Ecology

Tilman, D., May, R. M., Lehman, C. L. & Nowak, M. A. Habitat destruction and the extinction debt. Nature 371, 65–66 (1994).Article 

Google Scholar 
Newbold, T. et al. Global effects of land use on local terrestrial biodiversity. Nature 520, 45–50 (2015).Article 
CAS 
PubMed 

Google Scholar 
Urban, M. C. Accelerating extinction risk from climate change. Science 348, 571–573 (2015).Article 
CAS 
PubMed 

Google Scholar 
Fonseca, C. R. et al. Conservation biology: four decades of problem- and solution-based research. Perspect. Ecol. Conserv. 19, 121–130 (2021).
Google Scholar 
Smits, P. & Finnegan, S. How predictable is extinction? Forecasting species survival at million-year timescales. Philos. Trans. R. Soc. B Biol. Sci. 374, 20190392 (2019).Article 

Google Scholar 
Hanski, I. & Ovaskainen, O. Extinction debt at extinction threshold. Conserv. Biol. 16, 666–673 (2002).Article 

Google Scholar 
Kuussaari, M. et al. Extinction debt: a challenge for biodiversity conservation. Trends Ecol. Evol. 24, 564–571 (2009).Article 
PubMed 

Google Scholar 
Ridding, L. E. et al. Inconsistent detection of extinction debts using different methods. Ecography 44, 33–43 (2021).Article 

Google Scholar 
Berglund, H. & Jonsson, B. G. Verifying an extinction debt among lichens and fungi in northern Swedish boreal forests. Conserv. Biol. 19, 338–348 (2005).Article 

Google Scholar 
Jones, I. L., Bunnefeld, N., Jump, A. S., Peres, C. A. & Dent, D. H. Extinction debt on reservoir land-bridge islands. Biol. Conserv. 199, 75–83 (2016).Article 

Google Scholar 
Triantis, K. et al. Extinction debt on oceanic islands. Ecography 33, 285–294 (2010).
Google Scholar 
Wearn, O. R., Reuman, D. C. & Ewers, R. M. Extinction debt and windows of conservation opportunity in the Brazilian Amazon. Science 337, 228–232 (2012).Article 
CAS 
PubMed 

Google Scholar 
Pan, Y. et al. Spatial and temporal scales of landscape structure affect the biodiversity-landscape relationship across ecologically distinct species groups. Landsc. Ecol. 37, 2311–2325 (2022).Article 

Google Scholar 
Soga, M. & Koike, S. Mapping the potential extinction debt of butterflies in a modern city: Implications for conservation priorities in urban landscapes. Anim. Conserv. 16, 1–11 (2013).Article 

Google Scholar 
Knapp, S., Winter, M. & Klotz, S. Increasing species richness but decreasing phylogenetic richness and divergence over a 320-year period of urbanization. J. Appl. Ecol. 54, 1152–1160 (2017).Article 

Google Scholar 
McGill, B. J., Dornelas, M., Gotelli, N. J. & Magurran, A. E. Fifteen forms of biodiversity trend in the anthropocene. Trends Ecol. Evol. 30, 104–113 (2015).Article 
PubMed 

Google Scholar 
Chen, Y. & Peng, S. Evidence and mapping of extinction debts for global forest-dwelling reptiles, amphibians and mammals. Sci. Rep. 7, 1–10 (2017).
Google Scholar 
Krauss, J. et al. Habitat fragmentation causes immediate and time-delayed biodiversity loss at different trophic levels. Ecol. Lett. 13, 597–605 (2010).Article 
PubMed 
PubMed Central 

Google Scholar 
Cowlishaw, G. Predicting the pattern of decline of African primate diversity: An extinction debt from historical deforestation. Conserv. Biol. 13, 1183–1193 (1999).Article 

Google Scholar 
Figueiredo, L., Krauss, J., Steffan-Dewenter, I. & Sarmento Cabral, J. Understanding extinction debts: spatio–temporal scales, mechanisms and a roadmap for future research. Ecography 42, 1973–1990 (2019).Article 

Google Scholar 
Aerts, R. & Honnay, O. Forest restoration, biodiversity and ecosystem functioning. BMC Ecol. 11, 1–21 (2011).Article 

Google Scholar 
Haddad, N. M. et al. Habitat fragmentation and its lasting impact on Earth’s ecosystems. Sci. Adv. 1, e1500052 (2015).Article 
PubMed 
PubMed Central 

Google Scholar 
Maxwell, S. L. et al. Area-based conservation in the twenty-first century. Nature 586, 217–227 (2020).Article 
CAS 
PubMed 

Google Scholar 
IUCN. The IUCN Red List of Threatened Species, Version 2019-1. https://www.iucnredlist.org. Downloaded on 23 February 2022. (2019).Brown, J. L. et al. Spatial biodiversity patterns of Madagascar’s amphibians and reptiles. PLoS ONE 11, e0144076 (2016).Article 
PubMed 
PubMed Central 

Google Scholar 
Powney, G. D., Grenyer, R., Orme, C. D. L., Owens, I. P. F. & Meiri, S. Hot, dry and different: Australian lizard richness is unlike that of mammals, amphibians and birds. Glob. Ecol. Biogeogr. 19, 386–396 (2010).Article 

Google Scholar 
Pianka, E. R. Desert lizard diversity: additional comments and some data. Am. Nat. 134, 344–364 (1989).Article 

Google Scholar 
Chen, Y. H. Combining the species-area-habitat relationship and environmental cluster analysis to set conservation priorities: A study in the Zhoushan Archipelago, China. Conserv. Biol. 23, 537–545 (2009).Article 
PubMed 

Google Scholar 
Ricklefs, R. E. & Lovette, I. J. The roles of island area per se and habitat diversity in the species-area relationships of four Lesser Antillean faunal groups. J. Anim. Ecol. 68, 1142–1160 (1999).Article 

Google Scholar 
Souza, F. L., Martins, F. I. & Raizer, J. Habitat heterogeneity and anuran community of an agroecosystem in the Pantanal of Brazil. Phyllomedusa 13, 41–50 (2014).Article 

Google Scholar 
Kelt, D. A. & Van Vuren, D. H. The ecology and macroecology of mammalian home range area. Am. Nat. 157, 637–645 (2001).Article 
CAS 
PubMed 

Google Scholar 
McNab, B. K. Bioenergetics and the determination of home range size. Am. Nat. 97, 133–140 (1963).Article 

Google Scholar 
Powell, R. A. & Mitchell, M. S. What is a home range? J. Mammal. 93, 948–958 (2012).Article 

Google Scholar 
Hoffmann, S., Irl, S. D. H. & Beierkuhnlein, C. Predicted climate shifts within terrestrial protected areas worldwide. Nat. Commun. 10, 1–10 (2019).Article 

Google Scholar 
Giam, X. et al. Reservoirs of richness: least disturbed tropical forests are centres of undescribed species diversity. Proc. R. Soc. B 279, 67–76 (2012).Article 
PubMed 

Google Scholar 
Pillay, R. et al. Tropical forests are home to over half of the world’s vertebrate species. Front. Ecol. Environ. 20, 10–15 (2022).Article 
PubMed 

Google Scholar 
Li, H. et al. Large numbers of vertebrates began rapid population decline in the late 19th century. Proc. Natl Acad. Sci. USA 113, 14079–14084 (2016).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Pringle, R. M. Upgrading protected areas to conserve wild biodiversity. Nature 546, 91–99 (2017).Article 
CAS 
PubMed 

Google Scholar 
Forzieri, G., Dakos, V., McDowell, N. G., Ramdane, A. & Cescatti, A. Emerging signals of declining forest resilience under climate change. Nature 608, 534–539 (2022).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Diamond, J. M. Biogeographic kinetics: estimation of relaxation times for Avifaunas of southwest Pacific islands. Proc. Natl Acad. Sci. USA 69, 3199–3203 (1972).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Jackson, S. T. & Sax, D. F. Balancing biodiversity in a changing environment: extinction debt, immigration credit and species turnover. Trends Ecol. Evol. 25, 153–160 (2010).Article 
PubMed 

Google Scholar 
Foley, J. A. et al. Amazonia revealed: forest degradation and loss of ecosystem goods and services in the Amazon Basin. Front. Ecol. Environ. 5, 25–32 (2007).Article 

Google Scholar 
Asamoah, E. F., Beaumont, L. J. & Maina, J. M. Climate and land-use changes reduce the benefits of terrestrial protected areas. Nat. Clim. Chang. 11, 1105–1110 (2021).Article 

Google Scholar 
Hurtt, G. C. et al. Harmonization of land-use scenarios for the period 1500–2100: 600 years of global gridded annual land-use transitions, wood harvest, and resulting secondary lands. Clim. Change 109, 117–161 (2011).Article 

Google Scholar 
Peng, S. et al. Sensitivity of land use change emission estimates to historical land use and land cover mapping. Glob. Biogeochem. Cycles 31, 626–643 (2017).Article 
CAS 

Google Scholar 
Jain, A. K., Meiyappan, P., Song, Y. & House, J. I. CO2 emissions from land-use change affected more by nitrogen cycle, than by the choice of land-cover data. Glob. Chang. Biol. 19, 2893–2906 (2013).Article 
PubMed 

Google Scholar 
Poulter, B. et al. Plant functional type classification for earth system models: results from the European Space Agency’s Land Cover Climate Change Initiative. Geosci. Model Dev. 8, 2315–2328 (2015).Article 

Google Scholar 
Pongratz, J., Reick, C., Raddatz, T. & Claussen, M. A reconstruction of global agricultural areas and land cover for the last millennium. Global Biogeochem. Cycles 22, (2008).Dietz, F. C. The industrial revolution. In the Hands of a Child (1970).Gütschow, J., Jeffery, L. & Gieseke, R. The PRIMAP-hist national historical emissions time series (1850-2016). V. 2.0. GFZ Data Services (2019).Dinerstein, E. et al. An ecoregion-based approach to protecting half the terrestrial realm. Bioscience 67, 534–545 (2017).Article 
PubMed 
PubMed Central 

Google Scholar 
Protected Planet: The World Database on Protected Areas (UNEP-WCMC and IUCN, accessed 9 January 2022); www.protectedplanet.net.Butchart, S. H. M. et al. Shortfalls and solutions for meeting national and global conservation area targets. Conserv. Lett. 8, 329–337 (2015).Article 

Google Scholar 
R Core Team. R: A Language and Environment for Statistical Computing Version 4.0.2 (2020). More

Whale entanglements in fishing gear threaten whale populations, seafood production and long-term sustainability of commercial fisheries. While multiple mitigation strategies to reduce entanglements exist, there has been minimal consideration of the economic impact of these strategies. Here, we estimated retrospective losses to ex-vessel revenues for one of California’s most lucrative fisheries. Overall, we found fishery closures decreased ex-vessel revenue, with results showing some uncertainty due to large model prediction error. Regional differences in losses revealed interesting trends in the capacity for the fishery to recoup costs. For example, in the NMA, relatively small losses at the fishery level were predicted ($0.3 million in total) for the 2019 season despite an early closure to the season due to whale entanglement risk.NMA fishers collectively were able to meet predicted revenue for the season despite a shortening of the fishing 2019 season. In the 2020 season however, the NMA did not experience disturbances due to whale entanglements but larger ex-vessel losses (of $3.9 million) were predicted. This suggests that other disturbances such as a delay to the season due to crab meat quality, lost fishing opportunity related to the COVID-19 pandemic, or other unknown factors, had an influence on ex-vessel revenue during the 2020 season. While most of the 2020 season landings in the NMA occurred before COVID-19 arrived in the US, there is evidence that prices in latter part of the season may have been depressed due to loss of export markets for live crab47.In the CMA however, despite landing the majority of crab available during the 2019 season (see Fig. 2c), losses of $9.4 million were experienced across the fishery. While total fishery catch was not greatly reduced, closure to the fishery in the spring may be responsible for revenue losses through other mechanisms (e.g. price). In the 2020 season, whale entanglement risk substantially shortened the fishing season in the CMA, through a delay at the beginning of the season and an early closure in the spring. Estimated losses were largest ($14.4 million) during this season. It is likely that the COVID-19 pandemic was also responsible for some of this estimated loss in the CMA in the 2020 season47. Our model did not control for impacts of the COVID-19 pandemic. However, price trends suggest that that price of Dungeness Crab in California was not affected until mid-March 2020, at which point the fishery had caught 92% of the seasons catch (see Supplementary File S2). Prices then returned to normal levels in mid-May. If we apply extrapolated prices between mid-March and mid-May by replacing observed prices with linearly increasing prices by week, revenues would have been $753,754 higher in total across the fishery. This rough estimate suggests we can attribute 4.1% of overall estimated revenue losses during the 2020 season to COVID-19 impacts, with the caveat that we do not know what prices would have been in the absence of the pandemic. A counterfactual approach has been used to disentangle multiple stressors to infer causal impacts of management interventions elsewhere48, however as these closures, and the COVID pandemic, potentially impacted all fishers in the California Dungeness crab fishery, there are no control groups available for comparison and therefore this approach would not be appropriate.Closures and other disturbances appear to have been less impactful in the NMA and high price for Dungeness crab may have contributed to the ability of vessels operating in the NMA to withstand disturbances (Supplementary Fig. S2). Prices were particularly high during the summer portion of the season in 2020 during which time the CMA was closed to Dungeness crab fishing (Supplementary Fig. S2). The NMA did not experience closures due to whale entanglement during 2020 and was predicted to have lower than average pre-season abundance (lower catch potential) during 2020 (see Fig. 2.b), while the CMA was predicted to have high catch potential for 2020 (Fig. 2.c), therefore differences in management measures implemented, and seasons’ catch potential, also contributed to differences in losses estimated.The CMA also experienced high prices, including decadal high prices for crab during the November–December of the 2019 fishing season (Supplementary Fig. S2). However, losses observed overall across the two seasons suggest the fishery, unlike the NMA, did not get much overall benefit from the high price in 2019 or the high pre-season abundance of crab (i.e. catch potential) estimated for the 2020 season in the CMA. A number of factors may have contributed to a poor season in the CMA including catchability or biology of Dungeness crab as well as external factors such as the COVID-19 pandemic behavioral choice factors, for example deciding not to fish45. Temporally shifting or reducing the opportunity for participation through closed periods due to whale entanglement risk may have exacerbated other impacts on revenues in the CMA which were not as impactful on revenues in the NMA.The high variability in estimated economic impacts per vessel reported here demonstrates that closures did not affect all vessels equally, similarly to impacts observed following a climate related harmful algal bloom in the 2016 season which were variable by vessel size and between communities45. The estimated losses we present at the fishery level in the NMA and CMA may therefore be underestimated, or overestimated, for particular groups of vessels within those management areas. This reflects the diverse nature of the Dungeness Crab fishery in behaviour and fishing strategy and highlights the importance of capturing impacts at finer scales than the fishery level alone.Limitations to the estimation of closure impactsA limitation of the hurdle model is that there are other latent factors influencing fishery participation and revenues that our model does not incorporate, particularly those determining fisher behavior such as fuel price, shipyard backlogs and market demand. A behavioral choice model, for example one that incorporates location or fishing alternative choice given a closure50,51,52 would be a potential method to better understand how spatial management strategies affect fisher behavior and is recommended as a future analysis to assess trade-offs involving socio-economic risk. Our results, reporting losses from Dungeness crab fishing revenue only, also do not account for the ability of some fishers to mitigate revenue losses by participating in other fisheries. Dungeness crab fishing is highly connected within west coast fishery participation networks44,45. Thus, it is important to note that our results for the 2019 and 2020 seasons present only losses from Dungeness crab fishing and may overestimate total annual revenue losses by some vessels that are able to mitigate impacts with participation in other fisheries.The model, predicting out-of-sample, over-estimated revenues in recent years suggesting that our predictions of revenues may also be over-predicted. An improved estimation at the vessel level, given some over-estimation of vessels that did not fish, could be investigated through a selection model approach rather than a two-part model approach54. However, two-part models are most appropriate for estimation of conditional (actual) outcomes as was intended here rather than unconditional (potential) outcomes and they do not require separate drivers for the selection and estimation model, which we did not have available54. When the impacts of policy interventions are difficult to disentangle from other impacts, approaches such as a counterfactual synthetic control48 approach could be used to separate the impacts of the policy alone. In this context, however, it is useful to report the cumulative impact of disturbances given that these disturbances (e.g., delays due to crab quality, harmful algal blooms) happen frequently and therefore the closures will rarely happen in isolation.Whilst there are limitations to our approach, revenue predictions presented here offer more insight compared to predicting revenues based only on a 5-year average of total fishery revenues (Supplementary Table S3) as is commonly conducted to calculate disaster assistance requirement, as our analysis includes an estimation of crab abundance as well as historical vessel level data in its estimation. Accounting for the influence of crab abundance is critical in this fishery given abundance is highly variable and the majority of fishable biomass is taken each year. Estimation of revenue at the individual vessel level allows for consideration of fishery heterogeneity (e.g., by vessel size). Revenues calculated on a 5-year average would suggest total California Commercial Dungeness crab fishery revenues would have been $10.62 million higher than observed in 2019 and $12.73 million higher than observed in 2020 (Supplementary Table S3). Thus, revenues estimated on the 5-year average suggest that losses would have been $0.97 million higher than our model prediction across the fishery for 2019 and $5.56 million lower than our model prediction for 2020. Our predictions suggest that delays and closures due to whale entanglement mitigation and other disturbances in to the 2019 and 2020 seasons were similar to the impact of closures due to the HAB in the 2016 season, which were estimated at $13.6 million in losses from Dungeness Crab revenues across the fishery38.Economic cost of mitigationMany strategies that prevent fishery interactions with marine mammals exist, including gear reductions or modifications, depth limitations and dynamic or seasonal time-area closures13,14,22,23,24,25,26,55. Whilst the fishery does implement pro-active gear modification measures set out in the best practices guide34, only two management intervention options were enacted in the 2019 and 2020 seasons to mitigate against entanglements of marine life with Dungeness crab gear; delays to the start of the crab season in the winter and early closures in spring due to overlap with whale distribution in fishing grounds. These delays and closures can have differential impacts on the fishery as the fishing season is not heterogeneously prosperous. An example is that closures during the holiday season (Nov–Dec) when Dungeness crab is traditionally consumed can cause substantial lost revenue opportunity for fishers at a time when price and demand are highest35,49. The fishery operates as a derby in which the majority of revenues are made in the first month of the fishery being open. The strong seasonal dynamics of the Dungeness crab fishery, largely driven by rapid depletion of legal sized crab, mean that the timing of management actions can have important impacts on fishing revenues. Across the fishery, based on observed vessel level revenues during the 2011–2018 baseline period, vessels earned an average of 62.33% (SD 24.04) of annual ex-vessel revenue during the first month of the season (15th Nov–15th Dec for the CMA/1st Dec–31st Dec for the NMA). After April 1st, vessels on average earn 10.54% (SD 18.98) of annual ex-vessel revenue. This average, based only on vessels that historically have actively participate past April 1st, (283 vessels in the NMA, 346 vessels in the CMA) rises to 20.36% (SD 13.37) of ex-vessel revenue. Thus, while the majority of the overall fisheries revenue is taken at the start of the season, an April 1st closure could still have a substantial impact on the revenues of active fishing vessels in the spring. Determination of economic risk for the fishery, at a minimum, should consider timing of closures in addition to total revenue losses, in order to quantify losses that will be felt at the individual vessel level. We suggest further research to investigate how closures affect different groups of fishers through stakeholder participation.Socio-economic impacts from whale mitigation measures could permeate into communities further than our analysis (based on ex-vessel revenue only) conveys35,36,37,49, and further investigation into these community level impacts is necessary to understand and sustain an equitable fishery supply chain even where there is no absolute revenue loss. Some of the communities influenced by whale entanglement mitigation in California rely heavily on ocean resources for employment, through fishing occupations but also through hospitality and tourism. Managing this issue in a way that minimizes the burden on resource dependent communities is strongly in line with the objectives set out in the UN Sustainable Development Goals (SDG’s), especially SDG 14 (life below water) but also related goals such as human well-being, reducing inequality and reducing the impacts of climate change56.Management ImplicationsBalancing socio-economic impacts against whale entanglement risk is challenging given the legally protected status of whale populations. However, potential economic losses reported here should motivate the development of mitigation measures (through cooperative innovation between industry, researchers and managers) that allow fishery production to be optimized whilst ensuring successful whale protection. At present, entire management areas, which constitute large regions of the coast, are closed in response to whale entanglement risk in California. Investigating how to minimize the spatiotemporal footprint of closures, such as by defining high risk zones dynamically based on fine-scale information of whale density and fishing effort, could provide an alternative mitigation structure. This could better consider the economic and conservation trade-offs while still being sensitive to changing environmental conditions. The introduction of dynamic zone closures, often broadly referred to as dynamic ocean management, has been demonstrated to reduce risk whilst minimizing lost fishing opportunities12,26,57,58, especially when environmental variability is high or species have a dynamic distribution59. Moreover, analysis of policy instruments to reduce whale entanglements with the American lobster fishery on the US Northeast coast found that economic costs of risk reduction could be 20% lower when mitigation decisions considered fishing opportunity costs alongside non-monetary benefits (biological risk), compared to non-monetary benefits alone12. This is promising for the implementation of such strategies in the California Current System.The caveat of this strategy is that dynamic zone closures require spatially and temporally explicit information on whale density and fishing effort which can be costly to attain. The use of ropeless gear has also been suggested as an alternative whale entanglement mitigation measure that requires further research and development before being initiated as an alternative regulatory tool60. The costs of monitoring or technical advancements however may outweigh the financial and societal cost of fishery closures. Revenue losses for Dungeness crab estimated here for the 2019 and 2020 seasons are on par with losses experienced during the HAB period. During the delays to the 2016 fishing season an estimated $26.1 million was lost from ex-vessel revenues from all species that crab fishers target, including $13.6 million from Dungeness crab alone38, requiring $25 million in government aid. Whale mitigation under the RAMP regulation will potentially delay or close the fishery year after year with uncertain economic impact that cannot be sustainably resolved with government aid. Development of tools to mitigate against economic loss while achieving whale protection will be necessary to come to a sustainable solution. This can only be achieved by first including economic loss in risk assessments. Doing so may also provide balance to partnerships between fishery managers and fishers.Regulators are obligated to protect Humpback whales, blue whales and Leatherback turtles using the best available science33. In this fishery, current triggers to open and close are based on a range of factors, but thus ultimately depend on the number of whales present within a management region33. Regulators have a number of alternative regulatory options available to them, which include depth restrictions, gear restrictions or modifications and fleet advisories, if they can offer the same level of whale protection33. Yet, the RAMP process lacks the socio-economic information needed to consider the socio-economic risk of regulatory actions, and that of the alternatives, to the fishing community. Results presented here highlight that the economic effects and that risk to fishing communities should be considered when designing whale entanglement mitigation programs33. Having this economic information will facilitate the ability of managers, as set out in the RAMP regulation (subsection d4)33, to consider the socio-economic impact if deciding between management measures that equivalently reduce entanglement risk.We have used two fishing seasons as an example of the economic impacts of these new whale entanglement regulations which will be implemented each year going forward. Synthesis of ex-vessel revenues is not a complete picture of the socio-economic impacts of regulations, but it provides a starting point for protecting both whales and fishing communities. While reported whale entanglements remain higher than pre-2014 totals, reported whale entanglements in California have declined markedly in the years following the 2014–2016 large marine heatwave (Fig. 1b). This is a success for this fishery and attributed to increased awareness, development of best practices for fishing gear and the mitigation program to protect whales. We now need to be successful at protecting and mitigating the socio-economic impacts to fishery participants and the fishing communities they support. More

Jackson, R. B. et al. The Ecology of soil carbon: Pools, vulnerabilities, and biotic and abiotic controls. Annu. Rev. Ecol. Evol. Syst. 48, 419–445. https://doi.org/10.1146/annurev-ecolsys-112414-054234 (2017).Article 

Google Scholar 
Sanderman, J., Hengl, T. & Fiske, G. J. Soil carbon debt of 12,000 years of human land use. PNAS 114, 9575–9580 (2017).Article 
ADS 
CAS 

Google Scholar 
Amelung, W. et al. Towards a global-scale soil climate mitigation strategy. Nat. Commun. 11, 5427. https://doi.org/10.1038/s41467-020-18887-7 (2020).Article 
ADS 
CAS 

Google Scholar 
Hopkins, A. & Holz, B. Grassland for agriculture and nature conservation: Production, quality and multi-functionality. Agron 4, 3–20 (2006).
Google Scholar 
van Veen, J. A., Liljeroth, E., Lekkerkerk, L. J. A. & van de Geijn, S. C. Carbon fluxes in plant-soil systems at elevated atmospheric CO2 levels. Ecol. Appl. 1, 175–181. https://doi.org/10.2307/1941810 (1991).Article 

Google Scholar 
Jones, M. B. & Donnelly, A. Carbon sequestration in temperate grassland ecosystems and the influence of management, climate and elevated CO2. New Phytol. 164, 423–439. https://doi.org/10.1111/j.1469-8137.2004.01201.x (2004).Article 

Google Scholar 
Ward, S. E. et al. Legacy effects of grassland management on soil carbon to depth. Glob. Change Biol. 22, 2929–2938. https://doi.org/10.1111/gcb.13246 (2016).Article 
ADS 

Google Scholar 
Hungate, B. A. et al. The fate of carbon in grasslands under carbon dioxide enrichment. Nature 388, 576–579. https://doi.org/10.1038/41550 (1997).Article 
ADS 
CAS 

Google Scholar 
Six, J., Conant, R. T., Paul, E. A. & Paustian, K. Stabilization mechanisms of soil organic matter: Implications for C-saturation of soils. Plant Soil 241, 155–176. https://doi.org/10.1023/A:1016125726789 (2002).Article 
CAS 

Google Scholar 
Chang, J. et al. Climate warming from managed grasslands cancels the cooling effect of carbon sinks in sparsely grazed and natural grasslands. Nat. Commun. 12, 118. https://doi.org/10.1038/s41467-020-20406-7 (2021).Article 
ADS 
CAS 

Google Scholar 
IPCC. 2001. Climate change 2001: The scientific basis contribution of working group 1 to the third assessment report of the intergovernmental panel on climate change In (eds Houghton, J. T., Ding, Y., Griggs, D. J., Noguer, M., Van Der Linden, P. J., Dai, X., Maskell, K. & Johnson, C. A.) (Cambridge University Press).Gwin, L. Scaling-up sustainable livestock production: Innovation and challenges for grass-fed beef in the U.S. J. Sustain. Agric. 33, 189–209. https://doi.org/10.1080/10440040802660095 (2009).Article 

Google Scholar 
Iqbal, J., Siegrist, J. A., Nelson, J. A. & McCulley, R. L. Fungal endophyte infection increases carbon sequestration potential of southeastern USA tall fescue stands. Soil Biol. Biochem. 44, 81–92. https://doi.org/10.1016/j.soilbio.2011.09.010 (2012).Article 
CAS 

Google Scholar 
Robinson, R. A. & Sutherland, W. J. Post-war changes in arable farming and biodiversity in Great Britain. J. Appl. Ecol. 39, 157–176. https://doi.org/10.1046/j.1365-2664.2002.00695.x (2002).Article 

Google Scholar 
Law, Q. D., Bigelow, C. A. & Patton, A. J. Selecting turfgrasses and mowing practices that reduce mowing requirements. Crop Sci. 56, 3318–3327. https://doi.org/10.2135/cropsci2015.09.0595 (2016).Article 

Google Scholar 
White, L. M. Carbohydrate reserves of grasses: A review. Rangel Ecol. Manag. 26(1), 13–18 (1973).Article 
CAS 

Google Scholar 
Virkajarvi, P. Effects of defoliation height on regrowth of timothy and meadow fescue in the generative and vegetative phases of growth. Agric. Food Sci. 12, 177–193 (2003).Article 

Google Scholar 
Reicher, Z., Patton, A. J., Bigelow, C. A. & Voigt, T. Mowing, Thatching, Aerifying, and Rolling Turf (Turf Grass Sci. Purdue Univ, 2006).
Google Scholar 
Kaatz, P. Cutting management for cool-season forage grasses. Michigan State University Extension, https://www.canr.msu.edu/news/cutting_management_for_cool_season_forage_grasses (2011).Briske, D. D. Strategies of plant survival in grazed systems: A functional interpretation. Ecol. Manag. Graz. Syst. 37–67 (1996).Crider, F. J. Root-growth stoppage resulting from defoliation of grass (No. 156759). United States Department of Agriculture, Economic Research Service (1995).Lal, R., Negassa, W. & Lorenz, K. Carbon sequestration in soil. Curr. Opin. Environ. Sustain. 15, 79–86. https://doi.org/10.1016/j.cosust.2015.09.002 (2015).Article 

Google Scholar 
Coughenour, M. B., McNaughton, S. J. & Wallace, L. L. Modelling primary production of perennial graminoids – uniting physiological processes and morphometric traits. Ecol. Modell. 23, 101–134. https://doi.org/10.1016/0304-3800(84)90121-2 (1984).Article 
CAS 

Google Scholar 
Whipps, J. M. & Lynch, J. M. Energy losses by the plant in rhizodeposition. Plant products and the new technology / edited by K.W. Fuller and J.R. Gallon (1985).Johansson, G. Release of organic C from growing roots of meadow fescue (Festuca pratensis L.). Soil Biol. Biochem. 24, 427–433. https://doi.org/10.1016/0038-0717(92)90205-C (1992).Article 

Google Scholar 
Woodburn, A. T. Glyphosate: Production, pricing and use worldwide. Pest Manag. Sci. 56, 309–312. https://doi.org/10.1002/(SICI)1526-4998(200004)56:4%3c309::AID-PS143%3e3.0.CO;2-C (2000).Article 
CAS 

Google Scholar 
Duke, S. O. & Powles, S. B. Glyphosate: A once-in-a-century herbicide. Pest Manag. Sci. 64, 319–325. https://doi.org/10.1002/ps.1518 (2008).Article 
CAS 

Google Scholar 
Helander, M., Saloniemi, I. & Saikkonen, K. Glyphosate in northern ecosystems. Trends Plant Sci. 17, 569–574. https://doi.org/10.1016/j.tplants.2012.05.008 (2012).Article 
CAS 

Google Scholar 
Benbrook, C. M. Trends in glyphosate herbicide use in the United States and globally. Environ. Sci. Eur. 28, 3. https://doi.org/10.1186/s12302-016-0070-0 (2016).Article 
CAS 

Google Scholar 
Helander, M. et al. Glyphosate decreases mycorrhizal colonization and affects plant-soil feedback. Sci. Total Environ. 642, 285–291. https://doi.org/10.1016/j.scitotenv.2018.05.377 (2018).Article 
ADS 
CAS 

Google Scholar 
Helander, M., Pauna, A., Saikkonen, K. & Saloniemi, I. Glyphosate residues in soil affect crop plant germination and growth. Sci. Rep. 9, 19653. https://doi.org/10.1038/s41598-019-56195-3 (2019).Article 
ADS 
CAS 

Google Scholar 
Zaller, J. G. & Brühl, C. A. Editorial: Non-target effects of pesticides on organisms inhabiting agroecosystems. Front Environ. Sci. 7, 75. https://doi.org/10.3389/fenvs.2019.00075 (2019).Article 

Google Scholar 
Muola, A. et al. Risk in the circular food economy: Glyphosate-based herbicide residues in manure fertilizers decrease crop yield. Sci. Total Environ. 750, 141422. https://doi.org/10.1016/j.scitotenv.2020.141422 (2021).Article 
ADS 
CAS 

Google Scholar 
Fuchs, B., Saikkonen, K. & Helander, M. Glyphosate-modulated biosynthesis driving plant defense and species interactions. Trends Plant Sci. 26, 312–323. https://doi.org/10.1016/j.tplants.2020.11.004 (2021).Article 
CAS 

Google Scholar 
Fuchs, B. et al. A Glyphosate-based herbicide in soil differentially affects hormonal homeostasis and performance of non-target crop plants. Front Plant Sci. 12, 787958 (2022).Article 

Google Scholar 
Borggaard, O. K. & Gimsing, A. L. Fate of glyphosate in soil and the possibility of leaching to ground and surface waters: A review. Pest Manag. Sci. 64, 441–456. https://doi.org/10.1002/ps.1512 (2008).Article 
CAS 

Google Scholar 
Rueppel, M. L., Brightwell, B. B., Schaefer, J. & Marvel, J. T. Metabolism and degradation of glyphosate in soil and water. J. Agric. Food Chem. 25, 517–528. https://doi.org/10.1021/jf60211a018 (1977).Article 
CAS 

Google Scholar 
Carlisle, S. M. & Trevors, J. T. Glyphosate in the environment. Wat Air Soil Poll 39, 409–420 (1988).Article 
ADS 
CAS 

Google Scholar 
Torstensson, N. T. L., Lundgren, L. N. & Stenström, J. Influence of climatic and edaphic factors on persistence of glyphosate and 2,4-D in forest soils. Ecotoxicol. Environ. Saf. 18, 230–239. https://doi.org/10.1016/0147-6513(89)90084-5 (1989).Article 
CAS 

Google Scholar 
Stenrød, M., Eklo, O. M., Charnay, M.-P. & Benoit, P. Effect of freezing and thawing on microbial activity and glyphosate degradation in two Norwegian soils. Pest Manag. Sci. 61, 887–898. https://doi.org/10.1002/ps.1107 (2005).Article 
CAS 

Google Scholar 
Antier, C. et al. Glyphosate use in the European agricultural sector and a framework for its further monitoring. Sustainability 12, 5682. https://doi.org/10.3390/su12145682 (2020).Article 
CAS 

Google Scholar 
Jones, R. J. Effect of an associate grass, cutting interval, and cutting height on yield and botanical composition of Siratro pastures in a sub-tropical environment. Aust. J. Exp. Agric. 14, 334–342. https://doi.org/10.1071/ea9740334 (1974).Article 

Google Scholar 
Volenec, J. J. & Nelson, C. J. Responses of Tall Fescue leaf meristems to N fertilization and harvest frequency. Crop Sci. 23(4), 720–724. https://doi.org/10.2135/cropsci1983.0011183X002300040028x (1983).Article 

Google Scholar 
Saikkonen, K. et al. Fungal endophytes help prevent weed invasions. Agric. Ecosyst. Environ. 165, 1–5. https://doi.org/10.1016/j.agee.2012.12.002 (2013).Article 

Google Scholar 
Scavo, A. & Mauromicale, G. Integrated weed management in herbaceous field crops. Agronomy 10, 466. https://doi.org/10.3390/agronomy10040466 (2020).Article 

Google Scholar 
Clay, K. & Holah, J. Fungal endophyte symbiosis and plant diversity in successional fields. Science 285, 1742–1744. https://doi.org/10.1126/science.285.5434.1742 (1999).Article 
CAS 

Google Scholar 
Gundel, P. E., Pérez, L. I., Helander, M. & Saikkonen, K. Symbiotically modified organisms: Nontoxic fungal endophytes in grasses. Trends Plant Sci. 18, 420–427. https://doi.org/10.1016/j.tplants.2013.03.003 (2013).Article 
CAS 

Google Scholar 
Kauppinen, M., Saikkonen, K., Helander, M., Pirttilä, A. M. & Wäli, P. R. Epichloë grass endophytes in sustainable agriculture. Nat. Plants 2, 15224 (2016).Article 

Google Scholar 
Clay, K. Fungal endophytes of grasses. Annu. Rev. Ecol. Syst. 21, 275–297 (1990).Article 

Google Scholar 
Saikkonen, K., Young, C. A., Helander, M. & Schardl, C. L. Endophytic Epichloë species and their grass hosts: From evolution to applications. Plant Mol. Biol. 90, 665–675. https://doi.org/10.1007/s11103-015-0399-6 (2016).Article 
CAS 

Google Scholar 
Ahlholm, J. U., Helander, M., Lehtimäki, S., Wäli, P. & Saikkonen, K. Vertically transmitted fungal endophytes: Different responses of host-parasite systems to environmental conditions. Oikos 99, 173–183. https://doi.org/10.1034/j.1600-0706.2002.990118.x (2002).Article 

Google Scholar 
Easton, H. S. & Fletcher, L. R. in Proc. 6th International Symposium Fungal Endophytes of Grasses (eds Popay, A. J. & Thom, E. R.) 11–18 (New Zealand Grassland Association, 2007).Saari, S., Lehtonen, P., Helander, M. & Saikkonen, K. High variation in frequency of infection by endophytes in cultivars of meadow fescue in Finland. Grass Forage Sci. 64, 169–176. https://doi.org/10.1111/j.1365-2494.2009.00680.x (2009).Article 

Google Scholar 
König, J., Fuchs, B., Krischke, M., Mueller, M. J. & Krauss, J. Hide and seek: Infection rates and alkaloid concentrations of Epichloë festucae var. lolii in Lolium perenne along a land-use gradient in Germany. Grass Forage Sci. 73, 510–516. https://doi.org/10.1111/gfs.12330 (2018).Article 
CAS 

Google Scholar 
Krauss, J. et al. Epichloë endophyte infection rates and alkaloid content in commercially available grass seed mixtures in Europe. Microorganisms 8, 498. https://doi.org/10.3390/microorganisms8040498 (2020).Article 
CAS 

Google Scholar 
Brink, G. E., Casler, M. D. & Martin, N. P. Meadow Fescue, Tall Fescue, and Orchardgrass response to defoliation management. Agronomy J 102, 667–674. https://doi.org/10.2134/agronj2009.0376 (2010).Article 

Google Scholar 
Conant, R. T., Cerri, C. E. P., Osborne, B. B. & Paustian, K. Grassland management impacts on soil carbon stocks: A new synthesis. Ecol. Appl. 27, 662–668. https://doi.org/10.1002/eap.1473 (2017).Article 

Google Scholar 
Trlica, M. J. Distribution and utilization of carbohydrate reserves in range plants. In (ed Sosebee, R. E.) 73–96 (Rangeland Plant Physiology, 1977).Faeth, S. H. & Sullivan, T. J. Mutualistic asexual endophytes in a native grass are usually parasitic. Am. Nat. 161, 310–325. https://doi.org/10.1086/345937 (2003).Article 

Google Scholar 
Saikkonen, K., Saari, S. & Helander, M. Defensive mutualism between plants and endophytic fungi?. Fungal Divers. 41, 101–113. https://doi.org/10.1007/s13225-010-0023-7 (2010).Article 

Google Scholar 
Clay, K. & Schardl, C. Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am. Nat. 160, 99–127. https://doi.org/10.1086/342161 (2002).Article 

Google Scholar 
Rozpądek, P. et al. The fungal endophyte Epichloë typhina improves photosynthesis efficiency of its host orchard grass (Dactylis glomerata). Planta 242, 1025–1035. https://doi.org/10.1007/s00425-015-2337-x (2015).Article 
CAS 

Google Scholar 
Xia, C. et al. An Epichloë endophyte improves photosynthetic ability and dry matter production of its host Achnatherum inebrians infected by Blumeria graminis under various soil water conditions. Fungal Ecol. 22, 26–34. https://doi.org/10.1016/j.funeco.2016.04.002 (2016).Article 

Google Scholar 
Malinowski, D., Leuchtmann, A., Schmidt, D. & Nosberger, J. Symbiosis with Neotyphodium uncinatum endophyte may increase the competitive ability of meadow fescue. Agron. J. 89, 833–839 (1997).Article 

Google Scholar 
Schardl, C. L., Leuchtmann, A. & Spiering, M. J. Symbioses of grasses with seedborne fungal endophytes. Ann. Rev. Plant Biol. 55, 315–340. https://doi.org/10.1146/annurev.arplant.55.031903.141735 (2004).Article 
CAS 

Google Scholar 
Chen, Z. et al. Fungal endophyte improves survival of Lolium perenne in low fertility soils by increasing root growth, metabolic activity and absorption of nutrients. Plant Soil 452, 185–206. https://doi.org/10.1007/s11104-020-04556-7 (2020).Article 
CAS 

Google Scholar 
Franz, J. E., Mao, M.K. and Sikorski, J.A. (1997). Uptake, transport and metabolism of glyphosate in plants, in Glyphosate: A unique global herbicide, ed by Franz JE, ACS Monograph No 189, American Chemical Society, Washington, DC, pp 143–181.Pline, W. A., Wilcut, J. W., Edmisten, K. L. & Wells, R. Physiological and morphological response of glyphosate-resistant and non-glyphosate-resistant cotton seedlings to root-absorbed glyphosate. Pestic. Biochem. Phys. 73, 48–58. https://doi.org/10.1016/S0048-3575(02)00014-7 (2002).Article 
CAS 

Google Scholar 
Johansson, G. Carbon distribution in grass (Festuca pratensis L.) during regrowth after cutting—utilization of stored and newly assimilated carbon. Plant Soil 151, 11–20. https://doi.org/10.1007/BF00010781 (1993).Article 
ADS 
CAS 

Google Scholar 
Ergon, Å. et al. How can forage production in Nordic and Mediterranean Europe adapt to the challenges and opportunities arising from climate change?. Euro J. Agron. 92, 97–106. https://doi.org/10.1016/j.eja.2017.09.016 (2018).Article 

Google Scholar 
Niemelainen, O. et al. Increase in perennial forage yields driven by climate change, at Apukka Research Station, Rovaniemi, 1980–2017. Agric. Food Sci. 29, 139–153 (2020).Article 

Google Scholar 
Anwar, M. R., Liu, D. L., Macadam, I. & Kelly, G. Adapting agriculture to climate change: A review. Theor. Appl. Climatol. 113, 225–245. https://doi.org/10.1007/s00704-012-0780-1 (2013).Article 
ADS 

Google Scholar 
Farmit. Nurmea yli kymppitonni hehtaarilta. Farmit.net. (accessed 28 June 2022); https://www.farmit.net/nurmikasvit-lypsylehma/2016/05/24/nurmea-yli-kymppitonni-hehtaarilta (2016).Peltonen, S., Aalto, K., Hennola, I. & Anttila, S. (Eds.). Peltojen kunnostus. (Tieto Tuottamaan; No. 145), (ProAgria Keskusten Liiton julkaisuja; No. 1163). ProAgria maaseutukeskusten liitto (2019).Laihonen, M., Saikkonen, K., Helander, M. & Tammaru, T. Insect oviposition preference between Epichloë-symbiotic and Epichloë-free grasses does not necessarily reflect larval performance. Ecol. Evol. 10, 7242–7249. https://doi.org/10.1002/ece3.6450 (2020).Article 

Google Scholar  More

Semple, K. T., Morriss, A. W. J. & Paton, G. I. Bioavailability of hydrophobic organic contaminants in soils: Fundamental concepts and techniques for analysis. Eur. J. Soil Sci. 54, 809–818 (2003).Article 
CAS 

Google Scholar 
Ivshina, I. et al. Removal of polycyclic aromatic hydrocarbons in soil spiked with model mixtures of petroleum hydrocarbons and heterocycles using biosurfactants from Rhodococcus ruber IEGM 231. J. Hazard. Mater. 312, 8–17 (2016).Article 
CAS 

Google Scholar 
Varjani, S. J. Microbial degradation of petroleum hydrocarbons. Bioresour. Technol. 223, 277–286 (2017).Article 
CAS 

Google Scholar 
Chen, J. et al. Long-chain n-alkane biodegradation coupling to methane production in an enriched culture from production water of a high-temperature oil reservoir. AMB Express 10, 63 (2020).Article 
CAS 

Google Scholar 
Li, Y. & Xiong, Y. Identification and quantification of mixed sources of oil spills based on distributions and isotope profiles of long-chain n-alkanes. Mar. Pollut. Bull. 58, 1868–1873 (2009).Article 
CAS 

Google Scholar 
Stout, S. A., Payne, J. R., Emsbo-Mattingly, S. D. & Baker, G. Weathering of field-collected floating and stranded Macondo oils during and shortly after the Deepwater Horizon oil spill. Mar. Pollut. Bull. 105, 7–22 (2016).Article 
CAS 

Google Scholar 
Wang, X. et al. Polycyclic aromatic hydrocarbons, polychlorinated biphenyls and legacy and current pesticides in indoor environment in Australia—occurrence, sources and exposure risks. Sci. Total Environ. 693, 133588 (2019).Article 
ADS 
CAS 

Google Scholar 
Qiao, M., Qi, W., Liu, H. & Qu, J. Oxygenated polycyclic aromatic hydrocarbons in the surface water environment: Occurrence, ecotoxicity, and sources. Environ. Int. 163, 107232 (2022).Article 

Google Scholar 
Abbasnezhad, H., Foght, J. M. & Gray, M. R. Adhesion to the hydrocarbon phase increases phenanthrene degradation by Pseudomonas fluorescens LP6a. Biodegradation 22, 485–496 (2011).Article 
CAS 

Google Scholar 
Abbasnezhad, H., Gray, M. & Foght, J. M. Influence of adhesion on aerobic biodegradation and bioremediation of liquid hydrocarbons. Appl. Microbiol. Biotechnol. 92, 653–675 (2011).Article 
CAS 

Google Scholar 
Dewangan, N. K. & Conrad, J. C. Bacterial motility enhances adhesion to oil droplets. Soft Matter 16, 8237–8244 (2020).Article 
ADS 
CAS 

Google Scholar 
Rodrigues, E. M., Cesar, D. E., Santos de Oliveira, R., de Paula Siqueira, T. & Tótola, M. R. Hydrocarbonoclastic bacterial species growing on hexadecane: Implications for bioaugmentation in marine ecosystems. Environ. Pollut. 267, (2020).Wang, J. D., Qu, C. T. & Song, S. F. Temperature-induced changes in the proteome of Pseudomonas aeruginosa during petroleum hydrocarbon degradation. Arch. Microbiol. 203, 2463–2473 (2021).Article 
CAS 

Google Scholar 
Bastiaens, L. et al. Isolation of adherent polycyclic aromatic hydrocarbon (PAH)-degrading bacteria using PAH-sorbing carriers. Appl. Environ. Microbiol. 66, 1834–1843 (2000).Article 
ADS 
CAS 

Google Scholar 
Tao, K., Zhao, S., Gao, P., Wang, L. & Jia, H. Impacts of Pantoea agglomerans strain and cation-modified clay minerals on the adsorption and biodegradation of phenanthrene. Ecotoxicol. Environ. Saf. 161, 237–244 (2018).Article 
CAS 

Google Scholar 
Xu, X. et al. Biodegradation potential of polycyclic aromatic hydrocarbons by immobilized Klebsiella sp. in soil washing effluent. Chemosphere 223, 140–147 (2019).Wang, H. et al. Transmembrane transport of polycyclic aromatic hydrocarbons by bacteria and functional regulation of membrane proteins. Front. Environ. Sci. Eng. 14, 1–21 (2020).Article 

Google Scholar 
Tarasova, E. V., Grishko, V. V. & Ivshina, I. B. Cell adaptations of Rhodococcus rhodochrous IEGM 66 to betulin biotransformation. Process Biochem. 52, 1–9 (2017).Article 
CAS 

Google Scholar 
Bohinc, K. et al. Available surface dictates microbial adhesion capacity. Int. J. Adhes. Adhes. 50, 265–272 (2014).Article 
CAS 

Google Scholar 
Carniello, V., Peterson, B. W., van der Mei, H. C. & Busscher, H. J. Physico-chemistry from initial bacterial adhesion to surface-programmed biofilm growth. Adv. Colloid Interface Sci. 261, 1–14 (2018).Article 
CAS 

Google Scholar 
Dorobantu, L. S., Bhattacharjee, S., Foght, J. M. & Gray, M. R. Analysis of force interactions between AFM tips and hydrophobic bacteria using DLVO theory. Langmuir 25, 6968–6976 (2009).Article 
CAS 

Google Scholar 
Lehocký, M. et al. Adhesion of Rhodococcus sp. S3E2 and Rhodococcus sp. S3E3 to plasma prepared Teflon-like and organosilicon surfaces. J. Mater. Process. Technol. 209, 2871–2875 (2009).Hori, K. & Matsumoto, S. Bacterial adhesion: From mechanism to control. Biochem. Eng. J. 48, 424–434 (2010).Article 
CAS 

Google Scholar 
Ivshina, I. B. et al. Biosurfactant-enhanced immobilization of hydrocarbon-oxidizing Rhodococcus ruber on sawdust. Appl. Microbiol. Biotechnol. 97, 5315–5327 (2013).Article 
CAS 

Google Scholar 
Pen, Y. et al. Effect of extracellular polymeric substances on the mechanical properties of Rhodococcus. Biochim. Biophys. Acta – Biomembr. 1848, 518–526 (2015).Article 
CAS 

Google Scholar 
De Cesare, F., Di Mattia, E., Zussman, E. & Macagnano, A. A study on the dependence of bacteria adhesion on the polymer nanofibre diameter. Environ. Sci. Nano 6, 778–797 (2019).Article 

Google Scholar 
Bergeau, D. et al. Unusual extracellular appendages deployed by the model strain Pseudomonas fluorescens C7R12. PLoS ONE 14, 1–20 (2019).Article 

Google Scholar 
Jin, X. & Marshall, J. S. Mechanics of biofilms formed of bacteria with fimbriae appendages. PLoS ONE 15, 1–22 (2020).Article 

Google Scholar 
Tarafdar, A., Sarkar, T. K., Chakraborty, S., Sinha, A. & Masto, R. E. Biofilm development of Bacillus thuringiensis on MWCNT buckypaper: Adsorption-synergic biodegradation of phenanthrene. Ecotoxicol. Environ. Saf. 157, 327–334 (2018).Article 
CAS 

Google Scholar 
Rodrigues, A. C., Wuertz, S., Brito, A. G. & Melo, L. F. Fluorene and phenanthrene uptake by Pseudomonas putida ATCC 17514: Kinetics and physiological aspects. Biotechnol. Bioeng. 90, 281–289 (2005).Article 
CAS 

Google Scholar 
Yang, H. Y., Jia, R. B., Chen, B. & Li, L. Degradation of recalcitrant aliphatic and aromatic hydrocarbons by a dioxin-degrader Rhodococcus sp. strain p52. Environ. Sci. Pollut. Res. 21, 11086–11093 (2014).Auffret, M. D., Yergeau, E., Labbé, D., Fayolle-Guichard, F. & Greer, C. W. Importance of Rhodococcus strains in a bacterial consortium degrading a mixture of hydrocarbons, gasoline, and diesel oil additives revealed by metatranscriptomic analysis. Appl. Microbiol. Biotechnol. 99, 2419–2430 (2015).Article 
CAS 

Google Scholar 
Ahmed, R. Z. & Ahmed, N. Isolation of Rhodococcus sp. CMGCZ capable to degrade high concentration of fluoranthene. Water. Air. Soil Pollut. 227, 162 (2016).Ivshina, I. B., Kuyukina, M. S. & Krivoruchko, A. V. Hydrocarbon-oxidizing bacteria and their potential in eco-biotechnology and bioremediation. in Microbial Resources (ed. Kurtboke, I.) 121–148 (Elsevier Inc., 2017). https://doi.org/10.1016/B978-0-12-804765-1.00006-0.Pi, Y. et al. Microbial degradation of four crude oil by biosurfactant producing strain Rhodococcus sp. Bioresour. Technol. 232, 263–269 (2017).Article 
CAS 

Google Scholar 
Cappelletti, M., Fedi, S. & Zannoni, D. Degradation of alkanes in Rhodococcus. in Biology of Rhodococcus, Microbiology Monographs 16 (ed. Alvarez, H. M.) 137–171 (Springer Nature Switzerland AG, 2019). https://doi.org/10.1007/978-3-030-11461-9_6.Kuyukina, M. S. & Ivshina, I. B. Application of Rhodococcus in bioremediation of contaminated environments. in Biology of Rhodococcus, Microbiology Monographs 16 (ed. Alvarez, H. M.) 231–262 (Springer Nature Switzerland, 2019). https://doi.org/10.1007/978-3-642-12937-7_9.Krivoruchko, A. V. et al. Adhesion of Rhodococcus ruber IEGM 342 to polystyrene studied using contact and non-contact temperature measurement techniques. Appl. Microbiol. Biotechnol. 102, 8525–8536 (2018).Article 
CAS 

Google Scholar 
Rubtsova, E. V., Kuyukina, M. S. & Ivshina, I. B. Effect of cultivation conditions on the adhesive activity of Rhodococcus cells towards n-hexadecane. Appl. Biochem. Microbiol. 48, 452–459 (2012).Article 
CAS 

Google Scholar 
Pearlman, R. S., Yalkowsky, S. H. & Banerjee, S. Water solubilities of polynuclear aromatic and heteroaromatic compounds. J. Phys. Chem. Ref. Data 13, 555–562 (1984).Article 
ADS 
CAS 

Google Scholar 
Wrenn, B. A. & Venosa, A. D. Selective enumeration of aromatic and aliphatic hydrocarbon degrading bacteria by a most-probable-number procedure. Can. J. Microbiol. 42, 252–258 (1996).Article 
CAS 

Google Scholar 
Christofi, N., Ivshina, I. B., Kuyukina, M. S. & Philp, J. C. Biological treatment of crude oil contaminated soil in Russia. Geol. Soc. Eng. Geol. Spec. Publ. 14, 45–51 (1998).
Google Scholar 
Sorongon, M. L., Bloodgood, R. A. & Burchard, R. P. Hydrophobicity, adhesion, and surface-exposed proteins of gliding bacteria. Appl. Environ. Microbiol. 57, 3193–3199 (1991).Article 
ADS 
CAS 

Google Scholar 
Bellon-Fontaine, M.-N., Rault, J. & van Ossb, C. J. Microbial adhesion to solvents : a novel method to determine the electron-donor/electron-acceptor or Lewis acid-base properties of microbial cells. Colloids Surf. B Biointerfaces 7, 47–53 (1996).Article 
CAS 

Google Scholar 
Mattos-Guaraldi, A. L., Formiga, L. C. D. & Andrade, A. F. B. Cell surface hydrophobicity of sucrose fermenting and nonfermenting Corynebacterium diphtheriae strains evaluated by different methods. Curr. Microbiol. 38, 37–42 (1999).Article 
CAS 

Google Scholar 
Nikiyan, H., Vasilchenko, A. & Deryabin, D. Humidity-dependent bacterial cells functional morphometry investigations using atomic forcemicroscope. Int. J. Microbiol. 2010, 704170 (2010).Article 

Google Scholar 
Xu, J. L. et al. Rhodococcus qingshengii sp. nov., a carbendazim-degrading bacterium. Int. J. Syst. Evol. Microbiol. 57, 2754–2757 (2007).Lee, S. D. & Kim, I. S. Rhodococcus spelaei sp. nov., isolated from a cave, and proposals that Rhodococcus biphenylivorans is a later synonym of Rhodococcus pyridinivorans, Rhodococcus qingshengii and Rhodococcus baikonurensis are later synonym. Int. J. Syst. Evol. Microbiol. 71, (2021).Korshunova, I. O., Pistsova, O. N., Kuyukina, M. S. & Ivshina, I. B. The effect of organic solvents on the viability and morphofunctional properties of Rhodococcus. Appl. Biochem. Microbiol. 52, 53–61 (2016).Article 

Google Scholar 
de Carvalho, C. C. C. R., Wick, L. Y. & Heipieper, H. J. Cell wall adaptations of planktonic and biofilm Rhodococcus erythropolis cells to growth on C5 to C16 n-alkane hydrocarbons. Appl. Microbiol. Biotechnol. 82, 311–320 (2009).Article 
CAS 

Google Scholar 
Kuyukina, M. S. et al. Oilfield wastewater biotreatment in a fluidized-bed bioreactor using co-immobilized Rhodococcus cultures. J. Environ. Chem. Eng. 5, 1252–1260 (2017).Article 
CAS 

Google Scholar 
Abdel-Shafy, H. I. & Mansour, M. S. M. A review on polycyclic aromatic hydrocarbons: Source, environmental impact, effect on human health and remediation. Egypt. J. Pet. 25, 107–123 (2016).Article 

Google Scholar 
He, J. et al. Subchronic exposure of benzo(a)pyrene interferes with the expression of Bcl-2, Ki-67, C-myc and p53, Bax, Caspase-3 in sub-regions of cerebral cortex and hippocampus. Exp. Toxicol. Pathol. 68, 149–156 (2016).Article 
CAS 

Google Scholar 
Boente, C., Baragaño, D. & Gallego, J. R. Benzo[a]pyrene sourcing and abundance in a coal region in transition reveals historical pollution, rendering soil screening levels impractical. Environ. Pollut. 266, (2020).Cao, Y. et al. Interfacial interaction between benzo[a]pyrene and pulmonary surfactant: Adverse effects on lung health. Environ. Pollut. 287, 117669 (2021).Article 
CAS 

Google Scholar 
Gallardo-Moreno, A. M. et al. Thermodynamic analysis of growth temperature dependence in the adhesion of Candida parapsilosis to polystyrene. Appl. Environ. Microbiol. 68, 2610–2613 (2002).Article 
ADS 
CAS 

Google Scholar 
Kuyukina, M. S., Ivshina, I. B., Korshunova, I. O., Stukova, G. I. & Krivoruchko, A. V. Diverse effects of a biosurfactant from Rhodococcus ruber IEGM 231 on the adhesion of resting and growing bacteria to polystyrene. AMB Express 6, 1–12 (2016).Article 
CAS 

Google Scholar 
Letek, M. et al. The genome of a pathogenic Rhodococcus: Cooptive virulence underpinned by key gene acquisitions. PLoS Genet. 6, 1–17 (2010).Article 

Google Scholar 
Dayan, A. et al. The involvement of coordinative interactions in the binding of dihydrolipoamide dehydrogenase to titanium dioxide – Localization of a putative binding site. J. Mol. Recognit. 30, 1–11 (2017).Article 
ADS 

Google Scholar 
Choi, E. J. & Dimitriadis, E. K. Cytochrome c adsorption to supported, anionic lipid bilayers studied via atomic force microscopy. Biophys. J. 87, 3234–3241 (2004).Article 
ADS 
CAS 

Google Scholar 
Wright, C. J. & Armstrong, I. The application of atomic force microscopy force measurements to the characterisation of microbial surfaces. Surf. Interface Anal. 38, 1419–1428 (2006).Article 
CAS 

Google Scholar 
Salerno, M., Dante, S., Patra, N. & Diaspro, A. AFM measurement of the stiffness of layers of agarose gel patterned with polylysine. Microsc. Res. Tech. 73, 982–990 (2010).CAS 

Google Scholar 
Campbell, J. E., Yang, J. & Day, G. M. Predicted energy-structure-function maps for the evaluation of small molecule organic semiconductors. J. Mater. Chem. C 5, 7574–7584 (2017).Article 
CAS 

Google Scholar 
Wang, N. et al. Molecular elucidating of an unusual growth mechanism for polycyclic aromatic hydrocarbons in confined space. Nat. Commun. 11, 1079 (2020).Article 
ADS 
CAS 

Google Scholar  More

Further details about radiocarbon and thermal analysis, isotopic partitioning procedures and quantification of their uncertainty, and statistical analyses can be found in Supplementary Methods.Study soils, experimental design and soil samplingWe selected three soil types: eutric cambisol, chromic vertisol and silandic andosol70. The three soil profiles studied were found in long-term semi-natural grasslands located relatively close to each other ( More

Pan, H. et al. Archaea and bacteria respectively dominate nitrification in lightly and heavily grazed soil in a grassland system. Biol. Fert. Soils. 54(1), 41–54 (2018).Article 

Google Scholar 
Pan, H. et al. Understanding the relationships between grazing intensity and the distribution of nitrifying communities in grassland soils. Sci. Total Environ. 634, 1157–1164 (2018).Article 
ADS 

Google Scholar 
Dong, L., Li, J. J., Sun, J. & Yang, C. Soil degradation influences soil bacterial and fungal community diversity in overgrazed alpine meadows of the Qinghai-Tibet plateau. Sci. Rep. 11, 11538 (2021).Article 
ADS 

Google Scholar 
Oduor, C. O. et al. Enhancing soil organic carbon, particulate organic carbon and microbial biomass in semi-arid rangeland using pasture enclosures. BMC Ecol. 18, 45 (2018).Article 

Google Scholar 
Wang, S. Z., Fan, J. W., Li, Y. Z. & Huang, L. Effects of grazing exclusion on biomass growth and species diversity among various grassland types of the Tibetan Plateau. Sustainability 11(6), 1705 (2019).Article 

Google Scholar 
Simpson, A. C., Zabowski, D., Rochefort, R. M. & Edmonds, R. L. Increased microbial uptake and plant nitrogen availability in response to simulated nitrogen deposition in alpine meadows. Geoderma 336, 68–80 (2019).Article 
ADS 

Google Scholar 
Qasim, S. et al. Influence of grazing enclosure on vegetation biomass and soil quality. Int. Soil Water Conserv. 5(1), 62–68 (2017).Article 

Google Scholar 
Hirobe, M. et al. Effects of livestock grazing on the spatial heterogeneity of net soil nitrogen mineralization in three types of Mongolian grasslands. J. Soils Sediment. 13, 1123–1132 (2013).Article 

Google Scholar 
Luo, Y. K., Wang, C. H., Shen, Y., Sun, W. & Dong, K. H. The interactive effects of mowing and N addition did not weaken soil net N mineralization rates in semiarid grassland of Northern China. Sci. Rep. 9, 13457 (2019).Article 
ADS 

Google Scholar 
Wu, H. et al. Feedback of grazing on gross rates of N mineralization and inorganic N partitioning in steppe soils of Inner Mongolia. Plant Soil. 340(1–2), 127–139 (2011).Article 

Google Scholar 
Xu, Y. Q., Li, L. H., Wang, Q. B., Chen, Q. S. & Cheng, W. X. The patterns between nitrogen mineralization and grazing intensities in an Inner Mongolian typical steppe. Plant Soil. 300, 289–300 (2007).Article 

Google Scholar 
Wang, X. et al. Grazing improves C and N cycling in the Northern Great Plains: A meta-analysis. Sci. Rep. 6, 33190 (2016).Article 
ADS 

Google Scholar 
Pang, R., Sun, Y., Xu, X. L., Song, M. H. & Ouyang, H. Effects of clipping and shading on 15NO3− and 15NH4+ recovery by plants in grazed and ungrazed temperate grasslands. Plant Soil. 433(1–2), 339–352 (2018).Article 

Google Scholar 
Sun, Y., Schleuss, P. M., Pausch, J., Xu, X. L. & Kuzyakov, Y. Nitrogen pools and cycles in Tibetan Kobresia pastures depending on grazing. Biol. Fert. Soils. 54(5), 569–581 (2018).Article 

Google Scholar 
Andrioli, R. J., Distel, R. A. & Didone, N. G. Influence of cattle grazing on nitrogen cycling in soils beneath Stipa tenuis, native to central Argentina. J. Arid. Environ. 74(3), 419–422 (2010).Article 
ADS 

Google Scholar 
Norman, J. S., Lin, L. & Barrett, J. E. Paired carbon and nitrogen metabolism by ammonia-oxidizing bacteria and archaea in temperate forest soils. Ecosphere 6(10), 1–11 (2016).
Google Scholar 
Mukhtar, H., Lin, Y. P., Lin, C. M. & Petway, J. R. Assessing thermodynamic parameter sensitivity for simulating temperature responses of soil nitrification. Environ. Sci.-Proc. Imp. 21(9), 1596–1608 (2019).
Google Scholar 
Rütting, T., Schleusner, P., Hink, L. & Prosser, J. I. The contribution of ammonia-oxidizing archaea and bacteria to gross nitrification under different substrate availability. Soil Biol. Biochem 160, 108353 (2021).Article 

Google Scholar 
Pan, H. et al. Management practices have a major impact on nitrifier and denitrifier communities in a semiarid grassland ecosystem. J. Soils Sediment. 16, 896–908 (2016).Article 

Google Scholar 
Szukics, U. et al. Management versus site effects on the abundance of nitrifiers and denitrifiers in European mountain grasslands. Sci. Total Environ. 648, 745–753 (2019).Article 
ADS 

Google Scholar 
Chen, Q., Hooper, D. U. & Lin, S. Shifts in species composition constrain restoration of overgrazed grassland using nitrogen fertilization in Inner Mongolian steppe, China. PLoS ONE 6(3), e16909 (2011).Article 
ADS 

Google Scholar 
Raison, R. J., Connell, M. J. & Khanna, P. K. Methodology for studying fluxes of soil mineral-N in situ. Soil Biol. Biochem. 19, 521–530 (1987).Article 

Google Scholar 
Kurola, J., Salkinoja-Salonen, M., Aarnio, T., Hultman, J. & Romantschuk, M. Activity, diversity and population size of ammonia-oxidizing bacteria in oil-contaminated land farming soil. FEMS Microbiol. Lett. 250, 33–38 (2005).Article 

Google Scholar 
Tran, H. T. et al. Bacterial community progression during food waste composting containing high dioctyl terephthalate (DOTP) concentration. Chemosphere 265, 129064 (2021).Article 
ADS 

Google Scholar 
Hook, P. B. & Burke, I. C. Evaluation of a method for estimating net nitrogen mineralization in a semiarid grassland. Soil Sci. Soc. Am. J. 59, 831–837 (1995).Article 
ADS 

Google Scholar 
Liu, T. Z., Nan, Z. B. & Hou, F. J. Grazing intensity effects on soil nitrogen mineralization in semi-arid grassland on the Loess Plateau of northern China. Nutr. Cyc. Agroecosyst. 91(1), 67–75 (2011).Article 

Google Scholar 
Li, J. P., Ma, H. B., Xie, Y. Z., Wang, K. B. & Qiu, K. Y. Deep soil C and N pools in long-term fenced and overgrazed temperate grasslands in northwest China. Sci. Rep. 9, 16088 (2019).Article 
ADS 

Google Scholar 
Di, H. J. et al. Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nat. Geosci. 2(9), 621–624 (2009).Article 
ADS 

Google Scholar 
Li, J. P., Zheng, Z. R., Xie, H. T., Zhao, N. X. & Gao, Y. B. Increased soil nutrition and decreased light intensity drive species loss after eight years grassland enclosures. Sci. Rep. 7, 44525 (2017).Article 
ADS 

Google Scholar 
Luo, C. Y. et al. Effect of warming and grazing on litter mass loss and temperature sensitivity of litter and dung mass loss on the Tibetan plateau. Glob. Change Biol. 16, 1606–1617 (2010).Article 
ADS 

Google Scholar 
Shahzad, T. et al. Contribution of exudates, arbuscular mycorrhizal fungi and litter depositions to the rhizosphere priming effect induced by grassland species. Soil Biol. Biochem. 80, 146–155 (2015).Article 

Google Scholar 
Xie, Z. et al. Identifying response groups of soil nitrifiers and denitrifiers to grazing and associated soil environmental drivers in Tibetan alpine meadows. Soil Biol. Biochem. 77, 89–99 (2014).Article 

Google Scholar 
Clark, I. M., Hughes, D. J., Fu, Q. L., Abadie, M. & Hirsch, P. R. Metagenomic approaches reveal differences in genetic diversity and relative abundance of nitrifying bacteria and archaea in contrasting soils. Sci. Rep. 11, 15905 (2021).Article 
ADS 

Google Scholar 
He, J. Z. et al. Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long-term fertilization practices. Environ. Microbiol. 9, 2364–2374 (2007).Article 

Google Scholar 
Meyer, A. et al. Influence of land use intensity on the diversity of ammonia oxidizing bacteria and archaea in soils from grassland ecosystems. Microb. Ecol. 67(1), 161–166 (2014).Article 

Google Scholar 
Zhu, X. X. et al. Effects of warming, grazing/cutting and nitrogen fertilization on greenhouse gas fluxes during growing seasons in an alpine meadow on the Tibetan Plateau. J. Agric. Meteorol. 214–215, 506–514 (2015).Article 

Google Scholar 
Jia, Z. J. & Cornrad, R. Bacteria rather than archaea dominate microbial ammonia oxidation in an agricultural soil. Environ. Microbiol. 11(7), 1658–1671 (2009).Article 

Google Scholar 
Verhamme, D. T., Prosser, J. I. & Nicol, G. W. Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms. ISME J. 5, 1067–1071 (2011).Article 

Google Scholar 
Zhou, X. H. et al. Diversity, abundance and community structure of ammonia-oxidizing archaea and bacteria in riparian sediment of Zhenjiang ancient canal. Ecol. Eng. 90, 447–458 (2016).Article 

Google Scholar 
Martens-Habbena, W., Berube, P. M., Urakawa, H., de la Torre, J. R. & Stahl, D. A. Ammonia oxidation kinetics determine niche separation of nitrifying archaea and bacteria. Nature 461, 976–979 (2009).Article 
ADS 

Google Scholar 
Clark, D. R. et al. Mineralization and nitrification: Archaea dominate ammonia-oxidising communities in grassland soils. Soil Biol. Biochem. 143, 107725 (2020).Article 

Google Scholar 
Long, X. N., Chen, C. R., Xu, Z. H., Linder, S. & He, J. Z. Abundance and community structure of ammonia oxidizing bacteria and archaea in a Sweden boreal forest soil under 19-year fertilization and 12-year warming. J. Soils Sediment. 12, 1124–1133 (2012).Article 

Google Scholar 
Wessén, E. & Hallin, S. Abundance of archaeal and bacterial ammonia oxidizers-possible bioindicator for soil monitoring. Ecol. Indic. 11, 1696–1698 (2011).Article 

Google Scholar 
Yang, Y. et al. Responses of the functional structure of soil microbial community to livestock grazing in the Tibetan alpine grassland. Glob. Change Biol. 19(2), 637–648 (2013).Article 
ADS 

Google Scholar 
Zhang, C. J. et al. Impacts of long-term nitrogen addition, watering and mowing on ammonia oxidizers, denitrifiers and plant communities in a temperate steppe. Appl. Soil Ecol. 130, 241–250 (2018).Article 

Google Scholar 
Alves, R. J. E., Minh, B. Q., Urich, T., Haeseler, A. V. & Schleper, C. Unifying the global phylogeny and environmental distribution of ammonia-oxidising archaea based on amoA genes. Nat. Commun. 9, 1517 (2018).Article 
ADS 

Google Scholar 
DeLong, E. F. Everything in moderation archaea as ‘non extremophiles’. Curr. Opin. Genet. Dev. 8(6), 649–654 (1998).Article 

Google Scholar 
Jia, Z. J. et al. Evidence for niche differentiation of nitrifying communities in grassland soils after 44 years of different field fertilization scenarios. Pedoshpere 30(1), 87–97 (2019).
Google Scholar 
Wang, X. L. et al. Long-term fertilization effects on active ammonia oxidizers in an acidic upland soil in China. Soil Biol. Biochem. 84, 28–37 (2015).Article 

Google Scholar 
Li, Y. Y., Chapman, S. J., Nicol, G. W. & Yao, H. Y. Nitrification and nitrifiers in acidic soils. Soil Biol. Biochem. 116, 290–301 (2018).Article 

Google Scholar 
Olivera, N. L., Prieto, L., Bertiller, M. B. & Ferrero, M. A. Sheep grazing and soil bacterial diversity in shrub lands of the Patagonian Monte, Argentina. J. Arid. Environ. 125, 16–20 (2016).Article 
ADS 

Google Scholar  More

Hoegh-Guldberg O, Smith JG. The effect of sudden changes in temperature, light, and salinity on the population density and export of zooxanthellae from the reef corals Stylophora pistillata (Esper) and Seriatopora hysterix (Dana). J Exp Mar Biol Ecol. 1989;129:279–303.Article 

Google Scholar 
Glynn PW. Coral reef bleaching: ecological perspectives. Coral Reefs. 1993;12:1–17.Article 

Google Scholar 
Berkelmans R, van Oppen MJH. The role of zooxanthellae in the thermal tolerance of corals: a “nugget of hope” for coral reefs in an era of climate change. Proc R Soc B: Biol Sci. 2006;273:2305–12.Article 

Google Scholar 
Cunning R, Gillette P, Capo T, Galvez K, Baker AC. Growth tradeoffs associated with thermotolerant symbionts in the coral Pocillopora damicornis are lost in warmer oceans. Coral Reefs. 2015;34:155–60.Article 

Google Scholar 
Scharfenstein HJ, Chan WY, Buerger P, Humphrey C, van Oppen MJH. Evidence for de novo acquisition of microalgal symbionts by bleached adult corals. ISME J. 2022;16:1676–9.Article 

Google Scholar 
Goulet TL. Most corals may not change their symbionts. Mar Ecol Prog Ser. 2006;321:1–7.Article 

Google Scholar 
Jones A, Berkelmans R. Potential costs of acclimatization to a warmer climate: growth of a reef coral with heat tolerant vs. sensitive symbiont types. PLoS ONE. 2010;5:e10437.Article 

Google Scholar 
van Oppen MJH, Oliver JK, Putnam HM, Gates RD. Building coral reef resilience through assisted evolution. Proc R Soc B: Biol Sci. 2015;112:2307–13.
Google Scholar 
Buerger P, Alvarez C, Coppin CW, Pearce SL, Chakravarti LJ, Oakeshott JG, et al. Heat-evolved microalgal symbionts increase coral bleaching tolerance. Sci Adv. 2020;6:eaba2498.Kuffner IB, Toth LT. A geological perspective on the degradation and conservation of western Atlantic coral reefs. Conserv Biol: J Soc Conserv Biol. 2016;30:706–15.Article 

Google Scholar 
Young CN, Schopmeyer SA, Lirman D. A review of reef restoration and Coral propagation using the threatened genus Acropora in the Caribbean and western Atlantic. Bull Mar Sci. 2012;88:1075–98.Article 

Google Scholar 
Reich HG, Kitchen SA, Stankiewicz KH, Devlin-Durante M, Fogarty ND, Baums IB. Genomic variation of an endosymbiotic dinoflagellate (Symbiodinium fitti) among closely related coral hosts. Mol Ecol. 2021;30:3500–14.Article 

Google Scholar 
Baums IB, Devlin-Durante MK, Lajeunesse TC. New insights into the dynamics between reef corals and their associated dinoflagellate endosymbionts from population genetic studies. Mol Ecol. 2014;23:4203–15.Article 

Google Scholar 
Gantt SE, Keister E, Manfroy A, Merck D, Fitt W, Muller E, et al. Wild and nursery-raised corals: comparative physiology of two framework coral species. Coral Reefs. (In Press).Hume BCC, Smith EG, Ziegler M, Hugh J, Warrington M, Burt J, et al. SymPortal: a novel analytical framework and platform for coral algal symbiont next-generation sequencing ITS2 profiling. Mol Ecol Resour. 2019;19:1063–80.Article 

Google Scholar 
Randall CJ, Negri AP, Quigley KM, Foster T, Ricardo GF, Webster NS, et al. Sexual production of corals for reef restoration in the Anthropocene. Mar Ecol Prog Ser. 2020;635:203–32.Article 

Google Scholar 
Bay LK, Cumbo VR, Abrego D, Kool JT, Ainsworth TD, Willis BL. Infection dynamics vary between Symbiodinium types and cell surface treatments during establishment of endosymbiosis with coral larvae. Diversity. 2011;3:356–74.Article 

Google Scholar 
Abrego D, van Oppen MJH, Willis BL. Highly infectious symbiont dominates initial uptake in coral juveniles. Mol Ecol. 2009;18:3518–31.Article 

Google Scholar 
Cunning R, Silverstein RN, Baker AC. Investigating the causes and consequences of symbiont shuffling in a multi-partner reef coral symbiosis under environmental change. Proc R Soc B: Biol Sci. 2015;282:20141725.Chamberland VF, Petersen D, Latijnhouwers KRW, Snowden S, Mueller B, Vermeij MJA. Four-year-old Caribbean Acropora colonies reared from field-collected gametes are sexually mature. Bull Mar Sci. 2016;92:263–4.Silverstein RN, Correa AMS, Baker AC. Specificity is rarely absolute in coral–algal symbiosis: implications for coral response to climate change. Proc R Soc B: Biol Sci. 2012;279:2609–18.Article 

Google Scholar  More

Laboratory cultureOchrosphaera neapolitana (RCC1357) was precultured in K/2 medium without Tris buffer8 using artificial seawater (ASW) supplemented with NaHCO3 and HCl to yield an initial DIC of 2050 µM. In triplicate, 1-L bottles were filled with 150 mL of seawater medium with air in the bottle headspace and inoculated with a mid-log phase preculture at an initial cell concentration of 104 cells mL−1. Cultures were grown at 18 °C under a warm white LED light at 100 ± 20 µE on a 16h-light/8h-dark cycle. Bottles were orbitally shaken at 60 rpm to keep cells in suspension. Cell growth was monitored with a Multisizer 4e particle counter and sizer (Beckman Coulter). At ~1.4 × 105 cells mL−1, cells were diluted up to 300 mL to 2–3 × 104 cells mL−1 and harvested after 2 days of more exponential growth up to 7.9 ± 0.6 × 104 cells mL−1. More detailed culture results are listed in the Supplementary Note 1.Immediately after harvesting, pH was measured using a pH probe calibrated with Mettler Toledo NBS standards (it should be noted here that high ionic strength calibration standards would be optimal for pH measurement of liquids like seawater). There was a carbonate system shift during the batch culture and more details are shown in Supplementary Fig. S1. Cells in 50 mL were pelleted by centrifuging at ~1650 × g for 5 min. Seawater supernatant was analyzed for DIC and δ13CDIC by injecting 3.5 mL into an Apollo analyzer and injecting 1 mL into He-flushed glass vials containing H3PO4 for the Gas Bench.For seawater DIC, an Apollo SciTech DIC-C13 Analyzer coupled to a Picarro CO2 analyzer was calibrated with in-house NaHCO3 standards dissolved in deionized water at different known concentrations and δ13C values from −4.66 to −7.94‰. δ13CDIC in media were measured with a Gas Bench II with an autosampler (CTC Analytics AG, Switzerland) coupled to ConFlow IV Interface and a Delta V Plus mass spectrometer (Thermo Fischer Scientific). Pelleted cells were snap-frozen with N2 (l) and stored at −80 °C. For PIC analysis, pellet was resuspended in 1 mL methanol and vortexed. After centrifugation, the methanol phase with extracted organics was removed and the pellet containing the coccoliths was dried at 60 °C overnight. About 300 mg of dried coccolith powder were placed in air-tight glass vials, flushed with He and reacted with five drops of phosphoric acid at 70 °C. PIC δ13C and δ18O were measured by the same Gas Bench system. The system and abovementioned in-house standards were calibrated using international standards NBS 18 (δ13C = −5.01‰, δ18O = +23.00‰) and NBS 19 (δ13C = +1.95‰, δ18O = +2.2‰). The analytical error for DIC concentration and δ13C is More