutrient exchange and immune responses operate in partner specificity in the cnidarian-dinoflagellate symbiosis. Proc. Natl Acad. Sci. 114, 13194–13199 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Lin, M.-F., Takahashi, S., Forêt, S., Davy, S. K. & Miller, D. J. Transcriptomic analyses highlight the likely metabolic consequences of colonization of a cnidarian host by native or non-native Symbiodinium species. Biol. Open 8, bio038281 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Medrano, E., Merselis, D. G., Bellantuono, A. J. & Rodriguez-Lanetty, M. Proteomic Basis of Symbiosis: A Heterologous Partner Fails to Duplicate Homologous Colonization in a Novel Cnidarian– Symbiodiniaceae Mutualism. Front. Microbiol. 10, 1153 (2019).Schoepf, V., Stat, M., Falter, J. L. & McCulloch, M. T. Limits to the thermal tolerance of corals adapted to a highly fluctuating, naturally extreme temperature environment. Sci. Rep. 5, 17639 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Xiang, T., Hambleton, E. A., DeNofrio, J. C., Pringle, J. R. & Grossman, A. R. Isolation of clonal axenic strains of the symbiotic dinoflagellate Symbiodinium and their growth and host specificity1. J. Phycol. 49, 447–458 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    Bray, N. L., Pimentel, H., Melsted, P. & Pachter, L. Near-optimal probabilistic RNA-seq quantification. Nat. Biotechnol. 34, 525–527 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    Pimentel, H., Bray, N. L., Puente, S., Melsted, P. & Pachter, L. Differential analysis of RNA-seq incorporating quantification uncertainty. Nat. Methods 14, 687–690 (2017).CAS 
    PubMed 
    Article 

    Google Scholar  More