AGRICULTURAL AND FOOD SCIENCE IN FINLAND

Vol. 1010 (2001):(2001): 243Ð259.

Review Insecticidal, repellent, antimicrobial activity and phytotoxicity of essential oils: With special reference to limonene and its suitability for control of insect pests

Mohamed A. Ibrahim Department of Ecology and Environmental Science, University of Kuopio, PO Box 1627, FIN-70211 Kuopio, Finland, e-mail: [email protected] Pirjo Kainulainen MTT Agrifood Research Finland, Plant Production Research, Plant Protection, FIN-31600 Jokioinen, Finland. Current address: Department of Ecology and Environmental Science, University of Kuopio, PO Box 1627, FIN-70211 Kuopio, Finland Abbas Aflatuni MTT Agrifood Research Finland, Regional Research, Tutkimusasemantie 15, FIN-92400 Ruukki, Finland Kari Tiilikkala MTT Agrifood Research Finland, Plant Production Research, Plant Protection, FIN-31600 Jokioinen, Finland Jarmo K. Holopainen MTT Agrifood Research Finland, Plant Production Research, Plant Protection, FIN-31600 Jokioinen, Finland. Current address: Department of Ecology and Environmental Science, University of Kuopio, PO Box 1627, FIN-70211 Kuopio, Finland

The interest in the use of monoterpenes for insect pest and pathogen control originates from the need for pesticide products with less negative environmental and health impacts than highly effective synthetic pesticides. The expanding literature on the possibility of the use of these monoterpenes is reviewed and focused on the effects of limonene on various bioorganisms. Limonene is used as in- secticide to control ectoparasites of pet animals, but it has activity against many insects, mites, and microorganisms. Possible attractive effects of limonene to natural enemies of pests may offer novel applications to use natural compounds for manipulation of beneficial animals in organic agriculture. However, in few cases limonene-treated plants have become attractive to plant damaging insects and phytotoxic effects on cultivated plants have been observed. As a plant-based natural product limonene and other monoterpenes might have use in pest and weed control in organic agriculture after phyto- toxicity on crop plants and, effects on non-target soil animals and natural enemies of pest have been investigated. Key words: monoterpenes, limonene, essential oil, natural pesticides, plant protection, deterrent, in- sect control

© Agricultural and Food Science in Finland Manuscript received April 2001

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Ibrahim, M.A. et al. Limonene in pest control

penoids are sesquiterpenes (C ), diterpenes Introduction 15 (C20), triterpenes (C30), tetraterpenes (C40) and

polyterpenes (Cn). The plastids of plants are re- Historical perspective garded to be the site of monoterpene synthesis. All terpenoid compounds are biosynthesised Essential oil-bearing plants have been collected from isopentenyl diphosphate (IPP), which may from the forest and cultivated areas since pre- be derived by acetate/mevalonate or pyruvate/ Christian time for their flavour and fragrance glyceraldehydes-3-phosphate pathway. The properties. Their volatility, which made them head-to-tail condensation of one molecule of IPP easy to discover in fragrant plant material and at with one molecule of dimethylallyl diphosphate the same time readily obtainable by simple dis- (DMAPP), itself derived from the reversible tillation of plant parts, lent to them the term es- isomerization of IPP by IPP isomerase yields the sential oil. The monoterpenes with to a lesser C10 compound geranyl diphosphate (GPP) which extent the sesquiterpenes, comprise the major is the immediate precursor of the monoterpenes components of essential oils. Monoterpenes op- (Lichtenthaler et al. 1997, Little and Croteau erate as a chemical defence against herbivores 1999). and diseases, fragrances attractive to pollinators Hydrocarbon variations that differ only in the and allelopathic inhibition of seed germination arrangement of atoms are called isomers. De- and plant growth (Gershenzon and Croteau 1991, scription of isomers and their chemical and bi- Langenheim 1994). Well-documented records ological functions are summarized in Table 1 show that before 1850, 20 plant species belong- according to Fessenden et al. (1998). Enantiom- ing to 16 different families were used for con- ers are chiral molecules that have the same mo- trol of agricultural and horticultural pests in lecular formula but are mirror images of each Western Europe and China (Needham 1986, other. Absolute configuration of chiral carbon (R Smith and Secoy 1981). The rich knowledge of or S) is not dependent on the direction of optical plants with pesticide properties was not lost in rotation (+ or Ð), but in each specific compound China as evidenced by a recent report stating that are always related, e.g. limonene has two enan- in China different parts or extracts of 276 plant tiomers (R)Ð(+)-limonene and (S)Ð(Ð)-limonene, species are used as pesticides (Yang and Tang but the enantiomers of carvone are (R)Ð(Ð)-car- 1988). vone and (S)Ð(+)-carvone. In this review we use Insecticidal properties have been recognized (+ and Ð)-nomenclature, since optical isomers in the oil of many citrus fruits and in recent years, are related closely to the biological activity of several products containing (+)-limonene, lina- monoterpenes. Even human sense of smell is able lool, or a crude citrus oil extract have worked to discriminate the odours of the enantiomers of their way into the market place. Two of these α-pinene, carvone and limonene. R-limonene is oils, (+)-limonene and linalool are long-stand- the smell of lemon or orange, while smell of S- ing and widely used for food additives (Hooser limonene is close to that of pine turpentine (Las- 1990). ka and Teubner 1999).

Chemical properties of monoterpenes Natural occurrence and functions of monoterpenes Terpenes are hydrocarbons classified by the number of five-carbon (isoprene) units that they More than 1000 naturally occurring monoterpe- contain. Monoterpenes contain a basic skeleton nes have been isolated from higher plants (Ger- of 10-carbon atoms derived from of fusion of shenzon and Croteau 1991). Monoterpenes are two C5 isoprene units. The other classes of ter- volatile and responsible for the characteristic

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Vol. 10 (2001): 243Ð259.

Table 1. Description of isomers summarized from Fessenden et al. (1998) and chemical designation of some monoterpenes.

Type of the isomers Nomenclature Description Old New

A. Structural isomers Different compounds that have the same molecular formula, but differ in order of attachment of atoms B. Stereoisomers 1. Enantiomers Chiral molecules are mirror images of each other. (optical isomers) Chemical properties are similar, but physiological properties differ. The prefixes R (clockwise) and S (counter clockwise) D R indicate absolute configuration of group around chiral L S carbon. The prefixes (+)- and (Ð)- are used to designate the D + sign of optical rotation of plane-polarized light by the L Ð enantiomers 2. Diastereomers Cis Z Molecules are not mirror images of each other. including achiral Trans E Geometric isomers result from groups being Z (same) geometric isomers and E (opposite) side.

odours of many plants. Most monoterpenes oc- (Schütte 1984). Overall, the variability in essen- cur free in plant tissue, but some of them are tial oil composition is determined both by ge- found as glycosides. The monoterpenes occur in netic and epigenetic factors. a variety of acyclic, monocyclic, bicyclic, and Generally, plants can produce a diverse range tricyclic structural types and derivates, represent- of secondary metabolites such as terpenoids, ing one of the largest and most diverse families phenolic compounds and alkaloids (Benner of natural compounds (Croteau 1987). They ex- 1993). Terpenoids are among the vast reservoir ist as hydrocarbons or as oxygenated moieties of secondry compounds produced by higher with aldehyde, alcohol, ketone, ester, and ether plants evolved in defence against herbivores and functionalities. Overall monoterpenes are insol- pathogens (Duke et al. 1991). Monoterpenes may uble in water, however, monoterpenes contain- interfere with basic behavioural functions of in- ing oxygen have greater solubility than hydro- sects (Brattesten 1983). Some exhibit acute tox- carbons with comparable skeletons (Weidenham- icity whereas others are repellents (Watanabe et er et al. 1993). al. 1993), antifeedants (Hough-Goldstein 1990), Because of lipophilic properties most of or disrupt on growth and development (Karr and monoterpenes are stored in special structures as Coats 1992) or reproduction (Sharma and Saxe- resin ducts, secretory cavities and epidermal na 1974) and, interfere with physiological and glands (Dell and McComb 1981). Monoterpe- biochemical processes (Gershenzon and Croteau nes are most widely recognized constituents of 1991). conifers, mints (Lamiaceae), composites (Aster- Since monoterpene composition of plant spe- aceae), and citrus (Rutaceae). α-pinene and β- cies is very distinctive, specialist herbivore in- pinene are among the most widely distributed sects that have only one plant species or one plant monoterpenes in the plant kingdom and are the genus as host plant, use highly volatile monote- major constituents of the various volatile oils rpenes as a cue to locate their specific host plant.

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Ibrahim, M.A. et al. Limonene in pest control

For many oligophagous and polyphagous insect cymene, Z- and E-carveol, carvone, iso-piperi- herbivores monoterpenes have been demonstrat- tenone, p-mentha-1 (7), 8-dien-ol, and p-men- ed to act as toxins, feeding and oviposition de- tha-2, 8-dien-1-ol. (Takaisi-Kikuni et al. 2000). terrents. Thus, monoterpenes appear to play an The main constituents of the oil of Cala- important role in protecting plants from insect mintha nepeta (limonene, menthone, pulegone, attack (Gershenzon and Croteau 1991, Langen- menthol) were tested against some bacteria spe- heim 1994, Phillips and Croteau 1999). The best- cies, and only pulegone showed antimicrobial known insect neurotoxins among monoterpenes activity, particularly against all Salmonella spe- are the pyrethroids, a group of monoterpene es- cies (Flamini et al. 1999). The determination of ters found in the leaves and flowers of certain the minimal bactericidal concentration of the Chrysanthemum species (Harborne 1993). essential oil from the leaves of Peumus boldus Some compounds in essential oils have (main constituents: monoterpenes 90.5%, includ- shown promise as natural insect pest control ing 17% limonene) against several microorgan- agents because they naturally provide plants with isms showed antibacterial activities towards chemical defences against phytophagous insects Gram-positive and Gram-negative bacteria. and plant pathogens. These advances are re- Streptococcus pyogenes and Micrococcus sp. viewed in this paper with a focus on the monot- were the more sensitive in the case of Gram-pos- erpenes and especially limonene, a compound itive bacteria and Shigella sonnei in Gram-neg- with low toxicity to humans and having even ative bacteria (Vila et al. 1999). some antitumor activity (Crowell 1999). The antibacterial activity of the various oils (main constituents were (E)-anethole, limonene, fenchone, and methyl chavicol) hydrodistilled from the seeds of 3 varieties of Foeniculum vul- gare (dulce or sweet, vulgare or bitter, and azo- Effects of monoterpenes on ricum or Florence) against 25 microorganisms bio-organisms was evaluated. The essential oil from sweet fen- nel (at the early waxy seed stage) was the most effective antibacterial agent. Essential oils of Bacteria Rosmarinus officinalis (from Giza, Egypt) showed a high antimicrobial activity against Essential oil of plants has been shown to have Cryptococcus neoformans and Mycobacterium activity against human, animal and plant patho- intracellularae (Soliman et al. 1994). gens, as well as food poisoning bacteria. The In antibacterial assays, the essential oil of essential oils have effects on bacteria cells or Origanum onites, Thymus capitatus and orega- their activity. The essential oils from Melaleuca no were active against Bacillus subtilis, E. coli, alternifolia (tea tree oil) inhibit the respiration Hafnia alvei, Micrococcus luteus, Proteus vul- and increase the permeability of bacterial cyto- garis, S. aureus and Streptococcus faecalis but plasmic membranes of Gram-negative bacteri- not against Pseudomonas aeruginosa. O. onites, um Escherichia coli AG 100, the Gram-positive T. capitatus and oregano inhibited the growth of bacterium Staphylococcus aureus NCTC 8325. the 5 test fungi. It is suggested that the observed These essential oils also cause potassium leak- antimicrobial activities may be associated with age (Cox et al. 2000). The essential oil of Cym- the phenolic constituents in the essential oil of bopogon densiflorus showed a wide spectrum of O. onites, T. capitatus and oregano (Biondi et activity against Gram positive and Gram nega- al. 1993). Helander et al. (1998) tested the in- tive bacteria in the range of 250Ð500 and 500Ð hibitory activity of some essential oils, includ- 1000 ppm, respectively. The main essential oil ing (+)-carvone against E. coli 0157:H7 and Sal- components were limonene, cymenene, p- monella typhymurium, and determined that, (+)-

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Vol. 10 (2001): 243Ð259. carvone was among less inhibitory compounds. a range of fungal sugarcane pathogens. L. alba Chanegriha et al. (1994) reported that, limonene essential oil was fungistatic against Colletotri- and terpenyl acetate both inhibited the activity chum falcatum (Glomerella Tucumanensis) and of B. subtilis and E. coli. C. pallescens at 700 ppm or less, and fungicidal The essential oil of Tagetes minuta inhibited at higher concentrations against all the other test the multiplication of Gram-positive and Gram- pathogens such as: Fusarium moniliforme, Cer- negative bacteria showing 95Ð100% of inhibi- atocystis paradoxa, Rhizoctonia solani, Curvu- tion (Hethelyi et al. 1987). Similarly, Hyptis sua- laria lunata, Periconia atropurpuria and Epic- veolens’ essential oil including limonene inhib- occum nigrum (Singh et al. 1998). its the growth of both Gram-positive and Gram- A positive correlation between the monoter- negative bacteria (Iwu et al. 1990). pene content of the oils (other than limonene and The bark essential oil of Xylopia longifolia sesquiterpenes) and fungal inhibition was ob- exhibited antimicrobial properties against some served in an experiment testing the effect of vol- microorganisms including S. aureus and E. coli atile components of citrus fruit essential oils on (MIC values of 0.5 and 2 mg/l respectively) Penicillium digitatum and P. italicum. P. digi- (Fuornier et al. 1993). The antimicrobial activi- tatum was found to be more sensitive to the in- ty of the Cotinus coggygria oil was manifested hibitory action of the oils than P. italicum (Cac- by its strong inhibition of the multiplication of cioni et al. 1998). both Gram-positive and Gram-negative bacteria Essential oils extracted from leaves of Oci- (Hethelyi et al. 1986). The main components of mum canum (O. americanum) and seeds of the essential oil of leaves and stems of Ducrosia Anethum graveolens and Pimpenella anisum anethifolia (α-pinene, myrcene, limonene, ter- completely inhibited the growth of fungi at 3000 pinolene and E-β-ocimene) were active against ppm. P. anisum oil showed fungicidal activity at Gram-positive bacteria, yeast and fungi (Jans- 3000 ppm against C. falcatum, C. paradoxa and sen et al. 1984). P. solani (Singh et al. 1998). (+)-limonene, cin- eole, β-myrcene, α-pinene, β-pinene and cam- phor showed high antifungal activity against Fungi Botrytis cinerea (Wilson et al. 1997). Volatiles from crushed tomato leaves inhibited hyphal Cox et al. (2000) reported that fungal toxicity of growth of Alternaria alternata isolated from le- M. alternifolia essential oils to the yeast Can- sions of tobacco leaves and Botrytis cinerea iso- dida albicans is based on increased permeabili- lated from infected strawberry fruit. Aldehydes, ty of the plasma membranes. Essential oil of including C6 and C9 compounds, formed by H. suaveolens including limonene has mild an- lipoxygenase enzyme pathway upon wounding tifungal activity against C. albicans (Iwu et al. leaves, inhibited growth of both species. Terpene 1990). Monoterpenes (1R, 2S, 5R)-Isopulegol, hydrocarbons, 2-carene, and limonene had no (R)-carvone and Isolimonene showed good fun- significant effect on hyphal growth (Hamilton- gistatic activities against C. albicans (Naigre et Kemp et al. 1992). Cardamom oil inhibited the al. 1996). All essential oils hydrodistilled from growth of A. flavus, A. parasiticus A. ochraceus, the seeds of 3 varieties of Foeniculum vulgare Penicillium sp., P. patulum, P. roquefortii and (dulce or sweet, vulgare or bitter, and azoricum P. citrinum, and of its components α-terpinyl ac- or Florence) exhibited a marked antifungal ac- etate had the greatest antifungal spectrum, fol- tivity against Aspergillus niger (Marotti et al. lowed by linalool, limonene, and cineole (Badei 1994). 1992). In agar diffusion experiments the essen- Lippia alba essential oil was the most effec- tial oil of Tagetes minuta inhibited the multipli- tive of essential oils extracted from various parts cation of fungi and showed 100% of inhibition of 11 higher plants for their fungitoxicity against (Hethelyi et al. 1986, 1987).

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Nematodes via the respiratory system (fumigant effect) and via the digestive apparatus (ingestion effect) (+)-limonene at 100 ppm reduced the Heterod- (Prates et al. 1998). era schachtii population to less than 3% of the Insecticidal use of limonene has been suc- control after 3 months, when sugarbeet seedlings cessfully applied for the control of insect para- cv. SSY1 were inoculated with 2300 freshly sitoids of pet animals. Weekly application of (+)- hatched H. schachtii J2. However, root growth limonene reduced flea and tick infestations by was also reduced by phytotoxic effects of (+)- 80% in 24 dogs and one cat, with no adverse limonene (Viglierchio and Wu 1989). Aqueous effects on blood composition or liver and kid- extracts of H. suaveolens leaves gave 100% ney function (Tonelli 1987). (+)-limonene was mortality of Meloidogyne incognita larvae in 80 toxic to all life stages of the cat flea, Cteno- mins, whereas the whole oil gave 100% mortal- cephalides felis (Hink and Fee 1986). (+)- ity in 30 mins. The nematicidal activity is there- limonene has shown to have efficacy against fore linked to the essential oil of H. suaveolens, malathion-resistant fleas (Collart and Hink of which (+)-limonene and menthol are two main 1986), but dogs developed toxicity effects in- constituents (Babu and Sukul 1990). cluding extensive erythema, and therefore it should be used cautiously (Rosenbaum and Ker- lin 1995). Limonene has shown insecticidal prop- Mites erties against human blood-sucking insects when tested against early 4th instar larvae of the mos- β α ∆ (Ð)-limonene, -pinene, -pinene and 3-carene quito Culex quinquefasciatus. The LC50 was were toxic to adult females of the spruce spider 53.80 ppm after 24 h and 32.52 ppm after 48 h. mite Oligonychus ununguis when exposed for 24 Limonene-treated water was less favourable than hrs at concentrations below the calculated untreated water for oviposition by females of the LC50s. All four compounds decreased oviposi- mosquito (Kassir et al. 1989). The oil of Myrica tion in the mites while three of these compounds gale acts as a deterrent to biting midge Culi- (limonene, β-pinene, and α-pinene) influenced coides impunctatus, but limonene together with movement (Cook 1992). Monoterpene vapours camphene and terpinene-4-ol were at the bottom from peppermint have similar toxic effects on of the scale of the activity (Stuart and Stuart the spider mite Tetranychus urticae (Larson and 1998). Berry 1984). Acute toxicity of 34 naturally oc- Some monoterpene showed efficacy against curring monoterpenes were evaluated against food and wood pests. Components (cymol and T. urticae and most of the monoterpenes were limonene) of the essential oils of Eucalyptus lethal to the mite at high concentrations; carvo- camaldulensis, E. cameroni, and of the peal of menthenol and terpinen-4-ol were especially ef- Citrus aurantium have significant insecticidal fective (Lee et al. 1997). action, being lethal to the stored product pests Rhyzopertha dominica and Tribolium castaneum. (+)-limonene showed more effective control of Insects T. castaneum than of R. dominica (Santos et al. 1997). A study carried out by Sharma and Raina Secondary plant metabolites play an important (1998) indicated that linalool, citronellal, and role in plant resistance to insects. Monoterpe- carvone showed promising toxicity against the nes including limonene can be bioassayed to termite Odontotermes brunneus, while, euca- determine their possible fumigant, contact, and lyptol, terpinene, and limonene did not show ingestion activity against insect pests and other much activity. Application of high doses of (+)- pathogens. These substances can be toxic via limonene or linalool to oothecal (egg save) of penetration of the insect cuticle (contact effect), gravid female of German cockroach (Blatella

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Vol. 10 (2001): 243Ð259. germanica) decreased significantly the probabil- Most of the studies indicate the attractive role ity of young emerging from them, but did not of limonene for herbivorous insects of conifers, affect female mortality (Karr and Coats 1992). which have a high content of monoterpenes in Untreated diet was significantly preferred com- their oleoresin. For specialised herbivores pared with diet treated with high levels of (+)- limonene can be a signal compound to detect the limonene, linalool, and α-terpineol. However, right host plant species of certain plant family (+)-limonene among other tested compounds as shown with Trioza apicalis by Valterova et reduced significantly the time required by cock- al. (1997). The same carrot pest (T. apicalis) can roaches’ nymphs to reach the adult stage (Karr even avoid carrot varieties with high limonene and Coats 1992). content (Kainulainen et al. 2001). Limonene has been shown to be toxic to sev- eral bark beetles e.g. the Southern pine beetle, Dendroctonus frontalis (Coyne and Lott 1976), Phytotoxicity the Western pine beetle D. brevicomis (Smith 1975) and the mountain pine beetle D. pondero- Plant injuries from chemicals are called phyto- sae (Raffa and Berryman 1983). Laboratory bi- toxicity, and are manifested in several ways. Leaf oassay indicated that myrcene, limonene and β- tips, margins, or the entire leaf surface can ap- phellandrene applied topically at 20 ppm were pear burned, growing tips and buds can be killed toxic to 60% of adult spruce beetles, D. rufipen- and roots can also be burned. Chlorosis or yel- nis (Werner and Illmann 1994). The vapours of lowing of leaves (in spots, along margins) or a the monoterpenes present in grand fir (Abies general chlorosis of the entire leaf or leaf dis- grandis) phloem caused a significant mortality tortion may appear as curling, crinkling, or cup- of the fir engraver beetle (Scolytus ventralis). ping of the leaf. Stunting of growth on all or parts Toxicity was observed at doses normally found of the plant is also one of the phytotoxic impacts. in the host tree, either in the attacked phloem or Phytotoxic chemicals can also stimulate abnor- in the reaction tissue induced by the associated mal either excessive growth (as aerial roots and fungi (Raffa et al. 1985). suckering), or elimination and distortion of fruit The substances dihydrocarvone and carvone or flowers. Symptoms of phytotoxicity can be were repelled the blow fly, Protophormia ter- confused with insect or mite damage, diseases, raenovae in a net cage study. Other compounds and other abiotic problems such as nutrient de- like eucalyptol, limonene, p-cymene, gamma- ficiencies, or environmental conditions (Fink terpinene, dihydrocarvyl-acetate, β-pinene, β- 1999). myrcene, eugenol, and α-humulene seemed to Phytotoxicity of some naturally occurring have a deterrent effect mainly by contact of the monoterpenes were tested on maize plant, and fly with the treated bait at concentrations of 17Ð some of them have shown phytotoxicity to maize 25 µmolcmÐ2 (Thorsell et al. 1989). The essen- roots and leaves. On the other hand, D-Carvone tial oils of 0.5g citrus including (+)-limonene, was the most phytotoxic, whereas pulegone was α-pinene, and myrcene caused rapid knockdown the safest (Lee et al. 1997). But on the other hand, (KT50) on Musca domestica in 10Ð20s, and also carvone inhibited sprouting of treated potato tu- inhibition of the emergence rate of the pupae bers during storage with low persistence. Car- increased with the increased exposure time. The vone has to be reapplied about every 3 months same dose of oils killed all treated flies within during storage. The low persistence means that 24h (Liao and Liao 1999). tubers could be consumed as soon as 15 days The internal concentration of limonene in after treatment. Carvone also inhibited early plants or in artificial food of herbivorous insects sprouting of seed tubers (Reust 2000). In the has significant effects on the behaviour and food Netherlands, carvone has been introduced as a consumption of plant feeding insects (Table 2). commercial sprouting inhibitor for potatoes

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Table 2. Summary of reports indicating negative or positive effects of internal limonene concentrations in plants or in artificial food on plant damaging insects.

Insect species Host plant Response Reference Reduced activity of pest insect Pissodes strobi Paired agar disc Limonene inhibited feeding at high Alfaro et al. 1980 (Coleoptera: bioassay concentration. Curcullionidae) Ð Pine shoot feeder Diaphania nitidalis Treated on artificial A concentration of 20 µl of (Ð)- Peterson et al. 1994 (Lepidoptera, Pyralidae) sites limonene 96% caused slight but Ð Pickleworm moth significant reduction in oviposition. Trioza apicalis Various Apiacea Large amounts of either (Ð) or (+)- Valterova et al. 1997 (Homoptera: Psyllidae) species limonene were released by the Ð carrot sucker Apiacea species of low preference of T. apicalis. Dioryctria zimmermanni, Scots pine, Pinus Resistant proveniences emitted Sadof & Grant 1997 (Lepidoptera: Pyralidae) sylvestris relatively high levels of limonene. Ð pine trunk borer Increased activity of pest insect Pissodes strobi Paired agar disc Limonene stimulated feeding at low Alfaro et al. 1980 (Coleoptera: bioassay concentration. Curcullionidae) Ð Pine shoot feeder Pissodes strobi Eastern white pine, Limonene concentration was highest Wilkinson 1980 Ð pine shoot feeder Pinus strobus in trees attacked most frequently. Dioryctria abietivorella Eastern white pine, Ten microliters of a test solution Shu et al. 1997 (Lepidoptera: Pyralidae) Pinus strobus containing 10 µg (Ð)-limonene 95% Ð twig borer elicited a significant oviposition response, but was the least stimulating monoterpene in EAG tests. Cydia strobilella Norway spruce, Limonene elicited the highest Åhman et al. 1988 (Lepidoptera: Tortricidae) Picea abies electroantennogram response, Ð spruce seed moth probably cue compound for ovipositing females. Dioryctria amatella Loblolly pine, Combination of (+)-limonene, Hanula et al .1985 (Lepidoptera: Pyralidae) Pinus taeda α-pinene, and myrcene was attractive Ð Southern pine coneworm to females. Dioryctria sylvestrella Maritime pine, Attacked trees contained a significantly Jactel et al. 1996 (Lepidoptera: Pyralidae) Pinus pinaster higher percentage of limonene together Ð maritime stem borer with longipinene and copaene. Thecodiplosis japonensis Japanese pine, Higher limonene and β-pinene contents Kim et al. 1976 (Diptera: Cecidomyiidae) Pinus thunbergii were associated to resistance. Ð Pine gall midge

(Bouwmeester et al. 1995). Limonene oxide and Limonene and α-pinene did not inhibit sprout- linalool both inhibited sprouting and fungal ing, and fungal growth was present on every tu- growth but tubers were soft after exposure. ber treated (Vaughn and Spencer 1991). Because

250 AGRICULTURAL AND FOOD SCIENCE IN FINLAND

Vol. 10 (2001): 243Ð259. of the phytotoxicity, monoterpenes may be a (Table 2). Among these the carrot psyllid potential source of products used for haulm kill- (T. apicalis) has shown a reduced oviposition ing and weed control. rate on carrot varieties having a high concentra- (+)-limonene is highly phytotoxic to sugar- tion of limonene (Kainulainen et al. 2001). This beet seedlings (CV. SSY 1) at high concentra- observation suggests that, the selection of car- tions (Viglierchio and Wu 1989). Carvone, (+)- rot varieties with high limonene contents can be limonene, and (Ð)-limonene were either less ef- used to reduce carrot psyllid damages in the ar- fective and/or more phytotoxic to wheat, barley eas, where the risk of damage is high. The se- and perennial ryegrass when seed dressing to lection of resistant varieties may be a suitable control slugs were tested (Nijenstein and Ester method for pest control in organic farming, but 1998). Preliminary tests showed that limonene the factors determining pest deterrence should has phytotoxic activity at concentrations more be known. than 3% to strawberry (cv. Jonsok and Honeoye) Exogenous treatment of cultivated plants seedlings (Ibrahim 2000). Our preliminary ob- with limonene extracted from other plant spe- servations suggest that cabbage and carrot seed- cies have more often reduced insect attack than lings are sensitive to limonene at the concentra- increased and attracted pest insects (Table 3). In tion of 9% (Ibrahim et al., unpublished results). leaf disk tests to estimate deterrent effects of (+)- In general, there is not much information avail- limonene on larvae of Galerucella sagittariae able on the phytotoxicity threshold values of (Coleoptera: Chrysomelidae) (Holopainen et al. monoterpenes to different cultivated plants. 2000), plants from two strawberry varieties (Ho- neoye and Jonsok) were treated with 1% (+)- limonene, 1% mixture (75:25%) of (+)-limonene and (+)-carvone, and water in fumehood. The leaf discs (diam. 15 mm) were cut with a cylin- Suitability of limonene in control der tube from strawberry leaves. For choice tests of plant-damaging insect pests three leaf discs (one from each treatment) were put into Petri dish on filter paper, 2 hours and 24 hours after the treatment, one larva of G. sag- Insecticidal use ittariae was immediately released into the mid- dle of the Petri dish. After monitoring 24 hours Experiments dealing with the use of monoterpe- the eaten area from the leaf discs by the larva nes extracted from plants like insecticides in was estimated visually. plant protection are scarce. For insect pests that Spraying of leaves with limonene or mixture associated with plant roots, drenching with tox- of limonene and carvone did not significantly ic monoterpene solution might increase larval reduced the feeding ability of the larvae of mortality and reduce damage, but may also af- G. sagittariae on leaf discs of the variety Hone- fect other soil animals (Karr et al. 1990). A wide oye if offered to the larvae 2 or 24 hours after range of monoterpenes has larvicidal effects on spraying of leaves (Fig. 1a). In the test with the western corn rootworm in the soil and effec- strawberry variety Jonsok, larvae did not prefer tively protects corn roots from attack by this lar- feeding on leaf disk offered 2h after spraying, va under greenhouse conditions (Lee et al. 1997). but limonene and, limonene and carvone in mix- ture significantly reduced feeding when leaf disks were offered to larvae 24 hrs after spray- Deterrent ing (Fig. 1b). The result suggests that carvone in mixture with limonene can be as effective as Internal limonene concentrations in plants have pure limonene to reduce G. sagittariae larval shown deterrent effects on only few insect pests feeding on certain strawberry varieties. For the

251 AGRICULTURAL AND FOOD SCIENCE IN FINLAND

Ibrahim, M.A. et al. Limonene in pest control

Tiberi et al. 1999 Tiberi

Lindgren et al. 1996

Ntiamoah et al. 1996

Liuk et al. 1999

Aaltonen et al. 2000

Werner 1995 Werner

Kostal 1992

Al-Rouz et al. 1988

ResponseReduced activity of pest insect Reference (+)-limonene reduced the number

High limonene concentrations

of egg cluster on plants sprayed

a few hours Monoterpene mixtures deterred

oviposition of adult flies Limonene significantly acted as

Reduced damage and increased yield

repellent

(+)-limonene at 60 ppm killed

100% of the pests after 24 hrs of

Limonene from the surface part of

plant host was repellent

Limonene was repellent

6% solutions

Ð

Emulsified with water and

sprayed on the foliage of pine seedlings with it

Volatile mixture 3-carene, Volatile

releaser from capillary tubes near onion plants

(small amounts of carvone as contaminant)

the field in 1 Bioassayed for their toxicity

nylon fibre

Olfactory stimuli for

Olfactometer with two

, orientation behaviour

) Olfactory responses to pure

), Exposure to limonene

) vapours exhibited signs of poisoning within

Abies concolor

Picea abies

Pinus sylvestris

(Pinus nigra)

Pine

Pine ( Spruce (

Spruce spp. (e.g. Sitka,

white and Engelmann

Brassicaceae (e.g. Radish,

rape) Leek & onion, but able

develop on all Allium cropdevelop on all parallel air currents

and White fir (

Eastern larch spruce) exposure

,

, Onion, Shallot, Leek

(Col., Scolytidae)

(Hymenoptera: alpha-pinene and limonene

Spruce beetle

Seed wasps

Cabbage maggot

Leek moth speciesY-shaped containing a

Table 3. Summary of reports of exogenous application of limonene against plant damaging insects. Table

Insect species Host plant Limonene application Thaumetopoea pityocampa

(Lepidoptera: Notodontidae)

Hylobius abietis (Col., Curculionidae)

Delia antiqua

(Diptera, Anthomyiidae)(Diptera, limonene, and p-cymene

Trioza apicalisTrioza Carrot Sprayed on the carrot in

Megastigmus pinus M. rafini Torymidae) Ð (Homoptera, psyllidae) Dendroctonus rufipennis, Dendroctonus

D. simplex Ð continued on the next page beetle respectively Delia radicum

(Diptera, Anthomyiidae)(Diptera, turnip, cabbage, cauliflower Ð Acrolepiopsis assectella Acrolepiopsis

(Lepidoptera, plutellidae) Ð

252 AGRICULTURAL AND FOOD SCIENCE IN FINLAND

Vol. 10 (2001): 243Ð259.

El-Sayed et al. 1994

Ding et al. 1997

1999

Reddemann &

Schopf 1996

Saxena et al. 1975

fect Osborne & Boyd

fect Lindgren et al. 1996

2 days old moths

Ð

)-limonene showed maximum

-pinene attracted adults

Ð

Response Reference

Limonene had some repellent ef

Increased activity of pest insect Increased

Limonene activated oviposition

Low limonene levels did not af

Attractive to 1 feeding trial with adult beetles

No effect

(+)-limonene in mixture with

α

( attaraction to the larvae of this pest

) in 48h No antifeeding effects Klepzig & Schlyter

Pinus sylvestris

-pinene

α

chambers 1974

Electroantennogram

response to pure limonene

Electroantennography used to investigate electrophysiological

Field bioassay using

limonene dissolved in ethyl

Pheromone baited traps acetate solvent

with a mixture of limonene and

Orientation responses to

, citrus)

), Exposure to limonene

), Scots pine (

) vapours feeding activity

) twigs were treated with

Citrus

,

Cullen lenax,

Citrus

) and Rutaceae odours in Olfactory different

&

Picea abies

Picea abies

Pinus sylvestris

Pinus sylvestris

Murraya koenigii

Pasture grasses Host selection test in glass

Citrus limonum

decumana Spruce ( aurantium Polyphagous moth (e.g. Spruce ( cotton, maize cucurpitaceae, tomatoes, leguminous crops, conifers) responses Pine ( Spruce (e.g. Norway spruce)

Pine (

Fabaceae (e.g. Psralea spp. (e.g.

(Lepidoptera:

Grass grub

Cotton bollworm

Citrus Swallowtail

continued from the preceding page the preceding continued from

Insect species Host plant Limonene application

Costelytra zealandica (Col. Scarabaeidae) Ð

Prays citri

Hyponomeutidae) (Col., Curculionidae)

Helicoverpa armigera (Col., Curculionidae) (Lepidoptera, Noctuidae) Ð

Hylobius abietis Ips typographus

Hylobius abietis

(Col., Scolytidae)

Spruce bark beetle

Papilio demoleus (Lepidoptera, Papilionidae) Ð

253 AGRICULTURAL AND FOOD SCIENCE IN FINLAND

Ibrahim, M.A. et al. Limonene in pest control

major component of all citrus peel oils, (+)- limonene, were found to be bioactive, having a strong vapour insecticidal activity, against the cowpea weevil beetle Callosobruchus macula- tus (Coleoptera: Bruchidae) (Don-Pedro 1996). Limonene, mixed with the combination of α- pinene and ethanol on old clear cuttings, inhib- ited completely the catch of Hylobius pinastri (Coleoptera: Curculionidae) and that of H. abi- etis was reduced by two thirds. On fresh clear cuttings the inhibitory effect of limonene was small or absent (Nordlander 1990). Volatile oils of baladi orange and mandarin peels, which con- tain over 70% limonene, were highly toxic to 2nd larval instar stage of Spodoptera littoralis. Their toxicity consistently increased with increasing concentration of the volatile oils. The results from this experiment suggest that these volatile oils could be used as larval growth disruptors and also as repellent materials against moths for controlling programme of cotton leaf worm S. littoralis (Omer et al. 1997). Sesquiterpenes, in combination with tricyclene, camphene, myrcene, limonene, terpinolene, and the acetate fraction appear to be an effective mixture of de- fensive compounds against the western spruce Fig. 1. The effect of 1% limonene treatment on the feeding of the larvae Galerucella sagittariae on cv. Honeoye (A) budworm (Zou and Cates 1997). and cv. Jonsok (B) leaf discs when larvae were put into the Ntiamoah and Borden (1996) found that, a Petri dishes for feeding 2 h (black bars) and 24 h after spray- ternary mixture of carene, limonene and p- ing (grey bars). Asterisk above bar indicate significant (P < cymene in the choice bioassay significantly de- 0.05) difference from the control (water) treatment accord- terred the oviposition of cabbage maggots, but ing to oneway anova. the deterrence was slight in the non-choice bio- assay. Increasing the complexity of the blend to six monoterpenes increased the deterrent effect confirmation of results, field tests are needed, markedly. These results indicate that, as for on- since high concentration of volatile compounds ion maggots (Ntiamoah et al. 1996), monoter- inside closed Petri dishes may reduce larval feed- penes are oviposition deterrents for cabbage ing also on control treatment as observed with maggots. The results also suggest that monoter- the variety Jonsok when offered leaf discs penes may be oviposition deterrents for other sprayed only 2 h before feeding trial (Fig. 1b). anthomyiids. Combining various deterrents used Field sprays of Pinus uncinata with oleores- in different areas may develop a way of pest con- in extracts of P. cembra cones significantly re- trol more valuable than by using single deter- duced the overall damage of specialized cone rent. insects. None of the cones sprayed with oleoresin were attacked, whereas insects damaged 11% and 31% of the unsprayed control cones (Dormont et al. 1997). Several compounds including the

254 AGRICULTURAL AND FOOD SCIENCE IN FINLAND

Vol. 10 (2001): 243Ð259. Effects on non-target organisms and Summary and future perspectives manipulation of natural enemies Although the acute toxicity of monoterpenoids Monoterpenes distilled from plants have effects is low relative to that of conventional insecti- on many bacterial, fungal, nematode and arthro- cides (Lee et al. 1997), the effects of field scale pod species and some compounds are effective use on soil and water animals should be tested sprouting inhibitors. The monoterpene limonene further. Potential drifts to aquatic ecosystem may has shown deterrent and insecticide properties have effects on food chains, since mortality of suggesting that as a plant-based natural product aquatic dipterans have increased after limonene it might have use in pest control in organic agri- treatment (Kassir et al. 1989). Toxic effects on culture. Possible attractive effects of limonene earthworms (Karr et al. 1990) should be clari- to natural enemies of pests may offer novel ap- fied more extensively, since potential pesticide plications to use natural compounds for manip- use of limonene in organic farming may be harm- ulation of beneficial animals in organic agricul- ful for whole agroecosystem if earthworm pop- ture. However, since monoterpenes are phyto- ulations are reduced. toxic to several cultivated plants, critical thresh- Also selectivity and harmlessness of olds of limonene for plant physiology and limonene toward natural enemies and other bio- limonene sensitivity should be determined. Also logical agents needs testing. Interaction with the potential harmful effects on natural enemies entomopathogenes such as Bacillus thuringien- of pests and non-target soil animals should be sis should be understood. The potential use of investigated. After these evaluations, suitable limonene and other monoterpenes in integrated recommendations for the use of limonene on pest management can be achieved with the specific crop plant species and against specific knowledge of all these interactions. For rapid pest species can be given. attraction of large numbers of nestmates to newly discovered food sources, the polyphagous pred- ator ant Myrmicaria eumenoides uses an efficient Acknowledgements. We thank Dr. G.V.P. Reddy for discus- sions and the comments on the manuscript and Dr. Simo recruitment communication system based on the Lötjönen for the information of limonene nomenclature. poison gland secretion that includes mainly (+)- The work was funded by the Ministry of Agriculture and limonene (Kaib and Dittebrand 1990). This ob- Forestry in Finland (MTT-project no: 130581) and Jenny servation suggests that a better understanding of and Antti Wihuri Foundation. the communication systems of predators and parasitoids may offer novel ways to increase the efficiency of natural enemies of pest insects with limonene and other monoterpenes.

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SELOSTUS Monoterpeenit kasvinsuojelussa: erityisesti limoneenin vaikutus eri eliöryhmiin

Mohamed A. Ibrahim, Pirjo Kainulainen, Abbas Aflatuni, Kari Tiilikkala ja Jarmo K. Holopainen Kuopion yliopisto ja MTT (Maa- ja elintarviketalouden tutkimuskeskus)

Kiinnostus luonnonmukaisiin, kasveista peräisin ole- juntamenetelmänä, jossa tuholaisten luontaisia vihol- viin ja vähemmän terveys- ja ympäristöhaittoja ai- lisia houkutellaan kasvustoon ennen tuholaisia. Jois- heuttaviin torjunta-aineisiin on lisääntynyt luomuvil- sain tapauksissa limoneenilla käsitellyt kasvit voivat jelyn yleistyessä. Tässä katsauksessa selvitetään mo- kuitenkin altistua tuholaisille limoneenikäsittelyn noterpeenien käyttömahdollisuuksia kasvinsuojelus- seurauksena, ja korkeilla pitoisuuksilla limoneeni on sa ja arvioidaan erityisesti limoneenin vaikutuksia eri kasveille myrkyllinen. Kasviperäisinä luonnontuottei- eliöryhmiin. Limoneenilla on torjuttu lemmikkieläin- na limoneenista ja muista monoterpeeneistä voi tul- ten ulkoloisia, mutta sen on todettu tehoavan myös la luomuviljelyyn sopivia tuhoeläinten ja rikkakas- moniin muihin hyönteisiin, punkkeihin ja mikrobei- vien torjunta-aineita. Tämä kuitenkin edellyttää, että hin. Sekä karkottavaa että myrkkyvaikutusta on ha- aineiden mahdolliset haittavaikutukset viljelykasvei- vaittu. Limoneenin houkuttavuus tuhohyönteisten hin, maaperäeliöstöön ja tuholaisten luontaisiin vihol- luontaisille vihollisille voi tarjota mahdollisuuden lisiin ensin selvitetään. käyttää sitä luomuviljelyyn sopivana biologisena tor-

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