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Overall strategyThe aim of this project was to synthesize publicly available data on land use, pesticide use, and toxicity to generate a ‘toolkit’ of data resources enabling improved landscape-scale research on pesticide-pollinator interactions. The main outcomes are several novel datasets covering ten major crops or crop groups in each of the 48 contiguous U.S. states:

I)

Average application rate (kg/ha/yr) of >500 common pesticide active ingredients (1997–2017),

II)

Aggregate bee toxic load (honey bee lethal doses/ha/yr) of all insecticides combined (1997–2014), (Note that this dataset ends in 2014 because after that year, data on seed-applied pesticides were excluded29, and these contribute significantly to bee toxic load21)

III)

Reclass tables relating these pesticide-use indicators to land use/land cover classes to enable the creation of maps predicting annual pesticide loading at 30–56 m resolution.

An overview of the steps, inputs, and outcomes are provided in Fig. 1.Fig. 1Overview of the data synthesis workflow described in this paper.Full size imageData inputsA summary of input datasets is provided in Table 1.Table 1 Data inputs used in this study.Full size tablePesticide dataPesticide use data were last downloaded from the USGS National Pesticide Synthesis Project30,31 in June 2020. This dataset reports total kg applied of 508 common pesticide active ingredients by combinations of state, crop group, and year for the contiguous U.S. from 1992–2017 (crop groups explained in Table 2). The data are derived primarily from farmer surveys conducted by a private firm (Kynetec). For California, USGS obtains data from the state’s pesticide use reporting program32. USGS then aggregates and standardizes both data sources into a common national dataset that is released to the public and was used in this effort. The USGS dataset includes both a ‘high’ and a ‘low’ estimate of pesticide use, varying based on the treatment of missing values in the source data31. Because previous work on this dataset suggested that the ‘low’ estimate more closely matches independent pesticide estimates33, we used the ‘low’ estimate throughout, but assess the influence of this choice on the resulting estimates (see Technical Validation). While we focus on the ‘low’ estimate for the data and outputs presented in this manuscript, the workflow we developed can accommodate both the low and high estimates.Table 2 USGS crop categories in pesticide source data, based on metadata from USGS30,31 and personal communication with USGS staff scientists.Full size tableCrop area dataTo translate pesticide use estimates into average application rates, it was necessary to divide total kg of pesticide applied by the land area to which it was potentially applied. Crop area data were last downloaded from the Quick Stats Database of the USDA34 in May 2020, using data files downloaded from the ‘developer’ page. This USDA dataset contains crop acreage estimates generated from two sources: the Census of Agriculture (Census), which is comprehensive but conducted only once every five years35 and the crop survey conducted by the National Agricultural Statistics Service (NASS), which is an annual survey based on a representative sample of farmers in major production regions for a more limited subset of crops36.Honey bee toxicity dataTranslating insecticide application rates into estimates of bee toxic load (honey bee lethal doses/ha/yr) required toxicity values for each insecticide active ingredient in the USGS dataset. We used LD50 values for the honey bee (Apis mellifera) because this is the standard terrestrial insect species used in regulatory procedures, and so has the most comprehensive data available. This species is also of particular concern as an important provider of pollination services to agriculture. As previously reported21, the LD50 values were derived from two sources, the ECOTOX database37 of the U.S. Environmental Protection Agency (US-EPA), and the Pesticide Properties Database (PPDB)038. ECOTOX was queried in July 2017, by searching for all LD50 values for the honey bee (Apis mellifera) that were generated under laboratory conditions. Acute contact and oral LD50 values for the honey bee were recorded manually from the PPDB in June 2018.Land cover dataMapping pesticides to the landscape requires land use/land cover data indicating where crops are grown. We used the USDA Cropland Data Layer (CDL)39, a land cover dataset at 30–56 m resolution produced through remote sensing. This dataset is available starting in 2008 for states in the contiguous U.S., with some states (primarily in the Midwest and Mid-South) available back to the early 2000s.Data preparationRelating datasetsA major challenge in this data synthesis effort was relating the various data sources to each other, given that each dataset has unique nomenclature and organization. We created the following keys (summarized in Table 3) to facilitate joining datasets:

I)

USGS-USDA crop keys – Using documentation and metadata associated with the USGS pesticide dataset31,33,40, we created keys relating the USGS surveyed crop names (‘ePest’ crops) and the ten USGS crop categories to the large number of corresponding crop acreage data items in the Census and NASS datasets. For annual crops and hay crops we used ‘harvested acres,’ and for tree crops we used ‘acres bearing & non-bearing.’ These choices were made to maximize data availability and to correspond as closely as possible to the crop acreage from which the pesticide data were derived31. A separate key was developed for California because California pesticide data derives from different source data and covers a larger range of crops.

II)

USGS-CASRN compound key – Using USGS documentation as well as background information on pesticide active ingredients38,41, we generated keys relating USGS active ingredient names to chemical abstracts service (CAS) registry numbers to facilitate matching compounds to the ECOTOX and PPDB databases.

III)

USGS compound-category key – In this key we classified active ingredients into major groups (insecticides, fungicides, nematicides, etc.) and into mode-of-action classes on the basis of information from pesticide databases and resistance action committees38,41,42,43,44.

IV)

USGS-USDA compound key – To facilitate our data validation effort, we generated a key relating USGS compound names to USDA compound names, on the basis of information from several pesticide databases38,41.

V)

USGS-CDL land use-land cover keys – Using documentation from the USGS pesticide dataset describing the crop composition of each of the ten crop categories31, we created a key that matches these categories to land cover classes in the CDL. A separate key was developed for California given the differences in surveyed crops in this state, noted above.

Table 3 Keys generated to relate datasets.Full size tableProcessing crop area dataBecause of differences in the crops included in pesticide use estimates, crop acreage data were processed separately for California and for all other states, and then re-joined, as follows: Acreage data were first filtered to include only data at the state level, reporting total annual acreage for states in the contiguous U.S. after 1996. Acreage data were joined to the appropriate USGS-USDA crop key and only those crops represented in the pesticide dataset were retained. We then generated an acreage dataset with single rows for each combination of crop, state, and year using data from the Census when available (1997, 2002, 2007, 2012, 2017), data from NASS in non-Census years, and temporal interpolation to fill in remaining missing values (i.e. linear interpolation between values in the same state and crop in the nearest surrounding years). This process was repeated for California, using acreage data for only that state in combination with the CA crop key. Finally, acreage data in the two datasets were recombined, converted to hectares, and summed by USGS crop group.Processing honey bee toxicity dataProcessing for the honey bee toxicity data has been described in detail elsewhere21. Briefly, toxicity values were categorized as contact, oral, or other and standardized where possible into µg/bee. Records were retained if they represented acute exposure (4 days or less) for adult bees representing contact or oral LD50 values in µg/bee. To generate a consensus list of contact and oral LD50 values for all insecticides reported in the USGS dataset, we gave preference to point estimates and estimates generated through U.S. or E.U. regulatory procedures, taking a geometric mean if multiple such estimates were available. Unbounded estimates (“greater than” or “less than” some value) were only used when point estimates were unavailable, using the minimum (for “less than”) or the maximum (for “greater than”). If values for a compound were unavailable in both datasets, we used the median toxicity value for the insecticide mode-of-action group. And finally, in rare cases (n = 1/148 compounds for contact toxicity and 8/148 compounds for oral toxicity) we were still left without a toxicity estimate for a particular insecticide. In those cases, we used the median value for all insecticides.Data synthesisCompound-specific application rates for state-crop-year combinationsUSGS data on pesticide application were joined to data on crop area. Average pesticide application rates were calculated by dividing kg applied by crop area (ha) for each combination of compound, crop group, state, and year.Aggregate insecticide application rates for state-crop-year combinationsThe dataset from the previous step was filtered to include only insecticides, and then joined to LD50 data by compound name. Bee toxic load associated with each insecticide active ingredient was calculated by dividing the application rate by the contact or oral LD50 value (µg/bee) to generate a number of lethal doses applied per unit area. These values were then summed across compounds to generate estimates of kg and bee toxic load per ha for combinations of crop group, state, and year.Missing values were estimated using temporal interpolation, where possible (i.e. linear interpolation between values in the same state and crop group in the nearest surrounding years). This dataset ends in 2014 because after that year seed-applied pesticides were excluded from the source data29, and they constitute a major contribution to bee toxic load21.We focused bee toxic load on insecticides for three reasons. First, quality of LD50 data is highest for insecticides and uneven for fungicides and herbicides. Point estimates make up the majority of LD50 values for insecticides, whereas  100 µg/bee”, increasing the uncertainty of downstream estimates). Second, insecticides tend to have greater acute toxicity toward insects than fungicides and herbicides (median [IQR] LD50 = 100 [44–129] µg/bee for fungicides, 100 [75–112] µg/bee for herbicides, and 1.36 [0.16–12] µg/bee for insecticides). As a result, insecticides account for > 95% of bee toxic load nationally, even when herbicides and fungicides are included (and even though insecticides make up only 6.5% of pesticides applied on a weight basis). Third, focusing these values on insecticides increases their interpretability, reflecting efforts directed toward insect pest management, rather than a mix of insect, weed, and fungal pest management (which often have distinct dynamics and constraints for farmers).While we chose to include only insecticides in this aggregate value, users are welcome to adjust the workflow to include fungicides and herbicides if desired. To this end, we provide our best estimates for LD50 values for fungicides and herbicides in the USGS dataset (Table 4).Table 4 Data outputs generated by this study.Full size tableReclassification tablesTo generate reclassification tables for the CDL, the pesticide datasets described above were joined by crop group to CDL land use categories. The output of these processes was a set of reclassification tables for combinations of compound, state, and year. Also generated was a set of reclassification tables for aggregate insecticide use for combinations of state and year.Of the 131 land use categories in the CDL, 16 represent two crops grown sequentially in the same year (double crops, found on ~2% of U.S. cropland in 201245), which required a modified accounting in our workflow. Pesticide use practices on double crops are not well described, but one study suggested that pesticide expenditures on soybean grown after wheat were similar to pesticide expenditures in soybean grown alone46. Therefore, we assumed that pesticide use on double crops would be additive (e.g. for a wheat-soybean double crop, the annual pesticide use estimate was generated by summing pesticide use associated with wheat and soybean).Missing values in the reclassification tables resulted from several distinct issues. Some values were missing because a particular crop was not included in the underlying pesticide use survey (e.g. oats was not included in the Kynetec survey), or because the land use category was not a crop at all (e.g. deciduous forest). These two issues were indicated with values of ‘1’ in columns called ‘unsurveyed’ and ‘noncrop,’ respectively. For double crops, a value of 0.5 in the ‘unsurveyed’ column indicates that one of the crops was surveyed and the other was not. For compound-specific datasets, missing values may reflect that a given compound was not used in a state-crop group-year combination. For the aggregate insecticide dataset, even after interpolation there were some missing values, usually when a state had very little area of a particular crop or crop group.Finally, missing data for double crops were treated slightly differently in the aggregate vs. compound-specific reclassification tables. For the aggregate insecticide dataset, estimates for double crops were only included if estimates were available for both crops; otherwise the value was reported as missing. For the compound-specific datasets, estimates for double crops were included if there was an estimate for at least one of the crops, since specific compounds may be used in one crop but not another. More

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Insect rearingThe B. dorsalis strain collected from a carambola (Averrhoa carambola) orchard in Guangzhou, Guangdong Province, was reared under laboratory conditions (27 ± 1 °C, 12:12 h light:dark cycle, 70–80% RH). A maize-based artificial diet containing 150 g of corn flour, 150 g of banana, 0.6 g of sodium benzoate, 30 g of yeast, 30 g of sucrose, 30 g of paper towel, 1.2 mL of hydrochloric acid and 300 mL of water was used to feed the larvae. Adults were fed a solid diet (consisting of 50 g yeast and 50 g sugar) and 50 mL sterile water in a 35 cm × 35 cm × 35 cm wooden cage. For B. dorsalis, the female will start laying eggs once mated and the female will start mating 7 days after emergence. To make sure all females used in our study were gravid females, females were selected 10 day after emergence.Visualization of CF-BD with FISH and PCRFISH was carried out on dissected gut and ovary samples from B. dorsalis. The hybridization protocol for the gut and ovary was performed according to a previously described method32. Briefly, the gut and ovary were collected and immediately soaked in Carnoy’s fixative for 12 h. After sample fixation, proteinase K (2 mg/mL) treatment for 20 min at 37 °C and HCl (0.2 mol/L) treatment for 15 min at room temperature were performed successively. Then, followed by dehydration in ethanol, the samples were incubated in buffer (20 mM Tris-HCl (pH 8.0), 0.9 M NaCl, 0.01% sodium dodecyl sulfate, 30% formamide) containing 50 nM CF-BD specific probe (5′-AATGGCGTACACAAAGAG-3′) labeled with cy3 at the 5′ end for 90 min. After incubation, the samples were washed with buffer (0.1 M NaCl, 20 mM Tris/HCl (pH 8.0), 5 mM ethylenediaminetetraacetic acid (pH 8.0), 0.01% SDS) and observed under an epifluorescence microscope (Axiophot, Carl Zeiss, Shinjuku-ku, Japan).To further confirm CF-BD in rectum and ovary of mature females, rectums and ovaries of mature females were dissected and fixed in formalin fixation for 24 h. After soaking in graded alcohols and xylene, all samples were embedded in paraffin for section preparation. Samples were sliced into 4 µm each before pasting on the glass slide and then sent for FISH with the same probe (labeled with cy3 at the 5′ end) used above. Moreover, nested PCR was applied to detect CF-BD in 19 ovaries of mature females according to the method of Guo et al., 201733. Briefly, a 1149 bp region of gyrB gene of CF-BD was amplified by the specific outer primer gyrBP1-F (5′-CAGCCCACTCTGAACTGTAT-3′) and gyrBP1-R (5′-TCAGGGCGTTTTCTTCGATA-3′) under a temperature profile of 95 °C for 1 min, which was followed by 25 cycles of 95 °C for 30 s, 52 °C for 30 s, 72 °C for 90 s, and 72 °C for 5 min. Then, a 371 bp region of the gyrB gene of CF-BD was amplified by the specific inner primer gyrBP4-F (5′-ACGCTGGCTGAAGACTGCC-3′) and gyrBP4-R (5′-TGGATAGCGAGACCACGACG-3′) under a temperature profile of 95 °C for 2 min, which was followed by 35 cycles of 95 °C for 30 s, 57 °C for 30 s, 72 °C for 30 s, and 72 °C for 5 min.Influence of CF-BD on B. dorsalis ovary developmentTo evaluate the effect of CF-BD on ovary development, newly emerged B. dorsalis females were injected with streptomycin and CF-BD suspension (both dilute in sterile water). Specifically, 10 µL 25% glycerol solution containing CF-BD was added into 100 mL Luria-Bertani (LB) liquid medium and culturing for 1 day by shaking (180 rpm) in 30 °C incubator. After culturing, CF-BD was collected by centrifuging (3000 rpm, 15 min) the medium in a 50 mL centrifuge tube. Then collected CF-BD was re-suspended with 5 mL sterile water. CF-BD concentration was measured on a hemocytometer and CF-BD concentrations used in the following assays were prepared by diluting the original concentration with sterile water. A 0.5 mm inside diameter capillary needle with 1 μL streptomycin or CF-BD suspension was used for injection. The injection operation was carried out on a microinjector (Eppendorf FemtoJet), and every female was injected in the abdomen near the ovipositor. The concentrations of streptomycin used were 20 mg/mL, 10 mg/mL and 5 mg/mL, respectively. And CF-BD suspension concentrations were 3 × 107 cfu/mL, 1.5 × 107 cfu/mL and 7.5 × 106 cfu/mL, respectively. For control, the female fly was injected with 1 μL sterile water in the abdomen near the ovipositor. Then the development level of the ovary was assessed by comparing the width and length of ovary between streptomycin (or CF-BD suspension) injection flies and control. For CF-BD injected flies, developmental facilitation was observed for ovaries 2 days before the flies reached sexual maturity (flies will reach sexual maturity after 7 days). For antibiotic injected flies, ovaries were dissected after 7 days.Oviposition assaysThe method reported in previous studies was followed for the oviposition experiments17. Briefly, a 2-choice apparatus was assembled in a cage made up of wood and wire gauze (length: width: height = 60 cm: 60 cm: 60 cm) with two petri dishes (diameter: 3 cm) at the bottom of the cage (Fig. 2a). All devices were sterilized before each experiment. Fresh fruits of guava (Psidium guajava Linn.) and mango (Mangifera indica L.) were sourced from the local market in Guangzhou, China. These fruits were sterilized on the surface with ethanol and ground into puree with a sterilized grinder, and puree (2 g) was added to the sterilized Petri dishes of the cages (one dish with puree containing 100 μL CF-BD (0.8*108 cfu/mL) in sterile water, and one dish with puree containing 100 μL sterile water). Then the prepared cages were divided into two groups for different assays. Group 1: At 0 h, 50 gravid females of B. dorsalis were placed in the cages and egg numbers in the petri dishes were recorded after 2 h. Group 2: At 4 h, 50 gravid females of B. dorsalis were placed in the cages and egg numbers in the petri dishes were recorded after 2 h.To test the oviposition attraction of 3-HA, a 4-choice apparatus was assembled in a cage made up of wood and wire gauze (length: width: height = 60 cm: 60 cm: 60 cm) with four petri dishes (diameter: 3 cm) at the bottom of the cage. In the Petri dishes, 2 g puree, 2 g puree + 0.2 mg 3-HA, 2 g puree + 2 mg 3-HA and 2 g puree + 20 mg 3-HA were added. Then, the egg-laying behavior was observed31.To test the oviposition attraction of 3-HA to flies with genes knocked down, 20 females injected with dsRNA were placed into the above cage with two Petri dishes. In the Petri dishes, 2 g guava puree and 2 g guava puree + 20 mg 3-HA were added. Then, the egg-laying behavior was observed using the above method. Oviposition of normally reared females was performed as a control. The oviposition index was calculated using the following formula:Oviposition index = (O − C)/(O + C), where O is the number of eggs in the treatment and C is the number of eggs in the control.Volatile analysisThe volatile compounds in guava and mango purees were analyzed by GC–MS according to the method described in a previous study17. Briefly, 2 g puree mixed with sterile water or CF-BD was added into a 20 ml bottle, and then a 100-μm polydimethylsiloxane (PDMS) SPME fiber (Supelco) was used to extract the headspace volatiles for 30 min. GC–MS was performed with an Agilent 7890B Series GC system coupled to a quadruple-type-mass-selective detector (Agilent 5977B; transfer line 250 °C, source 230 °C, ionization potential 70 eV). The 3-HA concentrations in puree mixed with sterile water and CF-BD were measured with the standard curve drawn by the authentic standards of 3-HA. And 3-HA concentration in puree mixed with sterile water and CF-BD was compared with a paired sample Student’s t-test.Olfactometer bioassaysAn olfactometer consisting of a Y-shaped glass tube with a main arm (20 cm length*5 cm diameter) and two lateral arms (20 cm length, 5 cm diameter) was used. The lateral arms were connected to glass chambers (20 cm diameter, 45 cm height) in which the odor sources were placed. To ensure a supply of odor-free air, both arms of the olfactometer received charcoal-purified and humidified air at a rate of 1.3 L/min.To test the attraction effect of puree supplemented with CF-BD or 3-HA for females, puree mixed with CF-BD was prepared and placed in one odor glass chamber. In the control odor glass chamber, puree mixed with sterile water was placed. After 4 h, gravid females were individually released at the base of the olfactometer and allowed 5 min to show a selective response. The response was recorded when a female moved >3 cm into one arm and stayed for >1 min. Females that did not leave the base of the olfactometer were recorded as nonresponders. Only females that responded were included in the data analysis. Odor sources were randomly placed in one arm or the other at the beginning of the bioassay, and the experiment was repeated ten times. The system was washed with ethanol after every experiment. More than 100 females were selected for testing, and each female was used only once for each odor. A chi-square test was performed to compare the attraction difference between puree mixed with sterile water and CF-BD.Olfactory trap assaysThe attraction of purees supplemented with CF-BD to mature females was also tested. The test chamber was assembled with a plastic cylinder (120 × 30 cm) covered by a ventilated lid. The test chamber contained an odor-baited trap (2 g puree + 100 μL CF-BD (0.8*108 cfu/mL)) and a control trap (2 g puree + 100 μL sterile water). The traps were made of transparent plastic vials (20 × 6 cm) and were sealed with a yellow lid on which small entrances were present to let the flies in (Fig. 3a). After 0 h or 4 h of fermentation, 100 gravid females were released in the cage. The fly number in each trap bottle was recorded after 2 h. The number of flies was compared with a paired sample Student’s t-test.The attraction effect of puree supplemented with 3-HA on mature females was tested by placing four traps (2 g puree, 2 g puree + 0.2 mg 3-HA, 2 g puree + 2 mg 3-HA and 2 g puree + 20 mg 3-HA) in the test chamber. Then, the attraction effect was observed31.Video observation of egg-laying behaviorEgg-laying behavior was observed in a Petri dish. Briefly, guava puree was added to a centrifuge tube on which a hole was made. Then, one gravid female was placed into the petri dish, and the lid was closed. Above the petri dish, a camera was placed to record the behavior of the female before laying eggs.EAG analysisEAG analysis was performed to determine whether 3-HA could elicit electrogram responses in the ovipositors of gravid females and Obps knocked down gravid females. For EAG preparations, the ovipositor of a gravid female was cut off and mounted between two glass electrodes (one electrode connected with the ovipositor tip). The ovipositor tip was cut slightly to facilitate electrical contact. Dilution of 3-HA in ethanol (0.1, 1 and 10 mg/mL) was used as a stimulant. Ethanol was used as control. For each ovipositor, ethanol and 3-HA diluted in ethanol were used as stimulants. The signals from the ovipositors were analyzed with GC-EAD 2014 software (version 4.6, Syntech).Transcriptome sequencing and gene identificationTo identify the olfactory genes that contribute to B. dorsalis oviposition preference, the transcriptome sequencing results of the female ovipositors at different developmental times (0 day, 3 days, 6 days, 9 days and 12 days) were compared. For each time, 5 ovipositors were dissected for RNA extraction. In addition, five replicates were included for each time. In the next step, paired-end RNA-seq libraries were prepared by following Illumina’s library construction protocol. The libraries were sequenced on an Illumina HiSeq2000 platform (Illumina, USA). FASTQ files of raw reads were produced and sorted by barcodes for further analysis. Prior to assembly, paired-end raw reads (uploaded to National Genomics Data Center, Accession number: PRJCA004790) from each cDNA library were processed to remove adapters, low-quality sequences (Q  More

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