Log in

Larvicidal, molluscicidal and nematicidal activities of essential oils and compounds from Foeniculum vulgare

  • Original Paper
  • Published:
Journal of Pest Science Aims and scope Submit manuscript

Abstract

Plant-based products, namely essential oils (EOs), are environmentally friendly alternatives for the control of disease vectors, hosts and/or parasites. Here, we studied the general toxicity and biopesticidal potential of EOs and phenylpropanoids from Foeniculum vulgare var. vulgare (bitter fennel), a perennial plant well adapted to temperate climates. EO/compound toxicity was tested against a freshwater snail and potential intermediate host of Fasciola hepatica (Radix peregra), a mosquito and former European malaria vector (Anopheles atroparvus) and one of the most damaging plant-parasitic nematodes, the root-knot nematode (Meloidogyne javanica). Lethal concentrations (LC50; LC90) of EOs (infrutescences/stems with leaves) and compounds were calculated by probit analysis. All displayed noteworthy activity against R. peregra adults (LC50 21–39 µg ml−1) and A. atroparvus larvae (LC50 16–56 µg ml−1). trans-Anethole revealed acute nematicidal activity after 24 and 48 h (LC50 310 and 249 µg ml−1, respectively), and estragole (1,000 µg ml−1) showed some effectiveness against M. javanica hatching and juveniles after 15 days. Plant and EO yields were determined to evaluate the bitter fennel productivity. The chemical composition of the EOs was analyzed by gas chromatography coupled to mass spectrometry. EOs extracted from whole plants, infrutescences and stems with leaves were characterized by estragole-dominant profiles (28–65 %), considerable amounts of phellandrene (10–34 %) and fenchone (6–16 %), and minor trans-anethole contents (1–4 %). Although additional toxicological studies against nontarget organisms are required, our study demonstrates that bitter fennel is a productive source of molluscicides and larvicides, and thus a potential sustainable biological agent to control particular host species, namely freshwater snails and mosquitoes.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abrantes IM de O, Santos MCV dos, Conceição ILPM da, Santos MSN de A, Vovlas N (2008) Root-knot and other plant-parasitic nematodes associated with fig trees in Portugal. Nematologia Mediterranea 36:3–11

  • Amer A, Mehlhorn H (2006) Larvicidal effects of various essential oils against Aedes, Anopheles, and Culex larvae (Diptera: Culicidae). Parasitol Res 99:466–472

    Article  PubMed  Google Scholar 

  • Andrés MF, González-Coloma A, Sanz J, Burillo J, Sainz P (2012) Nematicidal activity of essential oils: a review. Phytochem Rev 11:371–390

    Article  Google Scholar 

  • Avci AB (2013) Effect of seeding rate on yield and quality of non-chemical fennel (Foeniculum vulgare Mill.) cultivation. Turkish J F Crops 18:27–33

    Google Scholar 

  • Barazani O, Cohen Y, Fait A, Diminshtein S, Dudai N, Ravid U, Putievky E, Friedman J (2002) Chemotypic differenciation in indigenous populations of Foeniculum vulgare var. vulgare in Israel. Biochem Syst Ecol 30:721–731

    Article  CAS  Google Scholar 

  • Bernath J, Nemeth E, Petheo F, Mihalik E, Kalman K, Franke R (1999) Regularities of the essential oil accumulation in develo** fruits of fennel (Foeniculum vulgare Mill.) and its histological background. J Ess Oil Res 11:431–438

    Article  CAS  Google Scholar 

  • Caboni P, Saba M, Tocco G, Casu L, Murgia A, Maxia A, Menkissoglu-Spiroudi U, Ntalli N (2013a) Nematicidal activity of mint aqueous extracts against the root-knot nematode Meloidogyne incognita. J Agric Food Chem 61:9784–9788

    Article  CAS  PubMed  Google Scholar 

  • Caboni P, Aissani N, Cabras T, Falqui A, Marotta R, Liori B, Ntalli N, Sarais G, Sasanelli N, Tocco G (2013b) Potent nematicidal activity of phthalaldehyde, salicylaldehyde, and cinnamic aldehyde against Meloidogyne incognita. J Agric Food Chem 61:1794–1803

    Article  CAS  PubMed  Google Scholar 

  • Chantraine JM, Laurent D, Ballivian C, Saavedra G, Ibanez R, Vilaseca LA (1998) Insecticidal activity of essential oils on Aedes aegypti larvae. Phytother Res 12:350–354

    Article  CAS  Google Scholar 

  • Correa AC, Escobar JS, Durand P, Renaud F, David P, Jarne P, Pointier J-P, Hurtrez-Boussès S (2010) Bridging gaps in the molecular phylogeny of the Lymnaeidae (Gastropoda: Pulmonata), vectors of Fascioliasis. BMC Evol Biol 10:381. doi:10.1186/1471-2148-10-381

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Decraemer W, Hunt DJ (2006) Structure and classification, In: Perry RN, Moens M (eds.) Plant Nematology, CAB International, Wallingford, Oxfordshire, pp. 3–32

  • Ebadollahi A (2011) Susceptibility of Two Sitophilus species (Coleoptera: Curculionidae) to essential oils from Foeniculum vulgare and Satureja hortensis. Ecologia Balkanica 3:1–8

    Google Scholar 

  • Evergetis E, Michaelakis A, Kioulos E, Koliopoulos G, Haroutounian SA (2009) Chemical composition and larvicidal activity of essential oils from six Apiaceae family taxa against the West Nile virus vector Culex pipiens. Parasitol Res 105:117–124

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Jimenez N, Perez-Alonso MJ, Velasco-Negueruela A (2000) Chemical composition of fennel oil, Foeniculum vulgare Miller from Spain. J Essent Oil Res 12:159–162

    CAS  Google Scholar 

  • Gross M, Lewinsohn E, Tadmor Y, Bar E, Dudai N, Cohen Y, Friedman J (2009) The inheritance of volatile phenylpropenes in bitter fennel (Foeniculum vulgare Mill. var. vulgare, Apiaceae) chemotypes and their distribution within the plant. Biochem Syst Ecol 37:308–316

    Article  CAS  Google Scholar 

  • Hunault H, Desmarest P, Du Manoir J (1989) Foeniculum vulgare Miller: cell culture, regeneration, and the production of anethole. In: Bajaj YPS (ed) Biotechnology in agriculture and forestry 7, medicinal and aromatic plants II. Springer, Berlin, pp 185–212

    Google Scholar 

  • Jaiswal P, Singh DK (2009) Molluscicidal Activity of Nutmeg and Mace (Myristica Fragrans Houtt.) against the vector snail Lymnaea acuminata. J Herbs Spices Med Plants 15:177–186

    Article  Google Scholar 

  • Jetten TH, Takken W (1994) Anophelism without malaria in Europe, a review of the ecology and distribution of the genus Anopheles in Europe. Agricultural University Papers 94.5, Wageningen, p 69

  • Jones JT, Haegeman A, Danchin EGT, Gaur HS, Helder J, Jones MGK, Kikuchi T, Manzanilla-López R, Palomares-Rius JE, Wesemael WML, Perry RN (2013) Top 10 plant-parasitic nematodes in molecular plant pathology. Mol Plant Pathol. doi:10.1111/mpp.12057

    Google Scholar 

  • Kim D-H, Ahn Y-J (2001) Contact and fumigant activities of constituents of Foeniculum vulgare fruit against three coleopteran stored-product insects. Pest Manag Sci 57:301–306

    Article  CAS  PubMed  Google Scholar 

  • Kulkarni RR, Pawar PV, Joseph MP, Akulwad AK, Sen A, Joshi SP (2013) Lavandula gibsoni and Plectranthus mollis essential oils: chemical analysis and insect control activities against Aedes aegypti, Anopheles stephensi and Culex quinquefasciatus. J Pest Sci 86(4):713–718

    Article  Google Scholar 

  • Kumar P, Singh DK (2006) Molluscicidal activity of Ferula asafoetida, Syzygium aromaticum and Carum carvi and their active components against the snail Lymnaea acuminata. Chemosphere 63(9):1568–1574

    Article  CAS  PubMed  Google Scholar 

  • Lee H-S (2006) Mosquito larvicidal activity of aromatic medicinal plant oils against Aedes aegypti and Culex pipiens pallens. J Am Mosq Control Assoc 22:292–295

    Article  PubMed  Google Scholar 

  • Maleita CM, Simões MJ, Egas C, Curtis RHC, Abrantes IM de O (2012) Biometrical, biochemical, and molecular diagnosis of Portuguese Meloidogyne hispanica isolates. Plant Dis 96 (6): 865–874

  • Marotti M, Piccaglia R, Giovanelli E, Deans SG, Eaglesham E (1994) Effects of variety and ontogenic stage on the essential oil composition and biological activity of fennel (Foeniculum vulgare Mill.). J Essent Oil Res 6:57–62

    Article  CAS  Google Scholar 

  • Martens P, Kovats RS, Nijhof S, de Vries P, Livermore MTJ, Bradley DJ, Cox J, McMichael AJ (1999) Climate change and future populations at risk of malaria. Glob Environ Change 9:S89–S107

    Article  Google Scholar 

  • Martins AMF (1991) Distribuição dos moluscos de água doce em São Miguel e na Terceira. Acoreana 7:257–276

    Google Scholar 

  • Miraldi E (1999) Comparison of the essential oils from ten Foeniculum vulgare Miller samples of fruits of different origin. Flavour Fragr J 14:379–382

    Article  CAS  Google Scholar 

  • Moens M, Perry RN, Starr JL (2009) Meloidogyne species- a diverse group of novel and important plant parasites. In: Perry RN, Starr JL, Moens M (eds) Root-knot nematodes. CAB International, Wallingford, Oxforshire, pp 1–17

    Chapter  Google Scholar 

  • Muckenstrum B, Foechterlen D, Reduron JP, Danton P, Hildenbrand M (1997) Phytochemical and chemotaxonomic studies of Foeniculum vulgare. Biochem Syst Ecol 25:353–358

    Article  Google Scholar 

  • Napoli EM, Curcuruto G, Ruberto G (2010) Screening the essential oil composition of wild Sicilian fennel. Biochem Syst Ecol 38:213–223

    Article  CAS  Google Scholar 

  • Ntalli NG, Caboni P (2012) Botanical Nematicides: A Review. J Agric Food Chem 60:9929–9940

    Article  CAS  PubMed  Google Scholar 

  • Ntalli NG, Ferrari F, Giannakouc I, Menkissoglu-Spiroudi U (2010) Phytochemistry and nematicidal activity of the essential oils from 8 greek Lamiaceae aromatic plants and 13 terpene components. J Agric Food Chem 58:7856–7863

    Article  CAS  PubMed  Google Scholar 

  • Ntalli NG, Ferrari F, Giannakouc I, Menkissoglu-Spiroudi U (2011) Synergistic and antagonistic interactions of terpenes against Meloidogyne incognita and the nematicidal activity of essential oils from seven plants indigenous to Greece. Pest Manag Sci 67:341–351

    Article  CAS  PubMed  Google Scholar 

  • Odolini S, Gautret P, Parola P (2012) Epidemiology of Imported Malaria in the Mediterranean Region. Mediterr J Hematol Infect Dis 4:e2012031. doi:10.4084/MJHID.2012.031

    Article  PubMed Central  PubMed  Google Scholar 

  • Oka Y (2001) Nematicidal activity of essential oil components against the root-knot nematode Meloidogyne javanica. Nematology 3:159–164

    Article  CAS  Google Scholar 

  • Oka Y, Koltai H, Bar-Eyal M, Mor M, Sharon E, Chet I, Spiegel Y (2000a) New strategies for the control of plant-parasitic nematodes. Pest Manag Sci 56:983–988

    Article  CAS  Google Scholar 

  • Oka Y, Nacar S, Putievsky E, Ravid U, Yaniv Z, Spiegel Y (2000b) Nematicidal activity of essential oils and their components against the root-knot nematode. Phytopathology 90:710–715

    Article  CAS  PubMed  Google Scholar 

  • Padmaja R, Arun PC, Prashanth D, Deepak M, Amit A, Anjana M (2002) Brine Shrimp lethality bioassay of selected Indian medicinal plants. Fitoterapia 73:508–510

    Article  CAS  PubMed  Google Scholar 

  • Pérez MP, Navas-Cortés JA, Pascual-Villalobos MJ, Castillo P (2003) Nematicidal activity of essential oils and organic amendments from Asteraceae against root-knot nematodes. Plant Pathol 52:395–401

    Article  Google Scholar 

  • Piccaglia R, Marotti M (2001) Characterization of some Italian types of Wild Fennel (Foeniculum vulgare Mill.). J Agric Food Chem 49:239–244

    Article  CAS  PubMed  Google Scholar 

  • Pitasawat B, Champakaew D, Choochote W, Jitpakdi A, Chaithong U, Kanjanapothi D, Rattanachanpichai E, Tippawangkosol P, Riyong D, Tuetun B, Chaiyasit D (2007) Aromatic plant-derived essential oil: an alternative larvicide for mosquito control. Fitoterapia 78:205–210

    Article  CAS  PubMed  Google Scholar 

  • Regnault-Roger C, Vincent C, Arnason JT (2012) Essential oils in insect control: Low-risk products in a high-stakes world. Annu Rev Entomol 57:405–424

    Article  CAS  PubMed  Google Scholar 

  • Relf V, Good B, McCarthy E, de Waal T (2009) Evidence of Fasciola hepatica infection in Radix peregra and a mollusc of the family Succineidae in Ireland. Vet Parasitol 163:152–155

    Article  CAS  PubMed  Google Scholar 

  • Sainz-Elipe S, Latorre JM, Escosa R, Masià M, Fuentes MV, Mas-Coma S, Bargues MD (2010) Malaria resurgence risk in southern Europe: climate assessment in an historically endemic area of rice fields at the Mediterranean shore of Spain. Malar J 9:221

    Article  PubMed Central  PubMed  Google Scholar 

  • Sam TW (1993) Toxicity testing using the brine shrimp: Artemia salina. In: Colegate SM, Molyneux RJ (eds.) Bioactive Natural Products: Detection, Isolation, and Structural Determination, CRC Press LLC, pp 441–456

  • Shaaya E, Rafaeli A (2007) Essential oils as biorational insecticides–potency and mode of action. In: Ishaaya I, Nauen R, Horowitz AR (eds) Insecticides design using advanced technologies. Springer, Berlin, pp 249–261

    Chapter  Google Scholar 

  • Solis PN, Wright CW, Anderson MM, Gupta MP, Phillipson JD (1993) A microwell cytotoxicity assay using Artemia salina (Brine Shrimp). Planta Med 59:250–252

    Article  CAS  PubMed  Google Scholar 

  • Sousa LA, Albuquerque JCR, Leite MN, Stefanini MB (2005) Sazonalidade dos ductos secretores e óleo essencial de Foeniculum vulgare var. vulgare Mill. (Apiaceae). Rev Bras Farmacogn 15:155–161

    Article  Google Scholar 

  • Sousa RMOF, Rosa JS, Oliveira L, Cunha A, Fernandes-Ferreira M (2013) Activities of Apiaceae essential oils against armyworm, Pseudaletia unipuncta (Lepidoptera: Noctuidae). J Agric Food Chem 61:7661–7672

    Article  CAS  PubMed  Google Scholar 

  • Suwansirisilp K, Visetson S, Prabaripai A, Tanasinchayakul S, Grieco JP, Bangs MJ, Chareonviriyaphap T (2013) Behavioral responses of Aedes aegypti and Culex quinquefasciatus (Diptera: Culicidae) to four essential oils in Thailand. J Pest Sci 86(2):309–320

    Article  Google Scholar 

  • Telci I, Demirtas I, Sahin A (2009) Variation in plant properties and essential oil composition of sweet fennel (Foeniculum vulgare Mill.) fruits during stages of maturity. Ind Crops Prod 30:126–130

    Article  CAS  Google Scholar 

  • Traboulsi AF, El-Haj S, Tueni M, Taoubi K, Nader NA, Mrad A (2005) Repellency and toxicity of aromatic plant extracts against the mosquito Culex pipiens molestus (Diptera: Culicidae). Pest Manag Sci 61:597–604

    Article  CAS  PubMed  Google Scholar 

  • Waliwitiya R, Kennedy CJ, Lowenberger CA (2009) Larvicidal and oviposition-altering activity of monoterpenoids, trans-anethole and rosemary oil to the yellow fever mosquito Aedes aegypti (Diptera: Culicidae). Pest Manag Sci 65:241–248

    Article  CAS  PubMed  Google Scholar 

  • WHO (World Health Organization) (1965) Memoranda – Molluscicide screening and evaluation. B World Health Organ 33(4):567–581

    Google Scholar 

  • WHO (World Health Organization) (1983) Reports of the scientific working group on plant molluscicides. World Health Organization TDR/SCH-SWG (4)/83.3, p 11

  • WHO (World Health Organization) (2005) Guidelines for laboratory and field testing of mosquito larvicides. WHO Communicable disease control, prevention and eradication. Pesticide evaluation scheme, p 39

  • WHO (World Health Organization) (2014) Foodborne trematode infections, Fascioliasis epidemiology. http://www.who.int/foodborne_trematode_infections/fascioliasis/en/, accessed 5 February 2014

Download references

Acknowledgments

We would like to thank José Ferreira and Diara Rocha from the IHMT for the mosquito colony maintenance and larvae production and collaborators from the Nematology Laboratory of the University of Coimbra for kindly providing the nematode isolate. The authors are grateful to Susana Chaves for improving the use of English in the manuscript. This research was supported by FEDER through POFC–COMPETE and by Portuguese funds through the projects (PIDDAC)-PEst-OE/BIA/UI4050/2014 and PEst-OE/AGR/UI4033/2014. R.M. Sousa was supported by the Portuguese Foundation for Science and Technology (FCT) through a PhD grant (SFRH/BD/66041/2009).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Manuel Fernandes-Ferreira.

Additional information

Communicated by J. Gross.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sousa, R.M.O.F., Rosa, J.S., Silva, C.A. et al. Larvicidal, molluscicidal and nematicidal activities of essential oils and compounds from Foeniculum vulgare . J Pest Sci 88, 413–426 (2015). https://doi.org/10.1007/s10340-014-0628-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10340-014-0628-9

Keywords

Navigation