Skip to main content

Advertisement

SpringerLink
Log in

Eco-friendly larvicide of Amphora coffeaeformis and Scenedesmus obliquus microalgae extracts against Culex pipiens

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

National and international organizations are working together with the World Health Organization to control vector-borne diseases. The extensive uses of synthetic insecticides have led to the development of insect resistance and cause adverse health effects on humans and ecosystem. The current study aimed to study the potential larvicidal activity of microalgae (Amphora coffeaeformis and Scenedesmus obliquus) against the mosquito Culex pipiens.  Toxicity on rats and an eco-toxicology study using the Microtox® test was performed. Liquid chromatography (HPLC) and gas chromatography-mass spectrometry (GC-MS) showed that A. coffeaeformis and S. obliquus extracts have high concentrations of polyphenolic compounds and unsaturated fatty acids. Both A. coffeaeformis and S. obliquus extracts had larvicidal activity with different mechanisms of toxic action against C. pipiens and the LC50 was 513.63 and 855.66 μg mL−1 compared with 173.16 μg mL−1 of the insecticide lambda-cyhalothrin. From toxicological studies on male rats and acute toxicity on bacterial strain of Vibrio fischeri using Microtox toxicity test, the A. coffeaeformis extract can be considered non-toxic to experimental animals and eco-friendly. Therefore, these findings propose the prospect use extracts of microalgae such as A. coffeaeformis as a safe and eco-friendly larvicide against C. pipiens.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abbassy MA, Marei AESM, Al-Ashkar MAM, Mossa ATH (2014) Adverse biochemical effects of various pesticides on sprayers of cotton fields in El-Behira Governorate, Egypt. Biomed Aging Pathol 4:251–256

    Article  CAS  Google Scholar 

  • Abbott WS (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18:265–267

    Article  CAS  Google Scholar 

  • Abdel-Hameed A, Kiviranta J, Sivonen K, Nimelä S, Carlberg G (1993) Algae in mosquito breeding sites and the effectiveness of the mosquito larvicide Bacillus thuringiensis H-14. World J Microbiol Biotechnol 9:156–159

    Article  CAS  PubMed  Google Scholar 

  • Abo El Khair EB, Aboulthana WM, El-Feky AM, Ibrahim NE, Seif MM (2018) Bio and phyto-chemical effect of Amphora coffeaeformis extract against hepatic injury induced by paracetamol in rats. Mol Biol Rep 45:2007–2023

    Article  CAS  Google Scholar 

  • Acheuk F, Doumandji-Mitiche B (2013) Insecticidal activity of alkaloids extract of Pergularia tomentosa (Asclepiadaceae) against fifth instar larvae of Locusta migratoria cinerascens (Fabricius 1781) (Orthoptera: Acrididae). Int J Sci Adv Technol 3:8–13

    Google Scholar 

  • Ahmad R, Chu WL, Ismail Z, Lee HL, Phang SM (2004) Effect of ten chlorophytes on larval survival, development and adult body size of the mosquito Aedes aegypti. Southeast Asian J Trop Med Public Health 35:79–87

    PubMed  Google Scholar 

  • Alarif WM, Abou-Elnaga ZS, Ayyad SEN, Al-Lihaibi SS (2010) Insecticidal metabolites from the green alga Caulerpa racemosa. Clean Soil Air Water 38:548–557

    Article  CAS  Google Scholar 

  • Ali MYS, Ravikumar S, Beula JM (2013) Mosquito larvicidal activity of seaweeds extracts against Anopheles stephensi, Aedes aegypti and Culex quinquefasciatus. Asian Pac J Trop Dis 3:196–201

    Article  PubMed Central  Google Scholar 

  • Álvarez-Díaz PD, Ruiz J, Arbib Z, Barragán J, Garrido-Pérez MC, Perales JA (2015) Wastewater treatment and biodiesel production by Scenedesmus obliquus in a two-stage cultivation process. Bioresour Technol 181:90–96

    Article  PubMed  CAS  Google Scholar 

  • Ananthakrishnan TN (1997) Gallic and salicylic acids: sentinels of plant defence against insects. Curr Sci 73:576–579

    CAS  Google Scholar 

  • Angerilli NP, Beirne BP (1974) Influences of some freshwater plants on the development and survival of mosquito larvae in British Columbia. Can J Zool 52:813–815

    Article  CAS  PubMed  Google Scholar 

  • Bahrami MN, Mikani A, Moharramipour S (2018) Effect of caffeic acid on feeding, α-amylase and protease activities and allatostatin-A content of Egyptian cotton leafworm, Spodoptera littoralis (Lepidoptera: Noctuidae). J Pestic Sci 43:73–78

    Article  CAS  Google Scholar 

  • Barbehenn RV, Peter Constabel C (2011) Tannins in plant-herbivore interactions. Phytochemistry 72:1551–1565

    Article  CAS  PubMed  Google Scholar 

  • Bulut O, Akın D, Sönmez Ç, Öktem A, Yücel M, Öktem HA (2019) Phenolic compounds, carotenoids, and antioxidant capacities of a thermo-tolerant Scenedesmus sp. (Chlorophyta) extracted with different solvents. J Appl Phycol 31:1675–1683

    Article  CAS  Google Scholar 

  • Buxton T, Takahashi S, Eddy Doh AM, Baffoe-Ansah J, Owusu EO, Kim CS (2020) Insecticidal activities of cinnamic acid esters isolated from Ocimum gratissimum L. and Vitellaria paradoxa Gaertn leaves against Tribolium castaneum Hebst (Coleoptera: Tenebrionidae). Pest Manag Sci 76:257–267

    Article  CAS  PubMed  Google Scholar 

  • Catelan TBS, de Arruda EJ, Oliveira LCS, Raminelli C, Gaban CRG, Cabrini I, Nova PCV, Carbonaro ES (2015) Evaluation of toxicity of phenolic compounds using Aedes aegypti (Diptera: Culicidae) and Artemia salina. Adv Infect Dis 05:48–56

    Google Scholar 

  • CEC (1993) Commission Directive 93/67/EEC of 20 July 1993 laying down the principles for assessment of risks to man and the environment of substances notified in accordance with Council Directive 67/548/EEC. Off J Eur Commun L227:9–18

  • Conte FP, Droukas PC, Ewing RD (1977) Development of sodium regulation and de novo synthesis of Na+K-activated ATPase in larval brine shrimp,Artemia salina. J Exp Zool 202:339–361

    Article  CAS  Google Scholar 

  • Czerniewicz P, Sytykiewicz H, Durak R, Borowiak-Sobkowiak B, Chrzanowski G (2017) Role of phenolic compounds during antioxidative responses of winter triticale to aphid and beetle attack. Plant Physiol Biochem 118:529–540

    Article  CAS  PubMed  Google Scholar 

  • Dhanker R, Tiwari A, Dahms H-U, Kumar R, Hwang JS (2019) Influence of three diatom aldehydes against the dengue vector Aedes aegypti (Diptera: Culicidae). Am J Plant Sci 10:1749–1762

    Article  CAS  Google Scholar 

  • Eaton DL, Gallagher EP (2010) General overview of toxicology. In: Eaton DL (ed) Comprehensive Toxicology, 2nd edn. Elsevier, Amsterdam, pp 1–46

    Google Scholar 

  • Finney D (1971) Probit analysis. Cambridge University Press, Cambridge

    Google Scholar 

  • Goławska S, Sprawka I, Łukasik I, Goławski A (2004) Are naringenin and quercetin useful chemicals in pest-management strategies? J Pest Sci 87:173–180

    Article  Google Scholar 

  • Goławska S, Kapusta I, Łukasik I, Wójcicka A (2008) Effect of phenolics on the pea aphid, Acyrthosiphon pisum (Harris) population on Pisum sativum L. (Fabaceae). Pestycydy/Pesticides 3–4:71–77

    Google Scholar 

  • Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chanley MH (eds) Culture of marine invertebrate animals. Plenum Press, New York, pp 29–60

    Chapter  Google Scholar 

  • Hannun YA, Loomis CR, Bell RM (1986) Protein kinase C activation in mixed micelles. Mechanistic implications of phospholipid, diacylglycerol, and calcium interdependencies. J Biol Chem 261:7184–7190

    Article  CAS  PubMed  Google Scholar 

  • Huang T, Jander G, De Vos M (2011) Non-protein amino acids in plant defense against insect herbivores: representative cases and opportunities for further functional analysis. Phytochemistry 72:1531–1537

    Article  CAS  PubMed  Google Scholar 

  • Ivask A, Bondarenko O, Jepihhina N, Kahru A (2010) Profiling of the reactive oxygen species-related ecotoxicity of CuO, ZnO, TiO2, silver and fullerene nanoparticles using a set of recombinant luminescent Escherichia coli strains: Differentiating the impact of particles and solubilised metals. Anal Bioanal Chem 398:701–716

    Article  CAS  PubMed  Google Scholar 

  • Jeyanthi S, Santhanam P, Devi A (2018) Halophilic benthic diatom Amphora coffeaeformis—a potent biomarker for lipid and biomedical application. Indian J Exp Biol 56:698–701

    CAS  Google Scholar 

  • Kang S, Obed WO, Saravanan T, David LH (2017) Toward mosquito control with a green alga: expression of cry toxins of Bacillus thuringiensis subsp. israelensis (Bti) in the chloroplast of Chlamydomonas. J Appl Phycol 29:1377–1389

    Article  CAS  PubMed  Google Scholar 

  • Kannathasan K, Senthilkumar A, Venkatesalu V, Chandrasekaran M (2008) Larvicidal activity of fatty acid methyl esters of Vitex species against Culex quinquefasciatus. Parasitol Res 103:999–1001

    Article  PubMed  Google Scholar 

  • Kauffman E, Payne A, Franke M, Schmid MA, Harris E, Kramer LD (2017) Rearing of Culex spp. and Aedes spp. Mosquitoes. Bio-Protocol 7:1–25

    Article  Google Scholar 

  • Koda Y, Wada A, Yanagihara N, Uezono Y, Izumi F (1989) cis-unsaturated fatty acids stimulate catecholamine secretion, tyrosine hydroxylase and protein kinase C in adrenal medullary cells. Neuroscience 29:495–502

    Article  CAS  PubMed  Google Scholar 

  • Makulla A (2000) Fatty acid composition of Scenedesmus obliquus: correlation to dilution rates. Limnologica 30:162–168

    Article  CAS  Google Scholar 

  • Manilal A, Selvin J, Thajuddin N (2012) Biopotentials of marine alga, Lobophora variegata collected from the south Indian littoral. Thalassas 28:47–54

  • Marques TR, Caetano AA, Alves DS, Ramos VO, Simao AA, Carvalho GA, Correa AD (2016) Malpighia emarginata DC. bagasse acetone extract: phenolic compounds and their effect on Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae). Chil J Agric Res 76:55–61

    Article  Google Scholar 

  • Marten G (1986) Mosquito control by plankton management: the potential of indigestible green algae. J Trop Med Hyg 89:213–222

  • Marten G (2007) Larvicidal algae. J Am Mosq Control Assoc 23:177–183

    Article  PubMed  Google Scholar 

  • Mohafrash SMM, Fallatah SA, Farag SM, Mossa ATH (2020) Mentha spicata essential oil nanoformulation and its larvicidal application against Culex pipiens and Musca domestica. Ind Crop Prod 157:112944

    Article  CAS  Google Scholar 

  • Morohashi M, Tsuchiya K, Mita T, Kawamura M (1991) Identification of (Na,K)ATPase inhibitor in brine shrimp, Artemia salina, as long-chain fatty acids. J Comp Physiol B 161:69–72

    Article  CAS  Google Scholar 

  • Mossa AH (2016) Green pesticides: essential oils as biopesticides in insect-pest management. J Environ Sci Technol 9:354–378

    Article  CAS  Google Scholar 

  • Mossa ATH, Mohafrash SMM, Shalaby AR (2017) Toxicity assessment of chlorpyrifos, malachite green and tetracyclines by microtox® assay: Detoxification by ultrasonic. J Environ Sci Technol 10:68–79

    Article  CAS  Google Scholar 

  • Mossa AH, Afia SI, Mohafrash SMM, Abou-Awad BA (2019) Rosemary essential oil nanoemulsion, formulation, characterization and acaricidal activity against the two-spotted spider mite Tetranychus urticae Koch (Acari: Tetranychidae). J Plant Prot Res 59:102–112

    CAS  Google Scholar 

  • Mossa A-TH, Mohafrash SMM, Ziedan E-SHE, Abdelsalam IS, Sahab AF (2021) Development of eco-friendly nanoemulsions of some natural oils and evaluating of its efficiency against postharvest fruit rot fungi of cucumber. Ind Crop Prod 159:113049

    Article  CAS  Google Scholar 

  • Naqqash MN, Gökçe A, Bakhsh A, Salim M (2016) Insecticide resistance and its molecular basis in urban insect pests. Parasitol Res 115:1363–1373

    Article  PubMed  Google Scholar 

  • National Institute of Standards and Technology (2014) PC Version 1.7 of the NIST/EPA/NIH Mass Spectral Library

  • National Research Council (2010) Guide for the care and use of laboratory animals. National Academies Press, Washington

    Google Scholar 

  • OECD (2001) OECD/OCDE 423 Organisation for Economic Co-Operation and Development (OECD) Guideline for testing of chemicals, acute oral toxicity-acute toxic class method. http://www.oecd.org/officialdocuments/publicdisplaydocumentpdf/?cote=env/jm/mono(2001)4&doclanguage=en. Accessed March 2020

  • Ohmura W, Doi S, Aoyama M, Ohara S (1999) Components of steamed and non-steamed Japanese larch (Larix leptolepis (Sieb. et Zucc.) Gord.) heartwood affecting the feeding behavior of the subterranean termite, Coptotermes formosanus Shiraki (Isoptera: Rhinotermitidae). Holzforschung 53:569–574

    Article  CAS  Google Scholar 

  • Ohmura W, Doi S, Aoyama M, Ohara S (2000) Antifeedant activity of flavonoids and related compounds against the subterranean termite Coptotermes formosanus Shiraki. J Wood Sci 46:149–153

    Article  CAS  Google Scholar 

  • Ow Y-Y, Stupans I (2005) Gallic acid and gallic acid derivatives: effects on drug metabolizing enzymes. Curr Drug Metab 4:241–248

    Article  Google Scholar 

  • Pates H, Curtis C (2005) Mosquito behavior and vector control. Annu Rev Entomol 50:53–70

    Article  CAS  PubMed  Google Scholar 

  • Pohlit AM, Rezende AR, Lopes Baldin EL, Lopes NP, Andrade Neto VFD (2011) Plant extracts, isolated phytochemicals, and plant-derived agents which are lethal to arthropod vectors of human tropical diseases - A review. Planta Med 77:618–630

    Article  CAS  PubMed  Google Scholar 

  • Rajaram MG, Nagaraj S, Manjunath M, Annakkili BB, Chidambaram K, Ramasamy R, Thanasekaran J, Joen-Rong S, Jiun-Yi L (2018) Biofuel and biochemical analysis of Amphora coffeaeformis RR03, a novel marine diatom, cultivated in an open raceway pond. Energies 11:en11061341

    Article  CAS  Google Scholar 

  • Ranson H, Lissenden N (2016) Insecticide resistance in African Anopheles mosquitoes: a worsening situation that needs urgent action to maintain malaria control. Trends Parasitol 32:187–196

    Article  CAS  PubMed  Google Scholar 

  • Rashed S, El-Ayouty Y (1991) Evaluation of certain algal species as biological-control agents against mosquito larvae. Bull Entomol Soc Egypt 19:1–7

    Google Scholar 

  • Sahin S (2019) Scenedesmus obliquus: a potential natural source for cosmetic industry. Int J Second Metab 6:129–136

    Article  Google Scholar 

  • Saldaña MA, Hegde S, Hughes GL (2017) Microbial control of arthropod-borne disease. Mem Inst Oswaldo Cruz 112:81–93

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schoonhoven LM, Van Loon JJA, Dicke M (2005) Plants as insect food: not the ideal. In: Insect-Plant Biology. Oxford University Press, Oxford, pp 83–120

  • Silva VCB, Ribeiro Neto JA, Alves SN, Lima LAR d S (2015) Larvicidal activity of oils, fatty acids, and methyl esters from ripe and unripe fruit of Solanum lycocarpum (Solanaceae) against the vector culex quinquefasciatus (diptera: Culicidae). Rev Soc Bras Med Trop 48:610–613

    Article  Google Scholar 

  • Sushanth VR, Rajashekhar M (2015) Effect of twelve species of marine phytoplankton on larval survival and development of the mosquito Culex quinquefasciatus. Int J Mar Sci 5:1–5

    Google Scholar 

  • Usha Rani P, Pratyusha S (2014) Role of castor plant phenolics on performance of its two herbivores and their impact on egg parasitoid behaviour. BioControl 59:513–524

    Article  CAS  Google Scholar 

  • Valentina J, Poonguzhali T, Josmin Laali Nisha L (2015) Mosquito larvicidal and pupicidal activity of seaweed extracts against Aedes aegypti, Anopheles stephensi and Culex quinquefasciatus. Int J Mosquito Res 2:54–59

  • van den Berg H, Zaim M, Yadav RS, Soares A, Ameneshewa B, Mnzava A, Hii J, Dash AP, Ejov M (2012) Global trends in the use of insecticides to control vector-borne diseases. Environ Health Perspect 120:577–582

    Article  PubMed  PubMed Central  Google Scholar 

  • Vieira C, Gaubert J, De Clerck O, Payri C, Culioli G, Thomas OP (2017) Biological activities associated to the chemodiversity of the brown algae belonging to genus Lobophora (Dictyotales, Phaeophyceae). Phytochem Rev 16:1–17

    Article  CAS  Google Scholar 

  • Vinagre TM, Alciati JC, Yunes JS, Richards J, Bianchini A, Monserrat JM (2002) Effects of extracts from the cyanobacterium Microcystis aeruginosa on ion regulation and gill Na+, K+-ATPase and K+-dependent phosphatase activities of the estuarine crab Chasmagnathus granulata (Decapoda, Grapsidae). Physiol Biochem Zool 75:600–608

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Zhao Z, Abou-Zaid MM, Arnason JT, Liu R, Walshe-Roussel B, Waye A, Liu S, Saleem A, Cáceres LA, Wei Q (2014) Inhibition of insect glutathione S-transferase (GST) by conifer extracts. Arch Insect Biochem Physiol 87:234–249

    Article  CAS  PubMed  Google Scholar 

  • War AR, Paulraj MG, Ahmad T, Buhroo AA, Hussain B, Ignacimuthu S, Sharma HC (2012) Mechanisms of plant defense against insect herbivores. Plant Signal Behav 7:1306–1320

    Article  PubMed  PubMed Central  Google Scholar 

  • World Health Organization (1981) Instructions for determining the susceptibility or resistance of mosquito larvae to insecticides. World Health Organization

  • World Health Organization (2005) Guidelines for laboratory and field testing of mosquito larvicides (No. WHO/CDS/WHOPES/GCDPP/2005.13). World Health Organization

  • World Health Organization (2014) Vector-borne diseases. WHO Regional Office for South-East Asia

  • World Health Organization (2018) Global report on insecticide resistance in malaria vectors: 2010–2016

  • Wu K, Zhang J, Zhang Q, Zhu S, Shao Q, Clark KD, Liu Y, Ling E (2015) Plant phenolics are detoxified by prophenoloxidase in the insect gut. Sci Rep 5:1–15

    Google Scholar 

  • Yu KX, Wong CL, Ahmad R, Jantan I (2015) Mosquitocidal and oviposition repellent activities of the extracts of seaweed Bryopsis pennata on Aedes aegypti and Aedes albopictus. Molecules 20:14082–14102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Toxicology Department, Research Institute of Medical Entomology, Giza, Egypt

    Marwa E. Hassan

  2. Pesticide Chemistry Department, National Research Centre (NRC), 33 El Bohouth Street (former El Tahrir St.), P.O. 12622, Giza, Dokki, Egypt

    Samia M. M. Mohafrash & Abdel-Tawab H Mossa

  3. Department of Biology, College of Science, Imam Abdulrahman Bin Faisal University, P.O. Box 4476, Dammam, 31491, Saudi Arabia

    Sahar A. Fallatah

  4. Fertilization Technology Department, Biological and Agricultural Research Division, National Research Centre, Giza, Egypt

    Abo El-Khair B. El-Sayed

Authors
  1. Marwa E. Hassan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Samia M. M. Mohafrash
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sahar A. Fallatah
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Abo El-Khair B. El-Sayed
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Abdel-Tawab H Mossa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Abdel-Tawab H Mossa.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hassan, M.E., Mohafrash, S.M.M., Fallatah, S.A. et al. Eco-friendly larvicide of Amphora coffeaeformis and Scenedesmus obliquus microalgae extracts against Culex pipiens. J Appl Phycol 33, 2683–2693 (2021). https://doi.org/10.1007/s10811-021-02440-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-021-02440-0

Keywords

Search

Navigation