Ecology

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Soil physicochemical propertiesTable 1 shows the basic chemical characteristics of the 81 soil samples. The pH values of most of the soil samples from the rape fields and the paddy fields ranged between 6.5 and 7.5, while the pH values of most of the soil samples from the wheat fields were less than 6.0. The relatively low pH values for soils from the wheat fields could be due to traditional farming practices adopted in the farms, including continuous cropping. In addition, acidic soil is conducive for wheat growth. Organic matter contents were generally low in all the soils, and soils from the rape fields had the lowest organic matter contents. Generally, the mean soil total N contents in the fields were in the order of rape fields (756 mg/kg)  Zn  > Cd, and the concentrations of metals in most soil samples collected from the wheat and paddy fields were in the order of Fe  > Mn  > Pb  > Cu  > Zn  > Cd. However, independent of the farmland use patterns, the concentrations of all the metals extracted using NH4OAC and NH4NO3 were much lower than those extracted with the other three types of extractants.Table 3 Extractable metal concentrations in the soils (mg/kg).Full size tableThe concentrations of 0.1 mol/L HCl-extracted heavy metals in soils from the rape fields at the R21, R23, and R32 sites, in the wheat fields at the W21 site, and in the paddy fields at the P1 and P2 sites were extremely low, especially in the cases of Fe and Pb. For example, 0.1 mol/L HCl-extracted Fe concentrations at the R21, R23, and R32 sites were 0.2 mg/kg, 0.6 mg/kg, and below the detection limit, respectively, whereas the range of 0.1 mol/L HCl-extracted Fe concentration in the other sites in the rape fields was 22.4–533 mg/kg. Therefore, 0.1 mol/L HCl-extracted heavy metal concentrations at the R21, R23, R32, W21, P1, and P2 sites were omitted from subsequent analyses to ensure homogeneity of variance. The basic pH values at the sites (pH values at R21, R23, R32, W21, P1, and P2 were 8.0, 8.0, 7.7, 8.0, 8.0, and 8.0, respectively) could explain this low HCl-extractability and reduced mobility35,36. Although HCl is considered a universal extractant, it may not be suitable under alkaline soil conditions.Heavy metal concentrations in rape, wheat and rice grainsFigure 4 illustrates the concentrations of six heavy metals in rape, wheat, and rice grains. Similar to the order of the soil metal concentrations, the Fe, Mn, Zn, and Cu concentrations in the grains were much higher than the Pb and Cd concentrations.Figure 4Concentrations of heavy metals ((a) Cu, (b) Zn, (c)Pb, (d) Cd, (e) Fe, and (f) Mn) in the grain of three different crops. (Rape grains (n = 36); Wheat grains (n = 25); Rice grains (n = 20), on dry weight basis).Full size imageThe results are similar to those reported in previous studies with regard to heavy metal concentration trends in rice grains16,37. The reason could be Fe, Mn, Zn, and Cu are all essential for crop growth as micronutrients, leading to the higher levels in soils. Among the studied crops, rice grains accumulated relatively lower amounts of Fe, Mn, and Zn than rape and wheat grains, where Pb and Cd concentrations exhibited opposite trends. The trends are consistent with the findings of Liu et al.38 and Du et al.1, and indicate that rice has a stronger Cd uptake capacity from soil. Williams et al.39 also reported higher rice Cd concentrations than wheat, barley, and maize Cd concentrations. The results could also be attributed to water management and soil oxidation–reduction status in soil-rice systems. Paddy fields are irrigated considerably more than wheat and rape fields. In addition, the water in the study area was contaminated by Cd, Cu, As, and Zn27. Previous studies have also reported that water management practices influence Cd uptake by rice and its bioavailability in soils19,20,40. In the cases of Zn and Pb, according to Feng et al.23, rice grains accumulated lower amounts of Zn than wheat grains, whereas rice grains accumulated higher Pb amounts than wheat grains. Although soil Cd concentrations were generally high in the rape fields, the concentrations of Cd in rape grains were lower than those in the wheat and rice grains.On the other hand, Cu concentrations in grains in all the three crops were below the maximum allowable Cu levels in food (10 mg/kg (GB 15199-94)). Similarly, Zn concentrations in rice grains were below the maximum allowable Zn levels in food (50 mg/kg (GB 13106-91)), while 25% of the rape grain samples and 20% of the wheat grain samples exceeded the threshold value. Although total Pb concentrations in soils were generally low in the three farmland use patterns, Pb concentrations in 70% of the rice grain samples exceeded the maximum allowable Pb levels in food (0.2 mg/kg (GB 2762-2005)). Only four rape and two wheat grain samples exceeded the Pb threshold values, respectively. The varying Pb trends are potentially linked to physical contamination from direct atmospheric deposition8, differences in physiological activities among the crops, and the fruit structures of the studied crops23. Similar to the soil Cd contamination, 96% and 60% of wheat and rice grain samples, respectively exceeded the maximum allowable Cd levels in food (0.1 mg/kg and 0.2 mg/kg for wheat and rice, respectively (GB 2762-2005)). Furthermore, Cd concentrations in approximately 10% of the rice grain samples exceeded 1.0 mg/kg. Conversely, only 14% of rape grain samples exceeded the maximum allowable Cd levels in food (Cd: 0.1 mg/kg for rape (GB 2762-2005)), and the maximum Cd concentration in rape grains was 0.18 mg/kg. According to the results, rape grains were generally safe for consumption whereas wheat and rice grains posed health threats in the study area.Soil to grain bioaccumulation factorsBAF values have been used widely to evaluate the capacity of crop grains to accumulate metals from soil30,41. Similar to a previous study on food crops37, Fe and Pb had the lowest BAF values (Fig. 5). Generally, metal accumulation in crop grains did not increase considerably with an increase in total concentrations of metals in soil. Heavy metal accumulation could have been regulated by crops, so that only low amounts were accumulated into grains. In addition, there were significant differences in some BAF values of the same metal across different crop species (Fig. 5). Different crop species have different accumulation capacities for the same metal42. Overall, the average BAF values of Cu (0.22), Zn (0.37), and Mn (0.14) in wheat grains were significantly higher than those in rape and rice grains. The average BAF value of Pb (0.005) in rice grains was significantly higher than those in rape and wheat grains, and the average BAF values of Cu (0.07) and Cd (0.06) in rape grains were significantly lower than those in wheat and rice grains. The results indicated that rape grains have lower heavy metal accumulation capacity than wheat and rice grains, except in the cases of Zn and Fe. However, the finding is not consistent with the results of a previous study43, which report that grasses have lower accumulation capacity than dicotyledonous plants. Nevertheless, as mentioned above, numerous factors could influence the accumulation capacity of metals in crop grains.Figure 5Bioaccumulation factors (BAF) of heavy metals ((a) Cu, (b) Zn, (c) Pb, (d) Cd, (e) Fe, and (f) Mn) from soil to the grains of three crop species. The error bars indicate the standard deviation. Different letters on bars indicate significant difference (p  More

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Lattice data geoprocessing and temporal extentWe latticed the data49 using a worldwide grid composed of 18,874 hexagonal 7774 km2 units, built using Discrete Global for R (https://github.com/r-barnes/dggridR)50. All the information we processed on yellow fever cases, on urban and sylvatic vectors presences, and on zoogeographic, spatial and environmental variables (see details on this information below) was aggregated at this spatial resolution. We used zonal statistics to calculate average variable values using ArcMAP 10.7.The temporal extent for our analysis was divided into three periods: the late 20th century (1970–2000), the early 21st century (2001–2017), and the period 2018–2020. Predictions estimated by the late 20th century models were validated using cases reported in the early 21st century, and predictions from the early 21st century models were validated with records from 2018‒2020. Although the limit between periods at the turn of the century is arbitrary, it reflects: 1) Distributional changes in the ranges of the Ae. aegypti and Ae. albopictus vectors51; 2) after 1999, the yellow fever genotype I has spread outside the endemic regions, and the genotype I modern-lineage has caused all major yellow fever outbreaks detected in non-endemic regions of South America since 200013; 3) the maximum potential of globalization was realised at the beginning of the 21st century with the opening of international borders, the widespread access to the Internet and to cell phones, and the generalization of online travel booking and of low-cost flights34. The end of the second period, 2017, was chosen in order to include three years with occurrence of yellow fever cases in south-western Brazil (and two since its occurrence in Angola and the DRC), while retaining three later years for predictive testing purposes (details on this testing are given below).Yellow fever datasetsWe used georeferenced cases of yellow fever in humans for a period of 51 years (from 1970 to 2020). This study period starts immediately after the suspension of the use of DDT due to to the appearance of resistance of Ae. aegypti in the late 1960s in several countries, after 50 years of eradication efforts10. We took from Shearer et al.6 the distribution of yellow fever cases for the period 1970–2016. We extracted additional cases for the period 1970–2020 from various sources (Supplementary data 1), including ProMED-mail: Program of International society for infectious diseases; World Health Organization (WHO): Yellow fever outbreak weekly situation reports, Rapport de situation fievre jaune en RD Congo and Weekly epidemiological record; Health Ministry of different countries: Epidemiological Bulletins of yellow fever in Brazil, Peru, Colombia, and Paraguay; Pan American Health Organization (PAHO): Epidemiological Update Yellow Fever; European Centre for Disease Prevention and Control (ECDC): Communicable disease threats report and Rapid risk assessment report; Nigeria Centre for Disease Control (NCDC): Situation report, yellow fever outbreak in Nigeria and Global Infectious Disease and Epidemiology Online Network (GIDEON). The reported cases were complemented with publications available since 2016 with geo-referenced information on case location (Supplementary data 1). In addition, information was also sought on cases reported in French and Portuguese from local news reports in Africa.We only represented in the hexagonal lattice the reported cases of yellow fever that had a precise location or that were referred to administrative unit was smaller than or of similar size to the hexagons. This dataset was transformed into a binary variable per study period representing the presence (n = 218 hexagons in the late 20th century; 493 hexagons in the early 21st century, see Supplementary data 2) or absence (n = 18,656 hexagons in the late 20th century; 18,381 hexagons in the early 21st century), hereafter the distribution of reported cases of yellow fever.Vector datasetThe georeferenced presences of vectors involved in the urban cycle of yellow fever (i.e., the mosquitoes Ae. aegypti and Ae. albopictus) were taken from “The global compendium of the Ae. aegypti and Ae. Albopictus occurrence”26 for the period 1970–2014. We complemented these records with georeferenced data scientifically validated for the period 2014–2017, taken from VectorBase (https://www.vectorbase.org/) and Mosquito Alert (http://www.mosquitoalert.com/). We included both species because, although Ae. Aegypti is the main vector of yellow fever, Ae. albopictus can also transmit the yellow fever virus to humans4,52.In addition, we included georeferenced occurrence data of sylvatic vectors (Haemagogus janthinomys, H. leucocelaenus and Sabethes chloropterus in South America; Ae. africanus and Ae. vittatus in Africa), which were obtained from Vectormap (vectormap.si.edu) and Gbif (https://gbif.org).We represented in the hexagonal lattice the reported occurrence of mosquitoes that had a precise location or were located in administrative smaller than or of similar size to the hexagons. With this information, we built binary variables representing the presence or absence of each mosquito species in each hexagon. For species involved in the urban cycle, we built two binary variables per species: one for the late 20th century, and another for the early 21st century. For species involved in the sylvatic cycle, we merged the data of late 20th century and early 21st century in order to build a binary variable per species, due the scarcity of data and under the assumption that their distributions have been stable during the four last decades53,54,55.Zoogeographic, spatial and environmental variablesWe built zoogeographic variables based on chorotypes, or types of distribution ranges, of all non-human primate species, as all are potentially vulnerable to yellow fever56. A chorotype is a distribution pattern shared by a group of species57. For obtaining these zoogeographic variables, we proceeded in 4 steps: (1) Distribution maps of non-human primates were obtained from the IUCN for South-America and Africa; (2) the species ranges were classified hierarchically using the classification algorithm UPGMA according to the Baroni-Urbani & Buser´s similarity index58; (3) we evaluated the statistical significance of all clusters obtained as a result of the classification using RMacoqui 1.0 software (http://rmacoqui.r-forge.r-project.org/)59; (4) in each hexagon, the number of species belonging to each chorotype was quantified. We generated a zoogeographic model based on the non-human primates chorotypes by running a forward-backward stepwise logistic regression using presence/absence of yellow fever cases and the number of species of each chorotype as dependent and predictor variables, respectively. This procedure was made for two periods: late 20th century and early 21st century. Henceforth, only the selected chorotype variables were considered in the baseline disease favourability models explained below.We built a yellow fever spatial variable for each continent (South-America and Africa), which were calculated through the trend surface approach, by performing a backward-stepwise logistic regression of the distribution of yellow fever cases on a ensemble of variables defined for polynomial combinations of longitude (X) and latitude (Y) up to the third degree: X, Y, XY, X2, Y2, X2Y, XY2, X3, and Y3. We transformed probability values derived from logistic regression into spatial favourability values by applying the Favourability Function60,61, using the following equation:$$F=frac{P}{1-P}Big/left(frac{{n}_{1}}{{n}_{0}}+frac{P}{1-P}right)$$
(1)
where P is the spatial probability of occurrence of at least a case of yellow fever at each hexagon, and n1 and n0 are the numbers of hexagons with presence and absence of yellow fever cases, respectively. We built a different spatial variable for each continent and time period.We used environmental variables related to the following factors: climate, human activity, topography, hydrography, biome, ecosystem type, and forest loss. For details about the source and description of the environmental variables selected, see Supplementary Table 3.Pathogeographical approach to transmission risk modellingOur objectives were to construct a global yellow fever transmission risk map, and to identify areas where primates contribute to increased risk, using the methodology previously used to analyse the worldwide dynamic biogeography of zoonotic and anthroponotic dengue34 (see flowchart in Fig. 1 and Supplementary Methods). We produced a transmission model focused on the late 20th century and another for the early 21st century.The risk of transmission was assessed by combining a first model describing areas favourable to the presence of yellow fever, i.e., the “baseline disease model”; and another model describing areas favourable to the presence of mosquitoes known to act as vectors, i.e., the “vector model”. For this combination, we used the fuzzy intersection62, i.e., the risk of transmission at each hexagon was valued at the minimum between favourability in the baseline disease model and favourability in the vector model.In this way, we considered that the vectors are a limiting factor, and that the risk of transmission derives from the degree to which the environmental conditions are simultaneously favourable for the presence of vectors and for disease cases to occur63. In order to analyze the spatio-temporal dynamic of yellow fever, we made comparable models for the late 20th century and the early 21st century, using predictor variables that are available for both periods. Later, we made a 21st-century enhanced model that optimized the predictive capacity of availabe information in the search for current risk areas. For this purpose, we included, in the variable set, predictors that are only accessible for the 21st century (e.g., high-resolution population density, livestock, irrigation, infrastructures, intact forest, and GlobCover land cover classes; see Supplementary Table 3).Baseline disease modelsThe baseline disease model in the late 20th century was expressed in terms of favourability values, using the Eq. (1) (see above). This time, P was calculated through a multivariable forward-backward stepwise logistic regression of the 20th-century yellow fever presences/absences on a set of zoogeographic, environmental and spatial variables. This was made in two blocks: 1) a stepwise selection of environmental and spatial variables; 2) a later stepwise addition of chorotypes whose presence contribute to improve significantly the likelihood of the model based only on the first block. Variables for each block were preselected using RAO´s score tests (which estimated the significance of its association to the distribution of yellow fever cases), and Benjamini and Hochberg´s (1995) false discovery rate (FDR) to control for Type I errors, which could pass due to the number of variables analysed. We also avoided excesive multicollinearity by preventing that variables with Spearman correlation values >0.8 were included in the same model. In case this happened, only the variable with the most significant RAO´s score-test value was retained, and the multivariable model was re-run. The parameters in the models were estimated using a gradient ascent machine learning algorithm, and the significance of these paremeters was assessed using the test of Wald. The goodness of fit of the models was established using the test of Hosmer and Lemeshow, which checks the significance of the difference between expected and observed values, so that non significant differences mean that the fit is good. We used IBM-SPSS Statistics 24 software package to perform the models and all the associated tests.We subsequently updated the baseline disease model to explain the distribution of yellow fever cases in the early 21st century. Compared to the procedure described for the 20th-century model, we included a new block before the two ones mentioned above. Thus, the methodological sequence was as follows: (1) forcing the input, as a predictor variable, of the logit of the late 20th century baseline disease model (the logit being the linear combination of variables in the 20th-century model); (2) making a later stepwise selection of spatial and environmental variables; and (3) a stepwise addition of chorotypes that contribute to improving the model’s likelihood. In this way, we took into account that the current spread of yellow fever is influenced by the inertia of previous situations. This is equivalent to assuming that there is temporal autocorrelation (i.e., disease cases in the early 21st century are more probable to occur in areas where they already occurred in the late 20th century). In the 21st-century model, the variables entering in blocks (2) and (3) represent the drivers potentially favouring the spread34. The preselection of variables for blocks (2) and (3) and the control for excessive multicollinearity between environmental variables were made as explained for the late 20th-century model.Vector modelsWe produced a favourabuility model for each vector species for the late 20th century and for the early 21st century separately. We built multivariable favourability models for urban vectors using the distribution of each urban mosquito species in the late 20th century and the spatial and environmental variables for the late 20th century, following the same procedure used for block (1) in the 20th-century baseline disease model. We also updated each urban vector model for the early 21st century as in the baseline disease model, using the procedure described for blocks (1) and (2).A single model, referred to both the late 20th and the early 21st centuries, was made for sylvatic vectors, for the reasons explained above. Finally, we built up the vector models for the late 20th century and for the early 21st century by joining all individual vector models of each period using the fuzzy union64 (i.e., considering for each hexagon the maximum value shown by any of the species models). This criterion was taken into account because, if the pathogen were present, the occurrence of a single vector species would involve potential for yellow fever transmission.Model fit assessment and validation of its predictive capacityFavourability models were assessed according to their classification and discrimination capacities respect to the training data set (i.e., to the observations used for model training). The classification capacity was based on two classification thresholds: F = 0.5, which represents the neutral favourability, and F = 0.2, below which the risk of transmission was considered to be low61. Six classification assessment indices were used65: (1) sensitivity (i.e., proportion of presences correctly classified in favourable hexagons), (2) specificity (i.e., proportion of absences correctly classified in unfavourable hexagons), (3) CCR (i.e., proportion of presences and absences correctly classified in favourable hexagons respectively), (4) TSS (that is sensitivity + specifity – 1), (5) underprediction rate (i.e., proportion of favourable areas that are recorded to have presences), and (6) overprediction rate (i.e., proportion of favourable areas that are not recorded to have presences). The discrimination capacity was assessed using the area under the receiver operating characteristic (ROC) curve (AUC)66.The validation of the predictive capacity of the late 20th century disease and transmission-risk models was done by evaluating, with the same indices used above, classification and discrimination capacities with respect to the cases of the period 2001‒2020. The predictive capacity of the models for the early 21st century was validated with respect to the yellow fever cases reported in the period 2018‒2020.Relative importance of the zoogeographical factorWe estimated the pure contribution of non-human primates to the baseline disease model, i.e., how much of the variation in favourability for yellow fever cases was explained exclusively by the zoogeographical factor, by performing a variation partitioning analysis67. This implied the use of the zoogeographic model and a spatio-environmental model constructed with the environmental and spatial variables that entered the baseline disease model. This approach also allowed us to calculate how much is the variation of the baseline disease model attributable simultaneously to the zoogeographical and other factors. We built maps identifying the zones where the non-human primates could increase yellow fever cases in humans, that is, where the presence of primates could favour the occurrence of yellow fever regardless of correlations with other factors. To map these areas we identified the hexagons that fulfilled these conditions: 1) favourability values for the baseline disease model were ≥ 0.2; and 2) the difference between the favourability values provided by the baseline disease model and the spatio-environmental model was positive and ≥ 0.01.Reporting summaryFurther information on research design is available in the Nature Research Reporting Summary linked to this article. More

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