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Efforts to keep oil-palm plantations from crowding out tropical rainforests could threaten biodiversity in other habitats1.

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doi: https://doi.org/10.1038/d41586-022-04179-1

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Overview of modeling frameworkWe have used a range of econometric, economic, and agricultural land surface models to analyze the factors driving land-use change in order to assess their ecological, agricultural, climatic and economic impacts. These multi-scale models differ in their methodologies, scale of interest, and resolution, but they are very complementary and could provide a unique opportunity to analyze public policy scenario effects on land-use and resulting changes in ecosystem carbon and biodiversity.Among these models, the economic land use model Nexus Land Use (NLU)29,30 and the agricultural supply-side model Agriculture, Recomposition de l’Offre et Politique Agricole (AROPAj)31 coupled with a spatial econometric model32 have allowed us to estimate the impact on EU land-use of a scenario involving a 50% reduction in N synthetic fertilizers compared to a baseline scenario. In the present study, we use these land-use scenarios to force ORCHIDEE-crop (Organising Carbon and Hydrology in Dynamic Ecosystems), an agricultural land surface model16,33 and Projecting Responses of Ecological Diversity in Changing Terrestrial Systems (PREDICTS)34, a biodiversity model to simulate, respectively, ecosystem C and biodiversity changes across the EU covering the domain 35.25°N and 69.25°N in latitude and 9.25°W and 34.25°W in longitude. The schematic (Fig. 1) provides a brief overview of the modelling framework applied in this study.Figure 1Schematic diagram illustrating the coupling of multi-scale land-use models. The multi-scale models coupled in this study are econometric, and economic models (NLU and AROPAj), an agricultural land surface model (ORCHIDEE-crop), and a biodiversity model (PREDICTS). Coupling means, we use the output of one model as an input to other models. In addition, we have performed one-way coupling and there is no two-way interaction between models. Each economic model generates two land-use maps corresponding to Baseline and Halving-N scenario which are inputs (2 from NLU and 2 from AROPAj) to ORCHIDEE-crop and PREDICTS. The ecosystem carbon (C) sequestration is simulated by ORCHIDEE-crop and biodiversity indicators are simulated by PREDICTS model. The abbreviations ‘BaseNLU’ and ‘HaNNLU’ means Baseline and Halving-N land-use map generated by NLU model. The abbreviations ‘BaseAR’ and ‘HaNAR’ means Baseline and Halving-N land-use map generated by AROPAj model.Full size imageIn order to link the land use output data from the AROPAj and NLU models with the ORCHIDEE-crop and PREDICTS models, the first step is to match land uses and crops between the models (see Table 1). AROPAj and NLU crops are classified into ORCHIDEE-crop plant functional types (PFTs): C3 winter and summer crops, C4 summer crop and C3/C4 natural grass (see “Model descriptions” section for a detailed description of ORCHIDEE-crop PFTs). The AROPAj and NLU crops are also classified into the PREDICTS crop types: annual, perennial, N-fixing. The AROPAj and NLU “rangeland” and “pasture” categories are found in PREDICTS but in ORCHIDEE-crop they are considered to fall within the C3 natural grassland PFT. Finally, NLU and AROPAJ forest and other natural areas are classified as “primary” natural areas (with low anthropogenic use) or “secondary” (intermediate to high anthropogenic environmental use) according to the land use map of these areas35. For ORCHIDEE-crop, they are classified as natural forest PFTs. Note that the fallow areas described in AROPAj that are part of crops are classified as “grass” PFT in ORCHIDEE-crop and as “minimum” intensity annual crops in PREDICTS.Table 1 Table of correspondences between the land uses and crops represented in the AROPAJ/NLU and ORCHIDEE models and PREDICTS.Full size tableThe land-use and land cover changes described in the following sub-section are used as inputs to ORCHIDEE-crop and PREDICTS from both the NLU and AROPAj models’ output.Land-use change scenariosLand-use changes in the EU are simulated for the present day using two scenarios: (1) a business as usual scenario (Baseline) and (2) a scenario involving a policy to reduce mineral nitrogen use by 50% from the Baseline (Halving-N). The land-use changes in Halving-N and Baseline are computed by both NLU and AROPAj models. In the latter model, the computed land-use changes result from coupling between AROPAj and a spatial econometric model. Since there are differences in the nature of the models (supply-side model versus partial equilibrium model) and their underlying data, the Baseline scenarios in the NLU and AROPAj frameworks are different. A detailed description of the differences and a discussion of their implications on the production and area of different land-uses is provided in Lungarska et al.36. EU plant production is 370 and 383 MtDM (Million tons of Dry Matter) respectively based on the application of 12 TgN (Tera grams) of N fertilizer in AROPAj and NLU. Crops, grasslands, and forests cover respectively, 116, 57 and 234 Mha in NLU and respectively 94 (including fallow land), 38 and 142 Mha in AROPAj. In AROPAj and NLU, the 50% N reduction is achieved indirectly by increasing the N input price from present-day figures36.The land-use changes output from AROPAj and NLU are supplied as inputs to the ORCHIDEE-crop and PREDICTS models. The land-use changes are matched with corresponding plant functional types (PFTs) in ORCHIDEE-crop and land-uses in PREDICTS (see Table 1). “Model descriptions” section provides a detailed description of the ORCHIDEE-crop and PREDICTS models.Model descriptionsHere, we describe the ORCHIDEE-crop and PREDICTS models that quantify the impacts of halving N fertilizer consumption in the EU. Table 2 presents a brief overview of the two models.Table 2 Overview of the ORCHIDEE-crop and PREDICTS models input and output.Full size tableA detailed description of ORCHIDEE-crop: This model is a process-based agricultural land surface model that integrates crop-specific phenology based on Simulateur mulTidisciplinaire pour les Cultures Standard (STICS)37,38. Carbon allocation is based on the plant-based hybrid model from the original ORCHIDEE allocation scheme39 and a crop specific formulation of STICS providing leaf, root, and shoot biomass, grain maturity time, litter production, and litter and soil carbon decomposition. The harvest date is calculated after grains reach maturity40. The ORCHIDEE-crop model has no explicit nitrogen cycle but accounts empirically for the effect of N fertilization by increasing the maximum Rubisco- and light-limited leaf photosynthetic rates as a function of the amount of N applied, using a Michaelis–Menten function40. Also, ORCHIDEE-crop is calibrated against observations, which showed a good match between modeled observed aboveground biomass, crop yield, and daily carbon40. This version of the model currently uses three crop PFTs: C3 winter, C3 summer and C4 summer. Forests are classified as Broadleaf, Needle leaf, Deciduous, Temperate and Boreal. Up to 11 non-cropland vegetation types can co-exist with crops on a grid point of the model, according to prescribed land cover information. A gridded simulation of ORCHIDEE-crop requires 30-min time step meteorological forcing (air temperature, specific humidity, incoming shortwave and longwave radiation, rainfall), which can be interpolated in time from gridded climate analysis data or atmospheric models. In this study, this model is used to quantify the ecosystem C variables.A detailed description of PREDICTS: The PREDICTS database was collated by searching the published literature for studies where terrestrial biodiversity (including plants, fungi, vertebrates, and invertebrates) was sampled using consistent methods across multiple sites, which vary in the pressures faced. The land use and intensity of each site have been assessed and categorized in a consistent way41,42,43. Authors of studies were contacted to ask for the raw biodiversity data where this was not already available41,42. Most records in the PREDICTS database refer to the number of individuals of a species at a site; this makes it possible to compute a range of biodiversity indices. To estimate biodiversity responses to human impacts across such a global and heterogeneous dataset, linear mixed-effects models are used; random intercepts account for differences in biogeographic factors, sampling methodology and taxonomic focus, and the spatial layout of sites within studies. Using the PREDICTS database to assess the impact of human pressures on biodiversity assumes that space-for-time substitution is valid44; it assumes that the sites have reached equilibrium and so the impact of pressures on biodiversity over time can be observed across space and that the relationship between biodiversity and drivers do not vary over time.SR is calculated as the number of species at each site; it is a widely used measure of biodiversity and is both simple and intuitive. Responses of SR to land use and intensity were modelled using generalized linear mixed effects models and with a Poisson error structure; an observation-level random effect was included to account for overdispersion45. This model is then used to project SR in each grid of a 0.5° map and expressed as a percentage of the SR level in primary vegetation from land use harmonization map35.To estimate BII change with land use and intensity, two models are required. Total abundance was first calculated as the sum of all individuals at each site; it was then rescaled within the study (so that the maximum within a study is 1) and was square-root transformed before modelling as a function of land use and intensity, to account for non-normality of the model residuals (a Poisson error structure could not be used as abundance data can include non-integer data e.g. densities). Inclusion of a random slope for land use within the study was supported (based on Akaike’s Information Criterion). Compositional similarity was then calculated as the asymmetric Jaccard index, comparing each baseline site (primary vegetation) with all other sites, and logit transformed with an adjustment of 0.01 (to account for non-normality of the model residuals). Compositional similarity was then modelled as a function of land use and intensity (coarsened so that only perennial crops were allowed to differ across intensities), including the environmental and geographic distance between sites as control variables, whose effects were permitted to differ among land use and intensity levels (these variables were cube-root and log-transformed respectively to improve residual distribution). To calculate BII, total abundance (expressed as a percentage of their level in primary vegetation) and compositional similarity (expressed as a percentage of their level in primary vegetation)46 are projected for each grid of a 0.5° map; these two maps are then multiplied to give abundance-based BII19. The PREDICTS models include different levels of management (intensive, light or minimal) and different types of land cover (forest, pasture, rangeland, annual cropland, perennial cropland, and urban zones). The coefficients of these mixed-effect models and a detailed description of the link between the PREDICTS models and NLU are available in Prudhomme et al.46. The spatial predictions of biodiversity were computed using a python pipeline, which was developed specifically for the PREDICTS project (https://github.com/ricardog/raster-project).In our modeling framework, the impact of halving N fertilizer goes through two steps: (i) we calculate the effect of this reduction of N fertilizer on agricultural yield, and (ii) calculate the effect of the yield reduction on biodiversity. By keeping yield as a proxy of agricultural land use intensification as proposed in Prudhomme et al.46, we include not only the direct effect of the reduction of N fertilizer on biodiversity but also the effects correlated to this reduction of N fertilizer such as the reduction of other chemical inputs (P and K fertilizers and pesticides). While the effect of the change in N fertilization on yield is calculated by the classical concave production function in agronomy29, the effect of the change in yield is calculated by coupling the NLU land use model and the PREDICTS biodiversity model46. For each category of crops (annual, perennial, leguminous), the coupling consists of estimating (using a Generalized Additive Model [GAM]) the share of each intensity class (minimum, light, intense) as a function of the average calorie yield based on the average crop yield maps from a plant growth model. The maps describing the share of land use intensities are from Newbold et al.19 Similarly for pasture, the share of each intensity class (light, intense) is estimated with the help of a GAM as a function of ruminant density.SimulationsOur experimental design focuses on assessing the effects of a 50% reduction in present-day N fertilizer use levels across the EU. The choice of halving N fertilizer in EU agriculture is related to the “Farm to Fork” strategy, which puts forward the ambition for 2030 to reduce nutrient losses to the environment from both organic and mineral fertilizers by at least 50%. The results from NLU (and its nitrogen balance module) show that this level of reduction corresponds to a 50% reduction in nutrient losses (nitrogen and phosphorus) aimed by the Farm to Fork strategy as a part of the European Green Deal. AROPAj models exclusively the EU countries (in 2012, there were 28 member states) while NLU simulations cover the EU and the rest of the world (EU being a part of the European region as represented by the model). However, the N reduction policy implemented in the EU alone and the comparison of the results conducted only for the EU. All EU member states are considered but for some of them we present results. A total of four simulations corresponding to four land-use maps (two from AROPAj and two from NLU, see Fig. 1) are performed in the ORCHIDEE-crop model and also in the PREDICTS model. In addition to changes in the area of different land-uses, changes in mineral N input are accounted for in both models. However, changes in organic N input and crop rotations are not accounted for. In ORCHIDEE-crop 55% of the carbon harvested from croplands is exported but the remaining residues are returned to the soils.ORCHIDEE-crop simulation details: the model simulations are performed over a domain covering the EU. Four idealized simulations are carried out using the ORCHIDEE-crop model by forcing present-day meteorological data (2006–2010), levels of N fertilizer (150 KgN/ha) and atmospheric CO2 concentration (385 ppm). The four simulations include Halving-N and Baseline corresponding to AROPAj and NLU land-use scenarios (two ORCHIDEE-crop simulations per economic model). All four simulations start from the year 2010 climate and carbon cycle conditions with a recycled climate (2006–2010) for 150 years. For the year 2010, climate and carbon cycle conditions are obtained from the output of historical simulations. Historical simulations from the year 1901 to the year 2010 are performed for both AROPAj and NLU Baseline scenario land-use land cover maps. In addition, these historical simulations started from an equilibrium state of soil carbon, energy and water cycle variables corresponding to the year 1901. The 1901 equilibrium state is determined by running a 350-year spin-up simulation corresponding to a recycled climate (1901–1910). The observation-based climate forcing data from the Global Soil Wetness Project was only available starting from the year 1901. The drift in soil carbon over the last 100 years of the 350-year simulations is less than 1%. The equilibrium state simulations corresponding to the year 1901 were necessary to have stabilized biophysical and ecosystem C variables across the EU. Other forcing variables, e.g. atmospheric CO2 concentration (296.57 ppm), N-fertilization rate (32 KgN/ha), harvest index (0.25), and also the phenology parameters for short-cycle variety winter and summer crops16 corresponding to the year 1901 were prescribed.PREDICTS simulation details: the PREDICTS model represents changes in broad-sense biodiversity in different land-uses and intensities of land-use relative to a reference land-use (as the biodiversity metrics assessed include all terrestrial biodiversity for which data are present in the PREDICTS database including plants, fungi, vertebrates and invertebrates). Here the reference ecosystem is a primary natural ecosystem. Biodiversity changes are then reported as a percentage by dividing the obtained biodiversity levels by the level of biodiversity present in the primary natural ecosystem. This simulation is performed for each grid point on a map of the EU for land-use scenarios corresponding to Baseline and Halving-N for both economic models, AROPAj and NLU (Fig. 1).Breakdown method for biodiversity and carbon changesThe Halving-N and Baseline scenarios provide contrasted land-use maps according to the assumptions of economic and land-use models36. This results in different plant and animal production, and different land-uses at the European scale in each model. A price shock on inputs, as represented in the Halving-N scenario compared to the Baseline scenario, can induce (1) a spatial reallocation of production or (2) production changes47. Here, we separate out the effects of these two mechanisms on biodiversity (species richness) and carbon indicators (NPP and soil carbon) by decomposing the overall environmental differences between the Halving-N and the Baseline scenarios. The breakdown is not possible for the BII indicator because this indicator is the product of two indicators: abundance and a similarity indicator of ecological communities.First, we breakdown the carbon and biodiversity differences by land-use type. The breakdown for carbon is straightforward because the carbon changes are computed for each land-use. The biodiversity changes associated with each land-use are computed by setting no changes in the other PREDICTS model land-uses. The sum of the biodiversity changes for each land-use is thus equal to the overall change in biodiversity.For each land-use i (forest, grassland and cropland), we separate out the carbon and biodiversity differences between the Halving-N and the Baseline scenarios into two effects in accordance with Eq. (1): (i) the carbon and biodiversity difference associated with the area difference—called “Area effect”, and (ii) the carbon and biodiversity difference associated with the difference in biodiversity and carbon sequestration per unit area—called “Intensity effect”. The “Area effect” corresponds to the change in carbon sequestration and biodiversity associated with a change in the land-use area. For example, a reduction in grassland area leads to reduction in the C sequestration and biodiversity associated with this area. The “Intensity effect” corresponds to a change in the C sequestration and biodiversity per unit area. For example, a reallocation of production toward places with high soil C content leads to an increase in the carbon stock per hectare or an increase in crop yield leads to a reduction in the biodiversity per unit of cropland. Thus, the “Intensity effect” corresponds to the effect of a production reallocation on C sequestration, and the effect of land-use intensity on biodiversity.We use the Logarithmic Mean Division Index (LMDI) method, which breaks down the target values into several main influencing factors based on mathematical identity transformation48 as follows.$$Delta {E}_{i}=Delta {E}_{i}^{A}+Delta {E}_{i}^{I}$$
(1)
(Delta {E}_{i}) is the difference in the environmental indicator between the Halving-N and the Baseline scenarios. Superscript ‘A’ denotes area effect and ‘I’ denotes intensity effect. Subscript ‘i’ denotes different land-use (e.g. forests, grassland, cropland etc.). (Delta {E}_{i}^{A}) is the difference in the environmental indicator between the Halving-N and the Baseline scenarios associated with the difference in area. (Delta {E}_{i}^{I}) is the difference between the Halving-N and the Baseline scenarios associated with the different intensity per unit of area of the environmental indicator.$$Delta {E}_{i}^{A}=frac{{E}_{i}^{hN}-{E}_{i}^{b}}{ln({E}_{i}^{hN})-{ln(E}_{i}^{b})}times lnleft(frac{{A}_{i}^{hN}}{{A}_{i}^{b}}right)$$
(2)
({E}_{i}^{hN}) is the level of the environmental indicator in the Halving-N (superscript hN) scenario. ({E}_{i}^{b}) is the level of the environmental indicator in the Baseline (superscript b). ({A}_{i}^{hN}) is the area of land-use i in the Halving-N scenario. ({A}_{i}^{b}) is the area of land-use i in the Baseline$$Delta {E}_{i}^{I}=frac{{E}_{i}^{hN}-{E}_{i}^{b}}{ln({E}_{i}^{hN})-ln({E}_{i}^{b})}times lnleft(frac{{e}_{i}^{hN}}{{e}_{i}^{b}}right)$$
(3)
Equation (3) is same as Eq. (2) but for the intensity of the environmental indicator ({e}_{i}).The breakdown of the differences in the environmental indicators is performed between the Halving-N scenario and the Baseline. A positive variation ((Delta {E}_{i} >0)) indicates a higher environmental indicator in the Halving-N scenario compared to the Baseline without implying any temporal variation since the scenarios compare the environmental indicator status in 2012 in the AROPAj and in the NLU land-uses. Conversely, a negative variation ((Delta {E}_{i} More

Honey bee colony loss and parasites across space and timeHoney bee colony loss strongly depends on spatio-temporal factors33,42, which in turn have to be jointly modeled with other stressors. Focusing on CONUS climatic regions, defined by the National Centers for Environmental Information40 (see Fig. 1), this is supported by the box plots in Fig. 2 which depict appropriately normalized honey bee colony loss (upper panel) and presence of V. destructor (lower panel) quarterly between 2015 and 2021. Specifically, Fig. 2a highlights that the first quarter generally accounts for a higher and more variable proportion of losses. Average losses are typically lower and less dispersed during the second quarter, and then tend to increase again during the third and fourth quarters. The Central region, which reports the highest median losses during the first quarter (larger than 20%) exemplifies this pattern, which is in line with existing studies that link overwintering with honey bee colony loss6,29,30,31,32,33,43. On the other hand, the West North Central region follows a different pattern, where losses are typically lower during the first quarter and peak during the third. This holds, albeit less markedly, also for Northwest and Southwest regions. These differing patterns are also depicted in Fig. 3, which shows the time series of normalized colony loss for each state belonging to Central and West North Central regions – with the smoothed conditional means highlighted in black and red, respectively. Figure 2b shows that also the presence of V. destructor tends to follow a specific pattern; in most regions it increases from the first to the third quarter, and then it decreases in the fourth – with the exception of the Southwest region, where it keeps increasing. This is most likely because most beekeepers try to get V. destructor levels low by fall, so that colonies are as healthy as possible going into winter, and also because of the population dynamics of V. destructor alongside honey bee colonies – i.e., their presence typically increases as the colony grows and has more brood cycles, since this parasite develops inside honey bee brood cells44,45. The West region (which encompasses only California since Nevada was missing in the honey bee dataset; see Data) reports high levels of V. destructor throughout the year, with very small variability. A comparison of Fig. 2a and b shows that honey bee colony loss and the presence of V. destructor tend to be higher than the corresponding medians during the third quarter, suggesting a positive association. This is further confirmed in Fig. 4, which shows a scatter plot of normalized colony loss against V. destructor presence, documenting a positive association in all quarters. Although with the data at hand we are not able to capture honey bee movement across states, as well as intra-quarter losses and honey production, these preliminary findings can be useful to support commercial beekeeper strategies and require further investigation.Figure 2Empirical distribution of honey bee (Apis mellifera) colony loss (a) and Varroa destructor presence (b) across quarters (the first one being January-March) and climatic regions; red dashed lines indicate the overall medians. (a) Box plots of normalized colony loss (number of lost colonies over the maximum number of colonies) for each quarter of 2015–2021 and each climatic region. At the contiguous United States level, this follows a stable pattern across the years, with higher and more variable losses during the first quarter (see Supplementary Figs. S2-S6), but some regions do depart from this pattern (e.g., West North Central). (b) Box plots of normalized V. destructor presence (number of colonies affected by V. destructor over the maximum number of colonies) for each quarter of 2015–2021 and each climatic region. The maximum number of colonies is defined as the number of colonies at the beginning of a quarter, plus all colonies moved into that region during the same quarter.Full size imageFigure 3Comparison of normalized honey bee (Apis mellifera) colony loss (number of lost colonies over the maximum number of colonies) between Central and West North Central climatic regions for each quarter of 2015–2021 (the first quarter being January-March). (a) Trajectory of each state belonging to Central (yellow) and West North Central (blue) climatic regions. (b) Smoothed conditional means for each of the two sets of curves based on a locally weighted running line smoother where the width of the sliding window is equal to 0.2 and corresponding standard error bands are based on a 0.95 confidence level46.Full size imageFigure 4Scatter plot of normalized honey bee (Apis mellifera) colony loss (number of lost colonies over the maximum number of colonies) against normalized Varroa destructor presence (number of colonies affected by V. destructor over the maximum number of colonies) for each state and each quarter of 2015–2021 (the first quarter being January-March). Points are color-coded by quarter, and ordinary least squares fits (with corresponding standard error bands based on a 0.95 confidence level) computed by quarter are superimposed to visualize the positive association.Full size imageUp-scaling weather dataThe data sets available to us for weather related variables had a much finer spatio-temporal resolution (daily and on a (4 times 4) kilometer grid) than the colony loss data (quarterly and at the state level). Therefore, we aggregated the former to match the latter. For similar data up-scaling tasks, sums or means are commonly employed to summarize the variables available at finer resolution47. The problem with aggregating data in such a manner is that one only preserves information on the “center” of the distributions – thus losing a potentially considerable amount of information. To retain richer weather related information in our study, we considered additional summaries capturing more complex characteristics, e.g., the tails of the distributions or their entropy, to ascertain whether they may help in predicting honey bee colony loss. Within each state and quarter we therefore computed, in addition to means, indexes such as standard deviation, skewness, kurtosis, (L_2)-norm (or energy), entropy and tail indexes48. This was done for minimum and maximum temperatures, as well as precipitation data (see Data processing for details).Next, as a first way to validate the proposed weather data up-scaling approach, we performed a likelihood ratio test between nested models. Specifically, we considered a linear regression for colony loss (see Statistical model) and compared an ordinary least squares fit comprising all the computed indexes as predictors (the full model) against one comprising only means and standard deviations (the reduced model). The test showed that the use of additional indexes provides a statistically significant improvement in the fit (p-(text {value}=0.03)). This test, which can be replicated for other choices of models and estimation methods (see Supplementary Table S5), supports the use of our up-scaling approach.Figure 5 provides a spatial representation of (normalized) honey bee colony losses and of three indexes relative to the minimum temperature distribution; namely, mean, kurtosis and skewness (these all turn out to be relevant predictors based on subsequent analyses; see Table 1). For each of the four quantities, the maps are color-coded by state based on the median of first quarter values over the period 2015-2021 (first quarters typically have the highest losses, but similar patterns can be observed for other quarters; see Supplementary Figs. S12-S14). Notably, the indexes capture characteristics of the within-state distributions of minimum temperatures that do vary geographically. For example, considering minimum temperature, skewness is an index that (broadly speaking) provides information on whether the data tends to accumulate at one end or the other of the observed range of minimum temperatures (i.e., a positive/negative skewness indicates that the data accumulates towards the lower/upper range, respectively). On the other hand, kurtosis is an index that captures the presence of “extreme” values in the tails of the data (i.e., a low/high value of kurtosis indicates that the tail minimum temperatures are relatively close/very far from the typical minimum temperatures). With this in mind, going back to Fig. 5, we can see that minimum temperatures in states in the north-west present large kurtosis (a prevalence of extreme values in the tails) and negative skewness (a tendency to accumulate towards the upper values of the minimum temperature range), while the opposite is true for states in the south-east. More generally, the mean minimum temperature separates northern vs southern states, kurtosis is higher for states located in the central band of the CONUS, and skewness separates western vs eastern states.We further note that the states with lower losses during the first quarter (e.g., Montana and Wyoming) do not report extreme values in any of the considered indexes. Although these states are generally characterized by low minimum temperatures, these are somewhat “stable” (they do not show marked kurtosis or skewness in their distributions) – perhaps allowing honey bees and beekeepers to adapt to more predictable conditions. On the other hand, states with higher losses during the first quarter such as New Mexico have higher minimum temperatures as well as marked kurtosis, and thus higher chances of extreme minimum temperatures – which may indeed affect honey bee behavior and colony loss. Overall, across all quarters of the years 2015-2021, we found that normalized colony losses and mean minimum temperatures are negatively associated (the Pearson correlation is -0.17 with a p-(text {value} More

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Suborder Glossiphoniiformes Tessler & de Carle, 2018Family Glossiphoniidae Vaillant, 1890Comments. Our two-locus phylogeny reveals the presence of two large clades, corresponding to the subfamilies Glossiphoniinae and Haementeriinae (Fig. 1). The subfamily Theromyzinae Sawyer, 1986, delineated by some authors2,10,22, was not supported as a distant phylogenetic clade and their representatives are clustered within the monophyletic Glossiphoniinae. The same pattern was recovered by earlier phylogenetic reconstructions3,30,33,34. These data indicate that Theromyzinae may represent a synonym of the latter subfamily. However, a subfamily-level revision of the Glossiphoniidae is beyond the framework of the present study.Subfamily Glossiphoniinae Vaillant, 1890Genus Alboglossiphonia Lukin, 1976Type species: Alboglossiphonia heteroclita (Linnaeus, 1761) (= Hirudo heteroclita Linnaeus, 1761; by original designation).Arctic occurrences. Our results reveal that members of this genus are not common inhabitants of the Arctic but two species, A. heteroclita (Linnaeus, 1761) and A. sibirica sp. nov., cross the Arctic Circle on the Yamal Peninsula through the Ob and Taz rivers (Table 1). Previously, it was shown that A. heteroclita occurs in the lower Ob Basin, northern edge of Western Siberia23.Comments. This genus contains inconspicuous minute leeches and is characterized by a nearly global distribution1. It definitely requires an integrative taxonomic revision. Available genetic evidence (Fig. 1 and Supplementary Fig. S1) reveals that the North American populations of what was traditionally assigned to A. heteroclita should be considered a separate species, A. pallida (Verrill, 1872) (type locality: West River near New Haven, Connecticut, USA)35,36. Other species, which occurs in Siberia and the Far East, was tentatively assigned to Alboglossiphonia cf. papillosa (Braun, 1805) based on a darker pigmentation of its dorsum37,38 but it represents a separate North Asian species, which is described here.
Alboglossiphonia sibirica Bolotov, Eliseeva, Klass & Kondakov sp. nov = Alboglossiphonia heteroclita Lukin (1957): 27339 (identification error). = Alboglossiphonia heteroclita papillosa Kaygorodova et al. (2014): 337; Kaygorodova (2015): 4140 (identification error). = Alboglossiphonia cf. papillosa Klass et al. (2018): 2638 (identification error).Figures 4a, 5a, 7a, Supplementary Figs. S2a, S3a, S4, Supplementary Table S2.LSID: https://zoobank.org/urn:lsid:zoobank.org:act:19B581C3-E912-487C-B9EC-8E50DDEFD380.Holotype. RMBH Hir_0542_2-H (non-sequenced), RUSSIA: Lake Torfyanka, 43.0761° N, 131.9620° E, Vladivostok, Primorye, August 12, 2021, Y. E. Chapurina leg.Paratypes (N = 13). RUSSIA: 1 specimen RMBH Hir_0542_2 (sequenced: COI sequence acc. No. ON873332), the type locality, the same date, and collector; 1 specimen RMBH Hir_0396 (non-sequenced), an oxbow lake of Taz River, near Tazovsky settlement, 67.5063° N, 78.6751° E, Yamal-Nenets Region, August 22, 2019, E. S. Babushkin leg.; 1 specimen RMBH Hir_0394 (DNA voucher; sequenced: COI sequence acc. No. ON548508), Vitim River, 57.2010° N, 116.4300° E, Lena River basin, Vitimsky Nature Reserve, Irkutsk Region, July 12, 2019, E. S. Babushkin leg.; 4 specimens RMBH Hir_0013 (3 sequenced with DNA vouchers and one placed on 36 permanent slides as a series of slices; COI sequence acc. No. MH286267, MH286268, and MH286269; 18S rRNA sequence acc. No. MH286273), between zooids of a bryozoan colony, small floodplain lake of the Lena River near Yakutsk, 62.3076° N, 129.8999° E, Yakutia Republic, August 20, 2017, I. N. Bolotov leg.; 1 specimen RMBH Hir_0417_2 (DNA voucher; sequenced: COI sequence acc. No. ON548511), Oron Lake, Gnilaya Kurya Bay, 57.1750° N, 116.4031° E, Lena River basin, Vitimsky Nature Reserve, Irkutsk Region, July 1, 2019, E. S. Babushkin leg.; 1 specimen RMBH Hir_0409_1 (sequenced: COI sequence acc. No. ON548509), a roadside ditch in Knevichi settlement, 43.3886° N, 132.1880° E, Primorye, September 10, 2020, O. V. Aksenova et al. leg.; 1 specimen RMBH Hir_0413 (sequenced: COI sequence acc. No. ON548510), a puddle near railway at Artem city, 43.3794° N, 132.2188° E, Primorye, September 10, 2020, O. V. Aksenova et al. leg.; 1 specimen RMBH Hir_0003_3 (DNA voucher; sequenced: COI sequence acc. No. MN393256), Tumnin River, 49.9451° N, 139.9181° E, Khabarovsk Region, July 14, 2014, I. N. Bolotov & I. V. Vikhrev leg.; 1 specimen RMBH Hir_0509_1 (sequenced: COI sequence acc. No. ON548516), a reservoir on the Bolshoy Alim River, near Tolstovka settlement, 50.1981° N, 127.9431° E, Amur Region, July 3, 2021, O. V. Aksenova et al. leg.; 1 specimen RMBH Hir_0510_1 (DNA voucher; sequenced: COI sequence acc. No. ON548517), an oxbow lake of Bureya River, near Novospassk, 49.6756° N, 129.7343° E, Amur Region, July 3, 2021, O. V. Aksenova et al. leg.Etymology. The name of this species reflects its broad distribution in Siberia.Differential diagnosis. Small leech, which could be distinguished from other congeners by a combination of the following characters: dorsum covered by numerous small, shallow, and indistinct papillae, light yellow, with multiple dark spots and short dashes arranged to 18–24 longitudinal rows; these spots and dashes merged into longitudinal lines in the anterior half of the body (the dark markings pattern often lost in ethanol-preserved animals). Externally, the new species is similar to A. heteroclita, A. hyalina (O. F. Müller, 1773), and A. striata (Apáthy, 1888). However, all these species do not have numerous dark spots and short dashes arranged to multiple longitudinal rows. Additionally, A. heteroclita differs from the new species by having a median row of segmentally arranged dark spots and a smooth dorsum without papillae. A. hyalina differs from A. sibirica sp. nov. by the general lack of dark pigmentation. A. striata differs from the new species by having a median row of segmentally arranged dark transverse stripes and a smooth dorsum without papillae.Molecular diagnosis. The new species represents a separate genetic lineage but is more closely related to A. heteroclita (mean pairwise COI p-distance = 5.1%; range 4.9–5.4%). The intraspecific pairwise COI p-distance ranges from 0.0 to 2.1% (mean ± s.e.m. = 1.31 ± 0.10%; N = 14 sequences and 91 pairwise distance values). The GenBank acc. numbers of reference DNA sequences (COI and 18S rRNA) are given in Supplementary Table S2 and Supplementary Datasets S1–S2.Description. Small leech (body length up to 11.9 mm). Measurements of the type series are given in Supplementary Table S2. Body broad, leaf-like, ovate. Dorsum with numerous small, shallow, and indistinct papillae. Posterior sucker small, circular (maximum diameter of 2.25 mm), ventrally directed. Proboscis pore in the center of anterior sucker. Coloration of living animals: body dirty yellow with multiple brown spots and dashes arranged to longitudinal rows; in the anterior half of the body, these spots and dashes merged into longitudinal lines. Coloration of ethanol-preserved animals: body light yellow; dorsum with multiple dark spots and short dashes arranged to 18–24 longitudinal rows; these spots and dashes merged into longitudinal lines in the anterior half of the body but the dark markings pattern often lost due to preservation. Three pairs of eyespots; the eyespots of the distal pair joined into a single spot; the eyespots of the next two pairs are spaced apart and fused together. Venter light yellow or whitish. Total number of annuli: 70. Somites I–IV joined to form a head region, somites V–XXIV triannulate, somites XXV–XXVII uniannulate. Gonopores joined and open in the furrow XIIa1/a2. Reproductive system: 6 pairs of large, bag-like testisacs inter-segmentally from XIII/XIV to XIX/XX; atrium small, spherical, the atrial cornua twisted anteriorly; paired ejaculatory ducts twisted, short; paired ovisacs narrow, very short. Digestive system: proboscis sheath massive, long, thick; salivary glands diffuse; crop with 6 pairs of crop caeca: 1st-5th uniform, bag-like, 6th pair (posterior caeca) with 3 blind processes; intestine with 4 pairs of rather short processes and an ovate extention after the last pair of processes.Distribution. North Asia: Western Siberia, Eastern Siberia, the Russian Far East, and Mongolia39.Habitats and ecology. This species is known to occur in a broad range of freshwater environments such as rivers, oxbow lakes, large to small natural lakes, reservoirs, road ditches, and even puddles (Supplementary Dataset S2). An unusual example of its association with a bryozoan species was described from Eastern Siberia38. Probably, the record of an Alboglossiphonia leech in the mantle cavity of an unidentified lymnaeid snail from the Altai Mountains, Russia41 could also be attributed to this species. The life cycle of the new species is unknown.Genus Glossiphonia Johnson, 1816Type species: Glossiphonia complanata (Linnaeus, 1758) (= Hirudo complanata Linnaeus, 1758; by subsequent designation).Arctic occurrences. Representatives of this genus are the most remarkable component of the Arctic Glossiphoniidae fauna. Altogether seven species were recorded north of the Arctic Circle, two of which are new to science and described here (Table 1).Comments. In general, sequenced representatives of the genus Glossiphonia could phylogenetically be delineated to three species groups (or subgenera): (1) the complanata-group (= subgenus Glossiphonia s. str.); (2) the verrucata-group (= subgenus Boreobdella Johansson, 1929; type species: Clepsine verrucata Müller, 1844); and (3) the concolor-group (= subgenus Paratorix Lukin & Epstein, 1960; type species: Torix baicalensis Stschegolew, 1922) (Table 1, Fig. 1 and Supplementary Fig. S1).
Glossiphonia arctica Bolotov, Eliseeva, Klass & Kondakov sp. novFigures 4B, 5b,c, 7c, Supplementary Figs. S2b, S3b, S5, Supplementary Table S2.LSID: https://zoobank.org/urn:lsid:zoobank.org:act:FADF0993-A946-413A-9680-25BA0F9BE90D.Holotype. RMBH Hir_0457_2_1-H (sequenced: COI sequence acc. No. ON810735; 18S rRNA sequence acc. No. ON819028), RUSSIA: a large lake near Sob’ railway station, 67.0480°N, 65.6316°E, Polar Urals, June 23, 2021, A. V. Kondakov et al. leg.Paratypes (N = 18). 18 specimens RMBH Hir_0457 (two specimens sequenced: COI sequence acc. No. ON810736 and ON810737; 18S rRNA sequence acc. No. ON819029; one specimen placed on 18 permanent slides as a series of slices), the type locality, the same date, and collectors.Etymology. The name of the new species indicates that its type locality is situated in the Arctic Region.Differential diagnosis. Medium-sized leech, which could be distinguished from other congeners by a combination of the following characters: dorsum with four rows of ovate, broad but very shallow and indistinct papillae on annulus a2 (outer paramedian and inner paramarginal series); each papilla bears ovate light yellow or white spot; dorsal black markings pattern absent. Externally, the new species is similar to G. mollissima. However, the latter species differs from G. arctica sp. nov. by having larger papillae and a well-developed black markings pattern dorsally.Molecular diagnosis. The new species represents a separate genetic lineage belonging to the verrucata-group (Fig. 1). The pairwise COI p-distance of the new species from other congeners varies from 7.0 to 12.4%. The intraspecific pairwise COI p-distance ranges from 0.0 to 0.2% (mean ± s.e.m. = 0.10 ± 0.05%; N = 3 sequences and 3 pairwise distance values). The GenBank acc. numbers of reference DNA sequences (COI and 18S rRNA) are given in Supplementary Table S2 and Supplementary Datasets S1–S2.Description. Medium-sized leech (body length up to 13.3 mm). Measurements of the type series are given in Supplementary Table S2. Body broad, leaf-like, ovate. Dorsum with four rows of ovate, broad but very shallow and indistinct papillae on annulus a2 (outer paramedian and inner paramarginal series). Posterior sucker small, circular (maximum diameter of 1.9 mm), ventrally directed. Proboscis pore in the center of anterior sucker. Coloration of living animals: body almost transparent, light brown, with multiple yellowish pigment cells. Coloration of ethanol-preserved animals: dorsum beige to light brown, with darker broad inner paramedian lines and light yellowish areas laterally and anteriorly; ovate light yellow or white spots at each papillae on annulus a2 arranged into four longitudinal rows (outer paramedian and inner paramarginal), sometimes with a few white spots between them. Three pairs of ovate eyespots arranged to two parallel rows; in some specimens eyes on each side are joined to a single large spot. Venter whitish to light brown, sometimes with irregular brownish shading. Total number of annuli: 70. Somites I–III uniannulate, IV biannulate, V–XXIV triannulate, XXV biannulate, XXVII uniannulate. The male and female genital pores are separated by two annuli and are located in the furrows XIa3/XIIa1 and XIIa2/a3, respectively. Reproductive system: 6 pairs of spherical testisacs inter-segmentally from XIII/XIV to XVIII/XIX; atrium spherical, the atrial cornua large, twisted anteriorly; paired ejaculatory ducts very long, extending to XVIII; paired ovisacs massive, long, with multiple lobes, arranged as loops, extending to XVIII (pregnant specimen with eggs). Digestive system: proboscis sheath massive, thick, elongated; esophagus narrow; salivary glands diffuse; crop with 7 pairs of crop caeca: 1st-6th uniform, bag-like, 7th pair (posterior caeca) with 4 blind processes and several smaller lobes; intestine enlarged, with 4 pairs of large, long, bag-like processes, expanding distally, each with several short lobes; a large circular extension after the last pair of processes.Distribution. Polar Urals (not known beyond the type locality).Habitats and ecology. The type series of this species was collected from a natural mountain lake with stony bottom. The leeches were recorded beneath flat stones (Fig. 3b); their feeding behavior and life cycle remain unknown.
Glossiphonia taymyrensis Bolotov, Eliseeva, Klass & Kondakov sp. novFigures 4E, 5d, 7b, Supplementary Figs. S2h, S3c, S6, Supplementary Table S2.LSID: https://zoobank.org/urn:lsid:zoobank.org:act:40269BF4-FE1C-4269-A7CC-41020789DC44.Holotype. RMBH Hir_0258_1-H (sequenced: COI sequence acc. No. ON810695), RUSSIA: small lake near Dudinka on Taymyr Peninsula, 69.4008°N, 86.3384°E, July 16, 2018, O. V. Aksenova et al. leg.Paratypes (N = 8). RUSSIA: 2 specimens RMBH Hir_0263_1 and RMBH Hir_0264_3 (sequenced: COI sequence acc. No. ON810701 and ON810705; 18S rRNA sequence acc. No. ON819017), the type locality, the same date, and collectors; 2 specimens RMBH Hir_0256_1 (one sequenced and one placed on 20 permanent slides as a series of slices; COI sequence acc. No. ON810693), small lake near Dudinka on Taymyr Peninsula, 69.3987° N, 86.3505° E, July 16, 2018, O. V. Aksenova et al. leg.; 1 specimen RMBH Hir_0261_2 (sequenced: COI sequence acc. No. ON810699; 18S rRNA sequence acc. No. ON819016), small lake near Dudinka on Taymyr Peninsula, 69.4014° N, 86.3250° E, July 16, 2018, O. V. Aksenova et al. leg.; 1 specimen RMBH Hir_0265_2 (sequenced: COI sequence acc. No. ON810706; 18S rRNA sequence acc. No. ON819021), Bolgokhtokh River near Dudinka, Taymyr Peninsula, 69.3780° N, 87.2215° E, July 21, 2018, O. V. Aksenova et al. leg.; 1 specimen RMBH Hir_0488 (sequenced: COI sequence acc. No. ON810755), a lake on Putorana Plateau, 68.7607° N, 91.9014° E, July, 2021, E. S. Chertoprud leg.; 1 specimen RMBH Hir_0449 (sequenced: COI sequence acc. No. ON810731), Pyzas River near Ust-Kabyrza settlement, 52.8277° N, 88.3973° E, Tashtagolsky District, Kemerovo Region, July 23, 2020, E. S. Babushkin & M. V. Vinarski leg.Etymology. The new species is named after the Taymyr Peninsula, where the majority of the type specimens were collected.Differential diagnosis. Small leech with broad, leaf-like, ovate body; three pairs of eyespots (distal pair joined; next two pairs separate); dorsal papillae absent; dorsal coloration with two inner paramedian rows of black spots, sometimes joining into unclear dashed lines; two annuli between the male (XIa3/XIIa1) and female (XIIa2/a3) genital pores. The new species largely resembles G. complanata but could be distinguished from it by having a smooth dorsum, without clear papillae. These taxa seem to have non-overlapping, allopatric ranges and, hence, could be separated on the basis of geographic criteria. However, the DNA approach seems to be the most appropriate way to distinguish these two species.Molecular diagnosis. The new species represents a separate genetic lineage belonging to the complanata-group (Fig. 1). The pairwise COI p-distance of the new species from other congeners varies from 6.0 to 12.2%. The intraspecific pairwise COI p-distance ranges from 0.0 to 1.1% (mean ± s.e.m. = 0.52 ± 0.07%; N = 8 sequences and 28 pairwise distance values). The GenBank acc. numbers of reference DNA sequences (COI and 18S rRNA) are given in Supplementary Table S2 and Supplementary Datasets S1–S2.Description. Small leech (body length up to 11.3 mm). Measurements of the type series are given in Supplementary Table S2. Body broad, leaf-like, ovate. Dorsum smooth, without clear papillae. Posterior sucker ovate (maximum diameter of 3.0 mm), ventrally directed. Proboscis pore in the center of anterior sucker. Coloration of living animals: not examined. Coloration of ethanol-preserved animals: (1) typical form having beige to light brown ground color without light spots but with darker brown coloration between inner paramedian lines; (2) melanic forms having dark brown ground color with four rows of large yellow spots (outer paramedian and marginal series) and yellow median stripe anteriorly (f. ‘maculosa’) or with strongly reduced yellow markings pattern. In all forms, there are two inner paramedian rows of black spots, sometimes joining into unclear dashed lines. Three pairs of ovate eyespots; the eyespots of the distal pair joined into a single spot; the eyespots of the next two pairs separate and are spaced apart. In the typical form, venter light yellow, with paired brown median and outer paramedian lines, which may be reduced to series of narrow brown longitudinal stripes. In melanic forms, ventral markings is more developed, with a series of brown longitudinal lines from median to inner paramarginal position and outer paramarginal brown spots. Posterior sucker with dense brown spots in melanic forms and with scarce brown spots in typical form. Total number of annuli: 68. Somites I–IV uniannulate, V–XXIV triannulate, XXV biannulate, XXVI–XXVII uniannulate. The male and female genital pores are separated by two annuli and are located in the furrows XIa3/XIIa1 and XIIa2/a3, respectively. Reproductive system: 6 pairs of spherical testisacs inter-segmentally from XII/XIII to XVIII/XIX; atrium ovate, the atrial cornua directed laterally; paired ejaculatory ducts twisted, short; paired ovisacs short, thick (undeveloped). Digestive system: salivary glands diffuse; proboscis sheath moderately thick; esophagus ovate; crop with 6 pairs of massive, bag-like, uniform crop caeca; intestine with 4 pairs of processes.Distribution. Western and Eastern Siberia.Habitats and ecology. The new species was recorded from natural lakes and rivers (Supplementary Dataset S2); its feeding behavior and life cycle are unknown.Genus Hyperboreomyzon Bolotov, Eliseeva, Klass & Kondakov gen. novLSID: https://zoobank.org/urn:lsid:zoobank.org:act:298FF41E-AF0D-4442-9F82-3022B8094A67.Type species: Hyperboreomyzon polaris gen. & sp. nov.Etymology. This name is compiled using two Greek words: ‘Hyperborea’ (meaning a mythical far northern land) and ‘myzon’ (meaning sucking).Diagnosis. Medium-sized, elongate, sub-fusiform glossiphoniid leeches; body and posterior sucker densely covered by shallow, ‘fish-scale’-like papillae; somite V biannulate; somites XII–XXIII secondarily sexannulate dorsally and ventrally due to the presence of very deep, prominent furrows separating each annulus to two semi-annuli; six rows of prominent dorsal tubercle-like papillae at a2 (inner paramedian, inner paramarginal, and marginal series) from V to XXVI; two pairs of circular eyespots on II and Va1 at inner paramedian position; gonopores at the furrows XIa3/XIIa1 (male) and XIIa2/a3 (female) and separated by two annuli; male atrium spherical; proboscis pore opens in a thick velar fold in the anterior half of oral sucker; one pair of compact, massive, elongated, incurved salivary glands, each gland with a bunch of a few short processes apically; 9 crop caeca pairs. Comparison of the new genus with other genera in the family based on morphological and anatomical features is presented in
Supplementary Table S3. Sexannulate condition was also recorded in the genus Actinobdella Moore, 1901 from North America36, but it differs from Hyperboreomyzon gen. nov. by having one pair of eyespots, diffuse salivary glands, and an apical position of proboscis pore (Supplementary Table S3).Comments. This genus is established for a single species, which is described below.
Hyperboreomyzon polaris Bolotov, Eliseeva, Klass & Kondakov gen. & sp. nov.Figures 4J, 5e, 6a-j, 7c, Supplementary Figs. S21, S8, S9, S10, S11, Supplementary Table S2.LSID: https://zoobank.org/urn:lsid:zoobank.org:act:503A9A26-CEDE-4747-952D-8416AE4EF4EB.Holotype. RMBH Hir_0486-H (sequenced: COI sequence acc. No. ON810753; 18S rRNA sequence acc. No. ON819030), RUSSIA: small alpine lake on Putorana Plateau, 68.9008°N, 94.1599°E, July, 2021, E. S. Chertoprud leg.Paratypes (N = 2). RUSSIA: 1 specimen RMBH Hir_0689 (dissected and placed on 60 permanent slides as a series of slices), small alpine lake on Putorana Plateau, 68.6659° N, 93.1365° E, August 11, 2021, E. S. Chertoprud leg.; 1 specimen RMBH Hir_0216 (sequenced and dissected; COI sequence acc. No. ON810677; 18S rRNA sequence acc. No. ON819005), water puddle on Kolguev Island, 68.9300° N, 49.0303° E, August 12, 2018, O. V. Travina & V. M. Spitsyn leg.Etymology. The name of the new species reflects its occurrences in polar (Arctic) areas of Eurasia.Differential diagnosis. As for the genus.Molecular diagnosis. None of congeneric species is known. Based on uncorrected pairwise COI p-distances between a haplotype of the new taxon and selected species-level haplotypes in each genus (Supplementary Table S1), Hyperboreomyzon seems to be more closely related to members of Hemiclepsis (mean distance ± s.e.m. = 11.62 ± 0.15%, range = 9.75–14.08%, N = 9) and Theromyzon (mean distance ± s.e.m. = 11.37 ± 0.07%, range = 10.47–12.64%, N = 9) without significant differences between distances from these two genera (Mann–Whitney test: p = 0.72). Other Glossiphoniidae genera are more distantly related, with a mean pairwise uncorrected COI p-distance of  > 13.0% (Mann–Whitney test: p  More