Imidacloprid exposure is detectable in over one third of wild bird samples from diverse Texas ecoregions

Abstract

Avian decline is occurring globally with neonicotinoid insecticides posed as a potentially contributing factor. Birds can be exposed to neonicotinoids through coated seeds, soil, water, and insects, and experimentally exposed birds show varied adverse effects including mortality and disruption of immune, reproductive, and migration physiology. However, few studies have characterized exposure in wild bird communities over time. We hypothesized that neonicotinoid exposure would vary temporally and based on avian ecological traits. Birds were banded and blood sampled at eight non-agricultural sites across four Texas counties. Plasma from 55 species across 17 avian families was analyzed for the presence of 7 neonicotinoids using high performance liquid chromatography-tandem mass spectrometry. Imidacloprid was detected in 36 % of samples (n = 294); this included quantifiable concentrations (12 %; 10.8-36,131 pg/mL) and concentrations that were below the limit of quantification (25 %). Additionally, two birds were exposed to imidacloprid, acetamiprid (18,971.3 and 6844 pg/mL) and thiacloprid (7022.2 and 17,367 pg/mL), whereas no bird tested positive for clothianidin, dinotefuran, nitenpyram, or thiamethoxam, likely reflecting higher limits of detection for all compounds compared to imidacloprid. Birds sampled in spring and fall had higher incidences of exposure than those sampled in summer or winter. Subadult birds had higher incidences of exposure than adult birds. Among the species for which we tested more than five samples, American robin (Turdus migratorius) and red-winged blackbird (Agelaius phoeniceus) had significantly higher incidences of exposure. We found no relationships between exposure and foraging guild or avian family, suggesting birds with diverse life histories and taxonomies are at risk. Of seven birds resampled over time, six showed neonicotinoid exposure at least once with three showing exposures at multiple time points, indicating continued exposure. This study provides exposure data to inform ecological risk assessment of neonicotinoids and avian conservation efforts.

Keywords: Ecotoxicology; Insecticide; Liquid chromatography-tandem mass spectrometry (LC-MS/MS); Neonicotinoid; Pesticide; Temporal analysis.

Figure 1.

A) The estimated agricultural use for imidacloprid, the most widely-used neonicotinoid, in the Texas based on 2019 data (lowest estimate; USGS, 2021). notably, this map and others created after 2015 do not include estimates for seed treatment applications. White circles indicate counties of sampling. B) Four counties of sample collection (white circles) atop the Texas Ecoregions (Wilkins et al., 2003).

Fig 2:

Sample pooling was necessary in some cases to reach the required volume of 50 μL for this method. In such cases, and as shown in the schematic above, plasma from birds that met the pooling criteria were pooled into one sample. In some cases, we used extra plasma from a bird that had previously been tested individually and assigned an unexposed (ND) status to pool with a bird of unknown status, thereby diluting the unknown bird plasma with known negative plasma. In other cases, plasma from two birds of unknown status were pooled together (Created with BioRender).

Figure 3:

Quantified concentrations of each of three compounds (acetamiprid, n=2; imidacloprid, n=35; thiacloprid, n=2) detected in avian plasma. Inset shows proportion of total samples (n=294) in each outcome; ND is no detection,

Figure 4:

Incidence of exposure to neonicotinoids by season, sex, age, foraging guild, and migratory status. Data points represent incidence of exposure at each level. Lines represent a 95% confidence interval estimated from a predictive model. “*” denotes a significance at p value ≤0.05, “**” at P<0.01, and “***” at P<0.001. Sp, Su, Fa, Wi signify spring, summer, fall, and winter respectively; F, M, U stand for female, male, and unknown sexes; Ad, Subad, and U refer to adult, subadult, and unknown ages; Frug, Gran, Insect, and Omni denote the foraging guilds frugivore, granivore, insectivore, and omnivore; Mig, Res, U stand for migratory, resident, and unknown migratory statuses.

Figure 5:

Incidence of exposure for all avian species for which more than 5 samples were tested. Data points represent incidence of exposure per species with lines representing the 95% confidence interval estimated using a predictive model; for two species, swamp sparrow and bronzed cowbird, confidence intervals could not be estimated, as all samples tested were negative (See Supplemental Materials “SM” Table 1). The vertical line represents the average percent exposure across all samples. Species with significant relationships (red-winged blackbird and American robin) are designated with species icons “*” denotes species significance compared to the mean positivity rate of all sampled species and refers to a p value <0.05; “**” denotes a p value < 0.01.

Figure 6:

Neonicotinoid exposure over time in individual birds that were recaptured at a Brazos County site, Ecological and Natural Resource Teaching Area. Individuals are shown in different colors over time, and neonicotinoid exposure is shown as a binomial on the y axis; the only compound detected was imidacloprid. †Two Carolina wrens and one swamp sparrow which were analyzed as part of a pool at one time point.