Abstract
The extensive use of insecticides can cause adverse side effects on pollinators, which negatively impact crop productivity. The pollination carried out by the honeybee Apis mellifera L. (Hymenoptera: Apidae) is crucial in increasing the productivity of the melon (Cucumis melo L.). The main objective of this study was to assess if insecticides applied in the cultivation of cantaloupe melon exhibit significant levels of toxicity toward A. mellifera. We tested the toxicity of azadirachtin, pyriproxyfen, chlorantraniliprole, and imidacloprid, which are commonly sprayed to manage melon pests such as the whitefly Bemisia tabaci (Genn.) (Hemiptera: Aleyrodidae), the pickleworm Diaphania nitidalis (Stoll) and the melonworm Diaphania hyalinata (L.) (Lepidoptera: Pyralidae). Three treatments were carried out, 0.0×, 0.1x and 1.0x the concentration recommended by the manufacturer for the control of those pests. Repellency tests, analysis of mortality through contact and ingestion, and flight tests were performed. The insecticide imidacloprid caused mortality rates above 90% in all tested exposure pathways, displaying high residue persistence on plants. Although not causing significant mortality in the ingestion test, pyriproxyfen caused significant mortality after exposure through contact, and change in flight ability. Azadirachtin caused mortality in the ingestion test and impaired the flight ability of bees, while chlorantraniliprole only impaired the flight ability. Moreover, bees were not repelled by these insecticides, suggesting that they may collect contaminated food in the field while foraging. Altogether, ecofriendly, alternative pest control options should be developed, as well as the adoption of more selective insecticides, in order to reduce the non-target effects on honeybees and guarantee their pollination services.
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References
Aktar MW, Sengupta D, Chowdhury A (2009) Impact of pesticides use in agriculture: their benefits and hazards. Interdisc Toxicol 2:1–12. https://doi.org/10.2478/v10102-009-0001-7
Barbosa WF, Meyer L, Guedes RNC, Smagghe G (2015) Lethal and sublethal effects of azadirachtin on the bumblebee Bombus terrestris (Hymenoptera: Apidae). Ecotoxicology 24:130–142. https://doi.org/10.1007/s10646-014-1365-9
Biddinger DJ, Robertson JL, Mullin C, Frazier J, Ashcraft SA, Rajotte EG, Joshi NK, Vaughn M (2013) Comparative toxicities and synergism of apple orchard pesticides to Apis mellifera (L.) and Osmia cornifrons (Radoszkowski). PLoS ONE 8(9):e72587. https://doi.org/10.1371/journal.pone.0072587
Biesmeijer JC, Roberts SPM, Reemer M, Ohlemuller R, Edwards M, Peeters T, Schaffers AP, Potts SG, Kleukers R, Thomas CD, Settele J, Kuni WE (2006) Parallel declines in pollinators and insect pollinated plants in Britain and the Netherlands. Science 313:351–354. https://doi.org/10.1126/science.1127863
Biondi A, Zappalà L, Stark JD, Desneux N (2013) Do biopesticides affect the demographic traits of a parasitoid wasp and its biocontrol services through sublethal effects? PLoS ONE 8(9):e76548. https://doi.org/10.1371/journal.pone.0076548
Biondi A, Mommaerts V, Smagghe G, Viñuela E, Zappalà L, Desneux N (2012a) The non-target impact of spinosyns on beneficial arthropods. Pest Manag Sci 68:1523–1536
Biondi A, Desneux N, Siscaro G, Zappalà L (2012b) Using organic-certified rather than synthetic pesticides may not be safer for biological control agents: Selectivity and side effects of 14 pesticides on the predator Orius laevigatus. Chemosphere 87:803–812
Bleicher E, Gonçalves MEC, Silva L (2007) Efeito de derivados de nim aplicados por pulverização sobre a mosca-branca em meloeiro. Horticultura Brasileira 25:110–113. https://doi.org/10.1590/s0102-05362007000100022
Bortolott L, Montanari R, Marcelino J, Medrzycki P, Maini S, Porrini C (2003) Effects of sub-lethal imidacloprid doses on the homing rate and foraging activity of honey bees. Bull Insectol 56:63–67
Brittain C, Potts SG (2011) The potential impacts of insecticides on the life-history traits of bees and the consequences for pollination. Basic Appl Ecol 12:321–331. https://doi.org/10.1016/j.baae.2010.12.004
Brittain CA, Vighi M, Bommarco R, Settele J, Potts SG (2010) Impacts of a pesticide on pollinator species richness at different spatial scales. Basic Appl Ecol 11:106–115. https://doi.org/10.1016/j.baae.2009.11.007
Chauzat MP, Faucon JP, Martel AC, Lachaize J, Cougoule N, Aubert MA (2006) Survey of pesticide residues in pollen loads collected by honey bees in France. J Econ Entomol 99:253–262. https://doi.org/10.1603/0022-0493-99.2.253
Chen YW, Wu PS, Yang EC, Nai YS, Huang ZY (2016) The impact of pyriproxyfen on the development of honey bee (Apis mellifera L.) colony in field. J Asia-Pac Entomol 19:589–594. https://doi.org/10.1016/j.aspen.2016.06.005
Córdova D, Benner EA, Sacher MD, Rauh JJ, Sopa JS, Lahm GP, Selby TP (2006) Anthranilic diamides: a new class of insecticides with a novel mode of action, ryanodine receptor activation. Pestic Biochem Physiol 84:196–214. https://doi.org/10.1016/j.pestbp.2005.07.005
Costa EM, Araujo EL, Maia AVP, Silva FEL, Bezerra CES, Silva JG (2013) Toxicity of insecticides used in the Brazilian melon crop to the honey bee Apis mellifera under laboratory condition. Apidologie 45:34–44. https://doi.org/10.1007/s13592-013-0226-5
Decourtye A, Lacassie E, Pham-Delegue M (2003) Learning performances of honeybees (Apis mellifera L) are differentially affected by imidacloprid according to the season. Pest Manag Sci 59:269–278. https://doi.org/10.1002/ps.631
Decourtye A, Armengaud C, Renou M, Devillers J, Cluzeau S, Gauthier M, Pham-Delegue M (2004a) Imidacloprid impairs memory and brain metabolism in the honeybee (Apis mellifera L.). Pestic Biochem Physiol 78:83–92. https://doi.org/10.1016/j.pestbp.2003.10.001
Decourtye A, Devillers J, Cluzeau S, Charreton M, Pham-Deleguea M (2004b) Effects of imidacloprid and deltamethrin on associative learning in honeybees under semi-field and laboratory conditions. Ecotoxicol Environ Saf 57:410–419. https://doi.org/10.1016/j.ecoenv.2003.08.001
de Paiva ACR, Beloti VH, Yamamoto PT (2018) Sublethal effects of insecticides used in soybean on the parasitoid Trichogramma pretiosum. Ecotoxicology 27:448–456
Desneux N, Decourtye A, Delpuech JM (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106. https://doi.org/10.1146/annurev.ento.52.110405.091440
Dively GP, Kamel A (2012) Insecticide residues in pollen and nectar of a cucurbit crop and their potential exposure to pollinators. J Agric Food Chem 60:4449–4456. https://doi.org/10.1021/jf205393x
Efrom CFS, Redaelli LR, Meirelles RN, Ourique CB (2012) Side-effects of pesticides used in the organic system of production on Apis mellifera Linnaeus, 1758. Braz Arch Biol Technol 55:47–53. https://doi.org/10.1590/s1516-89132012000100005
Environmental Protection Agency [EPA], USA. 2014. Pesticides: Regulating Pesticides. Washington, DC, US EPA. cited 19 July 2014. http://www.epa.gov/opprd001/workplan/reducedrisk.html
Fairbrother A, Anderson T, Fell R (2014) Risks of neonicotinoid insecticides to honeybees. Environ Toxicol Chem 33:719–731. https://doi.org/10.1002/etc.2527
FAO (2016) Food and Agriculture Organization of the United Nations. Food and agriculture data. (http://www.fao.org/home/en/). Accessed 28 Oct 2016
Fernandez FC, Da Cruz-Landim C, Malaspina O (2012) Influence of the insecticide pyriproxyfen on the flight muscle differentiation of Apis mellifera (Hymenoptera, Apidae). Microsc Res Tech 75:844–848. https://doi.org/10.1002/jemt.22003
Fischer J, Müller T, Spatz AK, Greggers U, Grünewald B, Menzel R (2014) Neonicotinoids interfere with specific components of navigation in honeybees. PLoS ONE 9(3):e91364. https://doi.org/10.1371/journal.pone.0091364
Fourrier J, Deschamps M, Droin L, Alaux C, Fortini D, Beslay D, Decourtye A (2015) Larval exposure to the juvenile hormone analog pyriproxyfen disrupts acceptance of and social behavior performance in adult honeybees. PLOS ONE 10(7):e0132985. https://doi.org/10.1371/journal.pone.0132985
Gentz MC, Murdoch G, King GF (2010) Tandem use of selective Insecticides and natural enemies for effective, reduced-risk pest management. Biol Control 52:208–215. https://doi.org/10.1016/j.biocontrol.2009.07.012
Giannini TC, Boff S, Cordeiro GD, Cartolano Jr EA, Veiga EAK, Imperatriz-Fonseca VL, Saraiva AM (2014) Crop pollinators in Brazil: a review of reported interactions. Apidologie 46:209–223. https://doi.org/10.1007/s13592-014-0316-z
Giannini TC, Cordeiro GD, Freitas BM, Saraiva AM, Imperatriz-Fonseca VL (2015) The dependence of crops for pollinators and the economic value of pollination in Brazil. J Econ Entomol 108:849–857. https://doi.org/10.1093/jee/tov093
Gill RJ, Ramos-Rodriguez O, Raine NE (2012) Combined pesticide exposure severely affects individual and colony-level traits in bees. Nature 491:105–108. https://doi.org/10.1038/nature11585
Gontijo LM, Celestino D, Queiroz OS, Guedes RNC, Picanço MC (2015) Impacts of azadirachtin and chlorantraniliprole on the developmental stages of pirate bug predators (Hemiptera: Anthocoridae) of the tomato pinworm Tuta absoluta (Lepidoptera: Gelechiidae). Fla Entomol 98:59–64. https://doi.org/10.1653/024.098.0111
Gradish AE, Scott-Dupree CD, Shipp L, Harris CR, Ferguson G (2009) Effect of reduced risk pesticides for use in greenhouse vegetable production on Bombus impatiens (Hymenoptera: Apidae). Pest Manag Sci 66:142–146. https://doi.org/10.1002/ps.1846
Guedes RNC, Smagghe G, Stark JD, Desneux N (2016) Pesticide induced stress in arthropod pests for optimized integrated pest management programs. Annu Rev Entomol 61:43–62
Han P, Niu CY, Biondi A, Desneux N (2012) Does transgenic Cry1Ac + CpTI cotton pollen affect hypopharyngeal gland development and midgut proteolytic enzyme activity in the honey bee Apis mellifera L. (Hymenoptera, Apidae)? Ecotoxicology 21:2214–2221
Henry M, Béguin M, Requier F, Rollin O, Odoux JF, Aupinel P, Aptel J, Tchamitchian S, Decourtye A (2012) A Common Pesticide Decreases Foraging Success and Survival in Honey Bees. Science 336:348–350. https://doi.org/10.1126/science.1215039
IBGE 2016 Instituto Brasileiro de Geografia e Estatística. Produção Agrícola Municipal. Sistema IBGE de Recuperação Automática –SIDRA. https://sidra.ibge.gov.br/tabela/1612. Accessed 21 Nov 2016
IPBES 2016 The assessment report of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services on pollinators, pollination and food production. https://www.ipbes.net/assessment-reports/pollinators. Accessed 18 Oct 2016
Ishaayat I, Horowitz AR (1995) Pyriproxyfen, a novel insect growth regulator for controlling whiteflies: mechanisms and resistance management. Pestic Sci 43:227–232. https://doi.org/10.1002/ps.2780430308
Isman M (2006) Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annu Rev Entomol 51:45–66. https://doi.org/10.1146/annurev.ento.51.110104.151146
Jan NA, Saber M (2018) Sublethal effects of imidacloprid and pymetrozine on the functional response of the aphid parasitoid, Lysiphlebus fabarum. Entomol Generalis 38:173–190
Kasiotis KM, Anagnostopoulos C, Anastasiadou P, Machera K (2014) Pesticide residues in honeybees, honey and bee pollen by LC–MS/MS screening: Reported death incidents in honeybees. Sci Total Environ 485-486:633–642. https://doi.org/10.1016/j.scitotenv.2014.03.042
Kiill LHP, Feitoza EA, Siqueira KMM, Ribeiro MF, Silva EMS (2016) Evaluation of floral characteristics of melon hybrids (cucumis melo l.) in pollinator attractiveness. Rev Bras Frutic 38:e-531. https://doi.org/10.1590/0100-29452016531
Klein AM, Vaissiere BE, Cane JH, Steffandewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proc R Soc B 274:303–313. https://doi.org/10.1098/rspb.2006.3721
Lahm GP, Cordova D, Barry JD (2009) New and selective ryanodine receptor activators for insect control. Bioorg Med Chem 17:4127–4133. https://doi.org/10.1016/j.bmc.2009.01.018
Laycock I, Lenthall KM, Barratt AT, Cresswell JE (2012) Effects of imidacloprid, a neonicotinoid pesticide, on reproduction in worker bumble bees (Bombus terrestris). Ecotoxicology 21:1937–1945. https://doi.org/10.1007/s10646-012-0927-y
Liu Z, Dai Y, Huang G, Gu Y, Ni J, Wei H, Yuan S (2011) Soil microbial degradation of neonicotinoid insecticides imidacloprid, acetamiprid, thiacloprid and imidaclothiz and its effect on the persistence of bioefficacy against horsebean aphid Aphis craccivora Koch after soil application. Pest Manag Sci 67:1245–1252. https://doi.org/10.1002/ps.2174
Mann LK (1953) Honey bee activity in relation to pollination and fruit set in the cantaloupe (Cucumis melo). Am J Bot 40:545–553. https://doi.org/10.1002/j.1537-2197.1953.tb06518.x
Mansour R, Belzunces LP, Suma P, Zappala L, Mazzeo G, Grissa-Lebdi K, Russo A, Biondi A (2018) Vine and citrus mealybug pest control based on synthetic chemicals. a review. Agron Sustain Dev 38:37
Martinelli LA, Naylor R, Vitousek PM, Moutinho P (2010) Agriculture in Brazil: impacts, costs, and opportunities for a sustainable future. Curr Opin Environ Sustainability 2:431–438. https://doi.org/10.1016/j.cosust.2010.09.008
MCgregor SE, Todd FE (1952) Cantaloup production with honey bees. J Economic Entomol 45:43–47. https://doi.org/10.1093/jee/45.1.43
Mullin CA, Frazier M, Frazier JL, Ashcraft S, Simonds R, vanEngelsdorp D, Pettis JS (2010) High levels of miticides and agrochemicals in north american apiaries: implications for honey bee health. PLoS ONE 5(3):e9754. https://doi.org/10.1371/journal.pone.0009754
Oerke EC (2005) Crop losses to pests. J Agric Sci 144:31–43. https://doi.org/10.1017/s0021859605005708
Passos L, Soares MA, Collares LJ, Malagoli I, Desneux N, Carvalho GA (2018) Lethal, sublethal and transgenerational effects of insecticides on Macrolophus basicornis, predator of Tuta absoluta. Entomol Generalis 38:127–143
Pisa LW, Amaral-Rogers V, Belzunces LP, Bonmatin JM, Downs CA, Goulson D, Kreutzweiser DP, Krupke C, Liess M, McField M, Morrissey CA, Noome DA, Settele J, Simon-Delso N, Stark JD, Van der Sluijs JP, Van Dyck H, Wiemers M (2015) Effects of neonicotinoids and fipronil on non-target invertebrates. Environ Sci Pollut Res 22:68–102
Pohorecka K, Skubida P, Miszczak A, Semkiw P, Sikorsk P, Zagibajł K, Teper D, Ko łtowski Z, Skubida M, Zdańska D, Bober A (2012) Residues of neonicotinoid insecticides in bee collected plant materials from oilseed rape crops and their effect on bee colonies. J Apicultural Sci 56:115–134. https://doi.org/10.2478/v10289-012-0029-3
Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evolution 25:345–353. https://doi.org/10.1016/j.tree.2010.01.007
Reyes-Carrillo MCJL, Cano-Rios P, Camberos UM (2009) Período óptimo de polinización del melón con abejas melíferas (Apis mellifera L.). Agricultura Técnica en México 35:371–378
Romeh AA, Mekky TM, Ramadan RA, Hendawi MY (2009) Dissipation of profenofos, imidacloprid and penconazole in tomato fruits and products. Bull Environ Contam Toxicol 83:812–817. https://doi.org/10.1007/s00128-009-9852-z
Romero RR, Chaufaux J, Pham-Delègue M (2005) Effects of Cry1Ab protoxin, deltamethrin and imidacloprid on the foraging activity and the learning performances of the honeybee Apis mellifera, a comparative approach. Apidologie 36:601–611. https://doi.org/10.1051/apido:2005039
Rosa AS, Teixeira JSG, Vollet-Neto A, Queiroz EP, Blochtein B, Pires CSS, Imperatriz-Fonseca VL (2016) Consumption of the neonicotinoid thiamethoxam during the larval stage affects the survival and development of the stingless bee, Scaptotrigona aff. Depilis. Apidologie 47:729–738. https://doi.org/10.1007/s13592-015-0424-4
Sandrock C, TanadinI LG, Pettis JS, Biesmeijer JC, Potts SG, Neumann P (2014) Sublethal neonicotinoid insecticide exposure reduces solitary bee reproductive success. Agric For Entomol 16:119–128. https://doi.org/10.1111/afe.12041
SAS Institute Inc (2008) SAS/STAT 9.2 User’s Guide. SAS Institute Inc, Cary, NC, USA
Sattelle D, Cordova D, Cheek T (2008) Insect ryanodine receptors: molecular targets for novel pest control chemicals. Invertebr Neurosci 8:107–119
Schmuck R, Schoning R, Stork A, Schramel O (2001) Risk posed to honeybees (Apis mellifera L, Hymenoptera) by an imidacloprid seed dressing of sunflowers. Pest Manag Sci 57:225–238. https://doi.org/10.1002/ps.270
Schneider CW, Tautz J, Grunewald B, Fuchs S (2012) RFID Tracking of sublethal effects of two neonicotinoid insecticides on the foraging behavior of Apis mellifera. PLoS ONE 7(1):e30023. https://doi.org/10.1371/journal.pone.0030023
Schreinemachers P, Tipraqsa P (2012) Agricultural pesticides and land use intensification in high, middle and low income countries. Food Policy 37:616–626. https://doi.org/10.1016/j.foodpol.2012.06.003
Smagghe G, Deknopper J, Meeus I, Mommaerts V (2013) Dietary chlorantraniliprole suppresses reproduction in worker bumblebees. Pest Manag Sci 69:787–791. https://doi.org/10.1002/ps.3504
Sousa RM, Aguiar OS, Freitas BM, Neto AAS, Pereira TFC (2009) Requerimentos de polinização do meloeiro (Cucumis melo L.) no município de Acaraú – CE – Brasil. Rev Caatinga 22:238–242
Sousa RM, Aguiar OS, Freitas BM, Maracajá PB, Andrade CBCM (2012) Grazing behavior of africanized honey bees (Apis mellifera L.) in flowers of yellow melon (Cucumis melo L.). Rev Verde 7:233–238
Stanley DA, Smith KE, Raine NE (2015) Bumblebee learning and memory is impaired by chronic exposure to a neonicotinoid pesticide. Sci Rep. 5:1–10. https://doi.org/10.1038/srep16508
Suchail S, Guez D, Belzunces LP (2000) Characteristics of imidacloprid toxicity in two Apis mellifera subspecies. Environ Toxicol Chem 19:1901–1905. https://doi.org/10.1002/etc.5620190726
Suchail S, Guez D, Belzunces LP (2001) Discrepancy between acute and chronic toxicity induced by imidacloprid and its metabolites in Apis mellifera. Environ Toxicol Chem 20:2482–2486. https://doi.org/10.1002/etc.5620201113
Taning CNT, Vanommeslaeghe A, Smagghe G (2019) With or without foraging for food, field-realistic concentrations of sulfoxaflor are equally toxic to bumblebees (Bombus terrestris). Entomol Generalis https://doi.org/10.1127/entomologia/2019/0784
Tavares DA, Roat TC, Carvalho SM, Silva-Zacarin ECMZ, Malaspina O (2015) In vitro effects of thiamethoxam on larvae of africanized honey bee Apis mellifera (Hymenoptera: Apidae). Chemosphere 135:370–378. https://doi.org/10.1016/j.chemosphere.2015.04.090
Thompson HM (2003) Behavioural effects of pesticides in bees–their potential for use in risk assessment. Ecotoxicology 12:317–330. https://doi.org/10.1023/a:1022575315413
Tilman D, Fargione J, Wolff B, D’Antonio C, Dobson A, Howarth R, Schindler D, Schlesinger WH, Simberloff D, Swackhamer S (2001) Forecasting agriculturally driven global environmental change. Science 292:281–284. https://doi.org/10.1126/science.1057544
Trindade MAS, Sousa AH, Vasconcelos WE, Freitas RS, Silva AMA, Pereira DS, Maracajá PB (2004) Avaliação da polinização e estudo comportamental de Apis mellifera L. na cultura do meloeiro em Mossoró, RN. Revista de Biologia e Ciências da. Terra 4:1–10
Tomé HVV, Martins GF, Lima MAP, Campos LAO, Guedes RNC (2012) Imidacloprid-induced impairment of mushroom bodies and behavior of the native stingless bee Melipona quadrifasciata anthidioides. PLoS ONE 7(6):e38406. https://doi.org/10.1371/journal.pone.0038406
Tomé HVV, Barbosa WF, Martins GF, Guedes RNC (2015) Spinosad in the native stingless bee Melipona quadrifasciata: Regrettable non-target toxicity of a bioinsecticide. Chemosphere 124:103–109. https://doi.org/10.1016/j.chemosphere.2014.11.038
Tschoeke PH, Oliveira EE, Dalcin MS, Silveira-Tschoeke CAC, Santos GR (2015) Diversity and flower-visiting rates of bee species as potential pollinators of melon (Cucumis melo L.) in the Brazilian Cerrado. Sci Horticulturae 186:207–216
van der Sluijs JP, Simon-Delso N, Goulson D, Maxim L, Bonmatin JM, lzunces LP (2013) Neonicotinoids, bee disorders and the sustainability of pollinator services. Current Opinion in Environmental Sustainability 5:292–305
Varikou K, Garantonakis N, Birouraki A (2019) Exposure of Bombus terrestris L. to three different active ingredients and two application methods for olive pest control. Entomologia Generalis 39:53–60
Xavier VM, Message D, Picanço MC, Chediak M, Júnior PAS, Ramos RS, Martins JC (2015) Acute Toxicity and Sublethal Effects of Botanical Insecticides to Honey Bees. J Insect Sci 15(137):1–6. https://doi.org/10.1093/jisesa/iev110
Yang EC, Chuang YC, Chen YL, Chang LH (2008) Abnormal foraging behavior induced by sublethal dosage of imidacloprid in the honey bee (Hymenoptera: Apidae). J Econ Entomol 101:1743–1748. https://doi.org/10.1603/0022-0493-101.6.1743
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This work was supported by ‘Fundação de Amparo a Pesquisa do Estado de Minas Gerais’ – FAPEMIG (grant FORTIS-TCT-10254/2014). Special thanks to Matheus de Almeida Vicente and Lucas Pacheco Raad who helped with some of the data collection.
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Naiara Gomes, I., Ingred Castelan Vieira, K., Moreira Gontijo, L. et al. Honeybee survival and flight capacity are compromised by insecticides used for controlling melon pests in Brazil. Ecotoxicology 29, 97–107 (2020). https://doi.org/10.1007/s10646-019-02145-8
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DOI: https://doi.org/10.1007/s10646-019-02145-8