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Essential oils as allelochemicals

Despina Vokou

Department of Ecology, School of Biology, Aristotle University, GR-54124 Thessaloniki, Greece
Email: vokou@bio.auth.gr

Abstract

The pervasiveness of the allelochemical concept in the literature is assessed based on a quantitative survey of the distribution of essential-oil-related research in different fields. A more refined definition of the term allelochemical is proposed to deal with persistent problems of consistency. The current trends regarding research on essential oils as allelochemicals mediating plant-plant, plant-animal, plant-microbe interactions are presented and the contribution of essential oils in shaping interactions between aromatic plants and microorganisms in the Mediterranean environment is discussed in the light of personal research in the field.

Media Summary

Quantitative analysis of the research effort involving essential oils, ecologically meaningful related research, pervasiveness of the allelochemical concept, and re-definition of allelochemicals.

Keywords

allelopathy, volatile oils, activity, interactions, semiochemical, microbes

Introduction

Allelochemicals and related terms - A new definition of allelochemicals

In the chemical ecology related literature, one finds the term semiochemical to be associated with interactions between organisms, whether inter- or intraspecific, pheromones to signify chemicals mediating intraspecific interactions, whereas allelochemicals to signify chemicals mediating interspecific interactions. Allelochemicals are also used to describe the chemicals that impose allelopathic effects (in absence of a relevant term deriving from allelopathy). As the use of the term pheromone is confined only to animals, chemicals mediating plant intraspecific interactions cannot be described. Also, if allelochemicals are defined as associated only with allelopathy, a large part of species interactions is excluded, unless the scope of allelopathy becomes widened enough to cover them. Terminological problems regarding allelochemicals started with the classification system suggested by Whittaker and Feeny (1971). In this system, chemicals associated with intraspecific interactions were described as pheromones, auto-toxins and auto-inhibitors, whereas the allelochemicals (associated with interspecific interactions) were further subdivided into ‘allomones’, ‘kairomones’, and ‘depressants’, based on whether they confer adaptive advantage for the producing organism, for the receiving organism, or for none. Major problems of this system (and its terms still in use as such or with modifications) are associated with the fact that the ‘adaptive advantage’ is not readily measurable, and therefore not an easy criterion to be applied, and also the exclusion of the possibility of any positive plant intraspecific interactions. Later, Reese (1979) defined allelochemicals as non-nutritional chemicals produced by one organism that affect growth, behaviour or population biology of other species. However, the latter definition puts aside microbes, since an allelochemical can be ‘nutritional’ for some of them, i.e. providing energy and nutrients (and hence violating the non-nutritional criterion of the definition), while at the same time drastically affecting the whole microbial community.

A multitude of terms (many notoriously strange) have been developed by authors in their attempt to deal with the complexity of relationships between organisms. However, instead of putting order into the chaos, this has resulted in ever increasing confusion. Scientific societies like the International Allelopathy Society should consider the option of developing a coherent scientific vocabulary for their field and widely communicating it. My contribution to this is the following: I suggest defining allelochemicals as secondary metabolites or non-nutritional primary metabolites that affect growth, reproduction or behaviour of individuals other than the ones producing them, or structure and dynamics of populations or communities of either plants or animals or microbes. It is obvious, from this definition, that I envisage the scope of allelochemicals to be far wider than that associated with allelopathy sensu stricto (i.e. involving only plant-plant interactions, direct or indirect, beneficial or harmful). I also believe that the term allelochemistry, which first appeared in the international literature twenty years ago and is only sporadically used even now, should find much wider use covering all interactions mediated by chemicals with the above properties; allelopathy, then, would be a subset of allelochemistry.

Essential oils and aromatic plants

Aromatic plants differ from all other plants in that they produce essential oils which give them their particular fragrance. Essential oils are mixtures of low molecular weight (hence volatile) isoprenoid compounds, mainly C10 and C15, oxygenated or not. Isoprenoid compounds are widespread in nature but in aromatic plants they are secreted and stored in specialized tissues (trichomes, cavities, ducts, canals, etc). Aromatic plants are widespread all over the world. Nevertheless, 49% of the essential-oil producing genera, mostly of the families of Labiatae and Compositae, occur in regions with Mediterranean-type climate (Ross and Sombrero 1991).

Objectives

This paper aims at detecting the allocation pattern of the research effort that involves essential oils, focusing on essential oil mediated interactions that are meaningful in the ecosystem context, and illustrating their role as allelochemicals in plant-microbe interactions in the Mediterranean environment.

Essential-oil-related research effort: quantitative features

Table 1 summarizes the results of a literature search conducted in early May (on the 9th and 10th) 2005. Showing in a quantitative way the distribution of the research effort, it reveals the main attractors of essential-oil-related research and can provide a basis for assessing future trends. It also provides some insight on the scientists’ perception of the type and context of research that they are doing, as well as on the pervasiveness of the allelochemical concept in the relevant scientific society.

I should first note the preponderance of the term ‘essential oil’ over the synonymous ‘volatile oil’, despite the more precise descriptive ability of the latter. Publications about essential oils or about essential oils and activity amount to 7,232 and 1,678, respectively. Publications about volatile oils or about volatile oils and activity amount only to 789 and 133, respectively. This remarkable difference puts the latter set of publications into an inferior position and limits their readability.

Table 1. Literature search (SCI journals) on essential-oil-related publications (May 2005).

Topic

Topic descriptors and operators

Counts

aromatic plant

aromatic plant*

270

essential/volatile oil

essential oil* OR volatile oil*

7819

essential oil

essential oil*

7232

volatile oil

volatile oil*

789

General activity

 

essential/volatile oil activity

essential oil* AND activit* or volatile oil* AND activit*

17771

essential oil activity

essential oil* AND activit*

1678

volatile oil activity

volatile oil* AND activit*

133

Allelochemicals, allelopathy, plant defense and other processes

 

allelochemicals

EO/VO2 AND allelochem* or monoterp* AND allelochem*

583

allelopathy

EO/VO AND allelopath* or monoterp* AND allelopath*

53

allelopathy/
allelochemicals

EO/VO AND allelopath* or allelochem*, monoterp* AND allelopath* or allelochem*

93

phytotoxicity

EO/VO AND phytotox*

41

seed germination

EO/VO AND seed germination

20

seedling growth

EO/VO AND seedling growth

14

defense

EO/VO AND defens*

48

plant defense

EO/VO AND plant defens*

13

anti-feeding

EO/VO AND antifeed*

28

herbivory

EO/VO AND herbiv*

31

growth promotion

EO/VO AND growth promot*

11

pollination

EO/VO AND pollination or pollinator*

23

decomposition

EO/VO AND decompos*

29

respiration

EO/VO AND respiration

30

ecosystem

EO/VO AND ecosystem*

12

community

EO/VO AND communit*

22

Organisms

 

bacteria

EO/VO AND bacter*

524

fungi

EO/VO AND fung*

416

insects

EO/VO AND insect*

253

mosquitoes

EO/VO AND mosquito*

48

acari/mites

EO/VO AND acar* or mite*

63

ruminants

EO/VO AND sheep or goat* or cow or cattle or ruminant* or rumen

36

other vertebrates

 

10

Specific activities

 

antimicrobial

EO/VO AND antimicrob*

687

antibacterial

EO/VO AND antibact*

392

antifungal

EO/VO AND antifung* or fungitox*

354

antiviral

EO/VO AND antivir*

33

anthelmintic/nematicidal

EO/VO AND anthelmintic or nematic*

26

insecticidal

EO/VO AND insectic*

135

antimalarial

EO/VO AND antimalar*

24

acaricidal/antimite4

EO/VO AND acaricid* or antimite

27

antioxidant

EO/VO AND antioxidant*

245

Pharmacological activities

 

analgesic

EO/VO AND analg*

48

anti-inflammatory

EO/VO AND anti-inflam*

58

anticancer

EO/VO AND cytotox* or anticancer* or chemoprevent* or antitum*

122

sedative

EO/VO AND sedativ*

45

antispasmodic

EO/VO AND antispasmo* or spasmoly*

51

antihypertensive

EO/VO AND vasorelaxant* or hypotens* or antihypertens*

21

anticonvulsant

EO/VO AND anticonvulsant* or antiepil*

25

anxiolytic

EO/VO AND anxiolytic* or stress relie*

15

1Ninety-nine out of 100 most recent publications deal with negative effects and only 1 with positive effects
2
EO/VO=essential oil* OR volatile oil*
3
total counts for the descriptor ‘allelochemicals’: 1348
4
primarily Tetranychidae, Varroidae, ticks

About one fourth of the essential/volatile oil related publications deal with some activity of these secondary metabolites. In fact, of the combinations that we examined, that of ‘essential/volatile oil and activity’ is second only to the combination ‘essential/volatile oil and composition’ (2465 counts; the other most highly represented combinations being essential/ volatile oil and analysis, isolation, extraction, and flavour, with 1307, 949, 603, and 370 counts, respectively). The variety of target-organisms and target-processes studied is high. However, much of this research is not of allelochemical nature: a large number of publications refer to various types of pharmacological effects and hence of the potential of these compounds to find therapeutic uses, with prominent among them that regarding anticancer activities. Our view is that the term allelochemical should be kept for chemicals affecting organisms other than humans, in either natural or anthropogenic settings, in which the encounter of donor and target organisms may occur.

Of a total number of 1348 publications including a descriptor of the term allelochemical (in their abstract, title or key words) for the period 1970-2005, only 58 contain in parallel descriptors of the terms ‘essential oils, volatile oils or monoterpenoids’(the latter being most highly represented in the essential oil mixtures). For comparison, 250 publications deal with phenolics (descriptor: phenol*) and 48 with only sorgoleone. Allelochemicals and/or allelopathy decribe only 93 of the essential-oil related publications. A large number of publications deal with bacteria (524) and fungi (416), whereas 687 publications refer to the antimicrobial activity of essential oils. Comparing all these numbers, we can conclude that the pervasiveness of the term ‘allelochemical’ in the vocabulary of the scientific community interested in the antimicrobial activity of essential oils is not high. Effects on insects and essential oil mediated plant-insect interactions seem to be one of the most prolific research areas (253 publications referring to insects; 135 dealing with insecticidal activity). Of these, pollination related research makes only a small fraction (23 publications).

The term allelochemical was introduced to describe ecologically meaningful interactions. Nevertheless, judging from the above and from the little use of indicator terms like ecosystem or community (with only 12 and 22 counts, respectively), it seems that ecological thinking does not prevail in this literature.

Essential oils acting as allelochemicals in natural settings

Plant-plant interactions

A lot of research in this field dealing with the inhibitory effect of essential oils on seed germination and seedling growth of various species and concomitantly on their potential to be used as herbicides can be described as traditional. Only a few publications examine other aspects of plants’ response in presence of essential oils (or of their constituents), as is mitochondrial respiration (Abrahim et al 2000; Mucciarelli et al 2001), stomatal opening (Rai et al 2003), lipid oxidation (Gadlo 2004; Zunino and Zygadlo 2004), chlorophyll fluorescence (Romagni et al 2000), and the ability of exposed seeds to metabolize some of their constituents (Dudai et al 2000). Interesting aspects of research in this area concern the contribution of essential oils in vegetation patterning (Wilt et al 1993; Tarayre et al 1995; Robles et al 1999; Ehlers and Thompson 2004) and in the invasive ability of aromatic plants behaving as weeds (Kong et al 1999; Barney et al 2005), as well as the interpretation of authopathic effects in an ecologically sound way, such as the diaspore dormancy caused by essential oils contained in diaspore tissues of some Lamiacae aromatic plants (Thanos et al 1995).

Plant-animal interactions

In the area of essential oil mediated plant-animal interactions, a lot of research has been done with essential oils (or individual lower isoprenoids) acting as defence chemicals against invertebrates, mainly insects and other arthropods attacking conifers (Yu 1992; Clancy et al 1993; Joseph et al 1993; Raffa and Smalley 1995; Holopainen et al 1995; Carisey and Bauce 1997; Guillet et al 1997; Wallin and Raffa 1998; Loreto et al 2000; Pasqua et al 2002; Cheng et al 2004) and other species (Mukherjee 2003; Knihinicki and Boczek 2003; Blaske et al 2003; Akhtar and Isman 2004), mollusks (Vokou et al 1998; Linhart and Thompson 1999), and nematodes (Walker and Melin 1996; Duschatzky et al 2004). The effects of the use of essential oils/aromatic plants on aspects of the animal physiology and behaviour have been examined for representatives of several classes of vertebrates. The animals studied are: ringtail possum (Foley 1992), kangaroo (Jones et al 2003), koala (Hume and Esson 1993), feral cat (Clapperton et al 1994), deer (Goralka and Langenheim 1996), mule deer (Bray et al 1991), goat (Pritz et al 1997), snakes (Clark and Shivik 2002), and from birds, quail (Denli et al 2004) and blue tit (Petit et al 2002), the latter being a clear experimental demonstration that a free-ranging animal makes use of smell to maintain an aromatic environment for offspring with plants. Attempts to explain the maintenance of chemical polymorphism in natural populations of aromatic plants as a result of selective herbivory (Linhart and Thompson 1999) constitute an interesting area of research.

In contrast to what holds true in other types of interactions, positive effects are frequently sought for in those involving plants and animals. Several publications deal with the constituents of essential oils (or oleoresins) acting as attractants: for aphids (Pope et al 2004), for Scolytidae beetles (Byers 1992; Macias-Samano et al 1998; Poland et al 2004; Sun et al 2004), for parasitoids (Salom et al 1992; Sullivan et al 1997; Petterson and Boland 2003), and for other insects (Katerinopoulos et al 2005), like the male Mediterranean flies attracted by a-copaene, which possibly serves as a cue to facilitate orientation of flies to the rendez-vous site (Nishida et al 2000).

Plant-microbe interactions

Publications regarding essential oils and microorganisms count in hundreds (Table 1), and a large variety of fungi and bacteria taxa, most being human or livestock/crop pathogens, have been tested. Publications regarding the ability of microbes to catabolize these secondary metabolites (Misra et al 1996; Vokou et al 2002; Harder et al 2000; Zorn et al 2004) amount to a mere drop in the ocean of publications regarding antimicrobial activities.

The contribution of essential oils/oleoresins or their constituents in nutrient (nitrogen primarily) cycling (Klopatek and Klopatek 1997; Ward et al 1997; Paavolainen et al 1998) as well as their effect on the structure of soil and phyllosphere microbial communities (Vokou et al 2002; Karamanoli et al 2000, 2005; Yadav et al in press) are interesting aspects of the plant-microbe interactions at the community level. Under plant-microbe interactions, we can also refer to most of the work done regarding aromatic plant-ruminant interactions, as these animals utilize microbial fermentation to digest food substrates. The degradability of aromatic plants and essential oils, and their effect on microbial protein production and flow, proteolytic or peptidolytic activity of rumen fluid, fatty acid and ammonia concentrations are among the parameters examined (Newbold et al 2004; McIntosh et al 2003).

Essential oils as allelochemicals in plant-microbe interactions in the Mediterranean environment

The mediterranean-type climate is characterized by a strong seasonality, with a rather mild and wet season alternating with a dry and hot one. In consequence, factors favouring growth do not coincide for a considerable part of the year. Aromatic plants are regular components of Mediterranean ecosystems; in phrygana (syn. batha in Israel, tomillares in Spain, gariga in Italy, coastal sage in California), in particular, they are dominant ones. The abundance of aromatic plants, in terms of both biomass and species number, implies that essential oil production is advantageous in this environment. My research with aromatic plants is an attempt to substantiate this theoretical claim. Of the work done (in collaboration with several students and colleagues), I will summarize here the part that refers to plant-microbe interactions, with the soil and the phyllosphere being the microbial habitats.

We investigated the effect of essential oils on soil metabolism and on the growth of soil bacteria and fungi. We added different quantities of essential oils from various aromatic plants or of their constituents in or above soil samples from the area where these plants grow (Vokou et al 1984; Vokou and Margaris 1988). We found a remarkable activation of soil respiration that could be retained at high levels for prolonged periods of time (about a year), accompanied by a manifold increase of the soil bacterial population size. These results provide strong evidence that these secondary compounds are used as a carbon and energy source by soil microbes. In parallel, we found the fungi that we tested to be severely inhibited. Based on these findings, we suggested that the decomposition process in phrygana is mediated by allelopathic interactions, that essential oils shift the population balance in soil from fungi to bacteria, and that the activation of soil bacteria by volatile oils from aromatic shrubs may be considered as an adaptive mechanism, where phryganic systems develop.

We further explored the possibility of microbes being adapted to substrates to which they are exposed. In particular, we examined the hypothesis that the response of soil microbes to a ‘known’ essential oil differs from that to ‘unknown’ essential oils. To this aim, we collected samples of aromatic plants of various species differing in the composition of their essential oil as well as soil samples from the area below each of these plants. We made all possible combinations of essential oils-soil samples (e.g. addition of thyme essential oil in soil samples from below thyme, addition of thyme essential oil in soil samples from below savory, etc), and we measured soil respiration of these combinations. We also examined the effect of essential oils on respiration of soil samples from cultivated areas (not supporting aromatic plants). Although there were differences in the intensity, the timing and the duration of the response, the overall pattern was the same in all combinations. So, our initial hypothesis did not hold good. Also, no differences were found in the magnitude of respiration of soil samples exposed or not to essential oils. This led us to conclude that bacteria able to decompose the isoprenoid compounds of essential oils have a more ubiquitous presence than we initially believed (Vokou and Liotiri 1999). Later, we found that our initial claim that essential oils shift the microbial balance in soil was correct, but not entirely. The shift is not from fungi to bacteria but from a more diverse bacterial community to another, dominated by a few bacterial strains (Vokou et al 2002).

Following our research with soil bacteria, we examined the interaction of aromatic plants with epiphytic bacteria. We found that the Mediterranean aromatic plant is characterized by scarce presence of ice-nucleation-active (INA) bacteria on its leaves (Yadav et al 2004; Karamanoli et al 2005). But we also found that the phyllosphere of essential oil producing species is not in general less colonized by epiphytic bacteria than is the phyllosphere of non-aromatic Mediterranean species (Yadav et al 2004). Species rich in compounds with antimicrobial activity (isoprenoid and phenolic compounds) harbor low leaf populations of the bacteria that they affect (Karamanoli et al 2000, 2005), but the opposite does not hold true: species with non- or moderately active leaf secondary metabolites are not always highly colonized, which suggests mediation of other factors influencing the size of epiphytic bacterial populations (Karamanoli et al 2005). The population size of epiphytic bacteria correlates positively with the density of both the glandular and the non-glandular trichomes, but essential oil concentration is not among the critical parameters (chemical or anatomical) that determine the magnitude of the phyllosphere colonization of Mediterranean species (Yadav et al in press). Still unpublished data show that epiphytic microbial communities of aromatic plants are not less diverse than other Mediterranean species and suggest that they, too, can use essential oils as a carbon source.

Conclusions

Having identified problems in the various definitions of the term allelochemical, I suggest a new more adequate definition. The survey regarding allocation of the research effort involving essential oils showed that (i) microbes are by far the most studied group of organisms, followed by insects, (ii) the antimicrobial activity is the most studied biological activity, followed by the antioxidant activity, (iii) research on the essential-oil-catabolizing activity of microbes is but a drop in the ocean of the antimicrobial-activity-related research, (iv) the pervasiveness of the word allelochemical in the relevant scientific community is not very high, (v) this community does not seem to be ecology oriented. The major effect of essential oils as allelochemicals, when mediating plant-microbe interactions in the Mediterranean environment, is shifting of the bacterial population balance in favour of those bacteria that can tolerate them or even use them as a carbon and energy source.

Acknowledgements

Aristotle University of Thessaloniki, Greece, Charles Sturt University, Australia, and General Secretariat for Research and Technology, Ministry of Development, Greece (programme 01 ED 317), are greatly acknowledged for supporting this contribution. The following colleagues and students have participated at various stages of the research briefly presented here: Bosabalidis AM, Chalkos D, Constantinidou H-I, Halley JM, Karamanlidou G, Karamanoli K, Liotiri S, Lynch JM, Margaris NS, Menkissoglu U, Papatheodorou E, Yadav RKP, and Yangou M.

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