Modeling Remobilization of Neonicotinoid Residues from Tree

Article Environmental Science & Modeling re-is published Technology by the American Chemical mobilization ofSixteenth Society. 1155 Street N.W., Washington, neonicotinoid residues DC 20036 Subscriber access provided by University of Published by American Newcastle, Australia Chemical Society. Copyright © American Chemical Society.

from tree foliage in streams – Environmental a relevant Science & Technology is published the American Chemical exposurebypathway Society. 1155 Sixteenth Street N.W., Washington, in risk assessment?

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Dominic Englert, Nikita Bakanov, Jochen Peter Zubrod, Ralf Environmental Science & Schulz, and Mirco Bundschuh Technology is published by the American Chemical

Environ. Sci. Technol., Just Society. 1155 Sixteenth Accepted Manuscript DOI: Street N.W.,• Washington,

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Modeling

neonicotinoid

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residues from tree foliage in streams – a

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relevant exposure pathway in risk assessment?

4

Dominic Englert,†,* Nikita Bakanov,† Jochen P. Zubrod,† Ralf Schulz,† and Mirco Bundschuh‡

5

†

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Fortstraße 7, D-76829 Landau, Germany

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‡

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Sciences, Lennart Hjelms väg 9, SWE-75007 Uppsala, Sweden

Institute for Environmental Sciences, University of Koblenz-Landau, Landau Campus,

Department of Aquatic Sciences and Assessment, Swedish University of Agricultural

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WORD COUNT (limit is 7,000):

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Abstract: 199; MS body: 5.104; Acknowledgments: 76; Description of Supporting

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Information: 94; Figures: 4 x 300; Tables: 1 x 300 Total: 6,973

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ABSTRACT

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Systemic neonicotinoid insecticides are increasingly used as a crop protection measure to

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suppress insect pests on trees. However, senescent foliage falling from treated trees represents

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a rarely studied pathway through which neonicotinoids may enter non-target environments,

17

e.g., surface waters. To estimate risk posed by this pathway, neonicotinoid residues were

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analyzed in foliage from black alder trees treated with one of three neonicotinoid insecticides

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(imidacloprid, thiacloprid, or acetamiprid) at five concentrations, each ranging from 0.0375 –

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9.6 g active ingredient/cm trunk diameter at breast height (n=3). Foliar residues measured at

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the time of leaf fall were used as input parameters for a model predicting imidacloprid water

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concentrations over a 100-m-long stream stretch as a consequence of re-mobilization from

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introduced foliage (input: 600 g foliage/m2 containing 80 µg imidacloprid/g). The water

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concentration (up to ~250 ng/L) predicted by the model exceeded the recently proposed

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Maximum Permissible Concentration of 8.3 ng/L for ~6.5 days. Moreover, dietary uptake was

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identified as an additional exposure route for aquatic organisms. The alternative pathway (i.e.,

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introduction via leaf fall) and exposure route (i.e., dietary uptake) associated with the

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systemic nature of neonicotinoids should be accounted for during their registration process in

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order to safeguard ecosystem integrity.

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INTRODUCTION

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Neonicotinoid insecticides are registered for use in agriculture, horticulture, forestry, and tree

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nurseries in more than 120 countries.1,2 Their success is attributed to their highly selective

34

toxic mode of action in which molecules bind specifically to the nicotinic acetylcholine

35

receptor of insects.3 Moreover, neonicotinoids have replaced older insecticides to which pests

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have developed resistance or are in the process of being withdrawn from the market (e.g.,

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organophosphates1,4). All commercially available neonicotinoids (e.g., imidacloprid (IMI),

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thiacloprid (THI), acetamiprid (ACE)) act – due to their physicochemical properties – as

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systemic insecticides which facilitates their rapid uptake and translocation within plant

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tissues. Given the high persistence of neonicotinoids in some plants (e.g., in eastern hemlock

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trees >7 years after a single IMI application5), they provide long lasting protection against

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herbivorous insects and plant viruses transmitted by these insects.1

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The extensive and often preemptive use of neonicotinoids,6 together with their high water

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solubility (up to 2,950 mg/L for ACE; Table 1) and environmental persistence in soils (e.g.,

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dissipation time (DT50) for IMI up to 1,250 days7) renders these compounds susceptible to

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off-site transport. Throughout the growing season, intense rainfall may wash neonicotinoid

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residues from coated seeds, agricultural soils or plant surfaces while, in northern latitude

48

environments, snowmelt runoff may re-mobilize residues accumulated in soils.8,9 Moreover,

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non-target ecosystems may be contaminated via spray drift or by dust drift during planting of

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neonicotinoid coated seeds.10 Once transported off-site, neonicotinoids can be taken up by

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non-target plants, such as flowers, weeds11-13 and – although not documented thus far – by

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trees growing in the vicinity of argicultural fields. At the same time, trees are increasingly

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being treated – via soil or trunk application – with neonicotinoids in urban areas (i.e., parks)

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as well as natural and planted forests to manage invasive insects. For instance, over 200,000

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eastern hemlock trees received – over a 8 year period – between one and eight IMI treatments


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(of 0.28 to 0.57 g active ingredient per cm trunk diameter at breast height each; AI/cm DBH)

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in the Great Smokey Mountains National Park.14

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During autumn when senecent foliage falls from deciduous trees, neonicotinoids taken up

59

by trees can potentially enter surface waterbodies directly or by lateral movement.15 Once

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submerged, the neonicotinoids can be re-mobilized (via leaching)16 from foliage into their

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surrounding aquatic environment and may lead to direct (e.g., impaired feeding16,17 and

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development18 or reduced survival16) and indirect (e.g., altered predator-prey interaction19)

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ecotoxicological effects in aquatic non-target organisms through both waterborne exposure

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and the consumption of contaminated foliage. Since most published studies in this context are

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limited to one neonicotinoid, namely IMI, a more general understanding about the fate of

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neonicotinoid residues in tree foliage and associated implications on aquatic organisms is not

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available. Given the predicted increased pressures by native and invasive insect pests that may

68

be combated involving neonicotinoids, this general understanding is urgently needed.20

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The aim of the present study was to (i) quantify the foliar residues of three neonicotinoids

70

in foliage of deciduous trees and ultimately (ii) estimate the potential amount of these

71

insecticides that might be re-mobilized in surface waters following an input of contaminated

72

foliage. Therefore, the model tree species Alnus glutinosa (L.) GAERTN. (black alder) was

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treated in early summer by soil drenching with one of three neonicotinoid insecticides –

74

namely IMI, THI and ACE – at different concentrations. At the time of leaf fall (i.e., autumn,

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four months post treatment), foliar neonicotinoid residues were extracted using accelerated

76

solvent extraction (ASE), analyzed with ultra-high performance liquid chromatography-mass

77

spectrometry (UHPLC-MS) and finally compared to environmentally relevant levels found in

78

literature. Though the assessment of differences in uptake and distribution of the

79

neonicotinoids directly after application was beyond the scope of the present study, it was

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hypothesized that neonicotinoid residues in foliage are a function of the applied dose. The

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residue levels of the tested neonicotinoids may, however, differ for the same amount of 4 ACS Paragon Plus Environment


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applied insecticide as a consequence of differing physicochemical properties. The foliar

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residues measured at the highest field-relevant application rate (i.e., 0.6 g AI/cm DBH; using

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IMI as a model substance) finally served as (iii) input parameter for a model predicting worst-

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case waterborne exposure in streams following the input of contaminated foliage and

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subsequent re-mobilization of neonicotinoids from the latter. Therefore, this mostly neglected

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pathway of neonicotinoid entry into aquatic systems – i.e., re-mobilization through leaching

88

from foliage16 – was examined with the ultimate goal to inform environmental risk

89

assessment.

90 91

MATERIAL AND METHODS

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Source of plant material & insecticide application

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Black alder trees were selected as model species as they are widely distributed within riparian

94

zones of temperate Europe21 and may receive neonicotinoids from adjacent agricultural fields

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(as previously shown for flowers11-13). Additionally, they might be treated with neonicotinoids

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directly as some commercially available neonicotinoid products (e.g., Merit®75WP, active

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ingredient (AI): IMI) are registered for use against insect pests that can infest alder trees, such

98

as the alder borer (Rosalia funebris).22 Black alder trees with a mean (±SE) height of 196±2

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cm and a mean (±SE) trunk diameter at breast height (DBH; i.e., 1.3 m above the ground) of

100

7.5±0.2 mm (n=50), were purchased from an ecological tree nursery (Baumschule von der

101

Mühlen, Küsten, Germany) in April 2014. According to the provider, the trees had never been

102

treated with any kind of pesticides or other chemical stressors prior to their use in the present

103

study, and no foliar IMI, THI and ACE residues were detected by our own analytical

104

measurements. All trees were situated in 3-L pots and watered with an automatic tap water

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irrigation system throughout the whole experimental period. At the beginning of June, trees

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were treated by soil drenching with either 500 mL tap water (=control; n=5) or one of the

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three commercially available neonicotinoid insecticides (Confidor®WG70 (70% IMI), 5 ACS Paragon Plus Environment

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Calypso® (40% THI) and Mospilan®SG (20% ACE)) dissolved in 500 mL tap water at one of

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five concentrations (0.0375, 0.15, 0.6, 2.4, 9.6 g AI/cm DBH; n=3; see Table 1). This

110

procedure was used despite recent criticism of this diameter-based dosing approach since it

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still is the manufacturer’s recommended application method.5 Although 0.6 g AI/cm DBH

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equals the maximum amount of IMI recommended for a single soil application on trees,22 two

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intentionally overdose treatments – i.e., 2.4 and 9.6 AI/cm DBH) – were used to allow

114

predictions of foliar residues (using non-linear models; see Calculations and statistics) under

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elevated application doses, which may be required in the future to combat the rising number

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of insect infestations. Stands were placed underneath every pot to prevent unintentional loss

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of the neonicotinoids. Plastic bags covered the pots of each tree to minimize the impact of

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precipitation on applied insecticides and mimic shade conditions of forest floors preventing

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potential photo-degradation on the soil surface.23 During the experimental period (early June

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to early October), environmental temperature ranged from 10.0 to 26.8°C, while daily

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precipitation remained below 17 mm (except for a single event of ~40 mm; Figure S1).

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Shortly before leaf fall in October 2014, tree height and trunk DBH were measured again

123

while the complete foliage of each tree was harvested and weighed on a fresh weight basis.

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Subsequently, all foliage was stored frozen at -20°C in re-sealable zipper storage bags to

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ensure the stability of the three neonicotinoids until further use.24

126 127

Sample preparation and extraction

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Neonicotinoid insecticides were extracted from foliage using an ASE™ 350 Accelerated

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Solvent Extractor system (Thermo Scientific™ Dionex™, Sunnyvale, CA; USA). A cellulose

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filter (Restek GmbH, Bad Homburg, Germany) was placed in a 34 mL stainless steel

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extraction cell (Agilent Technologies, Waldbronn, Germany) together with – depending on

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the neonicotinoid treatment – 0.5 or 3.0 g of previously freeze-dried foliage samples

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comprised of at least 20 leaves each. The cell was then filled with acid-washed, annealed sea 6 ACS Paragon Plus Environment


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sand (Altmann Analytik GmbH & Co. KG, Germany) and covered by another cellulose filter.

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Based on preliminary experiments and literature data25, a 5:1 (v:v) mixture of Milli-Q water

136

(Millipore, Bedford, MA, USA) and acetonitrile (LC-grade; Merck, Darmstadt, Germany)

137

was chosen as extraction solvent. For survey of optimal extraction conditions, two factors

138

were considered, namely the temperature regime (60, 80, 100, 120, and 140°C) and the

139

number of extraction cycles (one, two and four). Optimization experiments were run with

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homogenized foliage samples (n=4) harvested from trees treated with 2.4 g AI/cm DBH.

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Loaded cells were extracted under the following conditions: equilibration period of 5 min

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followed by one to four static cycles of 10 min at a temperature of 60 to 140°C with a rinse

143

volume of 40% and purge time of 30 sec. After centrifugation (at 3,500 rpm for 12 min) for

144

the removal of coarse particles, an aliquot of the foliage extracts was diluted (1:10 or 1:100;

145

v:v) with Milli-Q water and subsequently analyzed by UHPLC-MS.

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For validation of the final extraction method, 0.5 to 3.0 g of freeze-dried blank foliage

147

(n=8) were spiked with 500 µL of a stock containing the three investigated neonicotinoids

148

(analytical standards; Sigma Aldrich, Seelze, Germany) in methanol (LC-grade; Merck,

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Darmstadt, Germany) at a concentration of 20 ng/µL each. After the methanol was completely

150

evaporated, spiked neonicotinoids were extracted from foliage under the conditions described

151

above. Recovery rates (± relative standard deviation) were 109.2% (±10.9) for IMI, 105.0%

152

(±17.6) for THI and 106.8% (±14.0) for ACE. A more detailed assessment regarding methods

153

accuracy and precision is still pending but will be conducted together with future method

154

refinements.

155 156

Chemical analyses

157

Separation of neonicotinoid insecticides from foliage extracts was done with an UHPLC-

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MS equipped with an EQuan MAX system, while for quantification, a single quadrupole mass

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spectrometer equipped with an electrospray ionization source was used. Since deuterated 7 ACS Paragon Plus Environment

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analytical standards for internal calibration were available only for one of the investigated

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analytes, external calibration with matrix-matched standards – prepared out of blank foliage

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extracts – was used to have the same degree of potential matrix effects as in the real samples.

163

Limits of quantification (LOQ) and detection (LOD) were determined for IMI, THI and ACE

164

on a dry weight basis according to DIN standard 32645 and were 0.06, 0.11, 0.12 µg/g and

165

0.02, 0.03, 0.04 µg/g, respectively. Further details are given in the Supporting Information.

166 167

Review of foliar neonicotinoid residues in scientific literature

168

A literature search (using the online database ISI Web of Science; search string:

169

“neonicotinoid* and tree*”) was conducted in order to provide a general overview about

170

relevant neonicotinoid residue levels found in tree foliage to which the present study could be

171

related. References of the retained articles were also inspected for further relevant

172

publications. Only peer-reviewed publications reporting neonicotinoid residues (in leaves or

173

needles/twigs) were selected.

174

compound applied; the respective application dose and method; the studied tree species; the

175

respective days after treatment; as well as the foliar neonicotinoid residue levels (expressed

176

on fresh or dry weight basis) were extracted. Residues reported on fresh weight basis were

177

converted to dry weight basis if conversion factors were available. In situations where the

178

weight basis (fresh vs. dry weight) could not be clearly identified (121 out of 485

179

observations), it was assumed – following a conservative approach – that the concentrations

180

were related to dry weight. Hence, residues reported in this literature review might possibly

181

underestimate actual residue levels. Foliar residues reported as AI per leaf area (e.g., µg/cm2),

182

were not included in our analysis. If studies reported several foliar residues at a given point in

183

time for a single tree – e.g., to account for differences in neonicotinoids’ spatial distribution –

184

the average was calculated and used in our analysis. This approach resulted in a total of 485

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individual neonicotinoid residue levels extracted from 29 different studies (Table S1).

From those studies, information about the neonicotinoid



186 187

Simulation of waterborne neonicotinoid concentrations following the entry of contaminated

188

foliage in a model stream

189

Waterborne neonicotinoid concentrations resulting from the entry of neonicotinoid-

190

contaminated foliage into a model stream (modeled explicitly for 1-m long segments) were

191

simulated using the following equation: ௧ ௧ିଵ ௧ ௧ ௧ ܰ௜,௪௔௧௘௥ = ܰ௜,௪௔௧௘௥ + ܰ௟௘௔௖௛௜௡௚ + ܰ௜,௜௡௙௟௢௪ − ܰ௜,௟௢௦௦

192

௧ where ܰ௜,௪௔௧௘௥ = amount of the neonicotinoid dissolved in stream segment i at time t;

193

Nleaching = amount of the neonicotinoid leaching from submerged foliage into the water phase

194

between t-1 and t; Ni,inflow = amount of the neonicotinoid flowing into the stream section from

195

the adjacent upstream segment (i.e., i-1) between t-1 and t; and Ni,loss = amount of the

196

neonicotinoid lost due to the stream’s discharge between t-1 and t. The resulting value for

197

௧ ܰ௜,௪௔௧௘௥ (ng/stream segment) was then converted to a concentration (ng/L) by adjusting for

198

the stream segments’ volume (m3).

199

௧ The variable ܰ௟௘௔௖௛௜௡௚ is calculated by multiplying the initial amount of neonicotinoid

200

within foliage submerged per stream segment (for details see Supporting Information) with

201

the proportional loss of the neonicotinoid (for every second) from foliage into water. For the

202

present study, this proportional loss was derived from a non-linear model fitted to IMI

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leaching data published for ash leaves (Figure S2).16 It was assumed the leaching dynamics

204

from ash leaves equal those from black alder. If the presented model is to be used with

205

neonicotinoids other than IMI, the determination of a substance-specific leaching factor is

206

required (due to the diverging physicochemical parameters; Table 1). Using IMI – the most

207

common neonicotinoid applied to protect trees – as an example, the model was run using the

208

following parameters: a 100-m long stream stretch with a rectangular cross section (as used

209

during modeling of the European Union’s exposure assessment of pesticides;26 width: 1 m,

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depth: 0.3 m; current velocity: 0.3 m/s; divided into 1-m long segments with a surface area of 9 ACS Paragon Plus Environment

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1 m2) receives an instantaneous input of 600 g foliage/m2 containing 80 µg IMI/g. The

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streams’ current velocity of 0.3 m/s was prompted by average values measured for a second-

213

order stream in southwest Germany (i.e., Triefenbach).27 The amount of foliage used in the

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present scenario equaled ~70% of the annual input reported for a first order stream in central

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Germany,28 thereby accounting for the peak in leaf litter fall during autumn.15 Moreover, the

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initial IMI residue level corresponded to the mean of foliar residues measured in black alder

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trees receiving the highest field-relevant dose of 0.6 g IMI/cm DBH (Figure 1). The amount

218

of foliage was assumed to simultaneously enter the stream, therefore we refer to this scenario

219

as “worst-case” in the remainder of the manuscript. It should be noted, however, that the

220

model predictions are also markedly influenced by other parameters such as the stream

221

characteristics that are considered field relevant. Although, under laboratory conditions, IMI

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rapidly degrades in water through photolysis, these mechanisms are less effective under field

223

conditions.29 The impact of photolysis would clearly be limited in most forest streams shaded

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by riparian trees and shrubs, particularly under the low sunlight intensity during autumn

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leading to aqueous concentrations that can persist for several weeks (reviewed in ref 7).

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Therefore, a potential degradation of IMI within the water phase was not implemented in our

227

model. Further details on the calculations and a full list of parameters used are given in the

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Supporting Information and Table S2. The R script containing the model simulation is also

229

provided.

230 231

Calculations and statistics

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During the extraction method development, measured neonicotinoid residues were checked

233

for significant correlations with extraction temperature using Spearman’s rank correlation.

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Residue data sets were checked for normality by visual inspection, while homoscedasticity

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was tested using Levene’s test. In order to test for statistically significant differences, one-

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way analysis of variance (ANOVA) followed by Tukey tests were applied for neonicotinoid 10 ACS Paragon Plus Environment


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concentrations measured both during extraction method development (i.e., number of

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extraction cycles or temperature as independent variable) as well as from foliage of treated

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black alder trees (i.e., between compounds for each dose applied). A two-way ANOVA

240

(variables: dose and compound) was additionally applied to the combined foliar residue data

241

set. If assumptions for parametric testing (i.e., normal distribution and homogeneity of

242

variance) were violated, non-parametric Kruskal-Wallis tests were employed followed by

243

Nemenyi-Damico-Wolfe-Dunn tests (referred to as Nemenyi test in the remainder of the

244

manuscript; function: kruskalmc implemented in the R package “pgirmess”).30 Moreover,

245

Dunnett’s tests were used to compare the physiological parameters (i.e., trunk DBH, tree

246

height and the amount of foliage produced per tree) of neonicotinoid-treated trees with the

247

untreated control. Treatments that had – as consequence of low tree survival – only a

248

replication of one (i.e., 0.0375 and 9.6 g ACE/cm DBH), were excluded from statistical

249

analyses and instead, effect sizes were reported. Student’s t-tests instead of Tukey tests were

250

consequently applied to compare the remaining residues (i.e., IMI vs. THI) at these

251

treatments.

252

Non-linear dose-concentration models were fitted to each foliar residue data set (i.e., IMI,

253

THI and ACE) using the R extension package “drc”31 in order to predict neonicotinoid dose

254

required to achieve a certain residue level within the trees’ foliage as well as to compare dose-

255

concentration relationships among the different compounds used. Models fitting the data sets

256

best were selected based on the Akaike’s information criterion as well as visual inspection. In

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the following, the term significant(ly) is exclusively used with reference to statistical

258

significance (p < 0.05). For statistics and figures, R version 3.0.0 for Mac was used.32

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RESULTS AND DISCUSSION

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Extraction method development & validation

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During the development of the extraction method, only slight differences (Tukey or Nemenyi

263

test; p ≥ 0.14; n=4) in neonicotinoid residues were observed when foliage from neonicotinoid-

264

treated black alder trees was extracted using one, two, and four extraction cycles of 10 min

265

with a mixture of Milli-Q water and acetonitrile (5:1; v:v; Figure S3). In contrast, extraction

266

temperature had a non-significant (Tukey or Nemenyi test; p ≥ 0.24; n=4; Figure S4) but

267

consistent effect: in general, measured neonicotinoid residues rose with increasing extraction

268

temperature from 60 up to 100°C (Figure S4A). While THI and ACE residues remained

269

relatively stable at temperatures exceeding 100°C, IMI residues markedly declined at 120 and

270

140°C (Spearman’s rho = -0.71, p < 0.01; Figure S4B). A similar IMI decline, supposedly due

271

to thermal degradation, was observed for ASE extraction temperatures exceeding 120°C,

272

while the authors found the optimum temperature to lie between 80 and 100°C.33 Therefore,

273

two 10 min cycles and 100°C were chosen as optimum extraction conditions and confirmed

274

by successful recoveries (i.e., ranging from 105 to 110%; see Materials and Methods). Due to

275

the relatively high foliar neonicotinoid residues found in the present study, purification and

276

concentration of extracts was not necessary. However, a clean-up procedure (e.g., ref 34), that

277

reduces the amount of co-extracts interfering with the UHPLC-MS analysis, might be advised

278

for samples containing lower neonicotinoid residues.

279 280

Foliar neonicotinoid residues in black alder

281

Neonicotinoid treatments in June resulted in measureable foliar residues at the time of leaf fall

282

and thus four months after application (i.e., October), while none of the three neonicotinoids

283

were detected in foliage of control trees. Foliar neonicotinoid residues significantly depended

284

on the dose and compound applied as well as the interaction of these variables (two-factorial

285

ANOVA, p < 0.001), while THI residues were also influenced by the trees’ physiological 12 ACS Paragon Plus Environment


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parameters (see Supporting Information). Among the neonicotinoid compounds (but within

287

the same dose), no statistically significant difference in foliar neonicotinoid residue levels was

288

found for trees treated within field-relevant ranges (i.e., 0.0375, 0.15 and 0.6 g AI/cm DBH;

289

Tukey test or Student’s t-test: p ≥ 0.24; n=2-3), except for the higher IMI residues at 0.15 g

290

AI/cm DBH (compared to THI and ACE; Tukey test: p ≤ 0.03; n=3). Differences were more

291

distinct for overdose treatments (at 2.4 g AI/cm DBH only statistically significant for THI vs.

292

ACE; Tukey test: p = 0.04; n=3; at 9.6 g AI/cm DBH only statistically significant for IMI vs.

293

THI; Student’s t-test: p < 0.001; n=2-3; Figure 1). Observed differences in IMI, THI and ACE

294

residues may, among other reasons, be determined by their physicochemical parameters. For

295

instance, uptake and distribution of neonicotinoids in trees increase with increasing water

296

solubility.35 The solubility of neonicotinoids used in the current study (i.e., ACE > IMI > THI;

297

Table 1) would thus predict foliar residue concentrations in that same order. However, our

298

data showed the uptake of ACE was only higher than the other compounds at the highest

299

treatment level, and THI was markedly higher than IMI at the top two treatment levels (Figure

300

1). This result may, however, be influenced by the fact that only a single tree survived the

301

highest ACE dose until autumn, questioning the reliability of this point estimate. Moreover,

302

foliage biomass produced on this tree was 5-fold lower compared to trees treated with THI

303

and IMI at the same dose (see Supporting Information and Figure S5C). Hence, the total

304

amount of ACE taken up by the trees might have been allocated to a lower biomass of foliage

305

ultimately leading to higher foliar residues. Moreover, trees treated with ACE in the

306

application range of 0.0375 to 2.4 g ACE/cm DBH displayed similar or even lower residue

307

levels compared to IMI and THI at the respective concentration (Figure 1). Considering the

308

long-time span of four months between application and measurement of foliar residues, it is

309

also possible that observed differences result from a diverging degradation behavior (e.g.,

310

depending on the respective half-life times; Table 1) of the parent compounds within the soil

311

and trees. As the trees were irrigated thrice a day, faster degradation of ACE under wet soil 13 ACS Paragon Plus Environment

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312

conditions36 might have degraded ACE into metabolites that can be taken up into the plants

313

along with their parent compound. Such a formation of metabolites (not quantified during the

314

present study) may explain the similar or lower foliar residue levels of ACE compared to IMI

315

and THI (in the application range of 0.0375 to 2.4 g ACE/cm DBH; Figure 1). Additionally

316

the uptake and persistence of neonicotinoids seem to differ between tree species37, thereby

317

potentially limiting the transferability of dose-concentration relationships to other tree

318

species.

319

Overall, black alder trees treated at field-relevant levels of 0.0375 and 0.15 g AI/cm DBH)

320

displayed foliar neonicotinoid residues ranging from 440 ng/g to ~30 µg/g dry weight (Figure

321

1). Despite relatively high foliar residues (i.e., up to ~110 µg/g) measured in alder trees

322

treated at the maximum recommended dose of 0.6 g AI/cm DBH, they did not exceed the

323

upper residue limit found in the 29 reviewed studies, even if residues from overdosed trees

324

were excluded from these analyses (Figure 2). The reviewed studies, however, focused almost

325

exclusively on IMI, while only three investigated dinotefuran in addition to IMI (Table S1).

326

Thus, the present study’s findings constitute a considerable extension of the currently existing

327

knowledge regarding the fate of these insecticides in tree foliage by providing foliar residue

328

data for THI and ACE at field-relevant, as well as overdose, application levels.

329

Moreover, the evaluation of reviewed data indicates higher foliar neonicotinoid residues in

330

deciduous trees treated by trunk application (Figure 3), even though the method uses less

331

substance volume compared to soil application (Figure S6). Comparison of the current study’s

332

neonicotinoid residues (shown in Figure 1) to the distribution of residues found in the

333

literature (for deciduous trees; Figure 3) reveals a higher similarity to those residues achieved

334

by trunk rather than by soil application. This might on one hand be explained by the

335

commonly used constant dosage per unit DBH which overestimates the insecticide dose for

336

relatively small trees (as used throughout the present study) and consequently leads to higher

337

foliar residues.5,38,39 On the other hand, pot stands used to prevent an unintentional 14 ACS Paragon Plus Environment


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338

contamination (i.e., through leaching) of the adjacent environment following application14,40

339

may have extended the neonicotinoids’ residence time in the soil. This might have maximized

340

their uptake into trees, ultimately leading to foliar residue patterns comparable to those

341

usually observed following trunk application.

342

While neonicotinoid leaching from treated soils following (soil) application may result in a

343

rather imminent exposure of the (terrestrial and aquatic) environment, re-mobilization of

344

neonicotinoids from contaminated foliage might take place several months after their actual

345

application. This pathway is particularly relevant to deciduous trees, since they tend to build

346

up higher foliar residues (median: 3.5 µg/g) compared to evergreen species (median: 0.2 µg/g;

347

Figure 3). Moreover, they lose the majority of their foliage (up to ~70% of the annual leaf

348

fall15) during autumn. Downstream transport of neonicotinoids re-mobilized from this foliage

349

might ultimately lead to a potential secondary exposure of downstream habitats during a

350

season of low agricultural neonicotinoid use (e.g., planting of neonicotinoid-coated seeds) and

351

sparse neonicotinoid-occurrences in surface waters arising from the latter.41,42

352 353

Exposure simulation

354

Neonicotinoid-contaminated foliage falling from deciduous trees might enter water bodies

355

directly or by lateral movement.15 Once submerged in the surface water body, this foliage

356

constitutes a potential food source for aquatic macroinvertebrates as well as a source of

357

neonicotinoids leaching into their surrounding environment.16 Under the conditions of our

358

leaching simulation model (i.e., foliar residues of 80 µg/g and large amounts of foliage

359

entering the stream), the maximum concentration in the first 1-m segment was only ~2 ng

360

IMI/L. The water concentration, however, increased due to continued leaching and

361

downstream transport to maximum levels as high as ~250 ng IMI/L 100 m further

362

downstream (reached after ~34 h; Figure 4) and would continue to increase if the stream

363

stretch that receives IMI contaminated foliage was extended (Figure S7). Though the IMI 15 ACS Paragon Plus Environment

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364

concentration slowly declines in the segments where contaminated foliage was introduced

365

during a matter of days (Figure 4), the pesticide is transported to downstream segments,

366

which have not directly received any input of contaminated foliage. In downstream segments

367

that are less shaded by riparian vegetation, IMI concentrations may, depending on the

368

proportion of sunlight transmitted into water, decline due to photolytic degradation.7,43

369

The peak IMI water concentration predicted for the stream parameterized in our worst-case

370

model scenario was above several of the currently existing chronic ecological water quality

371

thresholds describing acceptable levels for neonicotinoids (mostly IMI) in surface waters

372

(reviewed in ref 44). For instance, the lowest thresholds of 8.3 ng IMI/L, recently

373

recommended as an update of the Maximum Permissible Concentration45 in accordance with

374

the European Water Framework Directive, was exceeded for ~6.5 days (Figure 4). Moreover,

375

even the Maximum Acceptable Concentration of 200 ng IMI/L,44 set by the European Food

376

Safety Authority as a threshold for short-term or peak exposure, was briefly exceeded for ~1

377

day (Figure 4).

378

Stream water concentrations calculated by the model would have been markedly lower under

379

scenarios assuming lower amounts of foliage that (simultaneously) enter the water body

380

(Figure S8) or lower internal neonicotinoid residue levels (Figure S9). Under otherwise

381

identical conditions, foliar residues of 3.5 µg IMI/g, which equals the median foliar residue

382

level found in our literature review for deciduous trees (Figure 3), would have resulted in

383

~95% lower maximum water concentrations (~11 ng IMI/L) in the 100th stream segment.

384

Changing the foliage input scenario from a simultaneous input to an input equally distributed

385

throughout autumn would likely predict a low but chronic IMI contamination of the stream

386

ecosystem. Besides these foliage-associated parameters, the water concentration calculated by

387

the model developed during this study strongly depends on stream characteristics. For

388

instance, an extension of the stretch receiving contaminated foliage from 100 to 1000 m

389

would result in a 10-times higher concentration (i.e., ~2.500 ng/L in the 1000th stream 16 ACS Paragon Plus Environment


Page 18 of 37

390

segment; Figure S7). An increase in stream velocity or depth, on the other hand, would cause

391

proportionally lower maximum water concentrations (see Figures S10&S11) while exposure

392

would be worse for streams characterized by a larger width-to-depth-ratio (i.e., >3.33), which

393

is for instance described for many small streams in Germany.46,47

394

While most ecotoxicological studies performed with aquatic macroinvertebrates found

395

adverse effects at concentrations exceeding those predicted by our worst-case model scenario

396

(e.g., reviewed in ref 48), insect nymphs displayed particularly lower effect concentrations

397

(ECx; i.e., in the ng/L-range). Cavallaro et al.49 reported an emergence reduced by 20% (EC20:

398

60 ng/L) and an altered sex ratio (EC20: 110 ng/L) for the Dipteran Chironomus dilutus after a

399

40-day laboratory life-cycle assay with IMI. Another laboratory study derived 28-day EC10-

400

values (immobility) of 24 and 33 ng IMI/L for the mayflies Caenis horaria and Cloeon

401

dipterum.50 Moreover, in two artificial stream mesocosm studies, a 12-h neonicotinoid pulse

402

of 100 ng AI/L reduced the body size of mayflies (Baetis sp. and Epeorus sp. exposed to

403

IMI18) and led to chronic community changes due to adverse effects on a group of sensitive

404

univoltine insect species (consisting of dipterans, ephemeropterans, plecopterans and

405

trichopterans exposed to THI) which showed no recovery during the 2-year post exposure

406

period.51 At higher pulse-concentrations (17.6 µg IMI/L), reductions observed in invertebrate

407

abundance and community diversity were accompanied by a significant reduction in leaf litter

408

decomposition.17 Based on the available literature (e.g., reviewed in ref 52), stream water

409

concentrations >100 ng IMI/L predicted by our model scenario for >2 days could put

410

sensitive aquatic invertebrates at risk.

411

In addition to neonicotinoid water concentrations predicted by our simulation, another risk

412

for aquatic organisms might arise from the neonicotinoid-contaminated foliage directly (i.e.,

413

via dietary exposure). Despite IMI’s high water solubility (Table 1), it can be found in

414

submerged foliage for several days following their input into the water body (cf. ref 16) with

415

simulated IMI retention times (RT) of RT50: ~1.9 and RT10: ~4.5 days (Figure 4). Organisms 17 ACS Paragon Plus Environment

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416

designated to the functional group of shredders heavily depend on allochthonous organic

417

matter (such as the introduced foliage) as a food source53 and are, therefore, likely to face

418

neonicotinoid exposure via their diet. However, information about adverse effects on aquatic

419

organisms following dietary exposure towards neonicotinoid-contaminated foliage is scarce,

420

except for the work published by Kreutzweiser et al.16,24,54. In these studies, the authors

421

observed reduced feeding and increased mortality in two aquatic insects, the stonefly

422

Pteronarcys dorsata and the crane fly Tipula sp., when exposed to foliage characterized by

423

IMI-residues between 5.6 and 346 µg/g.16,24 Since these insects were unable to detect and

424

avoid contaminated foliage,54 detrimental effects for aquatic leaf-feeding invertebrates and

425

ecosystem functioning might be expected.

426 427

In conclusion, the present study indicates that neonicotinoid treatment of deciduous trees

428

leads, even at field-relevant application rates, to high foliar residues that can ultimately be

429

released into aquatic environments following autumn leaf fall. Aquatic organisms may display

430

direct (e.g., impaired feeding16,17 and development18 or reduced survival16) and indirect (e.g.,

431

altered predator-prey interaction19) ecotoxicological effects if they are exposed to

432

neonicotinoids leaching from foliage into the water phase – as predicted by our model – or via

433

the consumption of contaminated foliage.16 The relevance of these exposure pathways might

434

become more important in the future as an increasing impact of native and invasive pests,

435

predicted under current climate change scenarios,20 will most likely be accompanied by an

436

intensified utilisation of chemical control agents (such as neonicotinoid insecticides) as

437

countermeasures. Thus, it would be prudent to account for these alternative exposure

438

pathways (e.g., aqueous concentrations in water bodies leached from contaminated foliage)

439

and exposure routes (e.g., dietary uptake through consumption of contaminated foliage)

440

during systemic insecticide registration processes to safeguard ecosystem integrity.



Page 20 of 37

441 442

FIGURES

443

Figure 1. Mean (±SE) residues of IMI (), THI () and ACE () measured in foliage from

444

treated black alder trees as well as the best fitting models (IMI: dot-dashed line; THI: dotted

445

line; ACE: dashed line). The inset displays the residues measured in the 0 to 200-µg/g range

446

in greater detail. Open symbols above error bars indicate significant differences (p < 0.05;

447

n=2-3) between neonicotinoid compounds (i.e., compared to IMI (), THI () or ACE (☐),

448

respectively) within the same dose applied. Missing SEs indicate a replication of only one.

449 450

Figure 2. Foliar IMI (black solid circles) and dinotefuran (gray solid circles) residues derived

451

from a literature review of peer-reviewed publications as well as IMI (), THI () or ACE (

452

☐) residues measured in alder foliage during the present study. A gray cross additionally

453

indicates foliar residues derived from trees treated above the maximum dose recommended

454

for soil application (i.e., 0.6 g IMI and 0.95 g dinotefuran/cm DBH) or trunk injection (i.e.,

455

0.25 g IMI).

456 457

Figure 3. Bean plots displaying the density trace (black and gray area) of the individual

458

neonicotinoid residues (small white lines) derived from a literature review of peer-reviewed

459

publications. Residue data is itemized by deciduous and evergreen trees as well as by soil and

460

trunk application. Black solid lines represent the median of the respective sub-group. Gray

461

dashed lines indicate the overall median for deciduous and evergreen trees respectively.

462 463 464

Figure 4. Modeled IMI concentration (solid line) in the water phase of the 100th stream

465

segment including the peak IMI concentration () as well as the lowest IMI threshold level of

466

8.3 ng/L (i.e., maximum permissible concentration;45 dashed line). Moreover, the total 19 ACS Paragon Plus Environment

Page 21 of 37


467

amount of IMI in foliage (dotted line; within each stream segment; surface area: 1 m2)

468

following a simulated input of 600 g foliage/m2 with an initial residue level of 80 µg IMI/g as

469

well as corresponding retention times (RT50: and RT10: ) are also displayed.

470 471



Page 22 of 37

472

TABLES

473

Table 1. Information about commercial products applied to black alder trees as well as the

474

physicochemical parameters, leaching properties and environmental persistence of their active

475

ingredient. Active ingredient

Imidacloprid (IMI)

Thiacloprid (THI)

Acetamiprid (ACE)

Product name

Confidor® WG 70

Calypso®

Mospilan®SG

Supplier

Bayer CropScience

Bayer CropScience

Cheminova Deutschland GmbH

Concentration of the active ingredient within the product

700 g/kg

480 g/L

200 g/kg

Molecular Mass (g/mol)55

255.66

252.72

222.67

Solubility in Water at 20°C (mg/L)55

610 (high)

184 (moderate)

2950 (high)

Octanol/Water partition coefficient (log Pow)55

0.57

1.26

0.8

GUS Leaching Potential Index56

3.76 (high)

1.44 (low)

0.94 (very low)

Soil Persistence (DT50 in days)7

100 - 1250

3.4 - >1000

31 - 450

Aqueous Photolysis (DT50 in days)55

0.2 (fast)

(stable)

(stable)

Water Hydrolysis (DT50 in days)55

>365 (at pH 9; 25°C; stable)

stable (pH 5 to pH 9)

420 (at pH 9; 25°C; stable)

476 477


Page 23 of 37


478

ASSOCIATED CONTENT

479

Supporting Information

480

The Supporting Information associated with this article contains information about the

481

environmental temperature and precipitation throughout the experimental period, details

482

regarding chemical analyses, a list of studies used to derive the literature review, details on

483

the model calculations as well as results of the development of the extraction method and

484

physiological tree parameters. Moreover, further information derived from the literature

485

review and illustrations of different model scenarios are provided together with the R code for

486

computation of the model simulation. This material is available free of charge via the Internet

487

at http://pubs.acs.org.

488 489

AUTHOR INFORMATION

490

Corresponding Author

491

*Dominic Englert

492

Institute for Environmental Sciences

493

University of Koblenz Landau

494

Fortstraße 7

495

76829 Landau/Palatinate

496

Germany

497

Phone: (+49) 6341 280 31324

498

Fax:

499

Email: [email protected]

(+49) 6341 280 31326

500



Page 24 of 37

501

Author Contributions

502

Idea and study design D.E., R.S. and M.B.; performance of experiment: D.E. and J.P.Z.;

503

insecticide extraction and quantification: D.E. and N.B.; model development and data

504

analysis: D.E. and J.P.Z. manuscript drafting: D.E. and M.B.; manuscript revision: all.

505 506

Funding Sources

507

D.E. received funding through a scholarship of the German Federal Environmental

508

Foundation (Deutsche Bundesstiftung Umwelt). Moreover, this study was partly funded by

509

the German Research Foundation (DFG; grant number: SCHU 2271/13-1 and SCHA 1720-

510

11/1).

511 512

Notes

513

The authors declare no competing financial interest.

514 515

ACKNOWLEDGMENT

516

The authors thank P. Baudy, T. Bürgi, K. Kenngott, M. Konschack, M. Link and N. Röder

517

for assistance in the field and laboratory, M. Moore for language editing as well as D. P.

518

Kreutzweiser for the provision of some raw data. D.E. received funding through a scholarship

519

of the German Federal Environmental Foundation (Deutsche Bundesstiftung Umwelt).

520

Moreover, this study was partly funded by the German Research Foundation (DFG; grant

521

number: SCHU 2271/13-1 and SCHA 1720-11/1).

522


Page 25 of 37


523

ABBREVIATIONS

524

ACE, acetamiprid; AI, active ingredient; ASE, accelerated solvent extraction; DBH, trunk

525

diameter at breast height; DT, dissipation time; EC, effect concentration; IMI, imidacloprid;

526

RT, retention time; SE, standard error; THI, thiacloprid; UHPLC-MS, ultra-high performance

527

liquid chromatography-mass spectrometry;

528



529

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Figure 1

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foliar neonicotinoid residues (µg/g)

Page 35 of 37


1000 100 10 1 0.1 0.01

0.001 1

10 Figure 2


100

days after treatment

1000


Page 36 of 37

foliar neonicotinoid residues (µg/g)

10000

1000

100

trunk

10

1

soil soil

0.1

trunk 0.01

0.001

0.0001

evergreen trees


deciduous trees Figure 3

Page 37 of 37



Figure 4

Modeling Remobilization of Neonicotinoid Residues from Tree

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