Stress Response of European Common Frog (Rana temporaria) Tadpoles to Bti Exposure in an Outdoor Pond Mesocosm.


Journal

Bulletin of environmental contamination and toxicology
ISSN: 1432-0800
Titre abrégé: Bull Environ Contam Toxicol
Pays: United States
ID NLM: 0046021

Informations de publication

Date de publication:
24 Mar 2023
Historique:
received: 23 01 2023
accepted: 25 02 2023
entrez: 24 3 2023
pubmed: 25 3 2023
medline: 28 3 2023
Statut: epublish

Résumé

The biocide Bacillus thuringiensis var. israelensis (Bti) is applied to wetlands to control nuisance by mosquitoes. Amphibians inhabiting these wetlands can be exposed to Bti multiple times, potentially inducing oxidative stress in developing tadpoles. For biochemical stress responses, ambient water temperature plays a key role. Therefore, we exposed tadpoles of the European common frog (Rana temporaria) three times to field-relevant doses of Bti in outdoor floodplain pond mesocosms (FPM) under natural environmental conditions. We sampled tadpoles after each Bti application over the course of a 51-day experiment (April to June 2021) and investigated the activity of the glutathione-S-transferase (GST) and protein carbonyl content as a measure for detoxification activity and oxidative damage. GST activity increased over the course of the experiment likely due to a general increase of water temperature. We did not observe an effect of Bti on either of the investigated biomarkers under natural ambient temperatures. However, Bti-induced effects may be concealed by the generally low water temperatures in our FPMs, particularly at the first application in April, when we expected the highest effect on the most sensitive early stage tadpoles. In light of the global climate change, temperature-related effects of pesticides and biocides on tadpoles should be carefully monitored - in particular since they are known as one of the factors driving the worldwide decline of amphibian populations.

Identifiants

pubmed: 36959482
doi: 10.1007/s00128-023-03708-6
pii: 10.1007/s00128-023-03708-6
pmc: PMC10036417
doi:

Substances chimiques

Disinfectants 0
Glutathione Transferase EC 2.5.1.18
Water 059QF0KO0R

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

70

Subventions

Organisme : Deutsche Forschungsgemeinschaft
ID : 326210499/GRK2360

Informations de copyright

© 2023. The Author(s).

Références

Adams E, Gerstle V, Brühl CA (2021) Dermal fungicide exposure at realistic field rates induces lethal and sublethal effects on juvenile European common frogs (Rana temporaria). Environ Toxicol Chem 40(5):1289–1297. https://doi.org/10.1002/etc.4972
doi: 10.1002/etc.4972
Allgeier S, Frombold B, Mingo V, Brühl CA (2018) European common frog Rana temporaria (Anura: Ranidae) larvae show subcellular responses under field-relevant Bacillus thuringiensis var. Israelensis (bti) exposure levels. Environ Res 162:271–279. https://doi.org/10.1016/j.envres.2018.01.010
doi: 10.1016/j.envres.2018.01.010
Baier F, Gruber E, Hein T, Bondar-Kunze E, Ivanković M, Mentler A, Brühl CA, Spangl B, Zaller JG (2016) Non-target effects of a glyphosate-based herbicide on common toad larvae (Bufo bufo Amphibia) and associated algae are altered by temperature. PeerJ. https://doi.org/10.7717/peerj.2641
doi: 10.7717/peerj.2641
Bates D, Mächler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. ArXiv Preprint ArXiv 1406:5823
Becker N (1997) Microbial control of mosquitoes: management of the upper rhine mosquito population as a model programme. Parasitol Today 13(12):485–487. https://doi.org/10.1016/S0169-4758(97)01154-X
doi: 10.1016/S0169-4758(97)01154-X
Becker N (2002) Sterilization of Bacillus thuringiensis israelensis products by gamma radiation. J Am Mosq Control Assoc 18(1):57–62
Becker N, Ludwig M, Su T (2018) Lack of resistance in Aedes vexans field populations after 36 years of Bacillus thuringiensis subsp. israelensis applications in the Upper Rhine valley, Germany. J Am Mosq Control Assoc 34(2):154–157
doi: 10.2987/17-6694.1
Bordalo MD, Gravato C, Beleza S, Campos D, Lopes I, Pestana JLT (2020) Lethal and sublethal toxicity assessment of Bacillus thuringiensis var. israelensis and Beauveria bassiana based bioinsecticides to the aquatic insect Chironomus riparius. Sci Total Environ. https://doi.org/10.1016/j.scitotenv.2019.134155
doi: 10.1016/j.scitotenv.2019.134155
Bravo A, Gill SS, Soberón M (2007) Mode of action of Bacillus thuringiensis cry and cyt toxins and their potential for insect control. Toxicon 49(4):423–435. https://doi.org/10.1016/j.toxicon.2006.11.022
doi: 10.1016/j.toxicon.2006.11.022
Brühl CA, Després L, Frör O, Patil CD, Poulin B, Tetreau G, Allgeier S (2020) Environmental and socioeconomic effects of mosquito control in Europe using the biocide Bacillus thuringiensis subsp israelensis (Bti). Science of the total environment. Elsevier, Amsterdam. https://doi.org/10.1016/j.scitotenv.2020.137800
doi: 10.1016/j.scitotenv.2020.137800
Charbonneau CS, Drobney RD, Rabeni CF (1994) Effects of Bacillus thuringiensis var. israelensis on non-target benthic organisms in a lentic habitat and factors affecting the efficiacy of the larvicide. Environ Toxicol Chem. https://doi.org/10.1002/etc.5620130211
doi: 10.1002/etc.5620130211
Dalle-Donne I, Rossi R, Giustarini D, Milzani A, Colombo R (2003) Protein carbonyl groups as biomarkers of oxidative stress. Clin Chim Acta 329(1–2):23–38. https://doi.org/10.1016/S0009-8981(03)00003-2
doi: 10.1016/S0009-8981(03)00003-2
Deutscher Wetterdienst (2023), January 8 Klimaüberwachung Deutschland, Monats- und Jahreszeitenbericht. https://www.dwd.de/DE/Home/home_node.html
Empey MA, Lefebvre-Raine M, Gutierrez-Villagomez JM, Langlois VS, Trudeau VL (2021) A Review of the Effects of the Biopesticides Bacillus thuringiensis Serotypes israelensis (Bti) and kurstaki (Btk) in Amphibians. Archives of Environmental Contamination and Toxicology. Springer, pp 789–800. https://doi.org/10.1007/s00244-021-00842-2
doi: 10.1007/s00244-021-00842-2
Freitas JS, Almeida EA (2016) Antioxidant defense system of tadpoles (Eupemphix nattereri) exposed to changes in temperature and pH. Zoolog Sci 33(2):186–194. https://doi.org/10.2108/zs150075
doi: 10.2108/zs150075
Freitas JS, Felício AA, Teresa FB, de Alves E (2017) Combined effects of temperature and clomazone (Gamit®) on oxidative stress responses and B-esterase activity of Physalaemus nattereri (Leiuperidae) and Rhinella schneideri (Bufonidae) tadpoles. Chemosphere 185:548–562. https://doi.org/10.1016/j.chemosphere.2017.07.061
doi: 10.1016/j.chemosphere.2017.07.061
Gerstle V, Manfrin A, Kolbenschlag S, Gerken M, Islam ASMMU, Entling MH, Bundschuh M, Brühl CA (2023) Benthic macroinvertebrate community shifts based on Bti-induced chironomid reduction also decrease Odonata emergence. Environ Pollut. https://doi.org/10.1016/j.envpol.2022.120488
doi: 10.1016/j.envpol.2022.120488
Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16(3):183–190
Günther R (1996) Die Amphibien und Reptilien Deutschlands. Springer, Berlin
Gutierrez-Villagomez JM, Patey G, To TA, Lefebvre-Raine M, Lara-Jacobo LR, Comte J, Klein B, Langlois VS (2021) Frogs respond to commercial formulations of the Biopesticide Bacillus thuringiensis var. Israelensis, especially their intestine microbiota. Environ Sci Technol 55(18):12504–12516. https://doi.org/10.1021/acs.est.1c02322
doi: 10.1021/acs.est.1c02322
Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases: the first enzymatic step in mercapturic acid formation. J Biol Chem 249(22):7130–7139. https://doi.org/10.1016/S0021-9258(19)42083-8
doi: 10.1016/S0021-9258(19)42083-8
Kästel A, Allgeier S, Brühl CA (2017) Decreasing Bacillus thuringiensis israelensis sensitivity of Chironomus riparius larvae with age indicates potential environmental risk for mosquito control. Sci Rep. https://doi.org/10.1038/s41598-017-14019-2
doi: 10.1038/s41598-017-14019-2
Kolbenschlag S, Gerstle V, Eberhardt J, Bollinger E, Schulz R, Brühl CA, Bundschuh M (2023) A temporal perspective on aquatic subsidy: Bti affects emergence of Chironomidae. Ecotoxicol Environ Saf 250:114503. https://doi.org/10.1016/j.ecoenv.2023.114503
doi: 10.1016/j.ecoenv.2023.114503
Lajmanovich RC, Junges CM, Cabagna-Zenklusen MC, Attademo AM, Peltzer PM, Maglianese M, Márquez VE, Beccaria AJ (2015) Toxicity of Bacillus thuringiensis var. Israelensis in aqueous suspension on the South American common frog Leptodactylus latrans (Anura: Leptodactylidae) tadpoles. Environ Res 136:205–212. https://doi.org/10.1016/j.envres.2014.10.022
doi: 10.1016/j.envres.2014.10.022
Leeb C, Schuler L, Brühl CA, Theissinger K (2022) Low temperatures lead to higher toxicity of the fungicide folpet to larval stages of Rana temporaria and Bufotes viridis. PLoS ONE. https://doi.org/10.1371/journal.pone.0258631
doi: 10.1371/journal.pone.0258631
Lenth Rv (2016) Least-squares means: the R package lsmeans. J Stat Softw 69:1–33
doi: 10.18637/jss.v069.i01
Madeira D, Narciso L, Cabral HN, Vinagre C, Diniz MS (2013) Influence of temperature in thermal and oxidative stress responses in estuarine fish. Comp Biochem Physiol - Mol Integr Physiol 166(2):237–243. https://doi.org/10.1016/j.cbpa.2013.06.008
doi: 10.1016/j.cbpa.2013.06.008
Margalith Y, Ben-Dov E (2000) Biological Control by Bacillus thuringiensis subsp. israelensis. In: Rechcigl JE, Rechcigl NA (eds) Insect pest management techniques for environmental protection. CRC Press, Boca Raton, pp 243–281
McKie BG, Taylor A, Nilsson T, Frainer A, Goedkoop W (2023) Ecological effects of mosquito control with Bti: evidence for shifts in the trophic structure of soil- and ground-based food webs. Aquat Sci. https://doi.org/10.1007/s00027-023-00944-0
doi: 10.1007/s00027-023-00944-0
Mingo V, Lötters S, Wagner N (2017) The use of buccal swabs as a minimal-invasive method for detecting effects of pesticide exposure on enzymatic activity in common wall lizards. Environ Pollut 220:53–62
doi: 10.1016/j.envpol.2016.09.022
Monaghan P, Metcalfe NB, Torres R (2009) Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecol Lett. https://doi.org/10.1111/j.1461-0248.2008.01258.x
doi: 10.1111/j.1461-0248.2008.01258.x
Munstermann MJ, Heim NA, McCauley DJ, Payne JL, Upham NS, Wang SC, Knope ML (2022) A global ecological signal of extinction risk in terrestrial vertebrates. Conserv Biol. https://doi.org/10.1111/cobi.13852
doi: 10.1111/cobi.13852
Noyes PD, McElwee MK, Miller HD, Clark BW, van Tiem LA, Walcott KC, Erwin KN, Levin ED (2009) The toxicology of climate change: environmental contaminants in a warming world. Environment International. Elsevier Ltd, Amsterdam, pp 971–986. https://doi.org/10.1016/j.envint.2009.02.006
doi: 10.1016/j.envint.2009.02.006
Pinheiro J, Bates D, DebRoy S, Sarkar D, Heisterkamp S, van Willigen B, Maintainer R (2017) Package ‘nlme.’Linear and Nonlinear Mixed Effects Models, Version, 3(1)
Poulin B, Lefebvre G, Hilaire S, Després L (2022) Long-term persistence and recycling of Bacillus thuringiensis israelensis spores in wetlands sprayed for mosquito control. Ecotoxicol Environ Safety. https://doi.org/10.1016/j.ecoenv.2022.114004
doi: 10.1016/j.ecoenv.2022.114004
R Core Team (2013) R: A language and environment for statistical computing
Schweizer M, Miksch L, Köhler HR, Triebskorn R (2019) Does Bti (Bacillus thuringiensis var. Israelensis) affect Rana temporaria tadpoles? Ecotoxicol Environ Saf 181:121–129. https://doi.org/10.1016/j.ecoenv.2019.05.080
doi: 10.1016/j.ecoenv.2019.05.080
Sparling DW, Fellers GM, McConnell LL (2001) Pesticides and amphibian population declines in California, USA. Environ Toxicol Chem 20(7):1591–1595
doi: 10.1002/etc.5620200725
Stehle S, Manfrin A, Feckler A, Graf T, Joschko TJ, Jupke J, Noss C, Rösch V, Schirmel J, Schmidt T, Zubrod JP, Schulz R (2022) Structural and functional development of twelve newly established floodplain pond mesocosms. Ecol Evol 12:8674. https://doi.org/10.1002/ece3.8674
doi: 10.1002/ece3.8674
Steinberg CEW (2012) Multiple stressors as environmental realism: synergism or antagonism. Stress Ecology. Springer, Berlin
doi: 10.1007/978-94-007-2072-5
Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues ASL, Fischman DL, Waller RW (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306(5702):1783–1786
doi: 10.1126/science.1103538
Tetreau G, Alessi M, Veyrenc S, Périgon S, David JP, Reynaud S, Després L (2012) Fate of Bacillus thuringiensis subsp. Israelensis in the field: evidence for spore recycling and differential persistence of toxins in leaf litter. Appl Environ Microbiol 78(23):8362–8367. https://doi.org/10.1128/AEM.02088-12
doi: 10.1128/AEM.02088-12
Venturino A, de D’Angelo AMP (2005) Biochemical targets of xenobiotics: biomarkers in amphibian ecotoxicology. Appl Herpetol 2(3):335–353
doi: 10.1163/1570754054507433
Wickham H, Chang W, Wickham MH (2016) Package ‘ggplot2’. Create Elegant Data Visualisations Using the Grammar of Graphics Version 2(1):1–189
Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, Berlin
doi: 10.1007/978-0-387-87458-6

Auteurs

Verena Gerstle (V)

iES Landau, Institute for Environmental Sciences, RPTU Kaiserslautern-Landau, Fortstraße 7, D-76829, Landau, Germany. verena.gerstle@rptu.de.

Priyanka Solanki (P)

iES Landau, Institute for Environmental Sciences, RPTU Kaiserslautern-Landau, Fortstraße 7, D-76829, Landau, Germany.

Alessandro Manfrin (A)

iES Landau, Institute for Environmental Sciences, RPTU Kaiserslautern-Landau, Fortstraße 7, D-76829, Landau, Germany.

Sara Kolbenschlag (S)

iES Landau, Institute for Environmental Sciences, RPTU Kaiserslautern-Landau, Fortstraße 7, D-76829, Landau, Germany.

Carsten A Brühl (CA)

iES Landau, Institute for Environmental Sciences, RPTU Kaiserslautern-Landau, Fortstraße 7, D-76829, Landau, Germany.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH