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    Quantitative environmental DNA metabarcoding shows high potential as a novel approach to quantitatively assess fish community

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    Revenue loss due to whale entanglement mitigation and fishery closures

    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

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    Different roles of concurring climate and regional land-use changes in past 40 years’ insect trends

    All statistical analyses were performed through R version 4.1.050. Besides the explicitly mentioned packages, the R packages cowplot51, data.table52, dplyr53, ggplot254, itsadug55, purrr56, raster57, sf58, sfheaders59, tibble60 and tidyr61 were key for data handling, data analysis, and plotting. Posterior distributions were summarised through means and credible intervals (CIs). CIs are the highest density intervals, calculated through the package bayestestR62. To summarise multiple posterior distributions, 5000 Monte Carlo simulations were used.Study regionThe study included data from the whole of Switzerland. As an observation unit for records, we chose 1 × 1 km squares (henceforth squares). Switzerland covers 41,285 km2, spanning a large gradient in elevation, climate and land use. It can be divided into five coarse biogeographic regions based on floristic and faunistic distributions and on institutional borders of municipalities63 (Fig. 1b). The Jura is a mountainous but agricultural landscape in the northwest (~4200 km2, 300–1600 m asl; annual mean temperature: ~9.4 °C, annual precipitation: ~1100 mm (gridded climate data here and in the following from MeteoSwiss (https://www.meteoswiss.admin.ch), average 1980–2020, at sites ~500 m asl.)). The Jura is separated from the Alps by the Plateau, which is the lowland region spanning from the southwest to the northeast (~11,300 km2, 250–1400 m asl, mostly below 1000 m asl; ~9.5 °C, ~1100 mm). It is the most densely populated region with most intensive agricultural use. For the Alps, three regions can be distinguished. The Northern Alps (~10,700 km2, 350–4000 m asl; ~9.2 °C, ~1400 mm), which entail the area from the lower Prealps, which are rather densely populated and largely used agriculturally, up to the northern alpine mountain range. The Central Alps (~11,300 km2, 450–4600 m asl; ~9.5 °C, ~800 mm) comprise of the highest mountain ranges in Switzerland and the inner alpine valleys characterised by more continental climate (i.e., lower precipitation). Intensive agricultural land use is concentrated in the lower elevations and agriculture in higher elevations is mostly restricted to grassland areas used for summer grazing. The Southern Alps (~3800 km2, 200–3800 m asl; ~10.4 °C, 1700 mm) range from the southern alpine mountain range down to the lowest elevations of Switzerland and are clearly distinguished from the other regions climatically, as they are influenced by Mediterranean climate, resulting in, e.g., milder winters. Besides differences between biogeographic regions, climate, land use and changes therein vary greatly between different elevations (Supplementary Fig. S9). To account for these differences, we split the regions in two elevation classes at the level of squares. All squares with a mean elevation of less than 1000 m asl were assigned to the low elevation, whereas squares above 1000 m asl were assigned to the high elevation (no squares in the Plateau fell in the high elevation). This resulted in nine bioclimatic zones (Fig. 1b), for which separate species trends were estimated in the subsequent analyses. The threshold of 1000 m asl enabled a meaningful distinction based on the studied drivers (climate and land-use change) and was also determined by the availability of records data (high coverage in all nine bioclimatic zones).Species detection dataWe extracted records of butterflies (refers here to Papilionoidea as well as Zygaenidae moths), grasshoppers (refers here to all Orthoptera) and dragonflies (refers here to all Odonata) from the database curated by info fauna (The Swiss Faunistic Records Centre; metadata available from the GBIF database at https://doi.org/10.15468/atyl1j, https://doi.org/10.15468/bcthst, https://doi.org/10.15468/fcxtjg). This database unites faunistic records made in Switzerland from various sources including both records by private persons and from projects such as research projects, Red-List inventories or checks of revitalisation measures. Only records with a sufficient precision, both temporally (day of recording) and spatially (place of recording known to the precision of 1 km2 or less), were used for analyses. Besides temporal and spatial information, information on the observer and the project (if any) was obtained for each record. All records made by a person/project on a day in a square were attributed to one visit, which was later used as replication unit to model the observation process (see below).We included records from the focal time range 1980–2020. Additionally, we included records from 1970–1979 for butterflies in occupancy-detection models to increase the robustness of mean occupancy estimates. We excluded the mean occupancy estimates for these additional years from further analyses to cover the same period for all groups. Prior to analyses, following the approach in ref. 26, we excluded observations of non-adult stages and observations from squares that only were visited in 1 year of the studied period, because these would not contain any information on change between years64. This resulted in 18,018 squares (15,248 for butterflies, 9870 for grasshoppers, 5188 for dragonflies) and 1,448,134 records (879,207 butterflies, 272,863 grasshoppers, 296,064 dragonflies) that we included in the analyses (Supplementary Fig. S2). The three datasets for the different groups were treated separately for occupancy-detection modelling, following the same procedures for all three groups. To determine detections and non-detections for each species and visit, which could then be used for occupancy-detection modelling, we only included visits that (a) did not originate from a project, which had a restricted taxonomic focus not including the focal species, (b) were not below the 5% quantile or above the 95% quantile of the day of the year at which the focal species has been recorded26 and (c) were from a bioclimatic zone, from which the focal species was recorded at least once.Occupancy-detection modelsWe used occupancy-detection models65,66 to estimate annual mean occupancy of squares for the whole of Switzerland and for the nine bioclimatic zones for each species (i.e., mean number of squares occupied by a species), mostly following the approach in ref. 26. We fitted a separate model for each species, based on different datasets for the three groups. We included only species that were recorded in any square in at least 25% of all analysed years. Occupancy-detection models are hierarchical models in which two interconnected processes are modelled jointly, one of which describes occurrence probability (ecological process; used to infer mean occupancy), whereas the other describes detection probability (observation process)65. The two processes are modelled through logistic regression models. The occupancy model estimates occurrence probability for all square and year combinations, whereas the observation model estimates the probability that a species has been detected by an observer during a visit. More formally, each square i in the year t has the latent occupancy status zi,t, which may be either 1 (present) or 0 (absent). zi,t depends on the occurrence probability ψi,t as follows$${z}_{i,t}sim {{{mbox{Bern}}}}left({psi }_{i,t}right)$$
    (1)
    The occupancy status is linked to the detection/non-detection data yi,t,j at square i in year t at visit j as$${y}_{i,t,, j}{{|}}{z}_{i,t}sim {mathrm {Bern}}({z}_{i,t}{p}_{i,t,j})$$
    (2)
    where pi,t,j is the detection probability.The regression model for occurrence probability (occupancy model) looked as follows$${{mbox{logit}}}({psi }_{i,t})={mu }_{o}+{beta }_{o1}{{{{{rm{elevatio}}}}}}{{{{{{rm{n}}}}}}}_{i}+{beta }_{o2}{{{{{rm{elevatio}}}}}}{{{{{{rm{n}}}}}}}_{i}^{2}+{alpha }_{o1,i}+{alpha }_{o2,i}+{gamma }_{r(i),t}$$
    (3)
    with μo being the global intercept, elevationi being the scaled elevation above sea level and αo1,i, αo2,i and γr(i),t being the random effects for fine biogeographic region (12 levels, Supplementary Fig. S10; these were again defined based on floristic and faunistic distributions and followed institutional borders63), square and year. The random effects for fine biogeographic region and square were modelled as follows:$${alpha }_{o1}sim {{{{{rm{Normal}}}}}}left(0,{sigma }_{o1}right)$$
    (4)
    and$${alpha }_{o2}sim {{{{{rm{Normal}}}}}}left(0,{sigma }_{o2}right)$$
    (5)
    The random effect of the year was implemented with separate random walks per zone following ref. 67, which allowed the effect to vary between the nine bioclimatic zones, while accounting for dependencies among consecutive years. Conceptually, in random walks, the effect of 1 year is dependent on the previous year’s effect, resulting in trajectories with less sudden changes between consecutive years. This was implemented as follows:$${gamma }_{r,t}sim left{begin{array}{c}{{{{{rm{Normal}}}}}}left(0,{1.5}^{2}right){{{{rm{for}}}}},t=1\ {{{{{rm{Normal}}}}}}left({gamma }_{r,t-1},{sigma }_{gamma r}^{2}right){{{{rm{for}}}}},t , > ,1end{array}right.$$
    (6)
    with$${sigma }_{gamma r}sim {{mbox{Cauchy}}}left(0,1right)$$
    (7)
    The regression model for detection probability (observation model) looked as follows$${{{{rm{logit}}}}}({p}_{i,t,j}) =, {mu }_{d}+{beta }_{d1}{{{{{rm{yda}}}}}}{{{{{{rm{y}}}}}}}_{j}+{beta }_{d2}{{{{{rm{yda}}}}}}{{{{{{rm{y}}}}}}}_{j}^{2}+{beta }_{d3}{{{{{rm{shortlis}}}}}}{{{{{{rm{t}}}}}}}_{j}+{beta }_{d4}{{{{{rm{longlis}}}}}}{{{{{{rm{t}}}}}}}_{j} \ quad+ {beta }_{d5}{{{{{rm{exper}}}}}}{{{{{{rm{t}}}}}}}_{j}+{beta }_{d6}{{{{{rm{projec}}}}}}{{{{{{rm{t}}}}}}}_{j}+{beta }_{d7}{{{{{rm{targeted}}}}}}_{{{{{rm{projec}}}}}}{{{{{{rm{t}}}}}}}_{j} \ quad+ {beta }_{d8}{{{{{rm{redlis}}}}}}{{{{{{rm{t}}}}}}}_{j}+{alpha }_{d1,t}$$
    (8)
    where μd is the global intercept, ydayj is the scaled day of the year of visit j, shortlistj and longlistj are dummies of a three-level factor denoting the number of species recorded during the visit (1; 2–3; >3), and expertj, projectj, targeted_projectj and redlistj are dummies of a five-level factor denoting the source of the data. The source might either be a common naturalist observation (reference level), an observation by an expert naturalist, an observation made during a not further specified project, an observation made in a project targeted at the focal species or an observation made during a Red-List inventory. An expert naturalist was defined as an observer that contributed a significant number of records, which was defined as the upper 2.5% quantile of all observers arranged by their total number of records, and that made at least one visit with an exceptionally long species list, which was defined as a visit in the upper 2.5% quantile of all visits arranged by the number of records. The proportions of records originating from these different sources changed across years, but change was not unidirectional and differed among the investigated groups (Supplementary Fig. S11), such that accounting for data source in the model should suffice to yield reliable estimates of occupancy trends. αd1,t is a random effect for year, which was modelled as$${alpha }_{d1}sim {{{{{rm{Normal}}}}}}left(0,{sigma }_{d1}right)$$
    (9)
    The occupancy and observation models were fitted jointly in Stan through the interface CmdStanR68. Four Markov chain Monte Carlo chains with 2000 iterations each, including 1000 warm-up iterations, were used. Priors of the model parameters are specified in Supplementary Table S5. For the prior distribution of global intercepts, a standard deviation of 1.5 was chosen to not overweight the extreme values on the probability scale. To ensure that chains mixed well, Rhat statistics for annual mean occupancy estimates were calculated through the package rstan69. For Switzerland-wide annual estimates (n = 18,140), 98.0% of values met the standard threshold of 1.1 (99.9% of values More

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    Siberian carbon sink reduced by forest disturbances

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    Re-examining extreme carbon isotope fractionation in the coccolithophore Ochrosphaera neapolitana

    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