Hostname: page-component-76fb5796d-vvkck Total loading time: 0 Render date: 2024-04-30T03:01:20.343Z Has data issue: false hasContentIssue false
  • English
  • Français

Less is more: partial larvicidal efficacy of plant leachate leads to larger Aedes aegypti mosquitoes

Published online by Cambridge University Press:  07 August 2023

Isabella Bodanese Marsaro ,
Gilberto Dinis Cozzer Open the ORCID record for Gilberto Dinis Cozzer [Opens in a new window] ,
Emanuel Rampanelli Cararo Open the ORCID record for Emanuel Rampanelli Cararo [Opens in a new window] ,
Raquel De Brito Open the ORCID record for Raquel De Brito [Opens in a new window] ,
William Gabriel Borges Open the ORCID record for William Gabriel Borges [Opens in a new window] ,
Jacir Dal Magro Open the ORCID record for Jacir Dal Magro [Opens in a new window] ,
Cássia Alves Lima-Rezende Open the ORCID record for Cássia Alves Lima-Rezende [Opens in a new window]  and
Renan de Souza Rezende Open the ORCID record for Renan de Souza Rezende [Opens in a new window]
Isabella Bodanese Marsaro
Affiliation:
Communitarian University of Chapecó Region – UNOCHAPECÓ, Servidão Anjo da Guarda, 295-D, Efapi, 89809-000 Chapecó, Santa Catarina, Brazil
Gilberto Dinis Cozzer
Affiliation:
Communitarian University of Chapecó Region – UNOCHAPECÓ, Servidão Anjo da Guarda, 295-D, Efapi, 89809-000 Chapecó, Santa Catarina, Brazil
Emanuel Rampanelli Cararo
Affiliation:
Communitarian University of Chapecó Region – UNOCHAPECÓ, Servidão Anjo da Guarda, 295-D, Efapi, 89809-000 Chapecó, Santa Catarina, Brazil
Raquel De Brito
Affiliation:
Communitarian University of Chapecó Region – UNOCHAPECÓ, Servidão Anjo da Guarda, 295-D, Efapi, 89809-000 Chapecó, Santa Catarina, Brazil
William Gabriel Borges
Affiliation:
Communitarian University of Chapecó Region – UNOCHAPECÓ, Servidão Anjo da Guarda, 295-D, Efapi, 89809-000 Chapecó, Santa Catarina, Brazil
Jacir Dal Magro
Affiliation:
Communitarian University of Chapecó Region – UNOCHAPECÓ, Servidão Anjo da Guarda, 295-D, Efapi, 89809-000 Chapecó, Santa Catarina, Brazil
Cássia Alves Lima-Rezende
Affiliation:
Communitarian University of Chapecó Region – UNOCHAPECÓ, Servidão Anjo da Guarda, 295-D, Efapi, 89809-000 Chapecó, Santa Catarina, Brazil
Renan de Souza Rezende*
Affiliation:
Communitarian University of Chapecó Region – UNOCHAPECÓ, Servidão Anjo da Guarda, 295-D, Efapi, 89809-000 Chapecó, Santa Catarina, Brazil
*
Corresponding author: Renan de Souza Rezende; Email: renanrezende30@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Major efforts to control the population of Aedes aegypti mosquitoes involve the use of synthetic insecticides, which can be harmful to the environment. Most plant compounds are eco-friendly and some of them have biocontrol potential, whereas a fraction of these compounds is released into the environment through the leaf-leaching process. We evaluated the effects of secondary compounds from Ateleia glazioviana and Eucalyptus grandis senescent leaf leachates on Ae. aegypti larval mortality, adult emergence time, and wing size using a microcosm approach. The microcosms consisted of 10 larvae kept in water (control) and under four treatments with leachates from a combination of plant species and leaching time (7 or 14 days). Chemical analyses of the leachates showed the presence of carboxaldehyde and Heptatriocotanol, which have antimicrobial properties, potentially reducing the food available for larvae. β-Sitosterol, Stigmasterol, α-Amyrin, and Lupeol are compounds with inhibitory, neurotoxic, and larvicidal effects. Both plant species’ leachates increased larval mortality and decreased emergence time due to the presence of compounds toxic to the larvae. Larger organisms emerged in treatments with 7-days leachates, likely due to the high concentration of dissolved organic matter in the leachates. The higher mortality in 7-days leachates may also increase the organic matter from co-specific decomposition, improving adult size. Therefore, if the mosquito population is not locally extinct, compounds present in leaf leachates may act as a resource enhancing larvae growth, potentially increasing survivors’ fitness. In conclusion, biocontrol attempts using urban green spaces may have unexpected outcomes, such as resulting in larger pest organisms.

Keywords

Adult sizebiopesticidegas chromatographylarval growthplant extractsmass spectrometry analysis
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 113 , Issue 5 , October 2023 , pp. 684 - 692
Check for updates
Copyright
Copyright © The Author(s), 2023. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alievi, K, Capoani, GT, Buzatto, M, Miorando, D, Serpa, PZ, Fogolari, O, Ignácio, ZM, Simões, DA, Busato, MA, Lutinski, JA and Junior, WAR (2021) Ateleia glazioveana and Ocimum basilicum: plants with potential larvicidal and repellent against Aedes aegypti (Diptera, Culicidae). Research, Society and Development 10, e228101724733–e228101724733.CrossRefGoogle Scholar
Barros, FAP, Radünz, M, Scariot, MA, Camargo, TM, Nunes, CFP, Rezende, RS, Gilson, IK, Hackbart, HCS, Radünz, LL, Oliveira, JV, Tramontin, MA, Radünz, AL and Dal-Magro, J (2022) Efficacy of encapsulated and non-encapsulated thyme essential oil (Thymus vulgaris L.) in the control of Sitophilus zeamais and its effects on the quality of corn grains throughout storage. Crop Protection 153, 105885.CrossRefGoogle Scholar
Beleza, S, Campos, D, Nunes, B and Pestana, JLT (2019) Ecotoxicological responses of Chironomus riparius to Eucalyptus and Alnus leaf leachates: from biochemical to life-history effects. Ecological Indicators 106, 105473.CrossRefGoogle Scholar
Bellamy, SK and Alto, BW (2018) Mosquito responses to trait- and density-mediated interactions of predation. Oecologia 187, 233–243.CrossRefGoogle ScholarPubMed
Caneppele, MAB, Andrade, PJ and Santaella, AG (2010) Diferentes dosagens de pó inerte e temperaturas em milho armazenado para controle de gorgulho-do-milho. Scientia Agraria 11, 343–347.CrossRefGoogle Scholar
Canty, A and Ripley, B (2016) Boot: Bootstrap R (S-Plus) functions, p. 117.Google Scholar
Clemensen, AK (2018) “Understanding plant secondary metabolites; above and below ground”. All Graduate Theses and Dissertations. 7090. Available at https://digitalcommons.usu.edu/etd/7090.Google Scholar
Cozzer, GD, Rezende, RS, Lutinski, JA, Júnior, WAR, Busato, MA and Simões, DA (2021) How long is long enough? Decreasing effects in Aedes aegypti larval mortality by plant extracts over time. Brazilian Journal of Environmental Sciences 56, 338–345.Google Scholar
Cozzer, GD, Rezende, RS, Lara, TS, Machado, GH, Magro, JD and Simões, DA (2022) Predation risk effects on larval development and adult life of Aedes aegypti mosquito. Bulletin of Entomological Research 113, 29–36.CrossRefGoogle ScholarPubMed
Crawley, MJ (2007) Statistical modelling. In Crawley, MJ (ed.), The R Book. England: John Wiley and Sons Ltd, pp. 368–386. Available at https://onlinelibrary.wiley.com/doi/book/10.1002/9780470515075.CrossRefGoogle Scholar
Davison, AC and Hinkley, DV (1997) Bootstrap Methods and Their Application, Cambridge Series in Statistical and Probabilistic Mathematics. Cambridge: Cambridge University Press, https://doi.org/10.1017/CBO9780511802843.CrossRefGoogle Scholar
Della Bruna, E, Fernandes, B, Borges, AC, Filho, JA and Barros, NF (1989) Efeito do extrato de serapilheira de Eucalyptus sobre o crescimento microbiano. Pesquisa Agropecuária Brasileira 24, 1523–1528.Google Scholar
Denno, RF, McClure, MS and Ott, JR (1995) Interspecific interactions in phytophagous insects: competition reexamined and resurrected. Annual Review of Entomology 40, 297–331.CrossRefGoogle Scholar
Ebadollahi, A (2013) Essential oils isolated from Myrtaceae family as natural insecticides. Annual Research and Review in Biology 3, 148–175.Google Scholar
Erharuyi, O, Imieje, VO, Oseghale, IO, Ubhenin, AE, Falodun, AB and Choudhary, MI (2017) Identification of compounds and insecticidal activity of the root of pride of Barbados (Caesalpinia Pulcherrima L). Journal of Applied Sciences and Environmental Management 21, 281–287.CrossRefGoogle Scholar
Fader, JE and Juliano, SA (2014) Oviposition habitat selection by container-dwelling mosquitoes: responses to cues of larval and detritus abundances in the field. Ecological Entomology 39, 245–252.CrossRefGoogle ScholarPubMed
Feitosa, FRS, Sobral, IS and Jesus, EN (2015) Indicadores socioambientais como subsídio à prevenção e controle da Dengue. Revista Eletrônica em Gestão, Educação e Tecnologia Ambiental 3, 351–368.CrossRefGoogle Scholar
Fraga, WG, Costa, NR, Almeida, FV, Rebelo, RM, Moraes, KOC, Rezende, JA, Santana, MHP and Maldaner, AO (2016) Identificação dos principais ingredientes ativos em agrotóxicos ilegais apreendidos pela polícia federal do brasil e quantificação do metsulfurom-metílico e tebuconazol. Revista Virtual de Química 8, 561–575.Google Scholar
Gade, S, Rajamanikyam, M, Vadlapudi, V, Nukala, KM, Aluvala, R, Giddigari, C, Karanam, NJ, Barua, NC, Pandey, R, Upadhyayula, VSV, Sripadi, P, Amanchy, R and Upadhyayula, SM (2017) Acetylcholinesterase inhibitory activity of stigmasterol and hexacosanol is responsible for larvicidal and repellent properties of Chromolaena odorata. Biochimica et Biophysica Acta (BBA) - General Subjects 1861, 541–550.CrossRefGoogle ScholarPubMed
Gallo, MB and Sarachine, MJ (2009) Biological activities of lupeol. International Journal of Pharmaceutical and Bio-Medical Science 3, 46–66.Google Scholar
Gallon, C, Martello, RH, Cozzer, G, Lima-Rezende, CA, Calisto, JFF, Floss, PA, Oliveira, JV, Rezende, RS, Dal Magro, J and Albeny-Simões, D (2020) Chemistry matters: biological activity of Eucalyptus essential oils on mosquito larval mortality. Entomologia Experimentalis et Applicata 168, 407–415.CrossRefGoogle Scholar
Gava, A, Barros, CSL, Pilati, C, Barros, SS and Mori, AM (2001) Intoxicação por Ateleia glazioviana (Leg. Papilionoideae) em bovinos. Pesquisa Veterinária Brasileira 21, 49–59.CrossRefGoogle Scholar
Gava, A, Molossi, FA, Ogliari, D, Melchioretto, E, Pasquali, E and Roso, J (2021) Spontaneous poisoning by Ateleia glazioviana (leg. Papilionoideae) in sheep and goats in the West region of Santa Catarina. Pesquisa Veterinária Brasileira 41, 1–6.CrossRefGoogle Scholar
George, DR, Finn, RD, Graham, KM and Sparagano, OA (2014) Present and future potential of plant-derived products to control arthropods of veterinary and medical significance. Parasites and Vectors 7, 28.CrossRefGoogle ScholarPubMed
Goetze, M and Thomé, G (2004) Efeito alelopático de extratos de Nicotiana tabacum e Eucalyptus grandis sobre a germinação de três espécies de hortaliças. Current Agricultural Science and Technology 10, 43–50.Google Scholar
Hanley, ME, Lamont, BB, Fairbanks, MM and Rafferty, CM (2007) Plant structural traits and their role in anti-herbivore defence. Perspectives in Plant Ecology, Evolution and Systematics 8, 157–178.CrossRefGoogle Scholar
Hidalgo, K, Dujardin, JP, Mouline, K, Dabiré, RK, Renault, D and Simard, F (2015) Seasonal variation in wing size and shape between geographic populations of themalaria vector, Anopheles coluzzii in Burkina Faso (West Africa). Acta Tropica 143, 79–88.CrossRefGoogle ScholarPubMed
Ju, YH, Clausen, LM, Allred, KF, Almada, AL and Helferich, WG (2004) β-Sitosterol, β-sitosterol glucoside, and a mixture of β-sitosterol and β-sitosterol glucoside modulate the growth of estrogen-responsive breast cancer cells in vitro and in ovariectomized athymic mice. The Journal of Nutrition 134, 1145–1151.CrossRefGoogle Scholar
Kleckner, CA, Hawley, WA, Bradshaw, WE, Holzapfel, CM and Fisher, IJ (1995) Protandry in Aedes Sierrensis: the significance of temporal variation in female fecundity. Ecology 76, 1242–1250.CrossRefGoogle Scholar
Koricheva, J, Gurevitch, J and Mengersen, K (2013) Handbook of Meta-Analysis in Ecology and Evolution. Princeton: Princeton University Press, p. 592.Google Scholar
Kuppusamy, C, Murugan, K, Arul, N and Yasodha, P (2009) Larvicidal and insect growth regulator effect of α-amyrin acetate from Catharanthus roseus Linn against the malaria vector Anopheles stephensi Liston (Diptera: Culicidae). Entomological Research 39, 78–83.CrossRefGoogle Scholar
Legros, M, Magori, K, Morrison, AC, Xu, C, Scott, TW, Lloyd, AL and Gould, F (2011) Evaluation of location-specific predictions by a detailed simulation model of Aedes aegypti populations. PLoS One 6, e22701.CrossRefGoogle ScholarPubMed
Lima-Camara, TN (2016) Emerging arboviruses and public health challenges in Brazil. Revista de Saúde Pública 50, 1–6.CrossRefGoogle Scholar
Liu, X, Chen, Q, Wang, Z, Xie, L and Xu, Z (2008) Allelopathic effects of essential oil from Eucalyptus grandis × E. urophylla on pathogenic fungi and pest insects. Frontiers of Forestry in China 3, 232–236.CrossRefGoogle Scholar
Mączka, W, Duda-Madej, A, Górny, A, Grabarczyk, M and Wińska, K (2021) Can eucalyptol replace antibiotics? Molecules 26, 4933.CrossRefGoogle ScholarPubMed
Marangoni, C, Moura, NF and Garcia, FRM (2013) Utilização de óleos essenciais e extratos de plantas no controle de insetos. Revista de Ciências Ambientais 6, 92–112.Google Scholar
Mascaro, UCP, Rodrigues, LA, Bastos, JK, Santos, E and Costa, JPC (1998) Valores de DL50 em peixes e no rato tratados com pó de raízes de Derris spp e suas implicações ecotoxicológicas. Pesquisa Veterinária Brasileira 18, 53–56.CrossRefGoogle Scholar
Müller, ES, Höhn, C, Almeida, MOP, Patussi, P, Calisto, JFF, Floss, P, Oliveira, AD, Albeny-Simões, D, Rezende, RS, Oliveira, JV and Dal Magro, J (2022) Influence of Eucalyptus spp. essential oils and tannins on herbivory. Research, Society and Development 11, e14611628903–e14611628903.CrossRefGoogle Scholar
Nobsathian, S, Bullangpoti, V, Kumrungsee, N, Wongsa, N and Ruttanakum, D (2018) Larvicidal effect of compounds isolated from Maerua siamensis (Capparidaceae) against Aedes aegypti (Diptera: Culicidae) larvae. Chemical and Biological Technologies in Agriculture 5, 8.CrossRefGoogle Scholar
Pimentel, B and Burgess, M (2014) Environmental and economic costs of the application of pesticides primarily in the United States. In Pimentel, D and Peshin, R (eds), Integrated Pest Management. Dordrecht: Springer, pp. 47–71.CrossRefGoogle Scholar
Poletti, M and Omoto, C (2003) Resistência de inimigos naturais a pesticidas. Revista Biotecnologia Ciência e Desenvolvimento 30, 1–17.Google Scholar
Quimbayo, M, Rúa-Uribe, G, Parra-Henao, G and Torres, C (2014) Evaluación de ovitrampas letales como estrategia para el control de Aedes aegypti. Biomédica 34, 473–482.CrossRefGoogle ScholarPubMed
R Development Core Team (2014) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing.Google Scholar
Rezende, RS, Leite, GFM, De-Lima, AKS, Silva-Filho, LAB, Chaves, CVC, Prette, ACH, Freitas, JS and Gonçalves, JF Jr (2015) Effects of density and predation risk on leaf litter processing by Phylloicus sp. Austral Ecology 40, 693–700.CrossRefGoogle Scholar
Rezende, RS, Medeiros, AO, Gonçalves, JF Jr, Feio, MJ, Gusmão, EP, Gomes, VÂA, Calor, A and Almeida, JSD (2019) Patterns of litter inputs, hyphomycetes and invertebrates in a Brazilian savanna stream: a process of degradative succession. Journal of Tropical Ecology 35, 297–307.CrossRefGoogle Scholar
Rezende, RS, Cararo, ER, Chimello, V, Lima-Rezende, CA, Albeny-Simões, D, Dal Magro, J and Gonçalves, JF Jr (2021) Land cover affects the breakdown of Pinus elliottii needles litter by microorganisms in soil and stream systems of subtropical riparian zones. Limnologica 90, 125905.CrossRefGoogle Scholar
Rezende, RS, Cararo, ER, Bernardi, JP, Chimello, V, Lima-Rezende, CA, Moretto, Y and Gonçalves, JF Jr (2023) Small hydropower plants lead to higher litter breakdown rates in by-passed sections than in impounded reaches. Aquatic Sciences 85, 26.CrossRefGoogle Scholar
Saito, M and Luchini, F (1998) Substâncias obtidas de plantas e a procura por praguicidas eficientes e seguras ao meio ambiente. Brasil: Embrapa-Meio Ambiente Jaguariúna, 46pp.Google Scholar
Saleemi, MA, Yahaya, N, Zain, NNM, Raoov, M, Yong, YK, Noor, NS and Lim, V (2022) Antimicrobial and cytotoxic effects of Cannabinoids: an updated review with future perspectives and current challenges. Pharmaceuticals 15, 1228.CrossRefGoogle ScholarPubMed
Sena, G, Gonçalves, JF Jr, Martins, RT, Hamada, N and Rezende, RS (2020) Leaf litter quality drives the feeding by invertebrate shredders in tropical streams. Ecology and Evolution 10, 8563–8570.CrossRefGoogle ScholarPubMed
Silva, RCM, Torre, PAD and Matos, JC (2021) O uso incorreto do inseticida fipronil e sua influência na morte das abelhas no sul do Brasil. Revista Processando o Saber 13, 93–110.Google Scholar
Simas, NK, Lima, EC, Conceição, SR, Kuster, RM, Oliveira Filho, AM and Lage, CLS (2004) Produtos naturais para o controle da transmissão da dengue: atividade larvicida de Myroxylon balsamum (óleo vermelho) e de terpenóides e fenilpropanóides. Química Nova 27, 46–49.CrossRefGoogle Scholar
Singer, TP and Ramsay, RR (1994) The reaction site of rotenone and ubiquinone with mitochondrial NADH dehydrogenase. Biochimica et Biophysica Acta 1187, 198–202.CrossRefGoogle ScholarPubMed
Soares, FSC, Soares, MS, Fernandes, FL, Visôtto, LE and Pires, EM (2015) Inseticidas botânicos: extração, identificação de metabólitos secundários e aplicação no controle de pragas. In Avanços Tecnológicos Aplicados à Pesquisa na Produção Vegetal. Available at https://www.posagroprodvegetal.crp.ufv.br/wp-content/uploads/2012/02/Livro-min.pdf.Google Scholar
Subramaniam, S, Keerthiraja, M and Sivasubramanian, A (2014) Synergistic antibacterial action of β-sitosterol-D-glucopyranoside isolated from Desmostachya bipinnata leaves with antibiotics against common human pathogens. Revista Brasileira de Farmacognosia 24, 44–50.CrossRefGoogle Scholar
Ukoroije, R and Otayor, R (2020) Review on the bio-insecticidal properties of some plant secondary metabolites: types, formulations, modes of action, advantages and limitations. Asian Journal of Research in Zoology 3, 27–60.Google Scholar
Viana, GA (2018) Prospecção fitoquímica e avaliação da atividade larvicida de extratos obtidos de Hyptis suaveolens, Ipomoea cairica e Cryptostegia grandiflora sobre Aedes albopictus (Skuse, 1894) (Diptera:Culicidae). Dissertação de Mestrado (MASTS), 1, 18–80.Google Scholar
Wattanachaiyinssgcharoen, W, Phanmuangma, W, Boonphong, S, Suphrom, N and Prasanpan, S (2020) Sex pheromone and pattern of mating communication of fireflies in subfamily Lampyrinae (Coleoptera: Lampyridae). PSRU Journal of Science and Technology 5, 35–46.Google Scholar
Yee, DA, Kesavaraju, B and Juliano, SA (2007) Direct and indirect effects of animal detritus on growth, survival, and mass of invasive container mosquito Aedes albopictus (Diptera: Culicidae). Journal of Medical Entomology 44, 580–588.CrossRefGoogle ScholarPubMed
Zara, ALSA, Santos, SM, Fernandes-Oliveira, ES, Carvalho, RG and Coelho, GE (2016) Estratégias de controle do Aedes aegypti: uma revisão. Epidemiologia e Serviços de Saúde 25, 391–404.Google Scholar