Continuing Persistence and Biomagnification of DDT and Metabolites in Northern Temperate Fruit Orchard Avian Food Chains

Abstract

Dichlorodiphenyldichlorethane (1,1,1-trichloro-2,2-bis(p-chlorophenyl)ethane) (DDT) is an organochlorine insecticide that was widely used from the late 1940s to the 1970s in fruit orchards in the Okanagan valley, British Columbia, Canada, and in the process, contaminated American robin (Turdus migratorius) food chains with the parent compound and metabolite dichlorodiphenyldichloroethylene (1,1-dichloro-2,2-bis(4-chlorophenyl)ethylene) (p,p′-DDE). In the present study, we examined the biological fate of these DDT-related (DDT-r) compounds at the same sites/region 26 years after a previous study by: (1) collecting soil, earthworms, and American robin eggs from apple, cherry, and pear orchards; (2) characterizing the diet and trophic positions of our biota using stable isotope analyses of δ 13 C and δ 15 N; and (3) estimating fugacity, biota-soil-accumulation factors (BSAFs), and biomagnification factors (BMFs). Mean p,p′-DDE concentrations (soil: 16.1 µg/g organic carbon-lipid equivalent; earthworms: 96.5 µg/g lipid equivalent; eggs: 568 µg/g lipid equivalent) revealed that contamination is present at elevated levels similar to the 1990s and our average soil DDE:DDT ratio of 1.42 confirmed that DDT is slowly degrading. American robins appeared to feed at similar trophic levels, but on different earthworms as indicated by egg stable isotope values (mean δ 15 N = 8.51‰ ± 0.25; δ 13 C = −26.32‰ ± 0.12). Lumbricidae and Aporrectodea worms shared a roughly similar δ 15 N value; however, Lumbricus terrestris showed a markedly enriched δ 13 C isotope, suggesting differences in organic matter consumption and physiological bioavailability. Biota-soil-accumulation factors and BMFs ranged over several orders of magnitude and were generally >1 and our fugacity analyses suggested that p,p′-DDE is still thermodynamically biomagnifying in American robin food chains. Our results demonstrate that DDT-r in fruit orchards remains bioavailable to free-living terrestrial passerines and may pose a potential toxicological risk.

Bluebirds Experience Impaired Hatching Success in Conventionally Sprayed Apple Orchard Habitats: A 31‐Year Study

“…Although those studies were conducted in the 1990s and early 2000s, more recent data indicate that p,p ′‐DDE persists at elevated concentrations in birds nesting in apple orchards in Canada (Kesic et al, 2021). In apple, cherry, and pear orchards in the Okanagan valley of British Columbia, p,p ′‐DDE detected in American robin eggs collected in 2019 remains at relatively high concentrations (mean 36.6 μg/g, range 3.28–107 μg/g) in eggs collected from study orchards which historically applied organochlorine pesticides including DDT (Harris et al, 2000; Kesic et al, 2021).…”

“…Although those studies were conducted in the 1990s and early 2000s, more recent data indicate that p,p ′‐DDE persists at elevated concentrations in birds nesting in apple orchards in Canada (Kesic et al, 2021). In apple, cherry, and pear orchards in the Okanagan valley of British Columbia, p,p ′‐DDE detected in American robin eggs collected in 2019 remains at relatively high concentrations (mean 36.6 μg/g, range 3.28–107 μg/g) in eggs collected from study orchards which historically applied organochlorine pesticides including DDT (Harris et al, 2000; Kesic et al, 2021). The concentrations measured in the mid‐1990s in Okanagan valley orchards (approximately 2‐fold higher than 2019 levels) were correlated with adverse effects on growth and brain development in American robins (Iwaniuk et al, 2006), close relatives of eastern bluebirds, belonging to the same family, Turdidae, and similarly feeding on ground‐dwelling invertebrates (Gowaty & Plissner, 2020; Vanderhoff et al, 2016).…”

“…Sublethal and lethal neurotoxic effects have occurred in songbirds exposed to azinphos‐methyl in agricultural habitats (Graham & DesGranges, 1993; Grue et al, 1997) including depression of cholinesterase in eastern bluebirds (Burgess et al, 1999) in the orchard study sites of the present study. Moreover, organochlorine pesticides including dichlorodiphenyltrichloroethane (DDT) were also used from the late 1940s until the early 1970s in apple orchards in Canada and were measured at concentrations >100 µg/g (wet wt) in eastern bluebird eggs in the 1990s (Bishop et al, 2000) and in American robin ( Turdus migratorius ) eggs as recently as 2019 (Kesic et al, 2021).…”

More than mortality: Consequences of human activity on migrating birds extend beyond direct mortality

“…All of the insecticide classes described here have the dose-dependent potential to be immediately lethal to birds, but sublethal effects can also occur depending on the exposure concentration, length of exposure, and other factors (Lopez-Antia et al 2013, Mitra et al 2011). Insecticide residues and metabolites can bioaccumulate in birds (Mora et al 1987, Lopez-Antia et al 2015, Kesic et al 2021) and may be mobilized from the catabolism of tissues during physically rigorous activities like migration (Tanaka et al 1986, Colabuono et al 2012). Some insecticides may impact neurological development and function (Iwaniuk et al 2006) or cause appetite suppression and anorexia (Grue 1982, Elliott and Bishop 2011, Lopez-Antia et al 2013), potentially delaying migration through reduced refueling.…”