Abstract
Bio-insecticides have been increasingly used worldwide as ecofriendly alternatives to pesticides, but data on their effects in non-target freshwater organisms is still scarce and limited to insects. The aim of this study was to determine the lethal and sub-lethal effects of the bio-insecticides Bac Control (based on Bacillus thuringiensis kurstaki—Btk) and Boveril (based on Beauveria bassiana—Bb) on regeneration, behavioral, and reproductive endpoints of the freshwater planarian Girardia tigrina. The estimated LC50–48h were > 800 mg a.i./L for Btk and 60.74 mg a.i./L for Bb. In addition, exposure to Btk significantly decreased locomotion and feeding activities of planarians (lowest observed effect concentration (LOEC) of 12.5 mg a.i./L Btk) and fecundity rate (LOEC = 3.12 mg a.i./L Btk), whereas exposure to Bb significantly delayed regeneration (LOEC = 0.75 mg a.i./L Bb) and decreased fecundity rate (1.5 mg a.i./L Bb) of planarians. Thus, both bio-insecticides induced deleterious sub-lethal effects on a non-insect freshwater invertebrate species. However, only Bb-based formulation affected the survival, fecundity rate, and regeneration at concentrations below the maximum predicted environmental concentration (PEC = 247 mg/L). Thus, care should be taken when using such formulations as alternatives to chemical insecticides near aquatic ecosystems.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Agboyi LK, Ketoh GK, Douro Kpindou OK, Martin T, Glitho IA, Tamo M (2020) Improving the efficiency of Beauveria bassiana applications for sustainable management of Plutella xylostella (Lepidoptera: Plutellidae) in West Africa. Biol Control 144:104233. https://doi.org/10.1016/j.biocontrol.2020.104233
Allgeier S, Kästel A, Brühl CA (2019) Adverse effects of mosquito control using Bacillus thuringiensis var. israelensis: reduced chironomid abundances in mesocosm, semi-field and field studies. Ecotoxicol Environ Saf 169:786–796. https://doi.org/10.1016/j.ecoenv.2018.11.050
Álvarez B, Biosca EG (2017) Bacteriophage-based bacterial wilt biocontrol for an environmentally sustainable agriculture. Front Plant Sci 8:1218. https://doi.org/10.3389/fpls.2017.01218
ASTM (1980) Standard practice for conducting acute toxicity tests with fishes, macroinvertebrates and amphibians. Report E −729–80. American Standards for Testing and Materials, Philadelphia, P.A.
Beetz S, Holthusen TK, Koolman J, Trenczek T (2008) Correlation of hemocyte counts with different developmental parameters during the last larval instar of the tobacco hornworm, Manduca sexta. Arch Insect Biochem Physiol 67:63–75. https://doi.org/10.1002/arch.20221
Becker N, Margalit J (1993) Use of Bacillus thuringiensis israelensis against mosquitoes and blackflies. In: Entwistle PF, Cory JS, Bailey MJ, Higgs S (eds) Bacillus thuringiensis: An Environmental Biopesticide: Theory and Practice. John Wiley, Chichester, pp 147–170
Benzina F, Hamid S, Mohand-Kaci H, Bissaad F, Halouane F (2018) Histological changes in the larvae of the domestic mosquito Culex pipiens treated with the entomopathogenic fungus Beauveria bassiana. Sci Res Essays 13:1–10. https://doi.org/10.5897/SRE2017.6544
Berlitz DL, Knaak N, Cassal MC, Fiuza LM (2014) Bacillus and biopesticides in control of phytonematodes, In: Sahayaraj K (ed) Basic and Applied Aspects of Biopesticides. Springer publishers, pp 3-16. https://doi.org/10.1007/978-81-322-1877-7_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 698:134155. https://doi.org/10.1016/j.scitotenv.2019.134155.
Campos D, Gravato C, Quintaneiro C, Golovko O, Žlábek V, Soares AMVM, Pestana JLT (2017) Toxicity of organic UV-filters to the aquatic midge Chironomus riparius. Ecotoxicol Environ Saf 143:210–216. https://doi.org/10.1016/j.ecoenv.2017.05.005
Cao CW, Sun LL, Wen RR, Li XP, Wu HQ, Wang ZY (2012) Toxicity and affecting factors of Bacillus thuringiensis var. israelensis on Chironomus kiiensis larvae. J insect Sci 12:126–128. https://doi.org/10.1673/031.012.12601
Castagnola A, Stock SP (2014) Common virulence factors and tissue targets of entomopathogenic bacteria for biological control of lepidopteran pests. Insects 5:139–166. https://doi.org/10.3390/insects5010139
Cerenius L, Lee BL, Söderhäll K (2008) The proPO-system: pros and cons for its role in invertebrate immunity. Trends Immunol 29:263–271. https://doi.org/10.1016/j.it.2008.02.009
Challa GK, Firake DM, Behere GT (2019) Bio-pesticide applications may impair the pollination services and survival of foragers of honey bee, Apis cdrana fabricius in oilseed brassica. Environ Pollut 249:598–609. https://doi.org/10.1016/j.envpol.2019.03.048
Charbonneau S, Drobney RD, Rabeni CF (1994) Effects of Bacillus thuringiensis var. israelensis on nontarget benthic organisms in a lentic habitat and factors affecting the efficacy of the larvicide. Environ Toxicol Chem 13:267–279. https://doi.org/10.1002/etc.5620130211
Dornelas ASP, Sarmento RA, Silva LCR, Saraiva AS, Souza DJ, Bordalo MD, Soares AVMM, Pestana JLT (2020a) Toxicity of microbial insecticides towards the non-target freshwater insect Chironomus xanthus. Pest Manag Sci 76:1–27. https://doi.org/10.1002/ps.5629
Dornelas ASP, Sarmento RA, Cavallini GS, Barbosa RS, Vieira MM, Saraiva AS, Bordalo MD, Soares AMVM, Pestana JLT (2020b) Lethal and sublethal effects of the saline stressor sodium chloride on Chironomus xanthus and Girardia tigrina. Environ Sci Pollut Res 27:1–11. https://doi.org/10.1007/s11356-020-09556-9
EFSA - European Food Safety Authority (2012) Conclusion on the peer review of the pesticide risk assessment of the active substance Bacillus thuringiensis subsp. kurstaki (strains ABTS 351, PB 54, SA 11, SA 12, EG 2348). EFSA Journal 10:1–66. https://doi.org/10.2903/j.efsa.2012.2540
EFSA - European Food Safety Authority (2013) Conclusion on the peer review of the pesticide risk assessment of the active substances Beauveria bassiana Strains ATCC-74040 and GHA. 10.2903/j.efsa.2010.1708.
EFSA - European Food Safety Authority (2015) Peer review of the pesticide risk assessment of the active substance Beauveria bassiana strain 147. EFSA Journal 13:10. https://doi.org/10.2903/j.efsa.2015.4261
Elliott SA, Sanchez Alvarado A (2013) The history and enduring contributions of planarians to the study of animal regeneration. Wiley Interdiscip. Rev Dev Biol 2:301–326. https://doi.org/10.1002/wdev.82
EPA - U.S. Environmental Protection Agency (2016) Ingredients used in pesticide products. Available in: https://www.epa.gov/ingredients-used-pesticide-products/what-are-biopesticides. Accessed on June 04, 2020.
Genthner FJ, Cripe GM, Crosby DJ (1994) Effect of Beauveria bassiana and its toxins on Mysidopsis bahia (Mysidacea). Archs. environ. Contam Toxicol 26:90–94. https://doi.org/10.1007/BF00212798
González-Santoyo I, Córdoba-Aguilar A (2012) Phenoloxidase: a key component of the insect immune system. Entomol Exp Appl 142:1–16. https://doi.org/10.1111/j.1570-7458.2011.01187.x
Grizanova EV, Dubovskiy IM, Whitten MMA, Glupov VV (2014) Contributions of cellular and humoral immunity of Galleria mellonella larvae in defence against oral infection by Bacillus thuringiensis. J Invertebr Pathol 119:40–46. https://doi.org/10.1016/j.jip.2014.04.003
Grisolia CK, Oliveira R, Domingues I, Oliveira-Filho EC, Monerat RG, Soares AMVM (2009) Genotoxic evaluation of different δ-endotoxins from Bacillus thuringiensis on zebrafish adults and development in early life stages. Mutat Res Genet Toxicol Environ Mutagen 672:119–123. https://doi.org/10.1016/j.mrgentox.2008.10.017
Guecheva TN, Erdtmann B, Benfato MS, Henriques JAP (2003) Stress protein response and catalase activity in freshwater planarian Dugesia (Girardia) schubarti exposed to copper. Ecotox Environ Safe 56:351–357. https://doi.org/10.1016/S0147-6513(02)00065-9
Gupta S, Dikshit AK (2010) Biopesticides: An eco-friendly approach for pest control. J Biopestic 3:186–188
Hagstrom D, Cochet-Escartin O, Zhang S, Khuu C, Collins EMS (2015) Freshwater planarians as an alternative animal model for neurotoxicology. Toxicol Sci 147:270–285. https://doi.org/10.1093/toxsci/kfv129
Hart DD, Merz RA (1998) Predator-prey interactions in a benthic stream community: a field test of low-mediated refuges. Oecologia 114:263–273. https://doi.org/10.1007/s004420050445
Hughes P, Stevens M, Park H, Federici B, Dennis E, Akhurst R (2005) Response of larval Chironomus tepperi (Diptera: Chironomidae) to individual Bacillus thuringiensis var. Israelensis toxins and toxin mixtures. J Invertebr Pathol 88:34–39. https://doi.org/10.1016/j.jip.2004.10.004
Kandpal V (2014) Biopesticides. Int J Environ Res Develop 4:191–196
Karmrin MA (1997) Pesticide profiles: toxicity, environmental impact, and fate. Lewis Publishers/CRC Press, Boca Raton
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 7:1–7. https://doi.org/10.1038/s41598-017-14019-2
Khawaled K, Ben-Dov E, Zaritsky A, Barak Z (1990) The fate of Bacillus thuringiensis var. israelensis in B. thuringiensis var. israelensis-killed pupae of Aedes aegypti. J Invertebr Pathol 56:312–316. https://doi.org/10.1016/0022-2011(90)90117-O
Knakievicz T, Ertdmann B, Vieira SM, Ferreira HB (2006) Reproduction modes and life cycle of freshwater planarians (Plathyhelminthes, Tricladida, Paludicula) from Southern Brazil. Invertebr Biol 125:212–221. https://doi.org/10.1111/j.1744-7410.2006.00054.x
Knakievicz T, Ferreira H (2008) Evaluation of copper effects upon Girardia tigrina freshwater planarians based on a set of biomarkers. Chemosphere 71:419–428. https://doi.org/10.1016/j.chemosphere.2007.11.004
Knakievicz T (2014) Planarians as invertebrate bioindicators in freshwater environmental quality: the biomarkers approach. Ecotoxicol Environ Contam 9:1–12. https://doi.org/10.5132/eec.2014.01.001
Kumar S (2015) Biopesticide: An environment friendly pest management strategy. J Biofertil Biopestici 6:3. https://doi.org/10.4172/2155-6202.1000e127
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
Lavarías S, Arrighetti F, Siri A (2017) Histopathological effects of cypermethrin and Bacillus thuringiensis var. israelensis on midgut of Chironomus calligraphus larvae (Diptera: Chironomidae). Pestic Biochem Physiol 139:9–16. https://doi.org/10.1016/j.pestbp.2017.04.002
Lee BM, Scott GI (1989) Acute toxicity of temephos, fenoxycarb, diflubenzuron, and methoprene and Bacillus thuringiensis var. israelensis to the mummichog (Fundulus heteroclitus). Bull Environ Contam Toxicol 43:827–832. https://doi.org/10.1007/bf01702051
López AMC, Sarmento RA, Saraiva AS, Pereira RR, Soares AMVM, Pestana JLT (2019) Exposure to Roundup® affects behaviour, head regeneration and reproduction of the freshwater planarian Girardia tigrina. Sci Total Environ 675:453–461. https://doi.org/10.1016/j.scitotenv.2019.04.234
Machado AAS, Zarfl C, Rehse S, Kloas W (2017) Low-dose effects: nonmonotonic responses for the toxicity of a Bacillus thuringiensis biocide to Daphnia magna. Environ Sci Technol 51:1679–1686. https://doi.org/10.1021/acs.est.6b03056
Mascarin GM, Jaronski ST (2016) The production and uses of Beauveria bassiana as a microbial insecticide. World J Microbiol Biotechnol 32:177. https://doi.org/10.1007/s11274-016-2131-3
Mazid S, Rajkhowa RC, Kalita JC (2011) A review on the use of biopesticides in insect pest management. Int J Sci Adv Technol 1:169–178
McConnell JV (1965) On the procuring and the care of planarians. In: McConnell JV (ed) A manual of psychological experiments on planarians: The Worm Runner's Digest. Michigan, Ann Arbor, pp 10–20
Monteiro HR, Pestana JLT, Novais SC, Soares AMVM, Lemos MFL (2019) Toxicity of the insecticides spinosad and indoxacarb to the non-target aquatic midge Chironomus riparius. Sci Total Environ 666:1283–1291. https://doi.org/10.1016/j.scitotenv.2019.02.303
OECD - Organisation for Economic Co-operation and Development (2012) Working Document to the Environmental Safety Evaluation of Microbial Biocontrol Agents. Series on Pesticides, n. 67.
Ofoegbu PU, Simão FCP, Cruz A, Mendo S, Soares AMVM, Pestana JLT (2016) Toxicity of tributyltin (TBT) to the freshwater planarian Schmidtea mediterranea. Chemosphere 148:61–67. https://doi.org/10.1016/j.chemosphere.2015.12.131
Ofoegbu PU, Campos D, Soares AMVM, Pestana JLT (2019a) Combined effects of NaCl and fluoxetine on the freshwater planarian, Schmidtea mediterranea (Platyhelminthes: Dugesiidae). Environ Sci Pollut R 26:11326–11335. https://doi.org/10.1007/s11356-019-04532-4
Ofoegbu OU, Lourenço J, Mendo S, Soares AMVM, Pestana JLT (2019b) Effects of low concentrations of psychiatric drugs (carbamazepine and fluoxetine) on the freshwater planarian, Schmidtea mediterrânea. Chemosphere 217:542–549. https://doi.org/10.1016/j.chemosphere.2018.10.198
Olson S (2015) An analysis of the biopesticide market now and where it is going. Outlooks Pest Manag 26:203–206. https://doi.org/10.1564/v26_oct_04
Pang Q, Liu X, Zhao B, Jiang Y, Su F, Zhang X, Nie M, Zhang M, Sun H (2010) Detection and characterization of phenoloxidase in the freshwater planarian Dugesia japonica. Comp Biochem Phys B Biochemistry and Molecular Biology 157:54–58. https://doi.org/10.1016/j.cbpb.2010.05.002
Pelizza S, Scorsetti A, Bisaro V, Lopez LC, García J (2010) Individual and combined effects of Bacillus thuringiensis var. Israelenses, temephos and Leptolegnia chapmanii on the larval mortality of Aedes aegypti. BioControl 55:647–656. https://doi.org/10.1007/s10526-010-9281-2
Ragavendran C, Dubey NK, Natarajan D (2017) Beauveria bassiana (Clavicipitaceae): a potent fungal agent for controlling mosquito vectors of Anopheles stephensi, Culex quinquefasciatus and Aedes aegypti (Diptera: Culicidae). RSC Adv. 7:3838–3851. https://doi.org/10.1039/C6RA25859J
Reddien PW, Alvarado AS (2004) Fundamentals of Planarian Regeneration. Annu Rev Cell Dev Bi 20:725–757. https://doi.org/10.1146/annurev.cellbio.20.010403.095114
Rehner SA, Minnis AM, Sung GH, Luangsa-ard JJ, Devotto L, Humber RA (2011) Phylogeny and systematics of the anamorphic, entomopathogenic genus Beauveria. Mycologia 103:1055–1073. https://doi.org/10.3852/10-302
Rink J (2013) Stem cell systems and regeneration in planaria. Dev Gene Evol 223:67–84. https://doi.org/10.1007/s00427-012-0426-4
Rodrigues ACM, Henriques JF, Domingues I, Golovkob O, Zlábek V, Barata C, Soares AMVM, Pestana JLT (2016) Behavioural responses of freshwater planarians after short-termexposure to the insecticide chlorantraniliprole. Aquat Toxicol 170:371–376. https://doi.org/10.1016/j.aquatox.2015.10.018
Rustiguel CB, Fernández-Bravo M, Guimarães LHS, Quesada-Moraga E (2018) Different strategies to kill the host presented by Metarhizium anisopliae and Beauveria bassiana. Can J Microbiol 64:191–200. https://doi.org/10.1139/cjm-2017-0517
Sanahuja G, Banakar R, Twyman RM, Capell T, Christou P (2011) Bacillus thuringiensis: a century of research, development and commercial applications. Plant Biotechnol J 9:283–300. https://doi.org/10.1111/j.1467-7652.2011.00595.x
Sandhu SS, Sharma AK, Beniwal V, Goel G, Batra P, Kumar A, Jaglan S, Sharma AK, Malhotra S (2012) Myco-biocontrol of insect pests: factors involved, mechanism, and regulation. J Pathog 2012:1–10. https://doi.org/10.1155/2012/126819
Sanjayan KP, Ravikumar T, Albert S (1996) Changes in the haemocyte profile of Spilostethus hospes (Fab) (Heteroptera: Lygaeidae) in relation to eclosion, sex and mating. J Biosci 21:781–788. https://doi.org/10.1007/BF02704719
Saraiva AS, Sarmento RA, Golovko O, Randak T, Pestana JLT, Soares AMVM (2018) Lethal and sub-lethal effects of cyproconazole on freshwater organisms: a case study with Chironomus riparius and Dugesia tigrina. Environ Sci Pollut Res 25:12169–12176. https://doi.org/10.1007/s11356-017-1180-y
Saraiva AS, Sarmento RA, Gravato C, Rodrigues ACM, Campos D, Simão FCP, Soares AMVM (2020) Strategies of cellular energy allocation to cope with paraquat-induced oxidative stress: Chironomids vs planarians and the importance of using different species. Sci Total Environ 741:140443. https://doi.org/10.1016/j.scitotenv.2020.140443
Sayed AMM, Behle RW (2017) Evaluating a dual microbial agent biopesticide with Bacillus thuringiensis var. kurstaki and Beauveria bassiana blastospores. Biocontrol Sci Technol 27:461–474. https://doi.org/10.1080/09583157.2017.1303662
Simão FCP, Gravato C, Machado AL, Soares AMVM, Pestana JLT (2020) Toxicity of different polycyclic aromatic hydrocarbons (PAHs) to the freshwater planarian Girardia tigrina. Environ Pollut 266:115185. https://doi.org/10.1016/j.envpol.2020.115185
Simão FCP, Gravato C, Machado AL, Soares AMVM, Pestana JLT (2021) Effects of pyrene and benzo[a]pyrene on the reproduction and newborn morphology and behavior of the freshwater planarian Girardia tigrina. Chemosphere 264:128448. https://doi.org/10.1016/j.chemosphere.2020.128448
Singh RK, Dhama K, Khandia R, Munjal A, Karthik K, Tiwari R, Chakraborty S, Malik YS, Bueno-Mara RP (2018) Prevention and control strategies to counter Zika virus, a special focus on intervention approaches against vector mosquitoes-current updates. Front Microbiol 9:87. https://doi.org/10.3389/fmicb.2018.00087
Sokolova IM, Frederich M, Bagwe R, Lannig G, Sukhotin AA (2012) Energy homeostasis as an integrative tool for assessing limits of environmental stress tolerance in aquatic invertebrates. Mar Environ Res 79:1–15. https://doi.org/10.1016/j.marenvres.2012.04.003
Subbanna ARNS, Stanley J, Rajasekhara H, Mishra KK, Pattanayak A, Bhowmick R (2019) Perspectives of microbial metabolites as pesticides in agricultural pest management. In: Merillon JM, Ramawat KG (eds) Co-evolution of secondary metabolites. Reference Series in Phytochemistry, Springer, Cham, pp 1–28
Thakore T (2006) The biopesticide market for global agricultural use. Industrial Biotechnology 2:194–208
Tyler MS (2000) Planarian Regeneration. In: Sundderland MA (ed) Developmental Biology: a guide for experimental study, 2 ed Sinauer Associates, Inc Publishers, pp 163-175.
Vila-Farré M, Rink JC (2018) The ecology of freshwater planarians. In: Jochen C Rink (ed) Planarian Regeneration: Methods and Protocols. Methods in Molecular Biology. Humana Press, New York, pp 173–205
Vivekanandhan P, Kavitha T, Karthi S, Senthil-Nathan S, Shivakumar MS (2018) Toxicity of Beauveria bassiana - 28 Mycelial Extracts on Larvae of Culex quinquefasciatus Mosquito (Diptera: Culicidae). Int J Environ Res Public Health 15:440. https://doi.org/10.3390/ijerph15030440
WHO - World Health Organization (1999) Microbial Pest Control Agent: Bacillus thuringiensis. Environmental Health Criteria 217. World Health Organization, Geneva, witzerland.
Wu JP, Li MH (2018) The use of freshwater planarians in environmental toxicology studies: Advantages and potential. Ecotoxicol Environ Saf 161:45–56. https://doi.org/10.1016/j.ecoenv.2018.05.057
Zimmermann G (2007) Review on safety of the entomopathogenic fungi Beauveria bassiana and Beauveria brongniartii. Biocontrol Sci Technol 17:553–596. https://doi.org/10.1080/09583150701309006
Acknowledgements
The authors thank the Instituto Federal de Educação, Ciência e Tecnologia Goiano–Campus Campos Belos, Brazil, for its support and partnership.
Data and materials availability
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
Funding
This work was supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Brazil (Edital 71/2013, Programa Ciência Sem Fronteiras, Modalidade Pesquisador Visitante Especial-PVE, Projeto: A058_2013). Thanks are due to FCT/MCTES for the financial support provided to CESAM (UIDP/50017/2020+UIDB/50017/2020), through national funds and the co-funding by the FEDER, within the PT2020 Partnership Agreement and Compete 2020. Renato A. Sarmento received a scholarship from Conselho Nacional de Desenvolvimento Científico e Tecnológico-CNPq, Brazil (Produtividade em Pesquisa, Projeto: 306652/2018-8).
Author information
Authors and Affiliations
Contributions
LCRS conducted experiments, analyzed data, and wrote the manuscript (writing—original draft, review and editing). ASPD conducted experiments. ASS, ASPD, CG, JLTP, AMVMS, and RAS analyzed data and review and edit the manuscript; RAS and AMVMS conceived (funding acquisition) and designed research. All authors read, made corrections, and approved the manuscript.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Philippe Garrigues
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Silva, .C.R., Dornelas, A.S.P., de Souza Saraiva, A. et al. Do bio-insecticides affect only insect species? Behavior, regeneration, and sexual reproduction of a non-target freshwater planarian . Environ Sci Pollut Res 29, 10665–10674 (2022). https://doi.org/10.1007/s11356-021-16493-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-021-16493-8