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    Diet-driven mercury contamination is associated with polar bear gut microbiota

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    Millimeter-scale vertical partitioning of nitrogen cycling in hypersaline mats reveals prominence of genes encoding multi-heme and prismane proteins

    Porewater concentrations of dissolved oxygen and nutrientsThe sampling location and appearance of the microbial mats used in this study in cross section are shown in Fig. 1. Profound changes in dissolved oxygen concentration were observed over the diel cycle because of high rates of oxygenic photosynthesis in the daytime and oxygen-requiring respiration at night (Table 1). Briefly, Layer 1 was characterized by oxygen concentration fluctuations in the range of 200–800 µM. Layers 2 and 3 ranged from 0–1200 µM and 0–200 µM, respectively. Mat Layer 4 (3–4 mm below the surface) may contain some dissolved oxygen near noon on days when there is high solar irradiance but stays anoxic for most hours of most days. Layers 5–7 (4–7 mm from the surface) remain anoxic.Table 1 Oxygen concentrations throughout the first 4 mm of the mat measured at 100 µm resolution using microsensors, measured on 22 August, 2019.Full size tableConcentrations of ammonium (Table 1) reveal a pattern of increasing concentration with depth (34–124 µM) through the layers examined here. Nitrate concentrations ranged between 26–33 µM, with low variation across depths. The concentration of phosphate ranged between 3–6 µM, with the highest concentration detected in Layer 1 (0–1 mm from surface) at 5.5 µM.Analysis of genes and transcripts in mat layers by qPCR and RT-qPCRGene-copy number ranges for both DNA and cDNA across all layers for all genes examined are summarized as follows: Bacteria, 104−1010 per g mat and 101−105, per ng nucleic acid; Archaea, 106−108 and 102−104; nifH, 108−1011 and 104−107; archaeal-amoA, 104−105 and 2–3; bacterial-amoA, 104−107 and 3–335; Nitrospira-nxrB, 105−107 and 27–372; nosZ, 103−105 and 2–10; nirS, 105−107 and 33–1941; Planctomycetes-16S rRNA gene and cDNA of transcripts, 104−106 and 6–66 (Fig. 2, S1).Fig. 2: Vertical patterns in the abundance (DNA) and expression (cDNA) of Bacterial and Archaeal ribosomal and nitrogen cycling genes.Number of copies of DNA and cDNA genes recovered for Bacteria (A), Archaea (B), nifH (C), Archaeal-amoA (D), Bacterial-amoA (E), Nitrospira-nxrB (F), nosZ (G), nirS (H) and Planctomycetes-16S rRNA gene marker (anammox proxy) (I), per g of microbial mat, quantified by qPCR and RT-qPCR in hypersaline microbial mat profiles from different depths. P-values from Kruskal–Wallis test are overlain on each, and different letters indicate significantly different values for the given gene based on a Conover-Iman test p-value of  0.8, Table 2).Fig. 4: Non-metric multidimensional scaling (NMDS) plots of quantification of all nitrogen genes across all layers examined in this study.Genes associated with the following nitrogen transformations were examined: nitrogen fixation (nifH), nitrification (Bacterial-amoA, Archaeal-amoA, Nitrospira-nxrB), denitrification (nosZ, nirS) and Planctomycetes-16S rRNA gene marker (anammox proxy). The biotic data was standardized, and a sample resemblance matrix was generated using Bray-Curtis coefficient of similarity. In order to analyze the influence of abiotic variables (porewater nutrient and oxygen concentration) on the patterns of the biotic data, monotonic correlations of the abiotic variables were performed. In the plots, the distance between the samples’ points reflects their relative similarity, according to Bray-Curtis similarity matrices based on cDNA/DNA ratios of nitrogen genes examined. The vectors in panel A represent the cDNA/DNA ratios of nitrogen gene examined. In panel B, the vectors represent the environmental variables.Full size imageTable 2 (A) Spearman correlations coefficient (r) between the ratios of cDNA/DNA of nitrogen fixation (nifH), nitrification (Bacterial-amoA, Archaeal-amoA, Nitrospira-nxrB), denitrification (nosZ, nirS) and Planctomycetes-16S rRNA gene marker (anammox proxy) and oxygen, ammonium, nitrate and phosphate concentrations. (B) Spearman correlation p-value.Full size tablenifH, Bacterial-amoA and Archaeal-amoA were positively correlated with oxygen concentration (r ≥ 0.22, Table 2), while Nitrospira-nxrB was negatively correlated with oxygen (r = −0.68, Table 2). Denitrification genes (nosZ, nirS) and Planctomycetes-16S rRNA genes were all positively correlated with ammonium (r ≥ 0.5) and orthophosphate (r ≥ 0.13) and negatively correlated with oxygen (r  > −0.70).Metagenome analysis of nitrogen cyclingA total number of 922 324 genes were identified; 1305 of these genes were annotated with KOs that are part of KEGG’s Nitrogen Metabolism pathway (Table S2, S3). A dendrogram based on Bray-Curtis similarities of normalized coverages of all recovered nitrogen metabolism genes is shown in Fig. 5A. Overall, the similarity between the layers was >75%. According to SIMPROF analysis, there was a significant difference in the N-related gene coverages (based on an alpha value of 0.05) between Layers 1-Layer 2, Layer 3, and Layer 4 (p = 0.001) and Layer 2-Layer 3, and Layer 4 (p = 0.001), but not between Layers 3 and Layer 4 (p = 1), where the similarity was >90%.Fig. 5: Functional nitrogen gene distribution based on metagenome analysis.A Cluster analysis illustrating the similarity of normalized coverages of all recovered nitrogen metabolism genes across the uppers 4 layers examined [(Layer 1 (0–1 mm from surface), Layer 2 (1–2 mm from surface), Layer 3 (2–3 mm from surface), Layer 4 (3–4 mm from surface)]. Red lines show non-significant differences, according to SIMPROF analysis (p  > 0.05). B The bar plots show the genes of the metabolic pathways in the nitrogen cycle identified in the mat, according metagenome analysis, with relative coverage of each nitrogen cycling gene across depths examined (Fraction of Depth Integrated Coverage, FDIC). 355 unique genes were recovered from KEGG’s Nitrogen Metabolism pathway: 60 annotated as involved in nitrogen fixation, 15 in assimilatory nitrate reduction, 38 in dissimilatory nitrate reduction to ammonia (DNRA), 52 in hydroxylamine dehydrogenase EC 1.7.2.6, 121 in hydroxylamine reductase, 69 in denitrification pathway. C Values of Nitrogen-focused Coverage per Million (N-CPM). The following enzymes perform nitrogen transformation in the mat: nitrogenase molybdenum-iron protein alpha chain (nifD), nitrogenase iron protein NifH, nitrogenase molybdenum-iron protein beta chain (nifK), hydroxylamine dehydrogenase EC 1.7.2.6 (hao), hydroxylamine reductase (hcp), nitrate reductase/nitrite oxidoreductase, alpha subunit (narG, narZ, nxrA), nitrate reductase/nitrite oxidoreductase, beta subunit (narH, narY, nxrB), nitrate reductase (cytochrome) (napA), nitrate reductase (cytochrome), electron transfer subunit (napB), nitrite reductase (NO-forming) / hydroxylamine reductase (nirS), nitrogenase molybdenum-iron protein beta chain (nirK), nitric oxide reductase subunit B (norB), nitric oxide reductase subunit C (norC), nitrous-oxide reductase (nosZ), nitrate reductase gamma subunit (narI, narV), cytochrome c nitrite reductase small subunit (nrfH), nitrite reductase (cytochrome c-552) (nrfA), ferredoxin-nitrite reductase (nirA), ferredoxin-nitrate reductase (narB), MFS transporter, NNP family, nitrate/nitrite transporter (NRT, nark, nrtP, nasA). D Nitrogen cycling genes recovered in this study and the transformation that they catalyze.Full size imageThe nitrogen fixation pathway was identified with nifD, nifH, and nifK genes (Fig. 5B, C, Table S4). Of the 60 genes detected in this metabolic pathway 17 genes were annotated as nifD, 22 genes as nifH, and 21 genes as nifK. The normalized coverage of these genes showed a decreasing trend with depth. Layer 1 was characterized by the highest values of Nitrogen-focused coverage per million (N-CPM, see Supplementary Text 1) of nifD, nifH, and nifK genes: 56264.7, 54934.2 and 60059.2, respectively. On average, the three genes involved in nitrogen fixation, nifD, nifH, and nifK, decreased with depth, (2.7-fold from Layer 1 to Layer 4, with a nearly 2-fold difference solely between Layer 1 and Layer 2).Genes involved in nitrate assimilation, annotated as nirA and narB which code for ferredoxin nitrate reductase, were 3 times as abundant in Layer 1 than Layer 2, but decreased less markedly from Layer 2 to Layers 3 and 4.Genes for dissimilatory nitrite reduction (nrfA, and nrfH) were 4 and 16 times more abundant in Layer 4 than Layer 1. Similarly, the nitrate/nitrite regulator protein genes narl and narV displayed a nearly inverse pattern, with Layer 1 having the least proportion of genes, a large increase from Layer 1 to Layer 2, and additional increases from Layer 2 to Layers 3 and Layer 4 (Fig. 5B, C, Table S4).Genes associated with nitrification were very poorly represented in the metagenome. No genes associated with ammonia oxidation (amoA) were detected. Genes associated with nitrite oxidation (nrxA, nrxB) that were detected are so closely related to denitrifier genes (narG, narZ, narH, narY) as to be annotated with the same KEGG KO models (K00370 representing narG, narZ, nxrA; and K00371 representing narH, narY, nxrB).The following genes involved in denitrification were detected: napA, napB, narG, narZ, narH, narY, narI, narV, nirK, nirS, norB, norC, and nosZ (Fig. 5B, C). The nitrate reduction metabolic pathway was represented by 4 genes encoding the nitrate reductase-nitrite oxidoreductase-alpha subunit (narG, narZ, nxrA genes), 6 genes encoding the nitrate reductase-nitrite oxidoreductase-beta subunit (narH, narY, nxrB genes), 31 genes encoding the nitrate reductase gamma subunit (narI, narV), 5 genes encoding the nitrate reductase -cytochrome electron transfer subunit (napB) and 7 genes encoding the nitrate reductase -cytochrome (napA) (Table S4). The N-CPM of nitrate reductase increased with depth, but with a similar proportion of those genes in Layers 3 and 4. With respect to nitrite reductase (nirk and nirS genes, 2 and 1 genes, respectively), no nirK genes were detected in Layer 1, where the highest N-CPM of nirS was recovered (Fig. 5B). In contrast, Layer 3 had no detected nirS and the highest N-CPM of nirK. Regarding nitric oxide reductase (norB and norC genes, 6 and 1 genes, respectively), the highest normalized coverage of norB was detected in Layer 3, while highest for norC was in Layer 1. Finally, nosZ (6 genes) was detected in all the layers, steadily decreasing in normalized coverage from the top layer to the deepest (Fig. 5B, C; Table S4).DNRA metabolism was represented by nrfA (26 genes) and nrfH (12 genes), and by narI, narV (31). Layer 1 was characterized by the lowest normalized coverage of narI, narV, nrfA, and nrfH genes (6880.2, 3724.6, and 284.6 N-CPM, respectively), while Layer 3 was characterized by the greatest coverage of narI, narV, nrfA, and nrfH genes (32760.5, 14417.9 and 4504.1, respectively; Fig. 5B, C; Table S4).Genes for hydroxylamine dehydrogenase EC 1.7.2.6 and hydroxylamine reductase (hao and hcp, respectively) were the most abundant nitrogen metabolism genes in the mat: hao having a cumulative N-CPM of ~150000 and hcp having a cumulative N-CPM of nearly 350,000 across the 4 depths (Fig. 5C). Both genes increased in abundance with depth; hcp increased two-fold between Layer 1 and Layer 2, and more gradually in Layer 3 and Layer 4. Hao exhibited a three-fold increase in relative abundance from Layer 1 to Layer 2 and remained relatively constant through Layer 3 and Layer 4 (Fig. 5B, C; Table S4). More

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    Temperature-dependent modelling and spatial prediction reveal suitable geographical areas for deployment of two Metarhizium anisopliae isolates for Tuta absoluta management

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    Modelling ocean acidification effects with life stage-specific responses alters spatiotemporal patterns of catch and revenues of American lobster, Homarus americanus

    Model speciesThe American lobster Homarus americanus, is a crustacean found in temperate regions across the Northwest Atlantic Ocean. It is a highly valuable fishery species, caught off the coast of Eastern Canada and Northeast USA. For the past decade, they have been the most valuable single-species fishery in all of Canada and the US30,48. In Canada, catch was estimated at 104,000 tonnes and 14% of all of Canada’s total marine fisheries catch in 2019. However, their landed value was almost $1.6 billion and 44% of the Canada’s total marine fisheries landed value, and over 49% of the landed value from Canada’s Atlantic coast fisheries30,49. Canada’s Atlantic marine fisheries provide employment to over 40,000 people in primary harvesting and processing sectors, and supports many rural populations30.Dynamic bioclimate envelope modelWe used a dynamic bioclimate envelope model (DBEM)31,50 to assess spatial and temporal changes in the abundance and fisheries catch under different scenarios of climate change and fishing pressure. The model infers the environmental preference of the modelled species51, and simulates future changes in biomass and maximum catch potential. Notably, the DBEM integrates growth models52, ecophysiological models53, advection–diffusion models54, and surplus production population dynamics models55 to determine ocean change effects on species distribution, abundance, and catch. Since H. americanus is primarily a benthic invertebrate, we used values at sea floor for environmental variables in our model. However, they also have a pelagic larval phase and we used surface environmental variables to model this life stage.Initial distribution and abundanceThe DBEM uses an initial species distribution determined using a rule-based algorithm56,57,58. This algorithm determines species’ distribution range base on a series of geographic constraints, including latitudinal range, depth range, occurring ocean basins, and published or expert provided ‘bounding box’. It assumes that the relative abundance of the species distributes along gradients within these geographic limits with the centroid of the range having the highest relative abundance (Palomares et al. 2016). Species distributions are mapped on a global grid with a resolution of 0.5° longitude by 0.5° latitude cells with values representing relative abundance. Historical reconstructed catch data (http://www.seaaroundus.org)59 was used to estimate the global abundance and distributed accordingly with relative abundance values60. These catch data are based on various government and non-government reports, primary and grey literature, and also mapped on a 0.5° longitude by 0.5° latitude grid.The initial species distribution is then overlaid on climatologies of historical environmental conditions (e.g. temperature, salinity, oxygen, pH) simulated from outputs of Earth system models (e.g. Bopp et al. 2013; Dunne et al. 2013). The DBEM assumes that species distribution is in equilibrium with the average historical environmental condition (1971–2000 average) and abundance in cells are assumed to be at carrying capacity.Modelling individual growthGrowth is modelled using a derived von Bertalanffy growth model to incorporate how environmental stressors affects body size of lobsters31,32,61. We model the following important life history parameters as a function of relative changes in temperature, oxygen content [O2], and pH [H+]. Growth rate (dB/dt) is dependent on weight-specific anabolic and catabolic rates:$$frac{dB}{{dt}} = H_{i,t} W^{d} – k_{i,t} W$$
    (1)
    where H and k represent the coefficients for oxygen supply (anabolism) and oxygen demand for maintenance metabolism (catabolism), respectively, for cell i at time t. Body weight is scaled to anabolism with the exponent d  40 ppt), mixoeuhaline ( > 29 ppt), polyhaline ( > 18 ppt), mesophaline ( > 5 ppt), oligohaline ( > 0 ppt)—and SAssoc is the association of the species with each salinity class; and Icei is the sea ice % area coverage in a cell and IceP is the ice-dependency of the species. For H. americanus, they are not specifically associated with any habitat and thus only restricted by depth parameters. However, they are limited to mixoeuhaline and polyhaline salinities62.The TPP was estimated using the initial predicted relative abundance (described above) overlaid with the inputs of earth system models of initial environmental conditions. The relative weight for each temperature class z of the temperature preference profile was calculated as (TPP_{z} = R_{z} /sum R_{z}), where Rz is the relative abundance in each temperature class.A fuzzy logic model was used to model the movement between neighbouring cells based on differences in habitat suitability50. Emigration into a cell is favoured if habitat suitability is higher than surrounding cells, and immigration out of a cell is favoured if habitat suitability is lower than surrounding cells.We estimated larval production as 30% of spawning population biomass for each cell i, while larval mortality was 0.85 day−1 and settlement rate was 0.15 day−1—these values were chosen based on the sensitivity testing of these parameters50.Larval dispersal is modelled using an advection–diffusion54 and a larval duration model based on temperature66, such that abundance Ai,t in each cell is numerically solved for using the equation:$$frac{{partial A_{i,t} }}{partial t} = frac{partial }{partial x}left( {D_{i,t} frac{{partial A_{i,t} }}{partial x}} right) + frac{partial }{partial y}left( {D_{i,t} frac{{partial A_{i,t} }}{partial y}} right) – frac{partial }{partial y}left( {u cdot A_{i,t} } right) – frac{partial }{partial y}left( {v cdot A_{i,t} } right) – lambda cdot A_{i,t}$$
    (16)
    while adult dispersal is similarly modelled,$$frac{{partial A_{i,t} }}{partial t} = frac{partial }{partial x}left( {D_{i,t} frac{{partial A_{i,t} }}{partial x}} right) + frac{partial }{partial y}left( {D_{i,t} frac{{partial A_{i,t} }}{partial y}} right)$$
    (17)
    Advection was modelled for larval dispersal using parameters u and v for horizontal (east–west) and vertical (north–south) directions for surface current velocity (m2 s−1), respectively, between neighbouring cells x and y in the east–west and north–south direction, respectively. Instantaneous rate of larval mortality, ML, and settlement, SL was integrated into Eq. (16), where (lambda = 1 – e^{{ – left( {M_{L} + S_{L} } right)}}). The coefficient Di,t is the diffusion parameter:$$D_{i,t} = frac{{D_{i,0} cdot m}}{{1 + e^{{(tau cdot P_{i,t} cdot rho_{i,t} )}} }}$$
    (18)
    and$$rho_{i,t} = 1 – frac{{emptyset_{i,t} }}{{left( {C_{i,t} /overline{W}_{i,t} } right)}}$$
    (19)
    where Di,0 is the initial diffusion coefficient and a function of the spatial grid size (GR): (D_{i,0} = left( {1.1 times 10^{4} } right) cdot GR cdot 1.33). Parameters m and (tau)—both set at 2 in the model—determine the curvature of the functional relationship between D, P, and (rho)50. Parameter (rho_{i,t}) represents density-dependent factors and a function of population density (number of individuals), (emptyset_{i,t}), carrying capacity ((C_{i,t})), and mean body weight ((overline{W}_{i,t})) in each cell i.Models of ocean acidification effectsThe DBEM operates to model larval dispersal using advection–diffusion models. Survival is calculated at each time step (biweekly) based on a static annual survival rate. We recently tested a simple linear relationship between survival rate and pH, represented by percent changes in the survival rate given a change in pH32. We used parameters derived from previous experimental studies, where they observed a ~ 15% increase in mortality in larval and juvenile stages37 from a doubling of hydrogen ion concentration.We explore the OA effects by modelling variations in life stage-specific sensitivities to OA. Larvae, juveniles, and adults are modelled based on size classes, and the weight at maturity determines the size at which juveniles transition into adults65. Therefore, impacts of OA on survival can be modelled for various size classes. We model the effects of OA on the three major life history stages—larval, juvenile, and adult—and use a correlative approach to link changes in ocean acidity with changes in survival.The length transition matrix (Eqs. (8) and (9)) is split up into 40 length size classes, divided evenly from 0 to (l_{infty ,i,t}). We assume larvae transition from the pelagic phase to the growth transition matrix, and enter as the ‘larval’ stage for only the first size class. Next, juvenile size classes comprise all size classes below the length at maturity, lmat, as determined in Eq. (12), and lobster in any size classes greater are considered adults. While our models do not incorporate lobster-specific life cycle traits (i.e. transitioning between larval stages then to juvenile stages), we use more general models that can be broadly applied to many species.Modelling effects on survivalOA effects can be modelled as relative changes in survival rate for all life stages in Table 2. In other words, percent changes in acidity (i.e. hydrogen ion concentration) from baseline initial conditions results in a percent change in baseline survival rate. We use a model structure similar to that of previous work we have done32:$$Surv_{t} = Surv_{init} *left[ {1 + left( {p*left( {frac{{left[ {H^{ + } } right]_{t} }}{{left[ {H^{ + } } right]_{init} }} – 1} right)^{w} } right)} right]$$
    (20)
    Table 2 Scenario settings explored with model projections.Full size tableSurv is the survival rate per year and used here as an example but can be applied to other life histories affected by OA (e.g. growth, reproduction). Survival rate in year t is derived from the initial (init) survival rate and the relative change in [H+] between year t and initial [H+] conditions. Note that in our previous model, p represents the point value of the percent change effect size with a doubling of [H+]. This model utilizes single point effect size estimates that have no underlying assumed relationship between acidity and survival. In our model, we used an exponent value, w, equal to 1, which assumes a linear relationship32.Fishing pressureFishing mortality was assumed to be at maximum sustainable yield (MSY), which is the theoretical maximum biomass that can be sustainably removed from the population indefinitely. MSY is calculated using a Gordon Schaefer population growth model67:$$MSY = frac{{B_{infty } cdot r}}{4}$$where B∞ is the population carrying capacity and r is the intrinsic population growth rate. We use this measure of MSY as a proxy for the maximum catch potential (MCP) into the future, thus we assume that fisheries management are optimized and operate at MSY.Furthermore, the fishing mortality rate, Fi,t—i.e. the annual proportion at which biomass is taken from the current population biomass—in each cell i at time t at MSY can be calculated as:$$F_{MSY,i,t} = frac{r}{2}$$The fishing mortality rate was adjusted to explore scenarios of reduced fishing pressure and interactions with climate change and OA on the population dynamics of lobster. Any reductions in fishing pressure began in 2010 to represent how changes in fishing implemented now could change the state of lobster populations with the added stressors of climate change.Fishing size limitsFishing size limits were set to represent management scenarios and to observe their effects on lobster populations and size distribution of the population. We set four scenarios of minimum body size restrictions of lobster catch: no limit, canner small ( > 0.5 lb, 220 g), canner large ( > 0.75 lb, 320), and market ( > 1 lb, 430 g). Canner lobsters are smaller lobsters that are often sold at a cheaper price. They range from 0.5 to 1 lb, and are largely caught in Northumberland Strait where size limits are currently set lower due to warmer waters and smaller size at maturity44. For these scenarios of fishing size limits, we continue to assume catch is at maximum sustainable yield. Therefore, the same catch biomass (calculated using fishing mortality rate, F) will be the same for the various size limit restrictions, and more biomass will be taken from upper size classes where size limits are implemented. The no size limit results in fishing mortality to all size classes (including undersized lobsters).Climate change scenariosWe use outputs from three Earth system models for projections of various future climate change outcomes: NOAA’s Geophysical Fluid Dynamics Laboratory (GFDL-ESM), Institute Pierre Simon Laplace Climate Modelling Centre (IPSL-ESM), and Max Planck Institute for Meteorology (MPI-ESM)68. These models are included in the Coupled Model Intercomparisons Projection Phase 5 (CMIP5). We used two Representative Concentration Pathways (RCPs)69 which are greenhouse gas (GHG) concentration trajectories derived to reflect possible combinations of various socioeconomic assumptions, RCP 2.6 and RCP 8.5. The number associated with RCPs represent the radiative forcing values by the year 2100 based on greenhouse gas concentrations. RCP 2.6 corresponds with a low climate change scenario and assumes immediate mitigation of GHG emissions where annual emissions peak by mid-decade (year 2025) but is reduced considerably. This scenario is more in line with the 2015 Paris Agreement to limit warming to + 1.5 °C relative to other emissions scenarios applied in most CMIP5 Earth system models. Conversely, RCP 8.5 corresponds to a high climate change scenario and our current trajectory where we continue to use fossil fuels, have little to no change to switch to renewable energy sources, and GHG emissions continue to increase with no implementation of any mitigation action. We chose these three Earth system models as they provide sea surface and bottom layers and the full range of environmental variables required by the DBEM (i.e. sea temperature, dissolved oxygen, primary production, pH, current advection, salinity, sea ice extent) for both RCP scenarios2.All statistical analyses and figures were generated using the programming software R v4.0.370. More

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    Global patterns of potential future plant diversity hidden in soil seed banks

    Our global database was derived from studies measuring soil seed bank diversity and density of natural plant communities across all continents, albeit with a strong data availability bias towards North America, Europe, eastern Asia and Oceania as compared to elsewhere (Fig. 1). The database contains 15,698 records for soil seed banks worldwide, including 6,480 for diversity (represented here by species richness) and 9,218 for density (number of seeds per soil surface area). The database represents more than a century of research with the oldest publication dating back to 191815. This most exhaustive and comprehensive set of research data on soil seed bank to date allowed us to identify the determinants and patterns of soil seed bank at the global scale.Fig. 1: Locations of the soil seed bank studies included in our database.a Diversity; b Density.Full size imageTo make data among studies comparable, we standardized them using a three-step process. First, we identified soil seed banks that showed seasonal patterns in both diversity and density, all of which peaked slightly in winter (Supplementary Fig. 1a, b). Thus, we standardized all data (from non-(sub-)tropical regions) for other seasons to winter. Second, sampling area for soil seed bank diversity varied among studies, with 0.01 m2 being the most commonly reported (Supplementary Fig. 2), to which we standardized all data using a species-area curve (Supplementary Table 1). Third, sampling depth also varied among studies, with 0–5 cm being the most frequently reported soil depth (Supplementary Fig. 3). Therefore, 0–5 cm was chosen as the soil depth for standardization of data in various soil depths. Such standardization is needed to find the relationships of seed bank data between different soil depths. We used the upper and lower limits of soil depths (e.g., for 0–5 cm, the upper limit was 0 cm and the lower 5 cm). The log-scale regressions showed that both soil seed bank diversity and density decreased significantly with lowering upper boundaries of soil depths but increased with lower ones (Supplementary Table 2), and thus we standardized all data to 0–5 cm depth using these relationships. To account for possible variation among biomes, the second and third standardization procedures were conducted for each biome separately. The analyses during standardization confirmed the need to standardize empirical findings when comparing seed bank patterns across studies, as previously stressed in a study on grassland soil seed banks10. Our standardization procedures made all data comparable in terms of season, sampling area and soil depth.Non-parametric Kruskal–Wallis tests showed that soil seed banks differed significantly among ecosystem types. Mangroves, tundra and tropical & subtropical dry broadleaf forests had a lower diversity of soil seed banks, whereas Mediterranean forests, woodlands & scrub, tropical & subtropical moist broadleaf forests and tropical & subtropical coniferous forests had a higher diversity (Supplementary Fig. 4a). For density, mangroves and flooded grasslands & savanna had the lowest value, while temperate broadleaf & mixed forests and temperate conifer forests had the highest value (Supplementary Fig. 4b).Prior to spatial analyses, we computed semivariograms to determine whether spatial autocorrelation could affect our models. We found that there was no obvious spatial autocorrelation in the data of soil seed bank diversity or density (Supplementary Fig. 5), indicating no spatial dependence in our data. We then used the random-forest algorithm (see Methods for details) to determine the importance (as increase in node purity) of the influence of 31 variables related to climate, soil, human disturbance and spatial coordinates (Supplementary Table 3) on diversity and density of soil seed banks. These variables previously were reported to affect plant performance at the global scale16,17,18, and thus they could affect soil seed banks via their effects on seed production. Moreover, we expected that potentially these variables could affect seed longevity in the soil. Full models using all 31 predictors showed that climate and soil were important in predicting soil seed banks (Fig. 2a and Supplementary Fig. 6). Moreover, spatial coordinates (absolute latitude) were the most important predictor for diversity, i.e., diversity of soil seed banks exhibit clear spatial patterns at the global scale. Net primary productivity (NPP) and soil characteristics were important in predicting the density of soil seed banks (Fig. 2b and Supplementary Fig. 6).Fig. 2: Variable importance (increase in node purity) of random forests run with all 31 predictors.a Soil seed bank diversity; b Density. abs.latit, absolute latitude; AMT, annual mean temperature; AP, annual precipitation; ATR, annual temperature range; AVWAC, available water capacity (%); BULK, bulk density; CEC, cation exchange capacity; CLAYC, clay (mass %); diversity, plant diversity; HFP, human footprint; Isoth, isothermality; npp, plant productivity (net primary production); ORGNC, organic carbon content; PCQ, precipitation of coldest quarter; PDM, precipitation of driest month; PDQ, precipitation of driest quarter; pH, pH measured in water; Pseason, precipitation seasonality (coefficient of variation); PWeQ, precipitation of wettest quarter; PWM, precipitation of wettest month; PWQ, precipitation of warmest quarter; SANDC, sand (mass %); SILTC, silt (mass %); TCM, min temperature of coldest month; TCQ, mean temperature of coldest quarter; TDQ, mean temperature of driest quarter; TDR, mean diurnal range (mean of monthly (max temp–min temp)); Tseason, temperature seasonality (standard deviation *100); TWeQ, mean temperature of wettest quarter; TWM, max temperature of warmest month; TWQ, mean temperature of warmest quarter.Full size imageWe then built final random-forest models using the most important predictors of seed banks selected from full models: nine variables for diversity and five for density (Supplementary Fig. 7). Final models explained more of the total variance than did full models (Supplementary Table 4), and they were robust to K-fold cross-validation (Supplementary Fig. 8), indicating that a small number of variables predicted soil seed bank diversity and density. Absolute latitude (abs.latit) was the most important predictor for diversity, which varied between 0–55° and then decreased beyond this range (Fig. 3a). Five climatic variables were important for diversity. Diversity peaked at intermediate annual temperature ranges (ATR), while it was the lowest at intermediate mean temperature of driest quarter of the year (TDQ), precipitation of the coldest quarter (PCQ) and precipitation of the driest quarter (PDQ). Diversity increased with increasing annual precipitation (AP). In addition, three soil variables were important for diversity. Diversity showed a humped relationship with soil pH, with pH 6–7 having the highest diversity. Diversity increased with soil cation exchange capacity (CEC) and soil silt content (SILT). These results indicate that diversity exhibits strong spatial patterns at the global scale. However, our spatial patterns differ from those found for a specific ecosystem worldwide (e.g., grasslands), where there were only weak latitudinal gradients in seed bank diversity10. In addition, climate emerged as an important predictor for seed bank diversity, which is consistent with the report that climate acts as environmental filters affecting soil seed bank of grasslands around the world13. Our results agree with a continental study in Europe, where ATR was more important than mean annual temperature for determining seed bank richness and warmer temperatures were associated with lower seed bank richness11. Possible mechanisms by which temperature affects soil seed banks are that it (1) influences seed bank inputs via its effects on seed production; (2) cues dormancy-breaking and germination1, thus determining germinable seed output from seed banks; and (3) affects seed metabolic activity and soil fungal activity19, thereby determining seed viability and persistence in the soil. Finally, our findings of a significant effect of soil pH are supported by some regional and local studies. For instance, seed bank composition is significantly associated with soil pH at high elevations on the Tibetan Plateau20. A negative effect of low pH also has been reported in a large-scale study of acidic and calcareous grasslands in England21. Two possible mechanisms for the effects of soil pH are that (1) low pH may cause loss of seed viability due to the toxicity from aluminum or other metals that become more readily available in soils with low pH22; and (2) high pH may accelerate decomposition and promote growth of pathogens that negatively affect seed persistence23. In our study, the two mechanism may operate synchronously, thereby resulting in the highest diversity of soil seed banks at intermediate pH at the global scale. Further, our results show that soil CEC and SILT affect seed bank diversity, which agrees with a study on the Tibetan Plateau20. The physical and chemical properties of soils can affect seed bank directly by affecting seed germination and aging via regulating soil water-holding capacity24, or indirectly by affecting seed viability via controlling the activity of soil pathogens21,22,25.Fig. 3: Partial feature contributions (the marginal effect of a variable on response) of the most important variables for soil seed banks.a diversity; b density. Variable importance (inc. node) is the decrease in the residual sum of squares that results from splitting regression trees using the variable. The percentage increase in mean squared error (% inc. MSE) is the increase in model error as a result of randomly shuffling the order of values in the vector. abs.latit, absolute latitude; AP, annual precipitation; ATR, annual temperature range; BULK, bulk density; CEC, cation exchange capacity; npp, plant productivity (net primary production); PCQ, precipitation of coldest quarter; PDM, precipitation of driest month; PDQ, precipitation of driest quarter; pH, pH measured in water; SILTC, silt (mass %); TDQ, mean temperature of driest quarter; TWM, max temperature of warmest month.Full size imageFor soil seed bank density, soil bulk density (BULK) was the most important predictor; density increased below 750 g/cm3 BULK but remained stable when BULK was higher than 800 g/cm3 (Fig. 3b). Density peaked when temperature of the warmest month (TWM) was 34 °C. Density showed similar variation with NPP, precipitation of the driest quarter of the year (PDQ) and of the driest month (PDM), i.e., it peaked at intermediate values of these variables. Precipitation influences the success of sexual reproduction of plants and the size of the seed bank through seed input26, and it also affects soil pathogenic fungi, which cause seed mortality27. Therefore, precipitation has a strong effect on seed bank density, as reported for 27 alpine meadows on the Tibetan Plateau28. Our results further illustrate that PDQ and PDM are the key factors determining seed bank density worldwide, suggesting that moisture fluctuation in soils triggered by precipitation of the driest time of the year can affect seed bank density. If soil moisture fluctuations are high, seed germination will be primed by increasing moisture24.At the global scale, we mapped soil seed bank diversity and density using the final random-forest models. Mapping soil seed bank values onto global maps revealed considerable geospatial variation, the pattern of which varied between diversity and density (Fig. 4). For diversity, western North America, central South America, central Africa, central Europe, southern and eastern Asia and eastern Oceania had high values. In contrast, eastern and central North America, northern Africa and central Asia had low values (Fig. 4a). For density, northern North America, northern Europe and northern Asia had higher values than elsewhere (Fig. 4a). Our results are consistent with the reports that larger seed banks are more common in cooler temperate climates19,29. The latitudinal pattern of higher density in colder regions in the Northern Hemisphere may be driven by lower seed mortality in colder soils6, resulting in stable seed bank densities of long-lived seeds that counteract low seed production in some years at cold northern latitudes, as shown in a study of temperate forests along a 1900 km latitudinal gradient in northwestern Europe29. The latitudinal pattern highlights that particularly species rich low-latitude biomes such as tropical rainforests generally have very low seed bank densities, while their seed bank diversity does not exceed that in higher latitudes biomes. However, our global assessment should be interpreted with caution since some studies in azonal vegetation or in rare habitats in our database did not fully reflect soil seed banks in that region, and thus these data shortcomings may have induced bias in our global predictions. Moreover, data gaps in our database are also likely to have had an effect on the global predictions, i.e., fewer data available from some continents (e.g., northern Asia and Africa) could lead to less confidence for prediction in these regions. For example, Russia has very few soil seed bank data, which may have led to an inaccurate prediction for this country. Nevertheless, based on our global patterns of soil seed bank diversity and density, the latitudinal pattern strongly suggests that the biodiversity of (sub-)tropical forests is particularly vulnerable to large-scale climatic or land-use disturbances. However, in-depth investigation is needed to quantify the extent to which temporal integration of seed bank effects for long-lived trees and seed masting events may buffer the effects of low seed bank diversity and density at any given time of sampling. In contrast, the higher-latitude plant diversity, while currently low compared to that in tropical rainforest, may rely on high soil seed bank densities to boost its resilience to large-scale climate- or land-use induced disturbances. Further, our analyses suggest that the least vulnerable ecosystems in terms of hidden diversity should be those that combine high seed-bank diversity with high density; and therefore the relationships between the two variables across the global map certainly would be an interesting topic worthy of further study.Fig. 4: Extrapolated global maps of soil seed banks.a diversity in terms of number of species per 0.01 m2; b density as number of seeds per m2. In b, values are log10-transformed to facilitate viewing. The spatial resolution of grid cells is 5 arcmin-by-5 arcmin.Full size imageOur global assessment reveals that both diversity and density exhibit clear spatial patterns of soil seed banks but differ in their environmental determinants. These findings alone do not necessarily mean that this biodiversity reservoir has strong buffering capacity under climate change, because both climate and soil conditions influence seed bank diversity and density. Based on a large number and long history of studies globally, we provide quantitative evidence of how environmental conditions shape soil seed bank distributions and spatially explicit maps of this biodiversity reservoir in plant communities worldwide. Our quantification of environmental determinants and global mapping can be readily applied to dynamic global vegetation and plant diversity models to enable a more complete and accurate prediction of the impact of ongoing environmental changes on plant diversity (both above- and belowground) at the global scale. The next research challenge will be to plot current (visible) aboveground plant diversity (ideally using the available data in the studies themselves) against soil seed bank diversity under global change scenarios in order to pinpoint even more accurately which plant communities, ecosystems and biomes (and their turn-over) are most at risk of losing their diversity due to global changes. More

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    Recapitulating whole genome based population genetic structure for Indian wild tigers through an ancestry informative marker panel

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