Terpenoids and Plant Communication Terpenoids N’És Un Dells

Butll. Inst. Cat. Hist. Nat., 64:125-133. 1996

SISTEMES I PROCESSOS SISTEMES I PROCESSOS plantes recorden exposicions prèvies i produei- PALABRAS CLAVE: Terpenoides; lenguaje ve- xen terpens (i compostos d’altres llenguatges getal; comunicación planta-planta, planta- químics com els dels fenols o els dels alcaloides) quan els necessiten. Per tant, les plan- animal y planta-microorganismos; memoria. tes també tenen llenguatges i el dels Terpenoids and Plant Communication terpenoids n’és un dells.

MOTS CLAU: Terpenoids; llenguatge vegetal; Introduction Joan Llusià, Marc Estiarte & Josep Peñuelas* comunicació planta-planta, planta-animal, planta-microorganismes; memòria. Increasing recognition of the ecological Rebut: 3.10.95 Acceptat: 29.04.96 importance of terpenoids is reflected by the Resumen several recent reviews of the ecological chemistry and role of terpenoids (Harborne, Los terpenoides y la comunicación Abstract KEYWORDS: Terpenoids, plant language, plant- 1991; Gershenzon & Croteau, 1991; Lerdau plant, plant-animal and plant-microorganism vegetal & Peñuelas, 1993; Langenheim, 1994; Terpenoids are compounds containing an inte- communication, memory. Gershenzon, 1994). A defensive role has ger number of 5C units, the «syllables». There Los terpenoides son compuestos que contienen persistently been presented as the main role is an astonishing array of structures, the un número integral de cinco unidades de carbo- and the function of secondary compounds, «words», resulting from the sequential no, las «sílabas». Existe un sorprendente núme- combination of these basic five-carbon units Resum ro de estructuras, las «palabras», que resultan including terpenoids, since the field of in the familiar categories of C10 (mono-), C15 de la combinación secuencial de estas unidades chemical ecology developed essentially básicas de cinco carbonos en categorías de C10 (sesqui-), C20 (di-), C30 (tri-) C40 (tetra-) and Els Terpenoids i la comunicació vegetal arround the concept of coevolution (Feeny, C>40 (poly-) terpenoids. Terpenoids are induced (mono-), C15 (sesqui-), C20 (di-), C30 (tri-), C40 1992). However, the fact that higher plant and emitted in response to internal (genetic (tetra-) i C>40 (poli-) terpenoides. Los terpe- and biochemical) and external (ecological) Els terpenoids són compostos que contenen noides son inducidos y emitidos en respuesta a terpenoids result in mediation of numerous factors, both abiotic and biotic. They are un nombre integral de cinc unitats de carboni, factores internos (genéticos y bioquímicos) y kinds of ecological interactions makes them emitted in quantitatively and qualitatively les «sil·labes». Hi ha un sorpenent nombre externos (ecológicos), tanto abióticos como d’estruc-tures, les «paraules», que resulten de also act as infochemicals (Dicke & Sabelis, diverse blends, the «messages», that arrive bióticos. Son emitidos en mezclas cuantitativa 1988). There is also a lively debate on the to the environment either through la combinació seqüencial d’aquestes unitats y cualitativamente diversas, los «mensajes», volatilization (mono- and sesquiterpenes), bàsiques de cinc carbonis en categories de los cuales llegan al ambiente a través de la vo- ecological and evolutionary significance of leaching or decomposition of plant debris. C10 (mono-), C15 (sesqui-), C20 (di-), C30 (tri- latilización (mono- y sesquiterpenos), la li- plant communication (Langenheim, 1994; Their information or effect is received and res- ), C40 (tetra-) i C>40 (poli-) terpenoids. Els xiviación, o la descomposición de los restos Bruin et al., 1995). We have proposed to ponded by other parts of the plant, other terpenoids són induïts i emesos en resposta a vegetales. Su información es recibida por otras factors interns (genètics i bioquímics) i externs merge both subjects, terpenoids and plant plants, animals and microorganisms. partes de la planta, por otras plantas, por ani- (ecològics), tant abiòtics com biòtics. Són Part of such terpenoid «words» are common males y por microorganismos. communication, by approaching terpenoids emesos en barreges quantitativament i to all plants. For example, carotenoids, Alguno de estos terpenoides («palabras») son as a chemical «language» of plants (Pe- qualitativa diverses, els «missatges», els quals chlorophylls or hormones such as cytokinins, comunes a todas las plantas. Por ejemplo, los arriben a l’ambient a través de la volatilització ñuelas et al., 1995a). Here we present the gibberellins, or abscicic acid, are terpenoid carotenoides, las clorofilas, algunas hormo- derivatives. But there are also «dialects» of (mono- i sesquiterpens), la lixiviació, o la development of such approach. Terpenoids descomposició de les restes vegetals. La seva nas como las citoquininas, las giberelinas o the terpenoid «language» that are qualitatively el ácido abscísico son derivados terpénicos. are emitted in response to internal and or quantitatively characteristic of each family informació és rebuda per altres parts de la external factors, and their information or planta, per altres plantes, per animals i per Pero también existen «dialectos» del «lengua- and each species, or even each cultivar and je» de los terpenos que son cualitativamente effect is received and responded by other each organ of the plant. They even seem to be microorganismes. Algun d’aquests terpenoids («paraules») són o cuantitativamente característicos de cada parts of the plant, other plants, animals and kept in «memory». Some plants might remember familia y de cada especie y, a menudo, de previous exposures and produce terpenes (and comuns a totes les plantes. Per exemple, els microorganisms. A survey of recently carotenoids, les clorofil·les o hormones com cada cultivar y de cada órgano de la planta. compounds of other chemical languages such Incluso parece ser que algunas plantas re- recorded ecological effectivity of terpenoids as phenolics or alkaloids) when they are ara les citoquinines, les giberelines o l’àcid abscísic són derivats terpènics. Però també hi cuerdan exposiciones previas y producen shows it to be concentration or dosage needed. Thus, plants also have languages, and terpenos (y compuestos de otros lenguajes that of terpenoids is one of them. ha «dialectes» del «llenguatge» dels terpens dependent (Harborne, 1991). For example, que són qualitativament o quantitativament químicos como los de los fenoles o los de los biological reaction of insects to terpenoids característics de cada família i de cada espè- alcaloides) cuando los necesitan. Por tanto, *Centre de Recerca Ecològica i Aplicacions Forestals cie, i sovint de cada cultivar i de cada òrgan las plantas también tienen «lenguajes» y el characteristically is one of attraction or (CREAF), Facultat de Ciències, Universitat Autònoma, de los terpenoides es uno de ellos. stimulation at low concentrations, with the E-08193 Bellaterra, Barcelona. de la planta. Fins i tot sembla ser que algunes

125 126 SISTEMES I PROCESSOS response becoming increasingly of repellence considerable ecological consequences 1994). There can even be a possible role of Allelochemicals and allelopathy. or inhibition as the concentration increases (Langenheim, 1994). They play an important biotic selection pressures in determining the Reese (1979) used the term «allelochemi- (Lovett, 1989). role in plant communication. They are distribution of plant terpenoids (Lincoln & cal» to describe «non-nutritional chemicals induced in response to internal (genetic and Lagenheim, 1978). produced by one organism that affect the «Syllables, words and messages» biochemical) and external (ecological) growth, health, behavior or population Terpenoids are compounds containing an factors and to both, abiotic and biotic factors, Internal communication (an immune biology of other species». Allelopathy is integral number of 5C units. We can and they get a dosage dependent response system) identified particularly with chemical activity consider those units as the «syllables». (Langenheim, 1994). Like in any other Portions of the plants seem to be able to between plants (Kolzowski et al., 1991); There is an astonishing array of structures language, the «dialects» or particular communicate with the other parts. For however, entomologists refer to allelopathy resulting from the sequential combination terpenoid classes characterize certain plant- example, the existence of some sort of in a broader sense as the communication of basic five-carbon units in the familiar families (Takabayashi et al., 1994). They internal communication system whereby between plants and other organisms. categories of C10 (mono-), C15 (sesqui-), also vary qualitative and quantitatively damaged portions of the plant rely Allelopathic roles are often ascribed to C20 (di-), C30 (tri-) C40 (tetra-) and C>40 intraspecifically (reviewed by Langenheim, information to other undamaged portions mono- and sesquiterpene messages. (poly-) terpenoids, which we can consider 1994 and Takabayashi et al., 1994). They has been suggested in the attack of ento- Terpenoid toxicity results from several the «words». Both the number and structural even vary qualitatively and quantitatively mophagous insects (Dixon & Payne, 1980; effects such as inhibition of ATP formation, diversity of terpenoids provide enormous among organs and during organ deve- Elzen et al.,1984; Turlings et al., 1991). alkylation of nucleophiles, disruption of hor- potential for mediating significant ecological lopment (Langenheim et al., 1978; 1986). Turlings & Tumlinson (1992) propose that monal activity, complexation with protein, terpenoids may even provide a plant an binding with free sterols, inhibition of interactions. They are emitted to the There is thus an enormous diversity of terpenoids. equivalent to an immune system, an idea respiration, or increasing relative electron environment either through volatilization further supported by Takabayashi & Dicke partitioning to the alternative oxidase (mono- and sesquiterpenes) (Seufert et al., Plant terpenoid content and emission (1993). pathway (Peñuelas et al., 1995b). 1995), leaching or decomposition of plant Although terpenoids contents are in the Allelopathic effects seem particularly evident debris (White, 1994). They are emitted range of 1-2 % dry weight, they can attain Plant-plant communication in Mediterranean and desert climates forming qualitatively and quantitatively 15-20 % plant dry weight (Langenheim, (Friedman, 1988). diverse blends with additive sinergic or 1994). Terpenoid content and emission Alarm against herbivores Studies of plant-plant chemical inte- antagonic effects (Asplund 1969; Fischer et respond to abiotic and biotic factors. There There is behavioral and chemical raction through allelopathy have often been al 1988; Langenheim, 1994), which we can are increases with light or CO2, and evidence for the involvement of the host controversial because of difficulty in consider the «messages». decreases with fertilization (our group, plant in production of volatile alleloche- unambigously demonstrating interference unpublished data). Decreases of 42 % of micals upon damage by herbivores, with the by chemical inhibition rather than through «Common language and dialects» total amount of monoterpenes have also consequence of attracting herbivore predators resource competition or other mechanisms Part of such terpenoid «words» are been reported during the summer months in (Takabayashi et al., 1994). These volatiles (Harper, 1977). However, Fischer (1991) common to all plants. For example Picea abies (Kotzias et al., 1992). The same not only influence predator behavior, but pointed out that it has long been known that photosynthesis depends on the existence of authors found little seasonal changes in also prey behavior and also the attracti- essential oils and individual monoterpenes certain terpenes and terpenoid derivatives relative proportions, but other reports have veness of nearby plants to predators. strongly inhibit seed germination and plant (carotenoids and chlorophylls). Besides, shown seasonal modifications (Gershenzon Herbivorous mites, for example, disperse growth. Fischer et al. (1988) showed many hormones such as cytokinins, gi- & Croteau, 1991). On the contrary, emission away from places with high concentrations selective action of monoterpenoids within bberellins, abscicic acid and, possibly, the of isoprene, the 5C unit, has been linked to of the volatiles, and undamaged plants a community (e.g. cineole was highly toxic xanthoxins are terpenoid derivatives. protection against higth temperatures attract more predators when previously to one grass but not to others) and seasonal But there are also «dialects» of the (Sharkey & Singsaas, 1995). The emission exposed to volatiles from infested conspecific variations in inhibition of germination and terpenoid «language» that are characteristic of isoprene has also been shown to be linked plants rather than from uninfested plants, thus growth (highest levels occurring during of each family and each species or even to the photosynthetic processes of the influencing the plant population beyond those June and July), and high inhibitory effects cultivar (Takabayashi et al., 1994). The chloroplasts (Sharkey et al., 1991). Some- being attacked (Bruin et al., 1992, 1995). of terpene mixtures on germination different relative proportions of the times the changes have been related to There seems thus to exist plant-plant contrasting with stimulatory effects of pure constituents in the emitted mixtures have herbivory pressure (Takabayashi et al., communication (Dicke et al., 1990). terpene solutions, which suggests strong

127 128 SISTEMES I PROCESSOS synergistic effects. Similar results had been pharnesene is a terpenoid from leaves of the Herbivore-induced synomones (Indirect digestive microorganisms (Oh et al., 1967). reported by Asplund (1969). However, wild potato Solanum berthaultii Hawkes that defense) However, some recent studies in vivo have Peñuelas et al. (1995b) have found clear is repellent to the aphid Myzus persicae There is also an indirect plant defense suggested that monoterpene concentrations inhibitory effects of pure "-pinene on plant (Sulzer) (Gibson et al., 1983). through the attraction of entomophages. in the rumen of deer and rabbits appear to respiration. Plants produce volatile allelochemicals upon be lower than those used in «in vitro» Insect growth and sex regulators damage by the herbivores with the studies and perhaps too low to interfere with Plant-insect communication Plants have also terpenoids that simulate consequence of attracting predators. microbial digestion (White et al., 1982), Volatile compounds are used by insects insect growth and sex regulators in order to Terpenoids behave thus as synomones, may be because of their volatility. for social communication. Therefore, insects inhibit their development or their sexual substances that enhance the effectiveness of can become sensitive to similar molecules activity. An example of insect growth natural enemies of herbivores (Takabayashi Fungi emitted by plants such as the terpenoids regulators are the juvocimones, potent et al., 1994). This phenomenon is termed Terpenoids are also defenses against (Harborne, 1993). In a mixture of terpenoids juvenile hormone mimics, discovered from «indirect defense», which may be induced insect-vectored fungi and potentially emitted by a plant, some may be feeding Ocimum basilicum (Bowers & Nishida, by herbivore damage («herbivore-induced pathogenic endophytic fungi such as stimulants for adapted specialist herbivores 1980; Bowers, 1991). The hormonally acti- synomone», HIS). The HIS vary among described in coastal redwoods (Espinosa- whereas others or the same may be toxic or ve compounds from O. basilicum are different plants species, depending upon: a) García et al., 1993). There is rapid de novo deterrent for non-adapted herbivores. This obtained by distillation. These compounds plant cultivar, b) leaf growth stage, c) the synthesis of resin near the site of infection deterrence has been applied to the possess exceedingly high juvenile hormone herbivore species that is attacking, and d) vectored by beetles. The induced resin often management of insect infestation (Salom & activity. They contain ocimene as a portion abiotic conditions (light intensity, time of has a different monoterpenoid composition Hobson 1995). Some insects specialize on of their chemical structure. This is another year, and water stress). than the constitutive resin (Raffa & Klepzig, terpenoid-producing plants even to the proof of coevolution of insects and plants 1992). Generally, those terpenoids of extent of exploiting the terpenoid molecules resulting in an incredibly complex chemical Attraction, and aggregation constitutive resins that occur in greatest themselves. There are complex relations interaction. The presence of insect hormo- Terpenoids are also used by plants to quantities are induced the least, whereas the e.g. some conifer species benefit at one life nal activity in plants was first demonstrated attract pollinators. Some terpenoids are rarer monoterpenes are induced in larger stage of diprionid sawflies, whereas the commonly found in flower odors (Knudson quantity. In general there is a dispro- by Slama & Williams (1965) when they insects benefit at another stage of plant et al., 1993), sometimes with dayly rithmi- portionately high increase in those found that paper bathed with extracts of the diterpenes (Larsson et al., 1986). Among city as in flowers pollinated by night-flying chemicals that have the most deleterious balsam fir induced juvenilization of the lin- these complex plant-insect commu-nication insects and bats (Dobson, 1993). effects on insects and fungi during the den bug Pyrrhocoris apterus (L). Some interactions, the following repellent and Conifer monoterpenes are also involved induced response (Raffa, 1991). However, plants such as the Podocarpaceae produce attracting ones are some of the better in beetle host-finding. In fact, aggregation there are also reports of terpenes having no known. substances that are inhibitory to insect pheromones frequently are allylic oxidation significant effect on hyphal growth of development. Moreover, several plant- products of host monoterpenes (Wood, Alternaria alternaria and Botrytis cinerea Alarm pheromones derived insecticide synergists, including 1982). (Hamilton-Kemp, et al., 1992). Some monoterpenoids may act as alarms sesamin and sesamolin, exhibit juvenile signaling the plant as an unfavorable host. hormone activity against both beetles (Tene- Plant-other organisms communication Microorganisms For example verbenone is released in brio molitor) and bugs (Oncopeltus fasciatus). Plant-microorganism communication increasing quantities as beetle attack Several plant extracts reproduced the Mammals also presents all kinds of repellent and progresses and thence completely inhibits intense courtship and mating behaviour There is also a complex and not well attracting interactions. Monoterpenoids the attractiveness of the host monoterpenes induced by the natural sex pheromone of the known response of mammals to plant scents defensive effects have been documented in to the beetle (Byers et al., 1989). In fact, american cockroach, Periplaneta americana (Peñuelas, 1993). There are some evidences bacteria and yeast (Andrews et al., 1980). animal alarm pheromones have been (Bowers & Bodenstein, 1971). The active that terpenes could in some cases inhibit Terpenoids in the soil may inhibit some bac- isolated in aphids and identified as (E)–ß– compounds were simple terpenes including digestion of hares and deer through odor teria or provide energy source for others, and pharnesene (Bowers et al., 1972) and (–)- (+)-bornil acetate, " and ß-santalol, and an deter based on quantity more than quality. may have significant consequences on germacrene A (Bowers et al., 1972, 1977a, unidentified C15H24 hydrocarbon (likely Dietary monoterpenes could be toxic to nutrient cycling (White, 1994). Monoterpenes 1977b, 1988; Nishino et al., 1977). (E)–ß– germacrene D, Tahara et al., 1975). ruminants by supressing the activity of their could potentially interact with herbivory,

129 130 SISTEMES I PROCESSOS decomposers, N mineralization, N immo- pine beetle to beetle- and host-tree-produced HARBORNE, J. B. 1993. Introduction to Ecological References volatiles. J. G. Entomol. Soc., 15: 378-389. Biochemistry. Academic Press, London. p. 318. bilization, nitrification, denitrification, and DOBSON, H. 1993. Floral volatiles in insect biology. HARPER, J. L. 1977. Population biology of plants. N fixation, thus having important effects on In: Insect-plant interaction, V. (E. A. Bernays. Ed.). Academic Press, New York. ANDREWS, R. E.; PARKS, L. W. & SPENCE, L. D. CRC Press, Boca Raton, Florida. p. 47-81. KNUDSON, J. T.; TOLLSTEN, L. & BERGSTRÖM, N cycling (White, 1994). 1980. Some effects of Douglas fir terpenes on certain ELZEN, G. W.; WILLIAMS, H. J. & WINSON, S. B. G. 1993. Floral scent: a checklist of volatile micro-organisms. Appl. Environ. Microsc., 40: 301- 1984. Isolation and identification of cotton compounds isolated by headspace techniques. 304. Network of communication synomones mediating searching behavior by Phytochemistry, 33: 253-280. ASPLUND, R. O. 1969. Some qualitative aspects of parasitoid Campoletis sonorensis. J. Chem. Ecol., KOTZIAS, D.; SPARTA, C. & DUANE, C. 1992. Terpenoids may then be considered as a the phytotoxicity of monoterpenes. Weed Sci., 17: 10: 1251-1264. Distribution of optical isomers of monoterpenes (+)- «language» in the «network of chemical 454-455. ESPINOZA-GARCIA, F. J.; SALDIVAAR-GARCIA, a-pinene in the leaf oil of conifers. Naturwi- BOWERS, S. W.; & BODENSTEIN, W. G. 1971. Sex P. & LANGENHEIM, J. H. 1993. Dose-dependent ssenschaften, 92: 24-26. communication» between plants and other pheromone mimics of the american cockroach. effects in vitro of essential oils on growth of two KOZLOWSKI, T. J.; KRAMER, P. J. & PALLARDY, organisms. Plants produce terpenes and Nature, 232: 259-261. endophytic fungi in coastal redwood leaves. S. G. 1991. The Physiological Ecology of Woody BOWERS, M. D. & PUTTICK, G. M. 1988. Response other chemical languages such as phenolic Biochem. Syst. Ecol., 21: 185-194. Plants. In: Physiological Ecology. (H. A. Mooney of generalist and specialist insects to qualitative FEENY, P. 1992. The evolution of chemical ecology: Ed.). Acedemic Press. INC. Ney York. p. 657 or alkaloid compounds for example once a allelochemical variation. J.Chem. Ecol., 14: 319- contributions from the study of herbivorous insects. LANGENHEIM, J. H.; FOSTER, C. E.; LINCOLN, D. plant has been attacked by an herbivore. It 334. In: Herbivores. Their interactions with secondary E. & STUBBLEBINE, W. H. 1978. Implications of BOWERS, M. D. 1991. Iridoid glycosides. In: plant metabolites, II. (G. A. Rosenthal & M. R. Ber- variation in resin composition among organs, tissues takes some minutes or some hours to get the Herbivores: Their interaction with secondary plant benbaum. Ed.). Ecological and evolutionary Pro- and populations in the tropical legume hymenaea. actual response, but this is not too slow metabolites. The chemical participants. (G. A. cesses, Academic Press, New York. p. 1-44. Biochem. Syst. Ecol., 6: 299-313. Rosenthal & M. R. Berenbaum. Ed.). Academic compared to the feeding rates of inverte- FISCHER, N. H. 1991. Plant terpenoids as allelo- LANGENHEIM, J. H.; MACEDO, C. A.; ROSS, M. Press, New York, 1: 297-325. pathic agents. In: Ecological chemistry and K. & STUBBLEBINE, W. H. 1986. Leaf deve- brate hervivores. It would be like a plant BOWERS, W. S. & NISHIDA, R. 1980. Juvocimenes: biochemistry of plant terpenoids. (J. B. Harborne lopment in the tropical leguminous tree Copaifera immune system. Plants could remember Potent juvenile hormone mimics from sweet basil. & F. A. Tomes-Barbeeran. Ed.). Clarendon Press, in relation to microlepidopteran herbivory. Biochem. Science, 209: 1030-1032. Oxford. p. 377-399. Syst. Ecol., 14: 51-59. previous exposures to pathogens or herbi- BOWERS, W. S.; NAULT, L. R.; WEBB, R. E. & FISCHER, N. H.; TANRISEVER, N. & WILLIAMSON, LANGENHEIM, J. H. 1994. Higher plant terpenoids: vores, and respond faster to the next attack DUTKY, S. R., 1972. Aphid Alarm Pheromone: G. B. 1988. Allelopathy in the Florida scrub a phytocentric overview of their ecological roles. J. Isolation, Identification, Synthesis. Science, l: 1121- community as a model for natural herbicide actions. Chem. Ecol., 20: 1223-1280. or interaction. 1122. In: Allelochemicals: Role in agriculture and forestry. LARSSON, S.; BJORKMAN, C. & GRAF, R. 1986. In conclusion, plants may be able to BOWERS, W. S.; NISHINO, C.; MONTGOMERY, M. American Society Symposium Series 330. (G. R. Responses of Neodiprion sertifer (Hym. Diprio- communicate among themselves and with E. & NAULT, L. R. 1977a. Structure-activity Waller. Ed.). American Chemical Society, Washing- nidae) larvae to variation in needle resin concen- relationships of analogs of the aphid alarm ton, DC. p. 233-249. tration in Scots pine. Oecologia, 70: 77-84. other organisms through chemical languages. pheromone (E)-B-farnesene. J. Insect Physiol., 23: FISHER, N. H. 1979. Allelopathic Effects of Goldenrod LERDAU, M. & PEÑUELAS, J. 1993. Los terpenos The language of terpenoids constitutes one 697-701. and Aster on Young Sugar Maple. Can. J. For. Res., en la atmósfera: vínculos entre la biosfera y la at- BOWERS, W. S.; NISHINO, C.; MONTGOMERY, M. 8: 1-9. mósfera. Mundo Cientifico, 131: 60-63. of the most versatile of these chemical E.; NAULT, L. R. & NIELSON, M. W. 1977b. FRIEDMAN, J. 1988. Allelopathy in desert ecosys- LINCOLN, D. E. & LANGENHEIM, J. H. 1978. languages. Sesquiterpene progenitor, germacrene A: An alarm tems. In: Allelochemicals: Role in agriculture and Effect of light and temperature on monoterpenoid pheromone in aphids. Science, 196: 680-681. forestry. American Society Symposium Series 330. yield and composition in Satureja douglasii. BROWN, D. G. 1967. Influence of Naturally Occuring (G. R. Waller. Ed.). American Chemical So-ciety, Biochem. Syst. Ecol., 6: 21-32. Compounds on Germination and Growth of jack Washington, DC. p. 53-68. LOVETT, J. V.; RYUNTYU, M. Y. & LIU, D. L. 1989. pine. Ecology, 48: 542-546. GERSHENZON, J. & CROTEAU, R. 1991. Terpenoids. Allelopathy, Chemical Communication and Plant BRUIN, J.; DICKE, M. & SABELIS, M. W. 1992. In: Herbivores, Their Interactions with Secondary Defense. J. Chem. Ecol., 15: 1193-1202. Plants are better protected against spider-mites after Metabolites, 1. (G. A. Rosenthal & M. R. Berembaum NISHINO, C.; BOWERS, W. S., MONTGOMERY, M. Acknowledgements exposure to volatiles from infested conspecifics. Ed.). The chemical Participants, Academic Press, E.; NAULT, L. R. & NIELSON, M. W. 1977. Alarm Experientia, 48: 525-529. New York. p. 165-219. pheromone of the spotted alfalfa aphid, Therioaphis BRUIN, J.; SABELIS, M. W. & DICKE, M. 1995. Do GERSHENZON, J. 1994. Metaboloic cost of terpenoid maculata. J. Chem. Ecol., 3: 349-357. This research was made possible by grant plants tap SOS signals from their infested accumulation in higher plants. J. Chem. Ecol., 20: OH, H.K.; SAKAI, T.; JONES, M. B. & LONGHURST, neighbours?. TREE, 10: 167-170. 1281-1328. W. M. 1967. The effect of various essential oils AGR94-0199 from the CICYT and grant BYERS, J. A.; LANNE, B. S. & LOFQUIST, J. 1989. GIBSON, R. W. & PICKETT, J. A. 1983. Wild Potato isolated from Douglas-fir needles upon sheep and SC94-011 from the INIA (Spain). We Host tree unsuitability recognized by pine shoot Repels Aphids by release of aphid alarm phero- deer rumen microbial activity. Appl. Microbiol., 15: gratefully acknowledge F.P.I. (Spain) fello- beetles in flight. Experientia, 45: 489-492. mone. Nature, 302: 608-609. 777-784. DICKE, M. & SABELIS, M.W. 1988. Infochemical HAMILTON-KEMP, T. R.; MCCRACKEN, C. T.; PEÑUELAS, J. 1993. El aire de la vida. Ariel, Barce- wships to J.LL. and M.E. and technical and terminology: Based on cost-benefit analysis rather LOUGHRIN, J. H.; ANDERSEN, R. A. & HILDE- lona. p. 260. economical assistance from Carburos Me- than origin of compounds?. Funct. Ecol., 2: 131-139. BRAND, D. F. 1992. Effects of some natural volatile PEÑUELAS, J.; LLUSIA, J. & ESTIARTE, M. 1995a. DICKE, M.; SABELIS, M. W.; TAKABAYASHI, J.; compounds on the pathogenic fungi alternaria alternata Terpenoids: a plant language. Trend. Ecol. Evol., tálicos S. A. BRUIN, J. & POSTHUMUS, M. A. 1990. Plant and botrytis cinerea. J. Chem. Ecol., 18: 1083-1091. 10(7): 289. strategies of manipulating predator-prey interactions HARBORNE, J. B. 1991. Recent advances in the PEÑUELAS, J.; RIBAS-CARBO, M. & GILES, L. through allelochemicals: prospects for application in ecologycal chemistry of plant terpenoids. In: 1995b. Allelochemical effects of plant respiration pest control. J. Chem. Ecol., 16: 3091-3118. Ecological Chemistry and Biochemistry of Plant and on oxygen discrimination by altternative oxi- DIXON, W. N. & PAYNE, T. L. 1980. Attraction of Terpenoids. (J. B. Harborne and F. A. Tomes- dase. J.Chem. Ecol., 22(4): 801-805. entomophagous and associate insects of the southern Barberan. Ed.). Clarendon Press, Oxford. p. 399-426. RAFFA, K.F. & KLEPZIG, K.D. 1992. Tree defense

131 132 mechanisms against fungi associated with insects. Ecosystem Nutrient Cycling. J. Chem. Ecol., 20: In: Defense Mechanisms of Woody Plants against 1381-1406. fungi. (R. A. Blanchette & A. C. Biggs. Ed.). WHITE, S. M.; WELCH, B. L. & FLINDERS, J. T. Springer-Verlag, Berlin. p. 354-390. 1982. Monoterpenoid content of pygmy rabbit RAFFA, K. F. 1991. Induced defenses in conifer-bark stomach ingesta. J. Range Manage, 35: 107-109. beetle systems. In: Phytochemical Induction by WOOD, D. L. 1982. The bark and ambrosia beetles of Herbivores. (D. W. Tallamy & M. J. Raupp. Ed.). North and Central America (Coleoptera: Academic Press, New York. p. 245-276. Scolytidae), a taxonomic monograph. Great Basin REESE, J. C. 1979. Interactions of allelochemicals Naturalist Memoirs, 6: 1359. with nutrients in herbivore food. In: Herbivores: WOOD, D. L. 1982.The role of pheromones, kairomo- Their Interactions with Secondary Plant Metabo- nes and allomones on the host selection and lites. (G. A. Rosenthal & D. H. Jansen. Ed.). colonization behavior of bark beetles. Annu. Rev. Academic Press, New York. p. 309-330. Entomol., 27: 411-446. SALON, S. M. & HOBSON K. R. 1995. Application of semiochemicals for management of bark beetle infestations. Proceedings of an informal conference. United States Department of Agriculture. General Technical Report INT-GTR-318. 54 p. SEUFERT, G.; KOTZIAS, D.; SPART-, C. & VERSINO, B. 1995. Volatile organics in mediterranean shrubs and their potencial role in a changing environment. In: Anticipated effects of a Changing Global Envi- ronment on Mediterranean Type Ecosystems. (W. C. Oechel & J. M. Moreno. Ed.). Springer Verlag, Ecological Monographs. 1995. SHARKEY, T. D.; LORETO, F. & DELWICHE, C. F. 1991. The biochemistry of isoprene emission from leaves during photosynthesis. In: Trace Gas Emission from Plants. (T. D. Sharkey, E. A. Holland & H. A. Mooney. Ed.). Academic Press. NY. p. 153-184. SHARKEY, T. D. & SINGSAAS, L. 1995. Why plants emit isoprene. Nature, 374: 769. SLAMA, K. & WILLIAMS, C. M. 1965. Juvenile hormone activity for the bug Pyrrhocoris apterus. Proc. Natl. Acad. Sci. U.S.A., 54: 411-414. TAHARA, S.; YOSHIDA, M.; MIZUTANI, J.; KITAMURA, C. & TAKAHASHI, S., 1975. A sex stimulant to the male American cockroach in Compositae plants. Agri. Biol. Chem., 39: 1517-1518. TAKABAYASHI, J. & DICKE, M. 1993. Volatile allelochemicals that mediate interactions in a tritrophic system consisting of predatory mites, spider mites and plands. In: Mutualism and Community Organization. (H. Kawanabee, J. E. Cohen & K. Iwasaki. Ed.). Oxford Univ. Press, NY., 280-295. TAKABAYASHI, J.; DICKE, M. & POSTHUMUS, M.A. 1994. Volatile Herbivore-induced Terpenoids in Plant-mite Intractions: Variation caused by biotic and abiotic factors. J. Chem. Ecol., 20: 1329-1353. TURLINGS, T. C. J.; TUMLINSON, J. H. 1992. Systemic release of chemical signals by herbivore- injured corn. Proc. Natl. Acad. Sci. U.S.A., 89: 8399- 8402. TURLINGS, T. C. J.; TUMLINSON, J. H.; HEATH, P. R.; PRAVEAUX, A. T. & DOOLITTLE, R. E. 1991. Isolation and identification of allelochemicals that attract the larval parasitoid, Cotasia margi-niventra (Cresson) to the microhabitat of one of its host. J. Chem. Ecol., 17: 2235-2251. WHITE, C. S. 1994. Monoterpenes: Their Effects on

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