Phytochemistry Reviews

, Volume 11, Issue 4, pp 371–390

Nematicidal activity of essential oils: a review

Authors

    • Instituto de Ciencias Agrarias, CSIC
  • Azucena González-Coloma
    • Instituto de Ciencias Agrarias, CSIC
  • Jesus Sanz
    • Instituto de Química Orgánica, CSIC
  • Jesus Burillo
    • Centro de Investigación y Tecnología Agroalimentaria de Aragón
  • Paula Sainz
    • Instituto de Ciencias Agrarias, CSIC
Article

DOI: 10.1007/s11101-012-9263-3

Cite this article as:
Andrés, M.F., González-Coloma, A., Sanz, J. et al. Phytochem Rev (2012) 11: 371. doi:10.1007/s11101-012-9263-3

Abstract

Plant parasitic nematodes are the most destructive group of plant pathogens worldwide and their control is extremely challenging. Plant Essential oils (EOs) and their constituents have a great potential in nematode control since they can be developed for use as nematicides themselves or can serve as model compounds for the development of derivatives with enhanced activity. This study reviews the plant EOs evaluated as potential nematicides and their toxic effects against pinewood nematode (Bursaphelenchus xylophilus) and root-knot nematodes (Meloidogyne spp.). Additionally, the nematicidal activity to M. javanica of several EOs from Spanish aromatic plants and their components is described.

Keywords

Essential oilsNematicidal activityRoot-knot nematodesMeloidogynePinewood nematodeBursaphelenchus xylophilusHyssopus officinalisLippia albaMentha arvensisM. longifoliaM. piperitaM. rotundifoliaM. spicataSatureja montanaThymus mastichinaT. vulgarisT. zygis

Abbreviations

EOs

Essentials oils

J2

Second-stage juveniles of Meloidogyne spp

GC-MS

Gas chromatography-mass spectrometry

GABA

Gamma-aminobutyric acid

AChE

Acetylcholinesterase

Introduction

Plant parasitic nematodes are the most destructive group of plant pathogens worldwide and their control is extremely challenging (Bird et al. 2009). They parasite a large variety of crops through worldwide and their impact on yield losses has been estimated to a billion of euros annually (Bleve-Zacheo et al. 2007). Plant parasitic nematodes attack theirs host by using a wide range of strategies. They can be ectoparasites, that feed on the outer plant tissues or endoparasitic that feed and live inside the plant tissues. Several important plant-parasitic nematodes are endoparasites. Sedentary endoparasites (cyst and root-knot nematodes), represent the most advanced and successful type of parasitism, they are biotrophic and induce profound changes in the roots of theirs host as they feed (Castagnone-Sereno et al. 2006). The root-knot nematodes, Meloidogyne spp, are one of the most economically damaging genera of plant-parasitic nematodes on horticultural and field crops. Migratory endoparasitic nematodes do not feed from a single site but move through the plant, causing extensive damage as they move and feed. Within this group should be noted the pine wood nematode, Bursaphelenchus xylophilus, that is the causal agent of pine wilt disease that causes serious economic losses in pine forests.

Synthetic nematicides have been used to protect moderate-to-high-value crops in intensive productions systems throughout most of the twentieth century. In the last decades, environmental and human health concerns have steadily reduced the availability of efficient commercial nematicides (Nyczepir and Thomas 2009; Sorribas and Ornat 2011). Therefore, less toxic pesticides need to be developed. Phytochemicals have a great potential in nematode control since they can be developed for use as nematicides themselves or can serve as model compounds for the development of derivatives with enhanced activity (Chitwood 2002).

Essential oils (EOs) are natural volatile substances found in a variety of plants. They are complex mixture of mainly terpenoids, particularity monoterpenes and sequiterpenes, and a variety of aromatic phenols, oxides, ethers, alcohols esters, aldehydes and ketones that determine the characteristic aroma and odor of the plant. Their chemical composition may vary considerably between aromatic plant species and varieties, and within the same variety from different geographic areas. In addition the effect of plant maturity at the time of oil extraction and the existence of chemotypic differences can also drastically affect their composition (Lahlou and Berrada 2003). Commercially, EOs are valuable natural products used in the cosmetic, food and pharmaceutical industries (Buchbauer 2000). Although aromatic plants and their essentials oils have been used since ancient times as antimicrobial and insecticidal agents, the interest in has been increased remarkably during the past decade. The presence of volatile monoterpenes on EOs provides an important defense strategy to the plant against insect pests and pathogenic organisms. These terpenoids also play a role in plant parasitic interactions, acting as signaling molecules (Batish et al. 2008). Thus, in the last few years much effort has been focused on the study of the nematicidal activity of plant EOs and their constituents as potential sources of commercial products for management of plan parasitic nematodes.

This study reviews the plant EOs evaluated as potential nematicides and their toxic effects against pinewood (B. xylophilus) and root-knot nematodes (Meloidogyne spp.). Additionally, the nematicidal activity to M. javanica of several EOs from experimentally cultivated Spanish aromatic plants and their components is described.

Essential oils with nematicidal effects

A large number of EOs extracted from different botanical families has been analyzed in vitro for nematicidal activity mainly against B. xylophilus and Meloidogyne spp (Table 1). Among EO-producing plants some families such Lamiaceae, Asteraceae, Myrtaceae, Rutaceae, Lauraceae and Poaceae have been widely studied. Especially the aromatic plants of the genera Artemisia, Cympogon, Lavandula, Mentha, Oreganum, Ocimum,Rosmarinus, Thymus, and aromatic trees of the genera Citrus, Eucalyptus,Eugenia and Melaleuca who have been traditionally used for protection of stored commodities, mainly in the Mediterranean region and in Southern Asia.
Table 1

Plant EOs tested for nematicidal activity against root-knot nematodes (Meloidogyne spp.) and pinewood nematode (B. xylophilus)

Nematode species evaluated

Plant source

Family plant

Part used

Country

Reference

Meloidogyne artiella

Chrysanthemun coronarium*

Asteraceae

Flowers

Spain

Pérez et al. (2003)

Meloidogyne exigua

Bixa Orellana*

Bixaceae

 

Brasil

Salgado et al. (2003)

Cymbopogon nardus

Poaceae

 

Brasil

Salgado et al. (2003)

Melia azedarach*

Meliaceae

 

Brasil

Salgado et al. (2003)

Xylopia brasiliensis*

Annonaceae

 

Brasil

Salgado et al. (2003)

Eucaliptus camadulensis*

Myrtaceae

 

Brasil

Salgado et al. (2003)

Eucaliptus saligma*

Myrtaceae

 

Brasil

Salgado et al. (2003)

Eucaliptus urophylla*

Myrtaceae

 

Brasil

Salgado et al. (2003)

Meloidogyne incognita

Cympogon flexuosus*

Poaceae

Foliage

India

Pandey et al. (2000), Sinha et al. (2006)

Eucaliptus citriodora*

Myrtaceae

Foliage

India

Pandey et al. (2000)

Eucaliptus hybrida*

Myrtaceae

Foliage

India

Pandey et al. (2000)

Mentha arvensis*

Lamiaceae

Foliage

India

India

India

Pandey et al. (2000)

Sinha et al. (2006)

Gupta et al. (2011)

Mentha piperita*

Lamiaceae

  

Pandey et al. (2000)

Mentha spicata*

Lamiaceae

Foliage

India

India

Pandey et al. (2000)

Sinha et al. (2006)

Ocimum basilicum*

Lamiaceae

Foliage

India

India

Pandey et al. (2000)

Sinha et al. (2006)

Pelargonium graveolensis*

Geraniaceae

Foliage

India

Pandey et al. (2000)

Foeniculum vulgare

Umbeliferae

Flowers

Libano

Ibrahim et al. (2006)

Cympogon martinii*

Poaceae

Foliage

India

Pandey et al. (2000), Sinha et al. (2006)

Cympogon nardus*

Poaceae

 

India

Sinha et al. (2006)

Mentha citrata*

Lamiaceae

 

India

Sinha et al. (2006)

Tagetes minuta*

Asteraceae

Whole plant

India

Adekunle et al. (2007)

Pectis apodocephala*

Asteraceae

Aerial part

Brasil

Albuquerque et al. (2007)

Pectis oligocephala*

Asteraceae

Aerial part

Brasil

Albuquerque et al. (2007)

Eugenia caryophyllata*

Myrtaceae

Buds

Sigma

India

Meyer et al. (2008)

Gupta et al. (2011)

Croton regelianus

Euphorbiaceae

Leaves

Brasil

Torres et al. (2008)

Cymbopogon winterianus*

Poaceae

 

Brasil

Moreira et al. (2009)

Cymbopogon citratus*

Poaceae

 

Brasil

India

Moreira et al. (2009)

Gupta et al. (2011)

Eucalyptus terenticornis

Myrtaceae

 

Brasil

Moreira et al. (2009)

Lippia alba*

Verbenacea

 

Brasil

Moreira et al. (2009), Marino et al. (2012)

Lippia sidoides*

Verbenacea

 

Brasil

Moreira et al. (2009)

Ocimum gratissimum

Lamiaceae

 

Brasil

Moreira et al. (2009)

Origanum vulgare*

Lamiaceae

Aerial part

Greece

Ntalli et al. (2011)

Origanum dictamnus*

Lamiaceae

Aerial part

Greece

Ntalli et al. (2011)

Mentha pulegium*

Lamiaceae

Aerial part

Greece

Ntalli et al. (2011)

Melissa officinales*

Lamiáceas.

Aerial part

Greece

Ntalli et al. (2011)

Chenopodium ambrosioides

Amaranthaceae

Aerial part

China

Chuan et al. (2011)

Carum capticum*

Apiaceae

 

India

Gupta et al. (2011)

Cedrus deodara

Pinaceae

 

India

Gupta et al. (2011)

Eucaliptus globulas*

Myrtaceae

 

India

Gupta et al. (2011)

Kadsura heteroclite*

Schisandraceae

Stems

China

Li et al. (2011)

Achillea millefolium

Asteraceae

Aerial part

Greece

Ntalli et al. (2011)

Eucaliptus meliodora*

Myrtaceae

Aerial part

Greece

Ntalli et al. (2011)

Foeniculum vulgare*

Apiaceae

Aerial part

Greece

Ntalli et al. (2011)

Juglans regia

Juglandaceae

Aerial part

Greece

Ntalli et al. (2011)

Laurus nobilis

Lauraceae

Aerial part

Greece

Ntalli et al. (2011)

Pimpinella anisum*

Apiaceae

Aerial part

Greece

Ntalli et al. (2011)

Pistacia terebinthus*

Anacardiaceae

Aerial part

Greece

Ntalli et al. (2011)

Meloidogyne javanica

Achillea fragrantissima

Asteraceae

Foliage

Israel

Oka et al. (2000)

Artemisia arboresses

Asteraceae

Foliage

Israel

Oka et al. (2000)

Artemisia dracunculus

Asteraceae

Foliage

Israel

Oka et al. (2000)

Artemisia judaica*

Asteraceae

Foliage

Israel

Oka et al. (2000)

Carum carvi*

Apiaceae

Foliage

Israel

Oka et al. (2000)

Coridothymus capitatus*

Lamiaceae

Foliage

Israel

Oka et al. (2000)

Cymbopogon citratus*

Poaceae

Foliage

Israel

Oka et al. (2000)

Foeniculum vulgare*

Lamiaceae

Umbels

Israel

Oka et al. (2000)

Laurus nobilis

Lauraceae

Foliage

Israel

Oka et al. (2000)

Lavandula officialis

Lamiaceae

Foliage

Israel

Oka et al. (2000)

Mentha piperita

Lamiaceae

Foliage

Israel

Oka et al. (2000)

Mentha rotundifolia*

Lamiaceae

Foliage

Israel

Oka et al. (2000)

Mentha spicata*

Lamiaceae

Foliage

Israel

Oka et al. (2000)

Micromeria fruticosa

Lamiaceae

Foliage

Israel

Oka et al. (2000)

Myrtus communis

Myrtaceae

Foliage

Israel

Oka et al. (2000)

Ocimum basilicum

Lamiaceae

Foliage

Israel

Oka et al. (2000)

Origanum dayi

Lamiaceae

Foliage

Israel

Oka et al. (2000)

Origanum syriacum

Lamiaceae

Foliage

Israel

Oka et al. (2000)

Origanum vulgare

Lamiaceae

Foliage

Israel

Oka et al. (2000)

Pelargonium graveolens

Geraniaceae

Foliage

Israel

Oka et al. (2000)

Rosmarinus officinalis

Labiatae

Foliage

Israel

Oka et al. (2000)

Salvia dominica

Lamiaceae

Foliage

Israel

Oka et al. (2000)

Salvia officinalis

Lamiaceae

Foliage

Israel

Oka et al. (2000)

Salvia triloba

Lamiaceae

Foliage

Israel

Oka et al. (2000)

Thymus vulgaris

Lamiaceae

Foliage

Israel

Oka et al. (2000)

Cinnamomum verum

Lauraceae

Bark

Korea

Park et al. (2005)

Leptospermun petersonii

Myrtaceae

Leaves

Korea

Park et al. (2005)

Haplophyllum tuberculatum*

Rutaceae

Aerial parts

Oman

Onifade et al. (2008)

Plectranthus cylindraceus*

Lamiaceae

Aerial parts

Oman

Onifade et al. (2008)

Bacharis salicifolia

Asteracea

Aerial parts

Argentina

Sosa et al. (2012)

Eupatorium arnotii

Asteracea

Aerial parts

Argentina

Sosa et al. (2012)

Eupatorium buniifolium

Asteracea

Aerial parts

Argentina

Sosa et al. (2012)

Eupatorium inulaefolium

Asteracea

Aerial parts

Argentina

Sosa et al. (2012)

Eupatorium viscidum*

Asteracea

Aerial parts

Argentina

Sosa et al. (2012)

Bursaphelenchus xylophilus

Agastache rugosa

Lamiaceae

Whole plant

Korea

Park et al. (2005)

Allium sativum

Liliaceae

Bulb

Korea

Park et al. (2005)

Angelica dahurica

Apiaceae

Roots

Roots

Korea

Korea

Park et al. (2005)

Choi et al. (2007b)

Armoracia rusticana

Brassicaceae

Roots

Korea

Park et al. (2005)

Asiarum sieboldi

Aristolochiaceae

Roots

Korea

Park et al. (2005)

Atractylodes japonica

Asteraceae

Roots

Korea

Choi et al. (2007b)

Boswellia carterii*

Burceraceae

Resin

Resin

Resin

Resin

Korea

Jin-Ah Korea

Korea

Ethiopia

Ethiopia

Park et al. (2005)

Kong et al. (2006)

Choi et al. (2007b)

Park et al. (2007)

Kim et al. (2011)

Cananga odorata

Annonaceae

Flower

Korea

Park et al. (2005)

Carum carvi

Apiaceae

Seeds

Seeds

Korea

Berje-USA

Egypt

Park et al. (2005)

Kong et al. (2006)

Park et al. (2007)

Chenopodium ambrosioides

Chenopodiaceae

Whole plant

Whole plant

Korea

Korea

Park et al. (2005)

Choi et al. (2007b)

Cinnamomum camphora

Lauraceae

Wood

Korea

Park et al. (2005)

Cinnamomum verum

Lauraceae

Bark

Korea

Park et al. (2005)

Citrus bergamia

Rutaceae

Peel

Korea

Jin-Ah-Korea

Park et al. (2005)

Kong et al. (2006)

Citrus limonum

Rutaceae

Peel

Korea

Jin-Ah-Korea

Park et al. (2005)

Kong et al. (2006)

Citrus paradise

Rutaceae

Peel

Jin-Ah Korea

Park et al. (2005), Kong et al. (2006)

Citrus reticulata

Rutaceae

Rind

Leaves

Italy/Brazil

Egypt

Park et al. (2005)

Kong et al. (2006), Kim et al. (2011)

Citrus sinensis

Rutaceae

Peel

Korea

Jin-Ah Korea

Park et al. (2005)

Kong et al. (2006)

Cnidium officindle

Apiaceae

Roots

Roots

Korea

Korea

Park et al. (2005)

Choi et al. (2007b)

Cupressus sempervirens

Cupressaceae

Leaves

Korea

Berje-USA

Park et al. (2005)

Kong et al. (2006)

Curcuma longa

Zingiberaceae

Roots

Korea

Korea

Park et al. (2005)

Choi et al. (2007b)

Cymbopogon citratus*

Poaceae

Whole plant

Korea

Jin-Ah Korea

Portugal

Park et al. (2005)

Kong et al. (2006)

Barbosa et al. (2010)

Cymbopogon nardus

Poaceae

Whole plant

Korea

Berje_USA

Park et al. (2005)

Kong et al. (2006)

Eucalyptus citriodora

Myrtaceae

Leaves

Korea

Jin-Ah Korea

Park et al. (2005)

Kong et al. (2006)

Eucalyptus dives

Myrtaceae

Leaves

Korea

Park et al. (2005)

Eucalyptus globulus

Myrtaceae

Leaves

Berje-USA

Kong et al. (2006)

Eucalyptus smithii

Myrtaceae

Leaves

Korea

Park et al. (2005)

Eucalyptus polybractea

Myrtaceae

Leaves

Korea

Park et al. (2005)

Eucalyptus radiata

Myrtaceae

Leaves

Korea

Park et al. (2005)

Eugenia caryophyllata*

Myrtaceae

Lower bud

Korea

Berje-USA

Park et al. (2005)

Kong et al. (2006)

Evodia officinalis

Rutaceae

Fruits

Fruits

Korea

Korea

Park et al. (2005)

Choi et al. (2007b)

Lavandula officinalis

Lamiaceae

Flowering plant

Korea

Park et al. (2005)

Leptospermum petersonii

Myrtaceae

Leaves

Korea

Park et al. (2005)

Melaleuca dissitiflora

Myrtaceae

Leaves

Korea

Park et al. (2005)

Melaleuca uncinata

Myrtaceae

Leaves

Korea

Park et al. (2005)

Melaleuca linariifolia

Myrtaceae

Leaves

Korea

Park et al. (2005)

Melaleuca quinquenervia

Myrtaceae

Leaves

Korea

Park et al. (2005)

Mentha spicata

Lamiaceae

Whole plant

Korea

Jin-Ah Korea

Park et al. (2005)

Kong et al. (2006)

Nardostachys chinensis

Valerianaceae

Roots

Roots

Roots

Korea

Korea

China

Park et al. (2005)

Choi et al. (2007b)

Kim et al. (2008)

Ocimum basilicum

Lamiaceae

Leaves

Korea

Berje-USA

Park et al. (2005)

Kong et al. (2006)

Pelargonium graveolens

Geraniaceae

Leaves

Leaves

Korea

Berje-USA

Reunion

Park et al. (2005)

Kong et al. (2006)

Park et al. (2007)

Pimenta racemosa

Myrtacea

Leaves

Korea

Jin-Ah Korea

Park et al. (2005)

Kong et al. (2006)

Pimpinella anisum

Apiaceae

Flower bud

Korea

Berje-USA

Park et al. (2005)

Kong et al. (2006)

Elbadri et al. (2008)

Piper nigrum

Piperaceae

Leaves

Korea

Jin-Ah Korea

Park et al. (2005)

Kong et al. (2006)

Zingiber officinale

Zingiberaceae

Rhizome

Korea

Park et al. (2005)

Abies alba

Pinaceae

 

Jin-Ah Korea

Kong et al. (2006)

Abies sibirica

Pinaceae

 

Berje-USA

Kong et al. (2006)

Achillea millefolium

Asteraceae

 

Berje-USA

Kong et al. (2006)

Acorus calamus

Acoraceae

 

Berje-USA

Kong et al. (2006)

Agothosma betulina

Rutaceae

 

Berje-USA

Kong et al. (2006)

Amyris balsamifera

Rutaceae

Wood

Berje-USA

Caribbean

Kong et al. (2006)

Park et al. (2007)

Anethum graveolens

Apiaceae

Seeds

Berje-USA

Bulgaria

Kong et al. (2006)

Park et al. (2007)

Angelica archangelica

Apiaceae

 

Jin-Ah Korea

Kong et al. (2006)

Aniba rosaeodora

Lauraceae

 

Berje-USA

Kong et al. (2006)

Anthemis nobilis

Asteraceae

Blossoms

Jin-Ah Korea

France

Kong et al. (2006)

Kim et al. (2008)

Apium graveolens

Apiaceae

Flowering plant

Berje-USA

Morocco

Kong et al. (2006)

Kim et al. (2008)

Artemisia absinthium

Asteraceae

Aerial parts

Jin-Ah Korea

Portugal

Kong et al. (2006)

Barbosa et al. (2010)

Artemisia dracunculus

Asteraceae

Aerial parts

Berje-USA

Portugal

Kong et al. (2006)

Barbosa et al. (2010)

Artemisia pallens

Asteraceae

Leaves

Berje-USA

India

Kong et al. (2006)

Park et al. (2007)

Bulnesia sarmienti

Zygophyllaceae

 

Berje-USA

Kong et al. (2006)

Cananga odorata

Annonaceae

 

Berje-USA

Kong et al. (2006)

Cinnamomum zeylanicum*

Lauraceae

Green leaves and bark

Berje-USA

Korea

Kong et al. (2006)

Kong et al. (2006)

Citrus aurantifolia

Rutaceae

 

Berje-USA

Kong et al. (2006)

Citrus aurantium

Rutaceae

 

Berje-USA

Kong et al. (2006)

Citrus reticulata

Rutaceae

Rind

Leaves

Italy/Brazil

Egypt

Kong et al. (2006)

Kim et al. (2011)

Commiphora myrrha

Burseraceae

 

Berje-USA

Kong et al. (2006)

Coriandrum sativum*

Apiaceae

Fruits

Herb

Berje-USA

Argentina

Slovenia

Kong et al. (2006)

Park et al. (2007)

Kim et al. (2008)

Croton eluteria

Euphorbiaceae

 

Berje-USA

Kong et al. (2006)

Cupressus funebris

Cupressaceae

 

Berje-USA

Kong et al. (2006)

Cymbopogon martini

Poaceae

 

Berje-USA

Kong et al. (2006)

Daucus carota

Apiaceae

Seeds

Berje-USA

France

Kong et al. (2006)

Park et al. (2007)

Ferula galbaniflua

Apiaceae

 

Berje-USA

Kong et al. (2006)

Gaultheria procumbens

Ericaceae

 

Berje-USA

Kong et al. (2006)

Helichrysum angustifolium

Asteraceae

 

Berje-USA

Kong et al. (2006)

Hyssopus officinalis

Lamiaceae

Flowering plant

Berje-USA

France

Kong et al. (2006)

Park et al. (2007)

Juniperus communis

Cupresaceae

 

Berje-USA

Kong et al. (2006)

Juniperus oxycedrus

Cupresaceae

 

Berje-USA

Kong et al. (2006)

Juniperus virginiana

Cupresaceae

 

Berje-USA

Kong et al. (2006)

Lavandula angustifolia

Lamiaceae

 

Jin-Ah Korea

Kong et al. (2006)

Lavandula intermedia

Lamiaceae

 

Berje-USA

Kong et al. (2006)

Levisticum officinale

Apiaceae

 

Berje-USA

Kong et al. (2006)

Litsea cubeba*

Lauraceae

Fruits

Berje USA

Vietnam

Kong et al. (2006)

Park et al. (2007)

Melaleuca alternifolia

Myrtaceae

 

Berje-USA

Kong et al. (2006)

Melaleuca viridiflora

Myrtaceae

 

Berje-USA

Kong et al. (2006)

Melissa officinalis

Lamiaceae

 

Berje-USA

Kong et al. (2006)

Mentha piperita

Lamiaceae

 

Berje-USA

Kong et al. (2006)

Mentha pulegium

Lamiaceae

Aerial parts

Berje-USA

Portugal

Kong et al. (2006)

Barbosa et al. (2010)

Mentha spicata

Lamiaceae

 

Jin-Ah Korea

Kong et al. (2006)

Myristica fragrans

Miristicaceae

 

Berje-USA

Kong et al. (2006)

Myrtus communis

Myrtaceae

Aerial parts

Jin-Ah Korea

Portugal

Kong et al. (2006)

Barbosa et al. (2010)

Origanum vulgare*

Lamiaceae

Aerial parts

Berje-USA

Portugal

Kong et al. (2006)

Barbosa et al. (2010)

Petroselinum crispum

Apiaceae

 

Berje-USA

Kong et al. (2006)

Pimenta dioica*

Myrtacea

Berries

Berje-USA

Jamaica

Kong et al. (2006)

Park et al. (2007)

Pimenta officinalis

Myrtacea

 

Berje-USA

Kong et al. (2006)

Pimpinella anisum

Apiaceae

 

Berje-USA

Kong et al. (2006), Elbadri et al. (2008)

Piper nigrum

Piperaceae

 

Jin-Ah Korea

Kong et al. (2006)

Pogostemon patchouli

Lamiaceae

Whole plant

Jin-Ah Korea

Indonesia

Kong et al. (2006)

Park et al. (2007)

Rosa damascene

Rosaceae

 

Berje-USA

Kong et al. (2006)

Rosmarinus officinalis

Labiatae

 

Berje-USA

Kong et al. (2006)

Salvia lavendulaefolia

Lamiaceae

 

Jin-Ah Korea

Kong et al. (2006)

Salvia officinalis

Lamiaceae

 

Jin-Ah Korea

Kong et al. (2006)

Salvia sclarea

Lamiaceae

 

Jin-Ah Korea

Kong et al. (2006)

Santalum album

Santalaceae

 

Jin-Ah Korea

Kong et al. (2006)

Sassafras albidum

Lauraceae

Wood

Berje-USA

India

Kong et al. (2006)

Kim et al. (2008)

Satureja hortensis

Lamiaceae

 

Berje

Kong et al. (2006)

Tagetes glandulifera

Asteraceae

 

Jin-Ah Korea

Kong et al. (2006)

Thuja occidentalis

Cupressaceae

 

Jin-Ah Korea

Kong et al. (2006)

Thymus capitatus

Lamiaceae

 

Berje USA

Kong et al. (2006)

Thymus mastichina

Lamiaceae

Aerial parts

Berje-USA

Portugal

Kong et al. (2006)

Barbosa et al. (2010)

Thymus vulgaris*

Lamiaceae

 

Berje USA

Kong et al. (2006), Elbadri et al. (2008)

Valeriana officinalis

Valerianaceae

Roots

Berje-USA

China

Kong et al. (2006)

Kim et al. (2011)

Vetiveria zizanoides

Poaceae

 

Jin-Ah Korea

Kong et al. (2006)

Zingiber officinale

Zingiberaceae

 

Jin-Ah Korea

Kong et al. (2006)

Acorus gramineus

Araceae

Roots

Korea

Choi et al. (2007b)

Agastache rugosa

Labiatae

Whole plant

Korea

Choi et al. (2007b)

Amomum cardamomum

Zingiberaceae

Fruit

Korea

Choi et al. (2007b)

Amomum globosum*

Zingiberaceae

Fruits

Korea

Choi et al. (2007b)

Artemisia capillaries

Asteraceae

Whole plant

Korea

Choi et al. (2007b)

Asiasarum heterotropoides

Aristolochiaceae

Root

Korea

Choi et al. (2007b)

Atractylodes japonica

Asteraceae

Root

Korea

Choi et al. (2007b)

Carpesium abrotanoides

Asteraceae

Fruits

Korea

Choi et al. (2007b)

Curcuma zedoaria

Zingiberaceae

Root

Korea

Choi et al. (2007b)

Cyperus rotundus

Cyperaceae

Root

Korea

Choi et al. (2007b)

Forsythia koreana

Oleaceae

Fruits

Korea

Choi et al. (2007b)

Juniperus chinensis

Cupressaceae

Wood

Korea

Choi et al. (2007b)

Myristica fragrans

Myristicaceae

Fruits

Korea

Choi et al. (2007b)

Paeonia moutan*

Paeoniaceae

Roots

Korea

Choi et al. (2007b)

Perilla frutescens*

Labiatae

Leaves

Korea

Choi et al. (2007b)

Poncirus trifoliata

Rutaceae

Fruits

Korea

Choi et al. (2007b)

Santalum album

Santalaceae

Wood

Korea

Choi et al. (2007b)

Saussurea lappa

Asteraceae

Roots

Korea

Choi et al. (2007b)

Schizandra chinensis

Schizandraceae

Fruits

Korea

Choi et al. (2007b)

Schizonepeta tenuifolia*

Labiatae

Whole plant

Korea

Choi et al. (2007b)

Styrax benzoin

Styraceae

Resin

Korea

Choi et al. (2007b)

Zanthoxylum piperitum

Rutaceae

Fruits

Korea

Choi et al. (2007b)

Allium cepa*

Liliaceae

Bulb

Germany

Choi et al. (2007c)

Cinnamonum cassia

Lauraceae

Leaves

Korea

Kong et al. (2006)

Amyris balsamifera

Rutaceae

Wood

Caribbean

Park et al. (2007)

Artemisia afra

Asteraceae

Flowering plant

South Africa

Park et al. (2007)

Cananga odorata

Annonaceae

Blossoms

Indonesia

Park et al. (2007)

Canarium luzonicum

Burseraceae

Resin

Phillipines

Park et al. (2007)

Citrus clementina

Rutaceae

Rind

South Africa

Park et al. (2007)

Copaifera reticulata

Fabaceae

Resin

Brazil

Park et al. (2007)

Dipterocarpus turbinatus

Dipterocarpaceae

Resin

Indonesia

Park et al. (2007)

Elettaria cardamomum

Zingiberaceae

Seeds

Equador

Park et al. (2007)

Ferula galbaniflua

Apiaceae

Resin

Iran

Park et al. (2007)

Fokienia hodgensii

Cupressaceae

Wood

Vietnam

Park et al. (2007)

Larix europea

Pinaceae

Resin

Austria

Park et al. (2007)

Lavandula hybrida

Lamiaceae

Flowering plant

France

Park et al. (2007)

Melaleuca cajuputii

Myrtaceae

Leaves

Indonesia

Park et al. (2007)

Myrocarpus fastigiatus

Fabaceae

Wood

Brazil

Park et al. (2007)

Trachyspermum ammi*

Apiaceae

Seeds

India

Park et al. (2007)

Brassica integrafolia*

Brassicaceae

 

Korea

Elbadri et al. (2008)

Pelargonium inquinans*

Geraniaceae

 

Korea

Elbadri et al. (2008)

Syzygium aromaticum*

Myrtaceae

 

Korea

Elbadri et al. (2008)

Ammi visnaga

Apiaceae

Flowering plant

Morocco

Kim et al. (2008)

Artemisia arborescens

Asteraceae

Flowering plant

Morocco

Kim et al. (2008)

Chrysanthemum morifolium

Asteraceae

Flowering plant

China

Kim et al. (2008)

Commiphora myrrha

Burseraceae

Resin

Somalia

Kim et al. (2008)

Cyperus scariosus

Cyperaceae

Roots

India

Kim et al. (2008)

Eriocephalus punctulatus

Asteraceae

Flowering plant

South Africa

Kim et al. (2008)

Helichrysum angustifolium

Asteraceae

Blossoms

Croatia

Kim et al. (2008)

Inula racemosa

Asteraceae

Roots

India

Kim et al. (2008)

Leptospermum ericoides

Myrtaceae

Leaves

New Zealand

Kim et al. (2008)

Lippia javanica

Verbenaceae

Flowering plant

Zimbabwe

Kim et al. (2008)

Liquidambar orientalis*

Altingiaceae

Resin

Turkey

Kim et al. (2008)

Michelia alba

Magnoliaceae

Leaves

China

Kim et al. (2008)

Miroxylon balsamum

Fabaceae

Resin

El Salvador

Kim et al. (2008)

Nigella sativa

Ranunculaceae

Seeds

India

Kim et al. (2008)

Ormensis multicaulis

Asteraceae

Blossoms

Morocco

Kim et al. (2008)

Pastinaca sativa

Apiaceae

Whole plant

Croatia

Kim et al. (2008)

Pogostemon patchouli

Lamiaceae

Whole plant

Indonesia

Kim et al. (2008)

Salvia stenophylla

Lamiaceae

Leaves

South Africa

Kim et al. (2008)

Styrax benzoin

Styracaceae

Resin

Indonesia

Kim et al. (2008)

Valeriana wallichii*

Valeraniaceae

Roots

India

Kim et al. (2008)

Calamintha baetica

Lamiaceae

Aerial parts

Portugal

Barbosa et al. (2010)

Chamaespartium tridentatum*

Fabaceae

Flowers

Portugal

Barbosa et al. (2010)

Chamomilla recutita

Asteraceae

Flowers

Portugal

Barbosa et al. (2010)

Cistus ladanifer

Cistaceae

Aerial parts

Portugal

Barbosa et al. (2010)

Crithmum maritimum

Apiaceae

Aerial parts

Portugal

Barbosa et al. (2010)

Cryptomeria japonica

Taxodiaceae

Leaves

Portugal

Barbosa et al. (2010)

Foeniculum vulgare

Apiaceae

Aerial parts

Portugal

Barbosa et al. (2010)

Juniperus brevifolia

Cupressaceae

Aerial parts

Portugal

Barbosa et al. (2010)

Laurus azorica

Lauraceae

Aerial parts

Portugal

Barbosa et al. (2010)

Laurus nobilis

Lauraceae

Leaves

Portugal

Barbosa et al. (2010)

Lavandula dentata

Lamiaceae

Aerial parts

Portugal

Barbosa et al. (2010)

Lavandula luisieri

Lamiaceae

Aerial parts

Portugal

Barbosa et al. (2010)

Lavandula stoechas

Lamiaceae

Aerial parts

Portugal

Barbosa et al. (2010)

Lavandula viridis

Lamiaceae

Aerial parts

Portugal

Barbosa et al. (2010)

Myrtus communis

Myrtaceae

Aerial parts

Portugal

Barbosa et al. (2010)

Pittosporum undulatum

Pittosporaceae

Aerial parts

Portugal

Barbosa et al. (2010)

Salvia officinalis

Lamiaceae

Aerial parts

Portugal

Barbosa et al. (2010)

Satureja montana*

Lamiaceae

Leaves

Portugal

Barbosa et al. (2010)

Thymbra capitata*

Lamiaceae

Aerial parts

Portugal

Barbosa et al. (2010)

Thymus caespititius*

Lamiaceae

Aerial parts

Portugal

Barbosa et al. (2010)

Thymus zygis

Lamiaceae

Aerial parts

Portugal

Spain

Barbosa et al. (2010)

Kim et al. (2011)

Artemisia dracunculus

Asteraceae

Plant

France

Kim et al. (2011)

Abelmoschus seminis

Malvaceae

Seeds

India

Kim et al. (2011)

Boswellia serrata

Burseraceae

Resin

India

Kim et al. (2011)

Bulnesia sarmientoi

Zygophyllaceae

Wood

Brazil

Kim et al. (2011)

Chamecyparia obutusa

Cupressaceae

Wood

Japan

Kim et al. (2011)

Croton niveous

Euphorbiaceae

Bark

Latin America

Kim et al. (2011)

Dipteryx odorata

Fabaceae

Seeds

Brazil

Kim et al. (2011)

Ferula galbaniflua

Apiaceae

Resin

Iran

Kim et al. (2011)

Gaultheria fragrantissima*

Ericaceae

Leaves

Nepal

Kim et al. (2011)

Hedychium spicatum

Zingiberaceae

Roots

India

Kim et al. (2011)

Helichrysum bracteiferum

Asteraceae

Blossoms

South Africa

Kim et al. (2011)

Hypericum perforatum

Asteraceae

Plant

France

Kim et al. (2011)

Lippia citriodora

Verbenáceas

Flowering plant

Morocco

Kim et al. (2011)

Myrtus communis

Myrtaceae

Flowering plant

Morocco

Kim et al. (2011)

Michelia alba

Magnoliaceae

Blossoms

China

Kim et al. (2011)

Nelumbo nucifera

Nymphaceas

Blossoms

India

Kim et al. (2011)

Osmanthus fragrans

Oleaceae

Blossoms

China

Kim et al. (2011)

Petroselinum sativum

Apiaceae

Herb

Hungary

Kim et al. (2011)

Populus balsamifera

Salicaceae

Leaves

Canada

Kim et al. (2011)

Tagetes minuta

Asteraceae

Blossoms

Egypt

Kim et al. (2011)

Polianthes tuberose

Salicaceae

Blossoms

Brazil

Kim et al. (2011)

Tasmannia lanceolata

Winteraceae

Fruits

New Zealand

Kim et al. (2011)

Vitis vinifera

Vitaceae

Yeast

France

Kim et al. (2011)

Zanthoxylum alatum*

Rutaceae

Fruits

Nepal

Kim et al. (2011)

Active plant EOs are marked with asterisk

The majority of studies evaluating the nematicidal activity of EOs against B. xylophilus have been carried out in Korea, where the pine wilt disease, caused by the pinewood nematode, is the most serious problem in forests of the southern parts of the country. Thus, it has been demonstrated that EOs extracted from Boswellia carterii, Cymbopogon citrates, Eugenia caryophyllata (Park et al. 2005), Cinnamomum zeylanicum, Coriandrum sativum, Litsea cubeba, Origanum vulgare, Pimenta dioica, Thymus vulgaris (Kong et al. 2006), Allium cepa, Paeonia moutan, Perilla frutescens, Schizonepeta tenuifolia(Choi et al. 2007b, Choi et al. 2007c), Trachyspermum ammi (Park et al. 2007), Brassica integrefolia, Pelargonium inquinans, Syzygium aromaticum (Elbadri et al. 2008), Coriandrum sativum, Liquidambar orientalis, Valeriana wallichii (Kim et al. 2008) and Gaultheria fragrantissima and Zanthoxylum alatum (Kim et al. 2011) had significant activity to pinewood nematode under in vitro conditions. Moreover, the recently occurrence and increasing dispersion of B. xylophilus in Portugal promoted the study of the nematicidal activity of EOs from selected species of aromatic plants from the Iberian flora. Strong lethal effects to pinewood nematode were achieved with EOs from Chamaespartium tridentatum, Origanum vulgare, Satureja montana, Thymbra capitata and Thymus caespititius (Barbosa et al. 2010).

The nematicidal effects of EOs from spices and medicinal plants on root-knot nematodes have been widely reported. Several studies described the high mortality that EOs of Cymbopogon grasses (Cymbopogon martini motia, C. flexuosus and C. winterianus) caused to juveniles (J2) of root-knot nematodes (Meloidogyne incognita and M. javanica) (Sangwan et al. 1985; Saxena et al. 1987). Oka et al. (2000) evaluated the nematicidal activity of 25 plant spices and aromatic plants against M. javanica. They showed that EOs from Artemisia judaica, Carum carvi, Corridothymus capitatus, Cybopogon citratus, Foeniculum vulgare, Mentha rotundifolia, Mentha spicata caused J2 immobilization and egg hatching inhibition at 1,000 μl/l. High toxicity of Cymbopogon (C. citratus, C. flexuous, C. martinii, C.nardus and C.winterianus), Mentha (M. arvensis, M. citrata, M. piperita, M. pulegium and M. spicata), Perlargonium graveolens and Ocimun basilicum EOs to M. incognita J2 at different concentrations has been reported (Leela et al. 1992; Pandey et al. 2000; Sinha et al. 2006; Moreira et al. 2009; Ntalli et al. 2010). Pérez et al. (2003) demonstrated that Chrysantemum coronarium oil (at 2, 4, 8, and 16 μl/ml), significantly reduced egg hatching, J2 survival and reproduction rate of M. artiella. EOs from Eucalyptus spp. also have nematicidal activity (Batish et al. 2008). Specifically, E. citriodora and E. hybrida, are toxic to M. incognita J2 (Saxena et al. 1987) even at low concentrations (Pandey et al. 2000), E. camadulensis, E. saligma and E. urophylla caused the mortality of M. exigua J2 (Salgado et al. 2003) and E. globulus and E. meliodora acted on M. incognita (Gupta et al. 2011; Ntalli et al. 2011). High mortality of M. exigua J2 was induced by Bixa orellana, Melia azedarach and Xylopia brasiliensis oils (Salgado et al. 2003). EOs from aerial parts of Pectis oligocephala and P. apodocephala exhibited mortality effects against M. incognita J2 (Albuquerque et al. 2007). A soy lecithin/detergent formulation of clove (Eugenia caryophyllata) oil induced egg and J2 mortality of M. incognita (Meyer et al. 2008) and the application of clove oil reduced M. hapla gall numbers of on carrots (Douda et al. 2010). Tagetes spp. are known for their ability to suppress plant-parasitic nematodes in the field (Krueger et al. 2007) and a further in vitro study has revealed that different oil concentrations (1–4 %) from T. minuta have strong toxicity to eggs and juveniles of M. incognita (Adekunle et al. 2007). The potential of Haplophyllum tuberculatum and Plectranthus cylindraceus oils to control root-knot nematodes have been investigated. Although both oils were toxic to M. javanica (12.5 μg/ml), the greatest juvenile toxicity and egg hatching inhibition effects were obtained by 1:1 mixtures of the two oils (Onifade et al. 2008). EOs from Lippia spp. (L. sidoides and L. alba) induced M. incognita J2 mortality (Moreira et al. 2009; Marino et al. 2012). Ntalli et al. (2010) have shown high nematicidal activity of Origanum vulgare and O. dictamnus EOs against M. incognita, with 1.55 and 1.72 μl/ml EC50 respectively. Moreover, O. majorana essential oil has been tested for M. hapla management on carrot (Douda et al. 2010). Recently, nematicidal effects against M. incognita of EOs from Chenopodium ambrosioides, Foenicum vulgare,Kadsura heteroclita,Pistacia terebinthus, Pimpinella anisum have been demonstrated (Chuan et al. 2011; Li et al. 2011; Ntalli et al. 2011), while Sosa et al. (2012) have shown strong toxic effects of Eupatorium viscidum essential oil to M. javanica juveniles.

Results and discussion

Nematicidal EOs from Spanish cultivated Lamiaceae

The nematicidal effects of the selected EOs from experimentally cultivated Spanish aromatic plants are shown in Tables 2, 3 and 4. Most of the tested oils, M. arvensis, M. rotundifolia, M. spicata, Satureja montana, Thymus mastichina, T. vulgaris and T. zygis, induced 100 % mortality of J2 M. javanica at 1 mg/ml after 12, 48 and 72 h exposure. S. montana oil was the most effective with the lowest LC50 (0.041 mg/ml) and LC90 (0.087 mg/ml). The rest of LC50 and LC90 values ranged from 0.300 to 0.204 and 0.456–0.320 mg/ml, respectively.
Table 2

Effects of 11 plant essentials oils (1 μg/μl) on mortality of second stage juveniles (J2) of Meloidogyne javanica

Botanical name

J2 mortality (%)a after

24 h

48 h

72 h

Hyssopus officinalis

0

0

0

Lippia alba

0

0

10.6

Mentha arvensis

100

100

100

M. longifolia

0

0

0

M. piperita

0

0

4.5

M. rotundifolia

100

100

100

M. spicata

100

100

100

Satureja montana

100

100

100

Thymus mastichina

100

100

100

T. vulgaris

100

100

100

T. zygis

100

100

100

aCorrected according to Scheider–Orelli’s formula. Values are means of four replicates

Table 3

LC50 and LC90 values of selected EOs against second stage juveniles (J2) of Meloidogyne javanica

Botanical name

LC50 mg/mla (95 % CLb)

LC90 mg/mla (95 % CLb)

Mentha arvensis

0.291 (0.284–0.298)

0.409 (0.396–0.425)

M. rotundifolia

0.204 (0.196–0.213)

0.320 (0.308–0.334)

M. spicata

0.293 (0.286–0.300)

0.403 (0.392–0.418)

Satureja montana

0.041 (0.037–0.044)

0.087 (0.083–0.094)

Thymus mastichina

0.300 (0.289–0.313)

0.456 (0.430–0.489)

T. vulgaris

0.224 (0.218–0.230)

0.337 (0.327–0.348)

T. zygis

0.226 (0.220–0.233)

0.333 (0.323–0.344)

aMortality was observed 72 h after treatment. Five concentrations were used to obtain LC50 and LC90, and four replicates were used for each treatment

bCL denotes confidence limit

Table 4

Effects of active essentials oils (1 μg/μl) on hatching of eggs in eggs masses of M. javanica in time

Botanical name

Relative hatch suppression rate (%)a in timeb

0

2

7

13

20

27

Mentha arvensis

86

67

35

42

37

36

M. rotundifolia,

41

73

67

71

67

58

M. spicata

94

95

70

69

63

61

Satureja montana

98

85

57

59

53

52

Thymus mastichina

0

30

6

11

10

10

T. vulgaris

96

76

69

62

60

59

T. zygis

99

90

51

38

35

34

aEach value represents the hatch inhibition in the respective treatment corrected according to the control (Scheider–Orelli’s formula). Values are means of four replicates

bTime 0: after 5 days of immersion in test solutions; time 2: 2 days of immersion in water after time 0; time 7:7 days of immersion in water after time 0; time 13: 13 days of immersion in water after time 0; time 20: 20 days of immersion in water after time 0; time 27: 27 days of immersion in water after time 0

Egg hatching tests are more accurate than counting immobile juveniles in a particular population (Oka et al. 2000). In soil, root knot nematode eggs are aggregated within egg masses surrounded by a gelatinous matrix which serve as a protective barrier against soil-borne antagonists (Kok et al. 2001; Orion et al. 2001). Therefore, the egg hatch inhibition activity tested on egg masses is an indication of the extract/compound ability to penetrate the gelatinous matrix and act on nematode eggs. The egg hatchability test (Table 4) indicated that Mentha arvensis, M. spicata,S. montana,T. vulgaris and T. zygis EOs strongly suppressed M. javanica egg hatching after 5 days of incubation. The percentage reduction ranged from 86 to 99 %. After their exposure to the EOs, the hatch rate of eggs masses immersed in water increased over time. At 27 days, M. spicata, M. rotundifolia, S. montana, and T. vulgaris oils inhibited over 50 % egg mass hatching, with a relative suppression rate of 61, 58, 52 and 59 % respectively. These results indicate that the effects of EOs tested are stronger on J2 mortality than on egg mass hatching.

The chemical compositions of the EOs evaluated are shown in Table 5. A total of 13 compounds were identified. In Mentha arvensis and M. spicata oils, the most abundant compound was carvone, followed by 1,8-cineole and menthol. The major components of M. rotundifolia oil were piperitone oxide and two unidentified compounds. Thymol was found as the main compound in T. vulgaris and T. zygis oil, followed by p-cymene, γ-terpinene and carvacrol. Carvacrol was the major constituent of S. montana oil. The most abundant compound in T. mastichina oil was 1,8-cineole, followed by α-terpineol, linalool and β-pinene.
Table 5

Main components of evaluated essential oils

Botanical name

Main components

Hyssopus officinalis

1,8-Cineole (53 %), β-pinene (12 %), pinocamphone (6 %)

Lippia alba

Linalool (77 %), 1,8-cineole (5 %)

Mentha arvensis

Carvone (75 %), 1,8-cineole (14 %), menthol (1 %)

M. longifolia

Menthone (49 %), menthol (24 %)

M. piperita

Menthone (41 %), menthol (31 %)

M. rotundifolia

Piperitone oxide (25 %), M+(166), 67, 138, 41 (25 %), M+(166), 67, 138, 41 (25 %)

M. spicata

Carvone (79 %), 1,8-cineole (12 %), menthol (2 %)

Satureja montana

Carvacrol (76 %), p-cymene (2 %)

Thymus mastichina

1,8-Cineole (79 %), α-terpineol (6 %), linalool (3 %), β-pinene (2 %)

T. vulgaris

Thymol (49 %), p-cymene (29 %) γ-terpinene (7 %), carvacrol (4 %)

T. zygis

Thymol (74 %), p-cymene (9 %) γ-terpinene (7 %), carvacrol (4 %)

Nematicidal activity of oils from Mentha species has been widely studied. High activity has been recorded in vitro for oils of M. rotundifolia and M. spicata against M. javanica (Oka et al. 2000) and for M. arvensis and M spicata oils to M. incognita (Pandey et al. 2000; Sinha et al. 2006). Nonetheless this is the first report of the nematicidal effects of M. arvensis oil to M. javanica. Among Thymus species, only T. vulgaris oil has been tested against root-knot nematodes by Oka et al. (2000), but only a moderate effect on J2 immobilization and egg hatching inhibition of M. javanica at 1,000 μl/l was reported. This divergence with the present findigs may be explained by intraspecific variability in plant chemical composition (Koul et al. 2008). T. vulgaris is native to the Mediterranean region. It grows wild in almost all the countries bordering Mediterranean area, Asia and Central Europe and it is extensively cultivated in Spain, Germany, France, England and various other neighboring countries, so there are a large number of ecotypic variations and chemotypic races or populations. The nematicidal activity of T. vulgaris oil could significantly increase its commercial value since the global production of oil is 20–30 tons per year and in Spain is the largest producer (Joy et al. 2001).

This study demonstrates for the first time the nematicida activity of S. montana, T. zygys and T. mastichina EOs against root-knot nematodes. Oils from T. zygys and S. montana have shown nematicidal effects against B. xylophylus (Kong et al. 2006; Barbosa et al. 2010) but no nematicidal activity was found of T. mastichina essential oil to the pinewood nematode (Kong et al. 2006; Barbosa et al. 2010). Both Thymus species, T. mastichina and T. zygys, are Iberian endemic plants. The nematicidal effects of their oils are of interest for future integrated pest management programmes (Koul et al. 2008) and to promote their cultivation in the Mediterranean region.

Nematicidal activity of EO major components

A series of 13 mono and sesquiterpenes (Fig. 1) and seven paired mixtures were selected to be tested on M. javanica based on the EOs composition (Tables 6 and 7). The highest mortality effects (100 %) on M. javanica J2 (0.5 mg/ml, 72 h incubation) were induced by carvacrol, geraniol and thymol, followed by citronellol. These compounds were also very effective at egg mass hatching inhibition and their values of relative suppression rate ranged from 71 % (geraniol) to 91 % (carvacrol). These results agreed with previous findings where carvacrol, geraniol and thymol showed high nematicidal activity against M. javanica (Oka 2001), M. incognita (Al-Banna et al. 2003; Ntalli et al. 2010), and B. xylophilus (Choi et al. 2007a; Kong et al. 2007; Park et al. 2007) while 1,8-cineole, menthol, menthone and pinene were not effective against M. javanica (Al-Banna et al. 2003). Interestingly, Echeverrigaray et al. (2010) indicated that among acyclic alcohols, those with the hydroxyl group at C1 (geraniol and citronellol) were more effective against M. incognita than linalool, with the hydroxy group at C3 (Fig. 1). Similarly to our results, geraniol exhibited higher nematicidal activity to M. incognita than citronellol, indicating that the position of the functional group and the double bond can also affect the activity of the monoterpenoid (Park et al. 2007).
https://static-content.springer.com/image/art%3A10.1007%2Fs11101-012-9263-3/MediaObjects/11101_2012_9263_Fig1_HTML.gif
Fig. 1

Chemical structure of the terpenoids tested against Meloidogyne javanica

Table 6

Effects of 13 compounds and seven paired mixtures (0.5 μg/μl) on mortality of second stage juveniles (J2) of Meloidogyne javanica

Compound/s

J2 mortality (%)a at 72 h

Carvacrol

100

Carvone

3.06

β-Caryophyllene

1.86

1,8-cineole

0

Citronellol

83.1

Eugenol

13.1

Geraniol

100

Linalool

0

Menthol

38.6

Menthone

0

β-Pinene

0

Terpineol

0

Thymol

100

Carvone/cineole (80-20)

100

Carvone/cineole (50-50)

1.53

Carvone/menthol (95-5)

97.3

Carvone/menthol (50-50)

5.94

Cineole/β pineno (95-5)

3.6

Cineole/terpineol (90-10)

2

Menthol/cineole (25:75)

6

aCorrected according to Scheider–Orelli’s formula. Values are means of four replicates

Table 7

Effects of active compounds and paired mixtures (0.5 μg/μl) on hatching of eggs in eggs masses of M. javanica in time

Compound

Relative hatch suppression rate (%)a in timeb

0

3

9

16

23

Carvacrol

98

96

94

92

91

Citronellol

82

79

77

79

80

Geraniol

21

70

63

68

71

Thymol

99

93

86

84

84

Carvone/cineole (80/20)

98

94

97

86

87

Carvone/menthol (95/5)

93

95

85

84

85

aEach value represents the hatch inhibition rate in the respective treatment corrected according to the control (Scheider–Orelli’s formula). Values are means of four replicates

bTime 0: after 5 days of immersion in test solutions; time 3: 3 days of immersion in water after time 0; time 9:9 days of immersion in water after time 0; time 16: 16 days of immersion in water after time 0; time 23: 23 days of immersion in water after time 0

Among the binary terpene mixtures, only carvone/cineole (0.4/0.1 mg/ml) and carvone/menthol (0.475/0.025 mg/ml) were active, causing 100 and 97 % J2 mortality and 87 and 85 % final egg mass hatch suppression respectively. It is noteworthy that each component alone (carvone, 1,8-cineole and menthol) and the same component mixtures at different concentrations showed no nematicidal activity, suggesting a synergistic interaction of these compounds at certain concentrations.

The nematicidal activity of S. montana, T. vulgaris and T. zygis EOs could be explained by their content in active carvacrol (88 %) and thymol (49 and 74 %) respectively. The nematicidal effects of M. arvensis and M. spicata EOs could be attributed to synergistic interaction of carvone with 1,8-cineole and menthol. The activity of M. rotundifolia EO could be due to other components such as isomers of 1,2-epoxymenthylacetate as suggested by Oka et al. (2000) since piperitone lacked nematicidal effects. On the other hand, the nematicidal activity of T. mastichina EO did not correlate with that of its major components alone (1,8-cineole, terpineol, linalool and β-pinene) or in binary mixtures of 1,8-cineole with other compounds. Therefore, the contribution of each component to the activity of an EO follows a complicated pattern of interactions (Ntalli et al. 2010) including synergistic and/or antagonistic interactions that contribute to the overall toxicity of the oil (Lahlou 2004).

The mode of action of EOs and their constituents is of practical importance for nematode control because it may give useful information on the most appropriate formulation and delivery means. Oka et al. (2000) have reported a strong relationship between nematicidal and insecticidal activity and suggested the involvement of EOs components in interrupting the nematode nervous system. Some EOs have been reported to interfere with the neuromodulator octopamine (Kostyukosky et al. 2000) or GABA-gated chloride channels of insect pests (Priestley et al. 2003) and Lee et al. (2001) showed evidence that EOs of Mentha species inhibited AChE activity. In addition, EOs may disrupt the cell membrane of the nematode and change its permeability (Oka et al. 2000). Lambert et al. (2001) and Bakkali et al. (2008) reported that EOs damaged bacteria and yeast membrane integrity, affecting pH cellular homeostasis and equilibrium of inorganic ions. The nematicidal activity of carvacrol and thymol, might be mediated through the tyramine receptor, as the two compounds were able to trigger a signaling cascade that lead to nematode mortality by interacting with a receptor like SER-2 (Lei et al. 2010). Likewise, it has been reported that the activity of geraniol and citronellol are essentially due to membrane and ion channel perturbations modifying membrane-bound protein activity and the intracellular signaling pathways (Warber 1998; Tsuchiya 2001; Kaur et al. 2011).

Conclusions

Essential oils contain functional nematicide compounds which could be used for the control of pinewood (B. xylophilus) and root-knot nematodes (Meloidogyne spp.). Experimentally cultivated Spanish aromatic plants EOs have nematicide properties, but, direct in vitro tests must be complemented by in vivo soil based experiments to confirm the efficacy of this aromatic plant EOs.

This review demonstrates the significant progress undertaken in the last decade to investigate the nematicidal activity of plant EOs and these constituents. Although commercial nematicides based on plant EOs have not yet appeared in the market place there is a clear need to develop novel products based on essential oil formulations. These formulations should target plant parasitic nematodes affecting high-value crops and substitute existing commercial nematicides coming off the market due to changes in the Plant Protection Products Directive (91/414/EEC). The main advantages of using essential oil-based pesticides are their low mammalian toxicity and environmental persistence. Their short residual half lives on plants also enhance their compatibility with biological control agents (Isman et al. 2011). Moreover, the potential disadvantages as limited persistence and phytotoxicity could be mitigated by the application of microencapsulation techniques EOs when formulated, to protect them from degradation, evaporation and to provide a controlled release. In this sense, exhaustive studies have been recently performed in order to obtain stable capsules of EOs using biodegradable polymers as carrier materials and high effectiveness of microencapsulation has been achieved by high-pressure technology application (supercritical fluids processes) (Martín et al. 2010; Varona et al. 2009; Varona et al. 2010). At present, nematicide EOs based products may be developed, with formulations that provide efficacy at low concentrations, to minimize risk to the environment. This will enhance user safety and is likely to provide more durable pest control due to the complexity of chemical composition and naturally occurring variability.

Materials and methods

Plant materials

A series of aromatic plant species were selected for their experimental cultivation based on their medicinal and/or condiment value (Burillo and García-Vallejo 2003). Among the species cultivated the following were selected to be tested for their nematicidal effects: Hyssopus officinalis, Lippia alba, Mentha arvensis, M. longifolia, M. piperita,M. rotundifolia, M. spicata, Satureja montana, Thymus mastichina, T. vulgaris and T. zygis.

Essential oil and extract preparation

Flowers and leaves were manually separated from the twigs and then hydrodistilled separately for 2 h in a Clevenger-type apparatus according to the method recommended by the European Pharmacopoeia.

Essential oil analysis

Flower and leaf EOs were analyzed by GC-MS using an Agilent 6890 N gas chromatograph (Agilent Technologies, Palo Alto, California, USA) coupled to an Agilent 5973 N mass detector (electron ionization, 70 eV) (Agilent Technologies, Palo Alto, California, USA) and equipped with a 25 m × 0.2 mm id HP-1 (methylpolyisiloxane, 0.20 μm film thickness) and a 30 m × 0.25 mm id Carbowax (polyethylene glycol, 0.25 μm film thickness) capillary columns (Hewlett-Packard). Working conditions were as follows: injector temperature, 260 °C; temperature of the transfer line connected to the mass spectrometer, 280 °C; column temperature 70–90 °C, 5 °C min−1. El mass spectra and retention data were used to assess the identity of compounds by comparing them with those of standards or found in the Wiley Mass Spectral Database (Wiley, 2001). Quantitative data were obtained from the TIC peak areas without the use of response factors.

Chemicals

Analytical standards of 1,8-cineole (99 %), (+)-carvone (98,5 %) and carvacrol (97 %) were purchased from Fluka (Buchs Switzerland). Eugenol (99 %), geraniol (98 %), β-caryophyllene (80 %), β-citronellol (99 %), linalool (99 %), (−)-menthone (90 %) menthol (99 %) β-pinene (99 %) α-terpineol (97 %) and thymol (99.5 %) were purchased from Sigma-Aldrich.

Nematodes

M. javanica population was maintained on Lycopersicon esculentum plants (var. Marmande) in pot cultures at 25 ± 1 °C, > 70 % relative humidity. Egg masses of M. javanica were handpicked from infected tomato roots. Second-stage juveniles (J2) were obtained from hatched eggs by incubating handpicked egg masses in a water suspension at 25 °C for 24 h.

Bioassays

Effect on J2

EOs and their components were suspended in distilled water containing DMSO with 0.5 % Tween 20. Test solutions (5 μl) were filled into a cell of a 96-cell plate (BD Falcon, San Jose, CA, USA) containing 90–150 nematodes in 95 μl of test solution. Thus, the total volume of the solution in a cell was 100 μl. The concentration of EOs and each components tested in a cell was 1 and 0.5 mg ml−1, respectively. As a control, four wells were treated with the water/DMSO/Tween 20 in the same volume as the tests. All treatments were replicated four times. The plates were covered to prevent evaporation and were maintained in the dark at 25 °C. After 72 h, the dead J2 were counted under a binocular microscope (20×). The J2 were considered dead when they did not move on probing with a fine needle (Cayrol et al. 1989). In addition, the most nematicidal essential oils, which exhibited over 99 % mortality rates, were further screened to asses J2 mortality after 24 and 48 h using the immersion bioassay and for the determination of LC50 and LC90 values after 72 h.

Effect on egg mass hatching

Three (for EOs) or two (for the components) sterilized healthy egg masses of nearly uniform size were transferred to a 96-well plate (BD Falcon, San Jose, CA, USA) containing different treatments solutions described above with nematicidal activity.

Egg masses placed in sterilized distilled water served as controls. Four replicates of each treatment and control were included. The plates were covered to prevent evaporation and incubated in the dark at 25 °C. After 5 days the hatched J2 were counted, test solutions were removed and wells with egg mass were washed and filled with sterilized distilled water. The egg hatch was monitored over 4 weeks, until hatching was complete in the control treatment, and then relative hatching percentages (compared with the controls) were recorded.

Statistical analysis

The data of nematicidal activity are presented as percent dead J2 corrected according to Scheider—Orelli’s formula. Effective lethal doses (LC50 and LC90) were calculated by Probit analysis. Five concentrations of selected EOs were used to obtain the LC50 and LC90 and four replicates were used in each concentration.

Acknowledgments

This work was supported by the grant CTQ2009-14629-CO2-01, MCIN-Spain. We thank F. De la Peña for technical assistance.

Copyright information

© Springer Science+Business Media Dordrecht 2012