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Chemical communication by behaviour-guiding olfactory signals

L. Gunnar W. Bergstro¨m

Received (in Cambridge, UK) 16th August 2007, Accepted 17th March 2008 First published as an Advance Article on the web 19th May 2008 DOI: 10.1039/b712681f

Chemical Ecology is a new interdisciplinary research area with close collaborations between chemists and biologists of different descriptions. It has developed during the last 40 years because of an interest in the structure, function and evolution of chemical signalling among organisms and also because of the hope to be able to use the ubiquitous phenomenon to control organisms, like pest insects. This feature article highlights the growth of the discipline and the progress made, through examples from the author’s own work on chemical communication in insects and flowering plants. The research deals with olfactory signals, i.e. volatile chemical compounds perceived by the sense of smell. Analytical techniques and methods are an important part of the work.

Introduction chemodiversity and contribute to establishing and maintaining the enormous biodiversity found among living organisms. All multicellular living organisms employ olfactory signals to Most of the work in this field, which now goes under the guide their behaviours. That is a rule with few, if any, excep- name of Chemical Ecology, has so far been done on insects and tions. The scents are mainly perceived through the sense of plants, which are the topics of this article, but chemical smell and they are linked to all vital needs such as development communication is increasingly being studied in micro- and feeding, recognition and nesting, mating, alarm and organisms, aquatic organisms, and mammalians—including defence. The chemical signals frequently consist of more than Man. From the chemical point of view there are many a single compound, most often either two or three, or complex similarities between them. The very same compounds can turn blends with many components, often members of homologous up in very diverse types of organisms. Applied aspects of series of compounds. They are the products of the acetogenic olfactory signals include the selective and non-toxic control (fatty acid derivatives), the mevalogenic (isoprenoids), the of organisms, such as pest insects of importance in agriculture, benzenoid (aromatic) and other biosynthetic pathways. They forestry and medicine. are often species-specific, like pheromones, defined as signals The famous entomologist Jean-Henri Fabre (1823–1915), a between individuals of the same species that could serve school teacher from Avignon, France, studied, among many recognition and sexual selection and be involved in speciation. other phenomena in the world of insects, the distant attraction When they represent chemical communication between differ- of malesofthegreatpeacock moth( Saturnia pyri), Fig. 1, to the ent organisms, like between plants and insects, we use the more females, and wrote poetically about this phenomenon at the Published on 28 July 2008. Downloaded by RUTGERS STATE UNIVERSITY 03/04/2018 18:28:06. general term semiochemicals. Chemical signals show a large beginning of the last century:1 ‘‘Like light, odour has its X-rays. Should science one day, instructed by the insect, endow us with a radiograph of smells, Laboratory for Ethological Chemistry, Kolonigatan 3, Goteborg, SE- 41321, Sweden. E-mail: [email protected] this artificial nose will open out to us a world of marvels.’’

Gunnar Bergstro¨m is Professor of Ethological Chemistry, Go¨teborg University. He received his PhD in 1973 and then became Docent in Biochemistry. Until 1983 he was Research Assistant in Medical Physics and held a Research Position in Ecological Chemistry. His principal supervisors and mentors were Professor Einar Stenhagen, Medical Biochemistry, Go¨te- borg University, and Professor Bertil Kullenberg, Entomology, Uppsala University. From 1973 until 1985 he was responsible for setting up and managing the Analytical Chemistry Unit at the Ecological Research Station of Uppsala University. He is a member of the Royal Swedish Academy of Sciences, the Finnish Society of Sciences and Letters, and Academia Europaea. He has been Visiting Professor at the University of Texas, Austin Gunnar Bergstrom¨ (1976) and the University of California, Berkeley (1995). He was the second president of ISCE (International Society of Chemical Ecology) and has published mainly in Ethological Chemistry and Chemical Ecology.

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c The Royal Society of Chemistry 2008 Chem. Commun., 2008, 3959–3979 | 3959 volatile compounds could be identified. This enabled us, in many cases, to achieve the goal of analysing volatiles from single individuals and thereby being able to compare them. You could, for instance, see the chemical variation between individuals or compare secretions during different stages in their development and find biological correlations to it. At the same time there were crucial improvements in the techniques of measuring and recording olfactory-elicited behaviour, both in the field and in the laboratory, and in making electrophy- siological recordings from insect antenna. Other reasons or motivations were the curiosity concerning the role played by chemical signals in guiding behaviour (ethology) and forming Fig. 1 Male Saturnia pyri, the great peacock moth. Observe the large, liaisons between organisms (ecology), and the applied aspect, feather-like antenna—the female has more thread-like ones and at the the possibility of using selective signals for the control of pest abdominal tip the sex pheromone gland. insects. Some pioneering work had been done since the 1930s at USDA (United States Department of Agriculture) labora- How right he was—even if he thought that the sense of smell tories, e.g. on the sex pheromone of the gypsy moth, was based on electromagnetic radiation! Collaborative, inter- Lymantria dispar, but its correct structure, (7R,8S)-7,8- disciplinary research efforts on natural chemical signals have epoxy-2-methyloctadecane (‘‘disparlure’’), was not determined now been going on for more than 40 years. So – Where are we until 40 years later.4 This illustrates the importance of the now? What do we know? And what are the future prospects of development of sensitive analytical techniques. this branch of Science? Much is known today about the structures and composi- tions of the chemical signals, their behavioural effects, the reception of odours, their practical use, and the optimal methods and techniques of analysing them; a certain amount is also known about their biosynthesis, their genetics, their ecological and evolutionary roles, for example. But much remains to be done, many fascinating problems and pheno- The chemical identities of the two moth sex pheromones, mena are left to be studied. This overview should exemplify ‘‘bombycol’’ and ‘‘disparlure’’, illustrate the common struc- some of what we know today, some of the fundamental facts tures of long chain fatty acid derivatives, so many identified and phenomena of olfactory signals. since then as moth pheromones, for instance in the laboratory The pioneering work of Adolf Butenandt in Munich (Nobel of W. Roelofs, attached to Cornell University. There, T. laureate in 1939 for his studies on hormones) on the female sex Eisner and J. Meinwald carried out pioneering studies, espe- attractant of the silk moth, Bombyx mori, led to its identifica- cially on defensive mechanisms of arthropods. tion as a doubly unsaturated straight chain alcohol called Important years in the further development of the inter-

Published on 28 July 2008. Downloaded by RUTGERS STATE UNIVERSITY 03/04/2018 18:28:06. bombycol:(E,Z)-10,12-hexadecadien-1-ol, published in 1959. disciplinary field are 1975: the first publication of the Journal of Chemical Ecology (JCE) under the dedicated editorship of the late R. M. Silverstein and J. Simeone, and 1984: the formation of the International Society of Chemical Ecology (ISCE), with annual meetings in different countries. From the job point of view, research laboratories, environmental agen- cies and pharmaceutical and other chemical companies devel- The report2 starts with a sigh: ‘‘After more than 20 years of oped a need for people experienced in working with small experimental effort, we have now succeeded in identifying the amounts of biologically active compounds. Recently they have female sexual attractant of the silk moth’’. In the same year the proved to be major employers, together with universities, for term pheromone was coined by Karlson and Luscher.¨ 3 These people trained in Chemical Ecology. are the grounds for counting that year as the starting point for Since the number of potential odour components, an esti- Chemical Ecology, although the term was introduced 10 years mate based on the number of known organic chemicals of later, in 1969, when some scientists had begun studies on enough volatility and other suitable characteristics, exceeds 1 olfactory signals. Pioneering work on the electrophysiology million, and since more than 1.5 million species of various of insect olfactory reception was done by D. Schneider and his multicellular organisms are known, named and descri- group. This type of study has been further developed. bed—about 800 000 species of insects and 250 000 species of There are some good reasons why work in this area com- higher plants—it is certainly correct to talk about both a rich menced in the 1960s and 1970s. A major one, really a chemodiversity and biodiversity. Chemical signals must have prerequisite, was the development of sensitive and informative been a fundamental aspect in the origin of life, even in an early analytical chemical techniques, especially isolation/enrichment phase characterized by chemical interactions, and as chemo- techniques and separation/identification through gas chroma- tactical agents for avoiding toxic chemicals and attraction to tography and mass spectrometry, by which small amounts of nutrients. The geneticist Theodor Dobzhansky stated5 that

3960 | Chem. Commun., 2008, 3959–3979 This journal is
c The Royal Society of Chemistry 2008 Published on 28 July 2008. Downloaded by RUTGERS STATE UNIVERSITY on 03/04/2018 18:28:06. tempted recordings (molecular) as of an when forgotten and giving micro an directly have obtained tations tion lyses individuals analysis This amounts The Analytical ‘‘ ment in altered, reference To nanogram, experiments separation, the the This other for revolving sometimes disciplinary do and preferably should chemical biology, les—many tical various we they direct times nothing 1. A The such an chemical odour ideal they are help out, chemical questions: this sometimes chemist journal correlate? the precision, somewhat procedure. and done in additional Preparatory statement body in pre-column encountering additional scale normal coming ideally a of coupled potent the elicit? either step tool in GC–MS is in combination. way and of by ecology. signal, and compounds for that fraction field-borne, some different some also biology the done is parts), analyses. fashion. or identification, (like of them compounds working this identity we and can micro-techniques at in are
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Chemistry applying techniques of during a collected A like highly (such 15 the tastings). good the a in isolation/concentration, the a a 13 are the which mass special end used compounds hint (GC–MS), often for Access very the ideally guiding material does effluent splitter Hydrogenation way especially working 18 chemical now chemical integrated (TLC) molecular with steps as indication potent the light , of trying spectral of procedure It observations in concurrently phase a guide a or valuable is 2008 and not the technique, and challenge from compound. what combination available—and find the to should all Methods high not this be chemical of near-natural, in principle can information yet well-defined in in three behaviours, to presence with instrument, carried has or evolution chemically structures, sometimes use, the identifica- behaviour and when glands sensitivity especially sequence, of fragmen- chemical the be elucidate an exist level state of supple- proved not volati- analy- some- of is single arises steps. and 14 inter types what on used ana- low- asks and out We but use the for at- do by be or of of of ’’. a a - spectral was Fig. compounds ments the mens, sensitivity of in analysis methods and optimal principle rigid field–laboratory–field. (the for through either foremost activity. flight with chromatographic oped nique: in compounds, auxiliary technique. tography check chemical a.—with time, tube General The adsorbent glandular one conditions. cold extraction; Among There Because The Other 5. 4. Behavioural 3. Alternatively, Possible A 2. our the extremely highest choice by the of sense two Behavioural 2 Isolation built trap; the Separation Identification of cleaning thereby molecules chambers towards directly laboratory area activity. and shows have gas many outcome area a and observations a techniques, identification techniques latter it the is change. methods tool coupled and of gas amounts collection of tissue d. heavier and chromatography–mass and with behavioural because (like tests. could possible b. Knowledge can been an volatile experiments/observations of olfaction), by risk the some sorption possible (retrieval) enriching driving is retrieved chromatograph; methods techniques. higher experiments analysis step information, tested. faithfulness be the ‘‘analytical and gas of, microgranular or experiments with usually This be of and (under made techniques. of to in instrumentation of recorded. technical of available. complementarily, coupling GC–MS. Chem. ‘‘X-ray compounds often chromatography, losing the like as may of olfactometers, electro-antennal the low in off (scent phase techniques. sensitivity, behaviourally a (adsorption/desorption) step, With tests from high defined in well-defined the about of can the well high IR analyses a analyses. volatile permanent sensitivity the complex, Commun., be volatile material microscope), We recovered crystallography field. as to (tests) window’’, accumulate (here and purity emission, improvements. a often should between of Unfortunately This Problems sensitivity it as This gas needed, data life the in by c. the rotational carbon, (for have NMR, in Laboratory compounds another spectrometry mainly step the and concentrating chromatographic It stands calls cycles natural material are working is a bank and which analyses ideally micro-chemical example, or compounds. isolates can dipole an 2008, active microwave the volatility GC–EAD, detection, sample. strived for of or is can important then which effecting of for especially restriction have volatile important most Tenax behaviour. of followed of be steps in in ‘‘hyphenated’’ the or instance). material, arise are spectra reference be from in 3959–3979 it the the with target compounds. a. some become moment—but into closes methods falls gradually by in receptor is performed the often summarizes to often in of preparation on instrument, (GC–MS). laboratory) in of a a or material an evaporation), samples the spectrometer gas the single a fractions gas to attain the very pre-column to cases in a organisms. aspect. with by limited of compound Porapak). unwanted combined the as and Improve- object arranged analyses. ascertain synthetic material, relatively chemical chroma- valuable analyses phase’’. method systems include volatile solvent well potent | devel- speci- cycle: other good mass tech- both 3961 high over in The use by an or or as to of in a Fig. 2 Examples of equipment for chemical analyses—improvements of techniques. Upper left: gas chromatographic micro-split for FID and NPD detectors, or for one detector and micro-fraction collection; upper centre: revolving micro-collection device with six micro glass tubes in a cooling mantle attached at the outlet of a gas chromatograph (glass capillary columns); upper right: a microwave (1 cm region) rotational spectrometer equipped with gas cell (long tube in the centre) and a 6 Kc s 1 Stark electrode; lower left: an early gas chromatograph fitted with a precolumn (upper left corner) and a packed glass column; lower centre: capillary glass tube with palladium catalyst for hydrogenation on a micro scale; lower right: gas chromatograph fitted with glass capillary column, splitter, and fraction collector (on the left side), equipped with both FID and NPD detectors. Reproduced with permission: Upper left: A.-B. Wassgren and G. Bergstrom,¨ J. High Resolut. Chromatogr. Chromatogr. Commun., 1984, 7, 155. Copyright Wiley-VCH Verlag GmbH & Co. KGaA. Upper centre: A.-B. Wassgren and G. Bergstrom,¨ J. Chem. Ecol., 1984, 10, 1547, with kind permission of Springer Science and Business Media. Lower centre: J. Bergstrom¨ and G. Bergstrom,¨ J. High Resolut. Chromatogr. Chromatogr. Commun., 1985, 8, 144. Copyright Wiley-VCH Verlag GmbH & Co. KGaA.

and of compounds of very low volatility. There is also a logical functions, and analytical techniques. The evolutionary minimum amount of compounds needed for detection; analyses background for the large variety of chemical compounds will be can be at the picogram level with the more sensitive techniques. discussed together with the links between the compositions of In some cases we encounter substances sensitive to chemical the chemical signals and the respective biological functions. change, like autoxidation. Therefore, behavioural tests are Since we have now, in this field, studied many species, represent- needed to ascertain biological activity. NMR has often proved ing some major groups of the 30 orders of insects, especially in to be too insensitive for the analyses of olfactory signals when Hymenoptera (bees, bumblebees, ants and sawflies), Coleoptera Published on 28 July 2008. Downloaded by RUTGERS STATE UNIVERSITY 03/04/2018 18:28:06. very small amounts are available and sufficient purity is not (beetles), Neuroptera (antlions) and Lepidoptera (butterflies and achieved, but this technique is improving so that this very potent moths), we have many good examples of the chemical and technique can be of use in some cases. A combined chemi- behavioural interactions of insects, and their relationships to cal–biological technique, which has proved to be most valuable, plants. The main primary examples discussed here represent, is GC–EAD, gas chromatography coupled with electro-antennal respectively, bees (sections 1 and 2), bumblebees (section 3), detection (of insect antenna, i.e. single sensilla or even single antlions (section 4), bark beetles (section 5), pine sawflies receptor cells). GC separation can also be combined with (section 6), larvae of butterflies and sawflies (section 7) and observation/measurement of insect behaviour in flight tunnels flowering plants (section 8), including the chemical interactions (such as for moths) and walking bioassays (such as with beetles). between the plants and insects. Some related work by colleagues, Of fundamental importance to our understanding of the which complements the examples given, is referred to briefly in structure and function of chemical communication is the connection with each example and finally some trends in the application of genetic methods, which are now increasingly development of Chemical Ecology are mentioned, with indica- being applied. The necessary ‘‘agreement’’ (coupling) between tions of a few possible further research directions in this field. the sender and the receiver in a chemical signal system can be Some of the basic texts in this area of Chemical Ecology are brought about by inheritance, by learning, or by a combina- referred to in references 19–27. tion of these mechanisms. 1. Chemical mimetism: discovery of the identical Scope of the article similarity of marking pheromones between host bees and parasitic bees The aim of this article is to give examples of chemical commu- nication between insects and between plants and insects, to We discovered this phenomenon when analysing volatile specifically address the phenomena of chemical structures, bio- compounds from exocrine glands of bees since we were

3962 | Chem. Commun., 2008, 3959–3979 This journal is
c The Royal Society of Chemistry 2008 Fig. 4 Females of Nomada sp. (left) and Andrena sp. (right).

as a new class, spiroketals, but none of the mimetic com- pounds.32–36 The production and emission of the mimetic sub- Fig. 3 Andrena cineraria female (host) at the nest opening (left) and stances exclusively by the parasitic males may imply sexual Nomada lathburyana female (parasite), waiting for entrance (right). selection through the composition and/or the quantity of the interested in their role as pollinators and also curious about male secretion. There has probably been a stronger selection their own olfactory signals. In females of certain species of pressure for males to produce mimetic compounds; in this way Andrena and Melitta bees (nest hosts), and in males of certain they can be said to have a nuptial gift for their females. The Nomada species (nest parasites), we found identical com- phenomenon ought to be investigated further by behavioural pounds: isoprenoid and straight chain esters of short experiments and linked genetic studies. We found the same acids.28–30 Why it is so was at first unknown since the phenomenon in Sweden (about 30 species studied) and in bees respective host females and parasitic males do not normally of these species from North America.37a meet, and they do not have an immediate functional relation- A dendrogram showing possible relations among the major ship. The nest-parasitic Nomada females gain entrance into the groups of bees was shown in Charles D. Michener’s book: The nests of host-bee females, Andrena or Melitta, in order to lay Social Behavior of the Bees, Belknap Press/Harvard, 1974. It can their eggs, Fig. 3. Fig. 4 compares the morphology of Nomada be seen that the host bees and the parasites are located far apart, and Andrena females. Andrena/Melitta and Nomada, respectively. One can ask how We found that the parasitic males (Nomada), in their the clepto-parasitic mimetism has evolved. The knowledge of mandibular glands (in the head) produce the very same phylogenetic/systematic relationships has developed, and a re- compounds as the host females produce in their Dufour glands cent treatment of some of the diverse opinions can be found in (in the abdomen). The male parasite transfers the mimetic the second edition of Michener’s book: The Bees of the World, compound to his female during mating, and thereby perfumes Johns Hopkins University Press, 2007, section 20, pp. 88–92. her with the marking pheromone of the host,31 Fig. 5a and b. The Nomadini and the Andreninae/Melittinae are placed some- In this way the parasitic Nomada female is recognized what closer together, but they are still clearly separated. The as a conspecific female when entering the nest of the host- former is in the Megachilidae family, long-tongued bees, bee females, Andrena or Melitta, in order to lay their eggs, whereas the latter two belong in short-tongued families. A recent Fig. 3, and there is no fight between host and parasite females. phylogenybyB.N.Danforthet al.37b is basedonfivegenesand The female parasite, hidden by this deceptive camouflage, morphology. It contains several important references. Published on 28 July 2008. Downloaded by RUTGERS STATE UNIVERSITY 03/04/2018 18:28:06. thereby avoids being attacked by the host bee. The dominating In another cleptoparasitic bee, Epeolus, females produce a mimetic compounds were identified as either geranyl octano- cephalic secretion containing spiro-compounds and ate or farnesyl hexanoate depending on the species of the pyrazines,38a Fig. 7. Andrena–Nomada pairs and as octadecyl butyrate for the It has been shown by Tengo¨ et al.39 that in the solitary bee Melitta–Nomada pair, Fig. 6a and b. Andrena wilkella only the naturally occurring enantiomer of The mandibular gland secretions of Andrena bees, both males the main component, 2,8-dimethyl-1,7-[5.5]undecane, with and females, include: monoterpenes, straight chain ketones and, (2S,6R,8S) configuration, attracted patrolling males in the

Fig. 5 (a) Left. Nomada and Andrena, females and males, respectively, showing (red) the Dufour gland of Andrena female, and the mandibular gland of Nomada male, producing the same marking compounds. (b) Right. Male and female Nomada bees in copula, showing how volatile compounds from the male mandibular gland can be transferred to the thorax of the female.

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c The Royal Society of Chemistry 2008 Chem. Commun., 2008, 3959–3979 | 3963 Published on 28 July 2008. Downloaded by RUTGERS STATE UNIVERSITY on 03/04/2018 18:28:06. substances pound, function. former, ponding’’ bee different emanate chemical Sphecodes widened to 2,6,10-trimethylundeca-(5 viours 3964 Fig. gram) field. Fig. mination from nor-sesquiterpene trail in found the parasitic cuckoo Besides Host–parasite Francke In the genus, Dufour 7 6 following | the olfactory 42 This studies, head), Examples (a) Chem. seem bee, species. bee hexyl whereas octyl Nomada from between and stingless Marking the communication bees two et was species: gland. (alkyl Nomada to Commun., their discovery of decanoate, octanoate to al. behaviour which specific (b) receptors. other involve of corroborated towards be male: in identified relationships ketones enantiomers. Nomada spiroacetals compounds Marking Epeolus and bee, the the means lathburiana species, geranyl glands, volatile main terpene 2008, Trigona other is produced of E their So, cruciger chemical parasites. in the )-2,5,9-trien-4-one. compound in interesting foragers. registration female of and T. octanoate component this insects 3959–3979 by dominant a halictid of Andrena spinipes and have . compounds esters) 40 pyrazines recursa, blend and EAG which is by mimetism, The cephalic This one from E. the also also new or females of main hosts. variegatus of (= seems trail-following labial there clear study found Ayasse farnesyl Melitta responsible no electrical sesquiterpene shows been T. secretions electro-antenno- emanating component 41 this fewer and case corvina. gland can in has to , These , hexanoate another other et respectively. example studied the that have now be of impulses al. than (located ‘‘corres- for discri- clepto- of In about beha- com- from have been they host was and this the the the 12 of in in have inating eicosanolide nonnestmates. Fig. related analysed. nestmates species same marking (muscone) isopentenyl Nature 2. Male pheromones 3. blend routes. 10 conspecific repetitive have study pounds and found hydrophobic formation the ent the chain twigs, employed secretion now and their Females bees, On hydrophobic mary straight females and cyclized they different tions The In different compounds. marking two the B. Evylaeus 38 are classified 8a Dual Species this each been own been bumblebees for products, of of species, represent leaves, b fatty volatile lapponicus occurring The musk of can components, other and is ideal chain compounds, which to accept species the substances long-lasting sizes. from serves marking The species. one used analysed. certain (sister and for economic—a function: This encounters. esters produce remain volatility ones of acid and secretions Dufour b, wall and (34 as by of smelling specificity: of hand, C16–C24 and blend different difference the wall the There As contain in new can journal as the shows This i-and species-, kin- (populations) the 22-docosanolide, , two in species secrete taxonomists male bees) derivatives in litter bee lining perfumery we and partners flights civet Dufour stable, acetogenic Scandinavia for 49–67 increases be one from which lining means species attracts o gland musk marking taxa nest discovered and genera: of is musk -hydroxy is polymerized that hydrocarbons, on weeks. from The macrocyclic and bumblebees C16–C24 cat (a from studied purposes. o The
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c hazel The 14 bees. in Royal leaf. cryptarum composition Reproduced Society (formerly of of Chemistry from Dufour’s Bombus ref. 38( gland 2008 lucorum b ) with secretions kind ‘‘dark’’) permission of individual of Fig. Springer E. 10 malachurum Male Science Bombus Chem. and bees. Business lapidarius (b) Commun., Dendrogram Media. scent-marking 2008, showing 3959–3979 a hazel the degree twig. | 3965 of Published on 28 July 2008. Downloaded by RUTGERS STATE UNIVERSITY on 03/04/2018 18:28:06. per single could and producing discern ably forms/new mating populations single the Megabombus flight pheromone position Megabombus 3966 occur Fig. of Fig. the lucorum ‘‘dark’’), They Within clearly relatively same individual. 11 11 concurrently originated | separation, individuals, at then, species Chem. and ( barrier formerly three Major B. represent the of area different subgenera, isoprenoids species lucorum 12. their theoretically, composition. Fig. same could high Commun., and are inhabiting at subgroups: components The between as treated 13 the just distinct Psithyrus, male differentiated, amount were compositions time in genetic ‘‘blonde’’) cases interbreed chemical same Major many like such and as made labial and 2008, the the a of differences. of interbreed. of air Among M. time, divergences components single fatty parts there as in the labial and same possible sympatric populations analyses, traffic—if gland 3959–3979 there hortorum the Pyrobombus, of Fig. marking there species. are acid Bombus of their gland some same geographical their some is secretion. 13 even Species Although might derivatives, of in which in marking the by pheromones speciation space. secretion, the and species cryptarum populations area chemical fact based early the terrain marking also in were M. Alpinobombus, of One chemical a They on in the region. pheromones, occurring be on behavioural distribution mainly consobrinus 0.1–1.0 ( made theory similarities allows because B. of since a secretions can subgenus different presum- vertical lucorum from Bombus They com- even with 9 it. mg the the Z of in a - of 10 begun heptadecene, nology B. omonal parasitic on followed Fig. turned nonadecene; variation ent tification on lapponicus pathway. duced specific studied long give secretions, ( Bombus bumblebee This The terrestris eggs the diterpenes; 12 off chain aimed semiochemistry by example of marking in out lapponicus complexity species-specific Major dominance bumblebees studies of in of It queen ( 71 a the Bombus aldehydes, species This comparative nest the B. M. to also and the at 2-nonanone components fatty and shows the terrestris journal subterraneus be Dufour on secretions B. queen and was scandinavicus within demonstrates lapponicus terrestris a chemical individual a signals, and acid 74 how group its alcohols, continued mixture of is have blends sex the gland . social species
the 73 way, c derivat male of by and subgenus The pheromone of Aggressive 72 by also and the bumblebee mimicry lapponicus ), using and of such and secretion formerly six and parasite bumblebees Royal how of collaborative ive by marking methyl M. been fatty specificity Megabombus group studies 21 acetates. the as blends Megabombus. route distinguendus species Society in ), studied, nr-and intra- acid compounds, treated analyses B. compounds B. relationships and components, oleate. pheromones and specific on vestalis and can of hypnorum derivatives, of specificity of concerning Bombus efforts. chemical compounds as produce including Chemistry Dufour the a of A species odours intercolonial . single make 75 the study isoprenoid of including 68,69 in 75 has monticola between species- Bombus exocri- can signals mainly species. 70 which differ which social gland pher- iden- been 2008 This pro and has be - - Fig. 14 Antlions. The larva (the antlion proper) lies buried at the bottom of a pit in the sand and is depicted with a possible prey, an ant, on the edge. The adult insect, in flight, to the right.

attained by the syntheses of characteristic blends of relatively few compounds, structurally related but different. The discovery of two chemically different forms (populations), in each of what was Fig. 15 A unique photo, taken at night, of antlions (Myrmeleon formerly considered as two species, probably represents the first formicarius) in copula; female above, male below. cases of chemical speciation involving olfactory signals in animals.

4. Minimal two-component species-specific sex The volatile compounds emitted represent variations of two pheromones in antlions biosynthetic routes, one isoprenoid and one acetogenic, Fig. 17. In the molecular scheme, the four uppermost compounds are Antlions proper are the three-year larvae of species of Myrme- monoterpenes resulting from the isoprenoid pathway. The other leontidae, a family of the insect order Neuroptera. They make two compounds are mono-unsaturated secondary alcohols of pits in the sand and lie in wait, ready at the bottom to catch different chain length (11 and 13 carbons) and result from the prey, such as ants, Fig. 14. Adults live for about two weeks, acetogenic pathway. This pattern of just two dominating sub- mating and egg-laying. Mating takes place typically in the tops stances in male sex pheromones is uncommon. of pine trees (Pinus silvestris), after the antlion adults have The pyranoid monoterpenes nerol oxide and 10-homo-nerol emerged from their pupae, dried their wings and flown a short oxide possess a characteristic sweetish-pungent scent which can distance. Fig. 15 shows the mating position with the female be encountered also from sun-exposed lacquered wood (such as holding onto a twig and the coupled male hanging down. from newly lacquered wooden boats), presumably formed in Male adult antlions possess a thoracic gland, which is only that case by photo-oxidation of nerol. This hint actually helped rudimentary in the female, Fig. 16a–c. The secretion of this gland, us in the chemical analysis. The antlions have an ‘‘archaic- which has a characteristic smell, serves as a male sex pheromone. looking’’, irregular flight. Myrmelion formicarius is said to be the Published on 28 July 2008. Downloaded by RUTGERS STATE UNIVERSITY 03/04/2018 18:28:06. It contains species-specific blends of just two components in each oldest species phylogenetically, and this is obviously reflected in of the five species analysed.76–79 Three of the species, Euroleon the most basic composition of its two-component secretion. It is nostras, Grocus bore and Myrmeleon formicarius,occurin worth stressing that the three Scandinavian species and the two Scandinavia; the other two species studied, Synclysis baetica from Israel have the same type of minimal two-component scent and Acanthaclisis occitanica, were collected in Israel. system.

Fig. 16 (a)–(c) Collage of three sweep-electron-microscope (SEM) pictures of (a) (left) the inner back of the wings with spreading organs, small brushes, marked with arrows; (b) (centre) enlargement of a brush fitting into a cleft in the thorax where the scent gland opens; (c) (right) further enlargement showing a comb-like structure at the gland opening in which the spreading brush fits at each stroke of the wing. Reproduced with permission from: R. Elofsson and J. Lofqvist,¨ Zool. Scripta, 1974, 3, 35, published by the Royal Swedish Academy of Sciences.

This journal is
c The Royal Society of Chemistry 2008 Chem. Commun., 2008, 3959–3979 | 3967 Published on 28 July 2008. Downloaded by RUTGERS STATE UNIVERSITY on 03/04/2018 18:28:06. 3968 to The 5. Fig. senting arrows), are contrasting species. aggregation beetle, communication results by chalcographus traps. project biological, verbenol area, for individuals penes either forest and yeast production ployed Blends The be four population oxygenated 17 active one Olfactory strains | which a was pest for involvement given Chem. successfully two blend of was are Molecular to Swedish Candida of studied monitoring, monoterpenes sex insects. responsible during and trans and different are to were in methylbutenol Commun., of , ways pheromone and was come refs. reduction, between products surveyed 2-methyl-3-buten-2-ol interconversion -verbenol system, signals found formulas and research a strain as studied of sex 80–89). biosynthetic of nine-year up for an also yeasts i.e. achieving to 2008, attack pheromones with the attractant and regularly linked ( from of and C. of convert which of relatively the in The species groups, and male ( the two that nitratophila control Candida (1 3959–3979 detail quantitative phases project the routes, S of ultimate to six cis calls )- cis bark Ips specificity of as in cis Ips the specificity -verbenol different wood, as -verbenols two few traps, -verbenol methods an ( typographus the and for Ips and typographus (part which, detoxification, a beetle ) ‘‘early practical traps collaborative chemical typographus). a related cis converts variation Hansenula Fig. of see compounds, large of -verbenol. have pairwise the for Fig. to to over warning’’, of the species: 18–20. five verbenone. verbenone, number goal Pityogenes was important male been monoter- 20, and chemical (1 between a analysed ) R by (dotted found in of larger effort right, repre- They Both )- This two em- cis the the the or of - omone, close identified blend lenging related also Fig. Fig. egg-laying phus (‘‘mass tree, see pump beetle through Finding By ; 18 19 contained the (at entrance colleague) contrast, attack’’), w of adsorption. species, Spruce since Signal Fig. two the Fig. has primarily the ‘‘chalcogran’’ This bottom upper 23. taken holes extracts 21 molecules two tree the large Pityogenes journal produces In and and ones lower ( place) end and synergistically Picea order by quantities methyl 22. of obtained attract with is (pheromones) ones Prof. abies to the
to c in (2-ethyl-1,6-dioxaspiro[4.4]nonane, leave The a chalcographus find red are ) minipump females, ( the E with Dr Royal tubing) , used of Z the by the active male )-2,4-decadienoate small W. volatiles tree. body active of as and Society to (centre a pioneer Francke, a glass compounds signal other collect , washing strongly compounds which emitted of tubes right) male (after males, Chemistry emitted Hamburg, fitted is the and Ips synergistic mating was to from a as typogra- volatiles we a the beetles closely to pher- larger chal- 2008 bark had and tree the a Published on 28 July 2008. Downloaded by RUTGERS STATE UNIVERSITY on 03/04/2018 18:28:06. repeated and l pheromone male, other the This Fig. not wood. typographus recombinations to Fig. phus plastic It bark perform arrows. 20 directly 23 journal is has with volatiles The an flask beetle A fractionations High evolved one collage interesting components, Most Pityogenes is related uses baited Fig. successive male resolution ‘‘
c in typographus The of of such the two 21 of, and the with fractions to left: Royal forest products oxidation/detoxification Male and question a volatile three sequestered acting chalcographus capillary highly specific the damage gas recombinations, ’’!; Society milieu, Pityogenes sex females; centre: in and materials, chromatographic pheromone. as strong to gas behavioural whereas of to the wood right: mating chromatograms Chemistry why chalcographus components inside synergy, signal, all bark substances. followed the Pityogenes the chambers, of large very beetles the bark, were closely testing. 2008 fractionations, by different peaks, . are identified of caught made behavioural related chalcogra an probably caused from are extract by from in oo and mono- as the Ips the a by ‘‘chalcogran’’ 2 - (body testing. butyrates. Major bark above) We 6. idae) to comprehensive Hylobius pheromones Tomicus pine because seven amounts a Diprionid Fig. washing) sesquiterpenes four-year Some It Other 8 have carbon 22 is Specificity beetles geranyl sawflies and compounds groups. worth in Molecular further of abietis forest analysed of of piniperda Andrena an sawflies atoms, European a (Scolytidae) the highly of isomer and/or single noting from review This . six studies insects challenge formulas of 91 / (Hymenoptera, in the the Melitta of Pityogenes species Chem. specific quite and ( Agriotes that multi-chiral study E methyl collaborative tree by female , E on studied are )-farnesyl Francke similar ( T. Tolasch Commun., of Picea the and of of has decadienoate, referred compounds—and the chalcographus brevis minor sex click the role abies Nomada two include since to attractant family and et esters chemical research , what of sex were beetles sex ). to 2008, al Identifications and volatile Dettner. been . in pheromone pheromones found see we (see Diprionidae) geranyl of pine one male. 3959–3979 the ( fatty molecular found project Agriotes, in continued analyses—small Fig. section compounds shoot 90 the ten as The pine and acids compounds. 6a female earlier are biological species involving two 34 formulas farnesyl above). beetles, done Elater- weevil, during | with of of active 3969 both (see the sex by of in 2 Published on 28 July 2008. Downloaded by RUTGERS STATE UNIVERSITY on 03/04/2018 18:28:06. of amounts 3970 branched Fig. activity, dual active present monitoring pounds cies, We attractivity. structural methyl are the tory male isomers!—give baited central chemistry isomers, The The non-active insect, four have 24 Microdiprion female. and | antenna, pheromone, with female pine Chem. and branched are structural Sex secondary in of including chiral found colleagues in analogue, which high southern sawfly acetate the sawflies active pheromones It Commun., the produces volatile strong is pheromone and centres stereochemical that secondary an acts alcohols. field. pallipes outbreaks. compounds which variations or potential have Europe, analytical full have Fig. specific as compounds. electrophysiological propanoate primarily and 2008, In of an behavioural occurs occasional 24 synthesized and (as Diprionid alcohols Neodiprion inhibitor consequently which stereoisomers—and second on practical 3959–3979 challenge in and Macrodiprion purity, in the an a 92–104 esters 1 can interfering theme. (the alcohol ng case outbreaks, from sawflies: (antagonist) reaction. all for be sertifer quantities application The of because precursors), the of monitored tests response 16 above, the The the precursor nemoralis pheromones possible esters possible large straight in Our we bark especially active of in the decreasing per present the of from two amounts found such by Fig. organic labora- beetle). stereo- , indivi- methyl of chiral chain small traps com- there spe- the the 24. re- as in in a Diprion active tion released have is In Larch (A monarch there possible insects. (Diprionidae) chemistry contorta the visual Fig. chemical esting phenomenon, ver) studied Many 7. So w found be Germany). with theoretical and ‘‘notice’’ pini arrested the adult. As We devices damaging Larvae Pine discharge larch understood but contorta store Covered colonial We The The There the stereospecific. and the many or germacradienol have larvae 24), to indirect of Larval sawfly preliminary much selectively, sawfly are deterrent. centra sawfly In extreme carried larch insects that larval pine pheromones Neodiprion the including B of the pini sawfly isomers, when together is needles there insect ( isomerism. so-called female 16 R studied as of agent, by a by and the caterpillars points active This , Chrysonotomyia develop kairomonal larvae of sawfly females S sawflies good larvae compared the regurgitate, possibilities. larvae producing defences. )-5-germacradien-4-ol. defence: patents. spend perceiving by Keeling are out true pine the egg case another, sex it journal The is larvae from as and results indicating They insects chemicals with might esters Anderbrant of review three defensive selectively sertifer a deposition pest chemistry sex and it pheromones for are of sawfly which In a larvae there. chromatograms view. present study in is Commercial the 108 large short have is achieving four pheromones et to and foraging insects interesting many stereochemical monarch the takes pine be animportant effects four P. deposit the of
Fig. c . C host For This al. showed This wesmaeli The Neodiprion one of to two species The the pupa, of also part secretions ruforum major chain and 106 enriched isomers. in 105 sawflies, and and place 25c, avoid different the the two (gives it trees pheromone Royal species, tritrophic seems the on Hilker their larvae found on and D). of is species caterpillars. 109 respond species product: biology simpler emission may acids. that both sex often other at leaves, , their really Pinus detection egg complex Its Fig. in Society (the is advantage one in eggs the pheromones to centra sertifer of with solitary, precursor Fig. that serve plants Pristiphora use from and larch function part the specificity Evidently, parasitoids. the we lives 25a–c, egg Gilpinia effect focusing be moment pine structures by silvestris represent needles, differing Chalcoprax biology of on 26A–D plants four of larval of many have of coworkers as larva activating quite producing the parasitoid) and blend in specific Chemistry sequester, and sawflies volatiles sawfly the turned an Fig. for 26A–D. chiral larval alcohols applied is studied disruption. regurgitate are species of that wood, additional of on by protective protective erichsonii and show a esterifica- herbivore the from not 107 an with 27. from sawflies release. Diprion general able (BASF, stereo- plants, larvae, semio- centra out direct form, is inter- Pinus recei- They Both from eight have 2008 fully and that two and was and (see etc are the the we P. to to , . Fig. 25 (a)–(c). Pine sawfly larvae (N. sertifer) feeding on needles of P. contorta. In (a) they are calmly eating; in (b) they react with a behaviour called ‘‘snap-bending’’ in response to a disturbance. Repellant chemicals are emitted concurrently. A major component is the germacradienol. (c) A cartoon showing secretion of the larval regurgitate.

exhibit a ‘‘snap bending’’ when disturbed, and this behaviour one, often referred to as an arms race. The plant often seems linked to the emission of species-specific odours. produces defensive compounds and the insect develops detox- Chemical analyses showed that the two species give off ification mechanisms to deal with them. partly related (five of them are monofunctional monoterpenes) but clearly different volatiles, three major compounds in each species, Fig. 28.110 8. Chemical communication and flowering plants: pollination attractants/stimulants Monarch caterpillars Flowering plants produce and give off a multitude of volatile compounds. It is generally thought that this emission primar- The Monarch butterfly (Danaus plexippus) caterpillar gives off ily acted as defence and secondarily, during the evolutionary highly volatile compounds when threatened. Major com- pounds are 3-hydroxy-2-butanone, which is not given off by adults, and Z-3-hexenol which is present in the food plants Asclepias curassavica and A. syriaca. The discharge of these compounds accompanies violent paroxysms elicited by pre- dators.111 Low-flying aircraft (such as Hawker Harrier jets, which we experienced in the greenhouses of the late Dame Dr Miriam Rothschild at Ashton Wold, Peterborough, UK) can also elicit this behaviour. It was quite alarming even to us human bystanders! The chemical relationship between plants, used for egg- laying and subsequent foraging, and insects is an intricate Published on 28 July 2008. Downloaded by RUTGERS STATE UNIVERSITY 03/04/2018 18:28:06.

Fig. 27 Behaviour pictures of Pristiphora larvae. Upper left: P. Fig. 26 (A)–(D). Gas chromatograms of extracts containing 1,6- erichsonii, calmly eating; upper right: alarm position – snap bending; germacradien-5-ol. (A) LC fraction 6 of extracted N. sertifer pupae; lower left: P. wesmaeli, single individual calmly eating; lower right: (B) N. sertifer larval regurgitate; (C) LC fraction 6 of P. contorta alarm position. Reproduced from: S. Jonsson, G. Bergstrom,¨ B. S. needle extract; (D) recombined LC fractions 1–10 of the P. contorta Lanne and U. Stensdotter, J. Chem. Ecol., 1988, 14, 714, with kind needle extract. permission of Springer Science and Business Media.

This journal is
c The Royal Society of Chemistry 2008 Chem. Commun., 2008, 3959–3979 | 3971 Published on 28 July 2008. Downloaded by RUTGERS STATE UNIVERSITY on 03/04/2018 18:28:06. We Actaea volatiles. Rosa pollen, routes. mevalogenic chemical compounds, One instance flower chemical flowering biosynthetic are cularly 3972 flower process, reward blend has specialized phological Fig. Fig. have often made can 28 | rugosa, of 29 can Chem. Here parts. and in in aldehydes, volatiles, Fig. say Volatile found profiles for stimuli, intricately the plants many the Rosa be on organisation. Rosa that are pathways: which (isoprenoids) 31, Fig. Commun., form attracting optimalized We insect. one that rugosa a compounds 32 species, the attract were few which and 29, noted ketones of major are and besides insect adapted 114,115 examples nectar The exposing also often—but the different 38. 2008, are and pollinators, produces this This type to and has flower shown given acetogenic and This with the produced and/or accommodate guide for the 3959–3979 first made of also is of flower esters), off from is fatty the anthers, results by scent especially pollinator. not a and by pollinators in pollen. the the mutual the pollinator through especially (fatty larvae parts those acid Actaea always—offer emits aromatic simple is flower pollen from which usually The derivatives the sepals of acid emitted interdependence. true In . specific studies the 112,113 the and monoterpenes by carry volatiles insect, flower in this insects. derivatives), (benzenoid) three for two and a visual their the pollen. by complex case Distinct of volatile them species. flowers organs see petals, (parti- flower major other plant from mor- The and the for a small are pollen. Fig. (geranyl tween edly methyl relation morphology this deception. by of plant. insects. few pubescens one In Cypripedium pollinating (defensive) These acetate; pollen, is the extreme benzenoids, Fig. times In Ranunculus trapped certain Ranunculus the three characteristic fact flower components. 32. of 30 different discerned lactone It the compounds scent which the Protoanemonin They eugenol), cis chemical that to Compounds acetate) is , species bee - The three Fig. inside a is insects. b compounds, This different and three respectively. and - of protective and specialized many represent attaches from genera 5-methylene-2(5 flowers acris the 31. journal some as variants and the pollen major disparity by It of trans Fig. species) flower, Each , animals, that may 117 may bee identified the to labellum, other a Cypripedium do to is fatty - device. few 30, Fig. b act is 116 and to volatiles. of classes
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cytological for three stimulated. c keep – as Lupinus and serve of Zygogynum front The were and pollinator or , the including and the primitive pollen other this an occurring the species as Royal produces to thorax. scents pollen, , aimed the remains potent direct ancient a pubescens and flower insects such polyphyllus can study old large calceolus point studies, Society and insects attractants/stimulants. (also Right: serve short at limonene (one the Sabatinca and be plant–pollinator as herbivore in and investigating whole-flower in and amount in was of to , insect comprehended ethyl with in called New of (lady’s the as genus Papaver behave Whole view, esters, it be . primitive L. carried emits 118 Chemistry can mating studied. flowers drastically so and polyphyllus Caledonia) moths, distinguish of the forms) In slipper). flower. deterrents. as of now of as characteristic 2-heptadecanone to methylpropyl rhoeas out Winteraceae) the full the volatiles primitive if sites pollination for pass 2008 be were intoxicated systems, Observe of different functional for role Flower from first some firmly and , the pronounced Cypripedium in Filipendula the pollen In studied. of pollinia. was one, relation- food, the Winter- the the time volatile with emitted pollen estab- where strat- scent acet- rela- ‘‘windows’’ very bio- first and and and the 119 Andrena by as is : flowers. Fig. ing which tants, The New Eupomatia haemorrhoa on In beetles the 34 short another Caledonia). Fig. may sides Two 36. chain, (a have (genus female of study major magnoliid Plant–pollinator the 120 their chiral labellum, stuck Elleschodes Fig. chiral components Eupomatia Chem. entire 33 inside esters genus esters which Commun., Ranunculus life the , with serve are of systems were Coleoptera cycle are labellum. the pollinated not just as found 2008, linked volatile acris damage species-specific where two species, Centre: . to 3959–3979 Curculionidae) to emission by these floral attract but the Bee guides host structures studied creeps pollinat- from weevils, attrac- | for plant. 3973 out the the of in Published on 28 July 2008. Downloaded by RUTGERS STATE UNIVERSITY on 03/04/2018 18:28:06. Exospermum tors pollinated analyses potent bouquets. three 3974 tion serve Fig. evolution The Fig. are evolved 35 Fig. | major as hypothesis Chem. herbivore 37 usually pollinator Volatiles of 36 in The cycad species. classes the (a) scents Chiral Commun., from compound Ophrys gymnospermous highly deterrents. (Cycadales) that identified of brood esters, from herbivore volatile speculum specific early 2008, acting cones classes substrate from chemical The compounds 3959–3979 deterrents species. (left), mutualisms. as and cycads, found attractant flowers results (b) through flowers 121 attractants Ophrys in and was suggest In made of the in in ovule the Eupomatia Zygogynum of cycads insectifera augmented the up four for flowers, convergent magnoliid the consump- are pollina- insect- odour . with also and by all Argogorytes insects, family. another The a pollination few known. ope, iterranean Orchids different cies—the and bees together viz. sex flower Fig. several nication insects. angiosperms, Sesquiterpenes, Potential The Chemical For highly in attractants 38 pollination bee tactile and have male Cypripedium general examples but These including Ophrys groups They Tentative with of system. genus attractants or developed taxonomy sphecid (centre), region are one the This strategy stimuli, analyses wasp their of are specializations reviews of attracted genus of of (see of journal species 124–130 with show visiting/pollinating the structures the Ophrys and visited and the wasps, corresponding . the species, which The are below) Fig. is system varying chemical Ophrys olfactory of a of (c) pollinators with is most complicated—is case and fatty by same plant
flower Ophrys c only orchids 37a, which calls of The some volatile of a for of , for acid specialized vis-a ring sesquiterpene distributed phenomenon volatiles, by signalling. pollinator-attraction highly Royal b, for cues the tenthredinifera volatiles some alcohols, do attracting ´ derivatives species in -vis males insects. structures, and a compounds species-rich combination not Society highly that the specialized species c. see pollinated of ways obtain have northwards mainly are pollinators hydrocarbons Each attract certain refs. occurs and of adapted and with characteristic Fig. of Chemistry of been which 122 food Ophrys Orchidaceae exciting isoprenoids. in pollinators. visitors. with pollination pollinating assortative 38, in only species by the and made commu- Ophrys call in on have deceit, mimic which, visual Med- by Eur- 2008 123. spe- the the for for of in a a , Published on 28 July 2008. Downloaded by RUTGERS STATE UNIVERSITY on 03/04/2018 18:28:06. disruption, toxic constructive, of cially between they chemical importance evolutionary environment, with ecological origin ious exocrine heritance, plines. Chemical minimal upon’’ viour-guiding cal This Molecular diversification For Conclusion sphecodes visiting distribution methods, tic and cular quiterpenes acid straight-chain continued electrophysiological Kullenberg, and compounds cunicularius available males sesquiterpenes 7. 6. 5. 3. 2. 1. 4. Herein Studies scientific in interactions many journal biological All Chemical It vital Chemical Practical The some Chemical excitation. derivatives, are and and on of approaching Several though; is the living pattern. chemical the chemistry life. a changes communication truly techniques systems needs. in we the or years precise, group relationships by Ecology by general Biology, prerequisite is signal, or may for relationship in developments Uppsala earlier which species an learning,
steps summarize which and colleagues, c organismic hydrocarbons population colleagues olfactory organisms application of knowledge signals in of signals different interdisciplinary, communication The however, systematics there studied 131–135 ‘‘anastrophe’’, be These them the including This science consist in signals selective statements: through outlook can Royal active and days. were is studies complex can and Biological and females has chemical can for or very represent one led and that are 136 be studies species in be signals genus biology, (possibly who the thinking. 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Chemistry and behaviours O. found evolutionary Thus, disciplines signal, example the understanding of taxonomic or matches carried fusca means only also receiver We designations that joins organisms first thereof. in direct out. something O. monitoring, technique highly via they and it that exception) way Still, chemical to receiver, adds did proliferation group. important exaltata is In 2008 focuses process—by some They together tests on through the of interconnected the out for truly contact. linked the which Biochemistry. and the on have have it not quanta— subjects some levels, potent to the pollinating interfacing 137 was and pollinator were cyclic attraction the in by evolution new synergis- subdisci- chemical of / was find such ‘‘agreed Colletes and ecology also employ on Ophrys to mating a chemi- micro- in which short, mole- beha- Bertil some espe- these fatty non- later var- and and and ses- not the the the the i.e. in- an as produce crimination towards modalities: like vironment, transduction coordination by signal assist pathways. functional molecular along component signals, to on isms produced number between a pounds. be cum Neuroptera, acids by sex separate assortment plants common. described can quite co-evolution which predominantly viours and article important members insects (all phenomena. stepwise 11. 10. An 9. 3. 8. 2. 4. The 1. polymerization specific) have a a are be the pheromones chemical Dual Chemical Sex The and the Living Species is a theme, series Possible A attempt in a is should there (orchids) involved, examples referred produce common hymenopteran a e.g. sencilla of repetitive a made components. sequence sensitive evolved The volatile chemical the good pheromones early of volatile functions for parameters by It theory functional pollinators species group as even based inside visual, (in are of species which a organisms between release has quite with (to specificity give ecology discovery the one well mimetism to possible example of combinations homologous produced Mezozoicum) to statements of the complex and several, which phenomenon more substances given a define their of first been of and (we signal some on as together signals of memory. flight a and insects. or as clear was coded Chem. in olfactory acoustic chemical genus. insects of specific protective adaptation. these biochemical guiding combinations like found and them In are more insects) musk distinct. in time meaningful should cyclization, specificity in by known idea signals. and more often of route in in in usually this blends when antlions. and evolved about, chain the the Commun., there the electrical bees. different can sympatric archaic in with male for and bees. series. of all in of relate with way and volatile signals. economy behaviour. represent bulb), the common specifically in emitted eight arrangements have insects, by what two one the some the disguise. in length, be has Likewise, of In flowering Nature, consists the In a The volatile bumblebees. marking through specificity events often signals information tactile the The these respectively, 38 chemicals bees, Bees used characteristic of three compares of a been, previous parts species special signal), chemical and 2008, chemicals 139 time, 28–31 group Scandinavian dual speciation from compounds the relatively relationships of double in another two-component represent bumblebees and facts Chemical often involving to perception depict of chemical from Nature. major of over stimuli, the the plants. species function may see a males 3959–3979 special structures of form (they of is few conduction, the combination bumblebees which sections communication and late species-specific reception section bond visual, achieved related time, and In about receptor other of the also clear simple body. biosynthetic components founded were It a Mimicry proportion makes an o the conditions Palaeozoi- signals mimetism, belong and reception, deposited expressed glands species the following are -hydroxy variation points position, and so a be between sensory when case the outline 8. of organ- strong | multi- found which These beha- often as com- quite for CNS cells, male 3975 of ants dis- this this en- are are on to of of to to to of is it a a chemical variation. Small chemical differences give species needed. Computer search algorithms of reference material specificity, based on the high discriminatory power of the (like stored mass spectra) can be further facilitated. olfactory receptors. Various genetic techniques and methods will certainly sweep 5. Bark beetle pheromones. The insect order Coleoptera is into this field and this is likely to have a major impact to add to the most numerous and widespread order. Defence com- our understanding of chemical communication, for instance of pounds have been studied previously and Coleoptera includes the evolutionary processes. There is clearly room for more and many species like bark beetles, which are important tree in depth studies of the ecological importance and implications destructors, and therefore of considerable economic impor- of chemical communication. Further studies in synthetic or- tance. We found the bark beetle behavioural ecology most ganic chemistry will likely give us access to more precise interesting, especially the distinct differences between the two chemicals, such as stereochemically pure, chiral compounds, species we studied in depth. Their species-specific sex phero- their role in pheromone science recently reviewed by Mori.141 mones are the products of the acetogenic and the mevalogenic More studies of the biosynthesis of behaviour-releasing com- pathways. Again, their signals are made up by two compo- pounds may be facilitated by the drastic improvments in nents each. genetic methodology. Regarding the study of receptor func- 6. Sex pheromones of pine sawflies. Sawflies also belong in tions, it is expected to give major advances in our under- the order Hymenoptera, but are clearly different from bees and standing of the biochemistry of the olfactory process, as well ants. They have a pronounced sexual dimorphism in the as the central nervous level, including the links to memory and female sex pheromone and the highly sensitive receptors behaviour. located on the large, featherlike antenna of the male. Also Further studies on various aspects of chemical communica- here the species-specific sex pheromones represent variations tion in the types of insects and plants which are described in on biochemical themes, and here their stereochemistry plays a this article have been performed in later years by several fundamental role, giving up to 16 stereoisomers in two of the groups. Work on behaviour-guiding olfactory signals in bees, species studied. bumblebees and flowering plants is among them. Examples are 7. Defence compounds of larvae. The three groups of larvae the enzyme genetic analyses by Pamilo et al. on the Bombus studied were found to have semiochemicals combined with lucorum complex143 and the study by Bertsch142 on the scent specific defensive behaviours. This serves to deter potential specificity in B. cryptarum and B. lucorum. Bumblebee inqui- predators. The volatile compounds are aposematic (serving to linism (an inquiline is an animal that lives as a visitor in the warn) signals for toxic compounds in the larvae. nest, burrow, or dwelling place of an animal of another 8. Volatiles of flowering plants. Most flowering plants have species) in B. sylvestris and the possible role of mimicking a special scent, and their scents differ characteristically, prob- volatiles were investigated by Dronnet et al.144 Savolainen and ably as a result of co-evolution among plants and visiting Vepsalainen¨ ¨ 146 discussed the possibility of sympatric specia- insects. One can observe products of all the three major tion through intraspecific social parasitism by a mitochondrial biosynthetic routes, often in combination, and often with a DNA phylogenetic analysis in three inquiline Myrmica ant rich bouquet of volatiles. The visual, tactile and chemical species. Luxova et al.145 determined the absolute configuration signals from the flowers combine to give either a more general- of some chiral terpenes, which act as marking pheromones in istic or a more specific relationship to visiting insects. bumblebees. An important study of intra- and interspecific

Published on 28 July 2008. Downloaded by RUTGERS STATE UNIVERSITY 03/04/2018 18:28:06. The three major ways of using pheromones for control variability in the labial gland secretion of male B. ruderarius purposes are monitoring (surveillance by pheromone-baited and B. sylvarum has been reported by Terzo et al.147 Very good traps), trap catches (for population decrease) and mating sources of further information on these phenomena are on the disruption (permeating the atmosphere with synthetic phero- one hand original articles, especially in the two dedicated mone). All three are being used in agriculture and in forestry publications: The Journal of Chemical Ecology and as a positive alternative to non-specific, destructive methods Chemoecology, on the other hand The Proceedings of which may be toxic. For example, the use of mating disruption Annual Meetings of ISCE. 148–150 Examples from ref. 149 in forestry, for the gypsy moth, has been used over areas of are Ayasse et al. who identified, synthesized and bioassayed altogether 230 000 ha; control of the grapevine and grapeberry 16 compounds from cuticle extracts of B. terrestris queens. moths in Europe together over 105 000 ha; for the pink boll- The compounds were found to have an effect as primer worm, which is a pest on cotton, over 50 000 ha; for the pheromone, inhibiting the ovarian development of the codling moth, the oriental fruit moth and leafroller moths workers. They also function as a recognition signal of the (fruit pests), together over 238 000 ha worldwide.140 There is queen. The Prague group reported (posters) age-dependent definitely room for a wider use of all three methods based on changes in exocrine glands of B. terrestris queens, and changes selective pheromones to control pests. over time in compounds from the labial gland secretion of What then for the future? New analytical techniques are B. lucorum. likely to appear, both for the chemical and biological sides, Much interest is today focused on the chemical arms race and combined instrumentation with higher sensitivity and the between food plants and insects. Jasmonic and salicylic acids capacity to provide more information. Through miniaturiza- are important for defensive responses of plants to attack by tion, some of these analytical means will be of much lighter herbivores and pathogens, both in chewing and non-chewing weight and functionable directly in the field, which is already insects. The compounds are often found in high concentra- developing to some extent. Further improved techniques for tions in eggs, which can be attacked by parasites. Induced studying behaviour both in the laboratory and in the field are defence is being studied, often as a part of tritrophic

3976 | Chem. Commun., 2008, 3959–3979 This journal is
c The Royal Society of Chemistry 2008 interactions. These types of studies represent an actual trend, 10 G. Bergstrom,¨ M. Appelgren, A.-K. Borg-Karlson, I. Groth, St. which is likely increasing. Stromberg¨ and Si. Stromberg,¨ Chem. Scr., 1980, 16, 173–180. 11 A.-B. Wassgren and G. Bergstrom,¨ J. High Resolut. Chromatogr. For use in the field one can hope for a wider acceptance and Chromatogr. Commun., 1984, 7, 154–155. use of control methods based on additional knowledge about 12 A.-B. Wassgren and G. Bergstrom,¨ J. Chem. Ecol., 1984, 10, chemical signals. In the field of medicine these methods have 1543–1550. not yet had a major breakthrough. Biological colleagues blame 13 B. S. Lanne, M. Appelgren, G. Bergstrom¨ and C. Lofstedt,¨ Anal. Chem., 1985, 57, 1621–1625. this to some degree on the basic fact that flies and mosquitos, 14 J. Bergstrom¨ and G. Bergstrom,¨ J. High Resolut. Chromatogr. which belong to the insect order of Diptera (two-wings), Chromatogr. Commun., 1985, 11, 144–145. notoriously appear in dense groups of both males and females, 15 G. Bergstrom¨ and C. Lagercrantz, Acta Chem. Scand., 1964, 18, where it is difficult to penetrate with synthetic chemical signals, 560–561. 16 L. Ahlquist, G. Bergstrom¨ and C. Liljenberg, Prog. Chem. Fats although they definitely exist and are known to some extent. Other Lipids, 1978, 16, 231–255. Some of the major medical pests call for new methods of 17 A. Johansson, T. Olsson and G. Bergstrom,¨ Tetrahedron Lett., attack. Genetic manipulation of vector populations has had 1996, 37, 7127–7128. 18 A.-B. Wassgren and G. Bergstrom,¨ J. Chem. Ecol., 1995, 21, some success, and attempts at control with juvenile hormones 987–994. have also been made. 19 E. Sondheimer and J. B. Simeone, Chemical Ecology, Academic Some groups of living organisms have not yet been studied Press, New York, 1970. to a large extent. There is much room for more studies of 20 W. J. Bell and R. T. Carde,´ Chemical Ecology of Insects, Chap- man and Hall, New York, 1984 resp. 1995, vol. 1 and 2. mammalian behaviour—including that of Man—in relation- 21 Chemical Ecology, The Chemistry of Biotic Interaction, ed. T. ship to exocrine chemical signals. Aquatic/marine organisms Eisner and J. Meinwald, National Academy Press, Washington represent a world quite unknown to us as to the use of DC, 1995. 22 J. B. Harborne, Introduction to Ecological Biochemistry, Aca- behavioural chemical signals. The same is certainly true for demic Press, London, 4th edn, 1997. microorganisms. One can hope that substantial biological and 23 Insect Olfaction, ed. B. S. Hansson, Springer, Berlin, 1999. chemical research will be directed to these large and important 24 The Chemistry of Pheromones and Other Semiochemicals, I, ed. S. groups of organisms. It will give us new fundamental knowl- Schulz, Topics in Current Chemistry, 239, Springer-Verlag, Hei- delberg, 2004The Chemistry of Pheromones and Other Semiochem- edge necessary to expand our understanding of the world we icals, II, ed. S. Schulz, Topics in Current Chemistry, 240, inhabit. Springer-Verlag, Heidelberg, 2005. 25 Chemical Ecology—From Gene to Ecosystem, ed. M. Dicke and W. Takken, Wageningen UR Frontis Series, vol. 16, Springer, Acknowledgements Dordrecht, 2006. 26 E. S. Albone, Mammalian Semiochemistry, Wiley, Chichester, The collaboration of all colleagues who have contributed to 1984. the basic findings presented in this article is gratefully and 27 Allelochemicals: Role in Agriculture and Forestry, ed. G. R. Waller, ACS Symp. Ser., 330, American Chemical Society, Wa- collectively acknowledged, in addition to the financial support shington DC, 1987. from Foundations and Research Councils. 28 G. Bergstrom¨ and J. Tengo¨, Chem. Scr., 1974, 5, 28–38. I specifically would like to thank the following colleagues 29 J. Tengo¨ and G. Bergstrom,¨ J. Chem. Ecol., 1975, l, 253–268. for use of photographs (numbers of figures in parentheses): 30 J. Tengo¨ and G. Bergstrom,¨ J. Chem. Ecol., 1976, 2, 57–65. 31 J. Tengo¨ and G. Bergstrom,¨ Science, 1977, 196, 1117–1119. Anders Nilsson (3, 31), Bertil Kullenberg (9, 37), Peter Berg- 32 J. Tengo¨ and G. Bergstrom,¨ Comp. Biochem. Physiol., B: Bio- Published on 28 July 2008. Downloaded by RUTGERS STATE UNIVERSITY 03/04/2018 18:28:06. man (10), Inga Thomasson (14), Jan Lofqvist/Rolf¨ Elofsson chem. Mol. Biol., 1976, 55, 179–188. (1, resp. 16), Andreas Yasseri (15), Goran¨ Birgersson (18, 20, 33 J. Tengo¨ and G. Bergstrom,¨ Comp. Biochem. Physiol., B: Bio- 21), Sten Jonsson (25), Heidi Dobson (29) and Sven-Olof chem. Mol. Biol., 1977, 57, 197–202. 34 W. Francke, W. Reith, G. Bergstrom¨ and J. Tengo,¨ Naturwis- Strandhede (33). senschaften, 1980, 67, 149. 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