Jump to content

Insect pheromones

Edit links
From Wikipedia, the free encyclopedia
500,000 scent glands of the female silkmoth (Bombyx mori) were needed to elucidate the molecular structure of bombycol.[1]
Structural formula ofbombycol,the first clearly chemically identified insect pheromone

Insect pheromonesareneurotransmittersthat serve the chemical communication between individuals of an insectspecies.They thus differ fromkairomones,in other words, neurotransmitters that transmit information to non-species organisms. Insects produce pheromones in specialglandsand release them into the environment. In the pheromone receptors of the sensory cells of the recipient, they produce a nervestimuluseven in very low concentrations, which ultimately leads to a behavioral response.Intraspecificcommunication of insects via these substances takes place in a variety of ways and serves, among other things, to find sexual partner, to maintain harmony in acolonyofsocially living insects,to mark territories or to find nest sites and food sources.

In 1959, the German biochemist and Nobel Prize winner Adolf Butenandt identified and synthesized theunsaturatedfatty alcoholbombycol, the sex pheromone of thedomestic silk moth(Bombyx mori), as the first known insect pheromone. The sex pheromones of femalebutterfliesare mostly mono- or bis-olefinicfatty acidsor theiresters,fatty alcohols, their esters or the correspondingaldehydes.Male butterflies use a wide range of chemicals as sex pheromones, for examplepyrrolizidine alkaloids,terpenesandaromatic compoundssuch asbenzaldehyde.

Research into the chemical communication of insects is expanding our understanding of how they locate their food sources or places to lay eggs. For example, beekeepers use an artificially producedNasanov pheromonecontaining terpenes such asgeraniolandcitralto attract bees to an unusedhive.The agriculture and forestry industries use insect pheromones commercially inpest controlusinginsect trapsto prevent egg laying and in practicing themating disruption.It is expected that insect pheromones can also contribute in this way to the control of insect-borne infectious diseases such asmalaria,denguefever orAfrican trypanosomiasis.

Etymology and classification

[edit]

Adolf Butenandt andPeter Karlsonproposed the term pheromones in 1959 for substances that serve intraspecific communication.[2]The definition of the term pheromone was given in the same year by Karlson and the Swiss zoologistMartin Lüscher.According to this, pheromones are

"Substances released externally by one individual that elicit specific responses in another individual of the same species." – Peter Karlson, Martin Lüscher, 1959.[3]

The word pheromone consists of theancient Greekparts of speechφέρειν phérein,überbringen,melden,andὁρμᾶν hormān, antreiben, erregen.[3][4]According to Karlson and Lüscher, the goal was to coin an internationally understandable scientific term for a class of substances based on a clear definition. It was to be a short word that could be spoken in many languages. The ending mone served as asuffix,as it occurs in the wordshormone,kairomone,andallomonethus emphasizing their relationship.[5]The term pheromone replaced the term ectohormone or homoiohormone, which Albrecht Bethe had already proposed in 1932 with the same definition.[6]Bethe's term was not accepted because, according to Butenandt, the terms ecto and hormone were mutually exclusive. The mechanism of action of a pheromone also does not correspond to that of a hormone absorbed into thecirculatory systemby another individual and was therefore considered misleading.

The classification of intraspecific pheromones in the group ofsemiochemicals,in other words,neurotransmittersthat serve communication between organisms, is shown in the following diagram:[7]

Karlson further divided them into thesense of smelland theoral-actinginsect pheromones according to the mode of reception.[8]In 1963,Edward O. Wilson,who had discoveredanttrace pheromones the year before, and William H. Bossert introduced the concepts of releaser and primer pheromones.[9][10]Releaser pheromones, which are usually perceived olfactorily, cause an instantaneously observablebehavioral reaction,whereas primer pheromones, which are often oral, trigger physiological changes in the recipient. Primerpheromones, for example, suppress the formation of ovaries inworker bees.

Often, pheromones are defined according to their behavior-triggering function. In addition to the well-known sex attractants, they act, among other things, asaggregation pheromones,dispersion pheromones, alarm pheromones, tracking pheromones, marker pheromones, brood recognition pheromones, egg-laying pheromones, recruitment pheromones, or as caste recognition agents.

Vincent Dethierdivided insect pheromones into six categories according to their general behavior-triggering effects.[11]These include prisoners, which are normally only perceptible at short distances and cause an insect in motion to stop, and locomotor stimulants, which increase the insect's speed or decrease the number of directional changes.Lockstoffeare attractants that trigger an oriented movement toward the odor source, whereas repellents trigger an escape movement away from it. Feeding and oviposition stimulants, respectively, trigger feeding or oviposition. Deterrents, on the other hand, inhibit feeding or oviposition.

Functionally defined insect pheromones often contain mixtures of different components in precisely defined proportions. These so-called pheromone cocktails often contain substances of different categories with near and far orientation functions. For example, the aggregation pheromone cocktail of theGerman cockroachBlattella germanicacontains both substances that act as attractants and substances that act as arrestants.[12]

In part, insect pheromones are named after the site of their biological production. Males of various moth species, such as the banana butterfly, possess so-called androconial organs in the abdomen that release pheromones. These insect pheromones are appropriately called androconial pheromones.[13]Thequeen beeof theWestern honey beeproduce the queen bee pheromone inmandibular glands.In English, they are therefore often referred to as queen mandibular gland pheromones.[14]

History

[edit]

First discoveries

[edit]
John Ray

In 1609, the EnglishbeekeeperCharles Butlerobserved that the sting of abeereleased a liquid. This liquid attracted other bees, which then began to sting en masse.[15]Butler thus demonstrated for the first time the effect of an alarm pheromone of bees, which was identified asisoamyl acetatein the 1960s.[16]Butler's observation was the first to show the effect of an alarm pheromone of bees, which was identified as isoamyl acetate in the 1960s.

As early as 1690, SirJohn Raysuspected thatpeppered mothsattracted male conspecifics by means of a scent:

"It emerged out of a stick-shaped geometer caterpillar: it was a female and came out from its chrysalis shut up in my cage: the windows were open in the room or closet where it was kept, and two male moths flying round were caught by my wife who by a lucky chance were into the room in the night: they were attracted, as it seems to me, by the scent of the female and came in from outside."

"It developed from a stick-shaped birch moth caterpillar: it was a female, and came out of her chrysalis, which was shut up in my cage: the windows were open in the room or chamber where she was kept, and two male moths flying about were caught by my wife, who by a lucky chance was in the room that night: they were attracted, it seems to me, by the scent of the female, and came in from outside."

– John Ray[17]

Jean-Henri Fabre

The FrenchentomologistJean-Henri Fabrealso reported in the mid-19th century on experiments withSaturniaandoak eggarin which females trapped in wire cages attracted hundreds of males within a few days at specific times.[18]In experiments with taggeddomestic silk moth,40% of males from a distance of four kilometers and 26% of males from eleven kilometers still found their way to a trapped female.[18]The morphology of the moths was also reported in the mid-19th century.

In many insect species, researchers long puzzled over the mechanism of mating: visual or acoustic stimuli could not explain Fabre's experiments, nor how moths found females ready to mate with great certainty. Theories of attraction byinfraredor other radiation were not confirmed.[18]The organization ofeusocialityremained equally inexplicable for a long time. The writer and bee researcherMaurice Maeterlinckspeculated about the spirit of the hive, the (team) Spirit of the hive, without being able to determine its essence in more detail.[19]Theories about the attraction by infrared or radiation also remained unexplained for a long time.

Definitions of Bethe

[edit]

At the beginning of the 20th century,Ernest Starlingdiscoveredhormonesas the first biological neurotransmitters.[20]In 1932, theneurophysiologistAlbrecht Bethe,who at that time headed the Institute ofAnimal Physiologyat theGoethe University Frankfurt,published an article on an expanded hormone concept in which he distinguished between endohormones and ectohormones.[6]According to this, endohormones act in the producing organism itself and correspond to the classical hormone definition. In contrast, the organism releases ectohormones externally and transfers them to other individuals. As an example, Bethe cited the effect of thelactation hormone,which is released by afetusto its mother and causes the growth of themammary glandand subsequently thesecretion of milk.[6]He also proposed this concept for chemical communication among insects.

"In bees, for example, the workers (i.e. not the mothers) are able to raise a sexually capable queen from an egg or a young larva [...] by special food and transfer of secretions of their salivary glands. There can hardly be any doubt (although it has not been proven) that ectohormones of the salivary gland secretions play the main role in this redifferentiation." – Albrecht Bethe[6]

Bethe further divided the ectohormones into homoiohormones, which – according to today's definition of a pheromone – act on individuals of the same species, and alloiohormones, which act on individuals of a different species. He thus coined the precursor term ofallelochemicals.[6]

Works from Butenandt

[edit]

Adolf Butenandt also suspected that communication among insects was based on neurotransmitters, and in the 1940s he began a project to identify the sexual attractant of the domestic silk moth (Bombyx mori). It is a butterfly originally native to China, belonging to thefamilyof theBombycidae,which is used forsericultureand its breeding and keeping was well known. It was only after almost 20 years of work that he finally succeeded inextractingand purifying a substance from more than 500,000 insects, which Butenandt later namedBombykol.

Byelemental analysis,Butenandt determined thechemical formulaof the substance to be C16H30O.Infrared spectroscopicstudies indicated the presence ofconjugated double bonds.Using methods common at the time, such as catalytichydrogenation,melting point determination,and oxidative degradation bypotassium permanganate,Butenandt showed that the substance sought was anunsaturatedfatty alcohol,(10E,12Z)-10,12-Hexadecadien-1-ol.[21]

Butenandt then synthesized bombycol fromvernolic acid[(12R,13S)-Epoxy-9-cis-octadecenoic acid] in several steps via diol formation, its cleavage to thealdehyde,double bond isomerization,andWittig reaction.He synthesized the four possiblestereoisomersand tested them for theirbiological activity.[22]Only one isomer showed the same activity as the extract. Butenandt thus provided evidence that communication among insects takes place on a substance-by-substance basis.

"By extraction and condensation experiments, however, it has been convincingly shown that a material principle must be present which is secreted by the female butterflies from scent organs of the last abdominal segments and perceived by the males with their antennae." – Adolf Butenandt[23]

Primer and releaser pheromones

[edit]
E. O. Wilson

Towards the end of the 1950s,Edward O. Wilsondefined substances that trigger the alarm and burrowing behavior of ants as chemical releaser.[24]In 1961, the BritishbiochemistRobert Kenneth Callowidentified another pheromone, also known as the queen bee pheromone, with the compound(E)-9-oxo-dec-2-enoic acid,or9-ODAfor short.[25]The effect of this pheromone was obviously of a different nature than that of the alarm pheromones, since it had a long-term effect on thephysiologyof the recipients.

In 1963, Wilson, who the year before had already discovered the trace pheromones of ants, and William H. Bossert introduced the term releaser and primer pheromones for this purpose, to distinguish the behavior-controlling effect of, for example, sex attractants from the pheromones that interfere with theendocrine systemof the receiver.[9][10]

Modern research directions

[edit]
Preparation ofHelicoverpa zea

As a result of the enormously refined extraction andanalytical chemistryover the years, chemists and biologists identified numerous other pheromones. For the detection of the second component of the pheromone cocktail ofBombyx mori,the bombycal [(10Z,12E)-hexadecadienal], an extract of 460 glands from which 15nanogramsof the aldehyde were isolated was already sufficient in 1978.[26]

In addition to studying the function and reception of pheromones and their chemical identification, scientists extensively investigated thebiochemistryof pheromone production. In 1984, Ashok Raina and Jerome Klun discovered that the production of the female sex attractant of theowlet mothsHelicoverpa zeais controlled by hormonal substances called pheromone biosynthesis-activating neuropeptides (PBANs) in the brains of female moths.[27]Other modern research focuses on the study of insect pheromone reception by means of the sense of smell and taste, genetic factors, and evolutionary biology issues, such as thecoevolutionof female sex pheromone production and reception in the male.[28]

Combating disease vectors such asAnophelesis another focus of research. According toWorld Health Organizationestimates, the number of malaria infections in 2012 was about 207 million with 627,000 deaths.[29]Culexmosquitoes transmit the causative agent offilariasisorWest Nile virus.Traps equipped with oviposition pheromones offer one way to contain these populations. To optimize these, the scent-binding proteins in the antennae of females, which play a critical role in detecting oviposition sites, are being intensively studied.[30]

Production

[edit]

The pheromones in insects are often the secondary products of fatty acids, such as saturated and unsaturated hydrocarbons, fatty alcohols, esters and aldehydes, but also isoprenoids and other compounds. Pheromones are often not pure substances, but so-called pheromone cocktails consisting of various components. Often, only one specific enantiomer of a compound triggers a behavioral reaction, while the other enantiomer triggers no reaction or a different reaction.

Sometimes the biosynthesis of the pheromone occurs only when the biochemical precursors in the form of certain alkaloids have been ingested from food plants. In this case, the sex pheromone simultaneously signals the presence of food sources.[31]

Due to the potential commercial application in crop protection, the intensity of the study of pheromones increased greatly after Butenandt's discovery, leading to the development of highly sensitive analytical methods[32]and the widespread application of chemo-, regio-, and stereoselective syntheses in organic chemistry.

Biosynthesis

[edit]
Male ofsilver-washed fritillarywith four elongated scent scale patches (scent scale stripes) on each forewing

Insect pheromones are produced by a variety ofexocrine glandsconsisting primarily of modifiedepidermal cellsat various sites on the insect body. For example, the abdominal glands of the female silkmoth release traces of the (E,E)-isomer ofalcoholas well as the analogous (E,Z)-aldehyde bombycal, in addition to the sex pheromone bombycol.[33][34]Suitable surface geometries in the vicinity of the glands, such as grooved pore plates, may favor effective evaporation of a leaked pheromone.[35]Honey bees possess 15 glands with which they produce and release a number of different substances, thus maintaining a complexcommunication systembased on pheromones.[36][37]Males of various butterfly species possess so-called androconial organs in the abdomen with which they can disseminate pheromones, while other moths release them viascent shedor scent bristles on their forewings or the end of the abdomen. The scent bristles and scent scales serve to increase surface area and facilitate the evaporation of insect pheromones.[35]

Rather than evolving a completely unique set ofenzymesfor pheromone biosynthesis, insects often modify normal metabolites into pheromones with high regio-, chemo-, (E/Z)-, diastereo-, or enantioselectivity and in well-defined ratios.[38]Biosynthesis of insect pheromones occurs eitherde novofollowing the scheme offatty acid synthesisby successive addition ofmalonyl-CoAto an initialacetylor by uptake ofprecursorsfrom the diet. Many butterflies use the biosynthetic possibility of producing a specific mixture ofderivativesof simple fatty acids. The evolution of the enzyme Δ-11-desaturasecombined with chain-shortening reactions allows them to produce a variety of unsaturatedacetates,aldehydes, and alcohols in various combinations.[39]

Dehydrogenationof thecarbon chainandreductionof the acid function to the alcohol occurs, if necessary, through special enzyme systems. Further steps can beoxidationto the aldehyde oracetylationto theacetate.[40]InBombyx mori,the biosynthesis is activated diurnally by pheromones through aneurohormone,the so-called pheromone biosynthesis-activating neuropeptide (PBAN).[40]The pheromone biosynthesis-activating neuropeptide (PBAN) is a neurohormone.

The hormonal mechanisms of pheromone production vary considerably from species to species.[41]Juvenile hormones,for example, control pheromone production in the owl butterflyMythimna unipuncta.These are produced in mostly pairedcorpora allatalocated behind the brain and released into thehemolymph.There they bind to certain transport proteins. If the corpora allata are removed, the females do not produce pheromones. Juvenile hormones, however, interfere more indirectly with thecircadianrelease of PBAN.[42]

Male butterflies of theDanainaefamily sometimes wound caterpillars that have ingested alkaloids frommilk weedswith tiny claws on their feet to ingest the exuding fluid, a behavior described as kleptopharmacophagy. The moths use the ingested alkaloids for defense against predators and to produce sex pheromones.[43]

Pheromones from plant ingredients

[edit]
Retronecine,from which manypyrrolizidine alkaloidsare derived by esterification of the twohydroxyl groups.

Malefire-coloured beetlesof the speciesNeopyrochroa flabellataand also various other beetle species use theterpenoidcantharidinas a sex pheromone and aphrodisiac pheromone, respectively. Thisisoprenoidis ingested byNeopyrochroa flabellatawith food and transferred to females and subsequently to the brood during the mating act.[44]Females test the content of a gland on the head of the male before mating. The cantharidin acts as a feeding toxin and renders the eggs unpalatable to predators; females therefore prefer males with a high cantharidin content.[47]

Moths such asUtetheisa ornatrixandTirumala limniaceingestpyrrolizidine alkaloidsfrom food plants such ascrotalaria,heliotropium,orAchillea ageratumin thecaterpillar,which the adult male converts by oxidation into pheromones such ashydroxydanaidal.As in the fire beetle, the alkaloids, which are potent feeding poisons and act against predators such asspiders,ants,ornet-winged insects,are transferred to females and eggs.[45]Adultmonarch butterfliesingestplant secondary metabolismto increase their pheromonal attractiveness.[46]Sometimes biosynthesis of the pheromone occurs only when biochemical precursors in the form of certainalkaloidshave been ingested from food plants. In this case, the sex pheromone simultaneously signals the presence of food sources.[47]

The uptake of pheromone precursors from plants is also known for certain species oforchid beesandpeacock flies.Male bees collect a mixture ofterpenoidsfromorchidsand use them as an aggregation pheromone to formlek mating.Sometimes the plant constituents control the development of the pheromone glands of male butterflies.[48]

Laboratory synthesis

[edit]

Karl ZieglerandGünther Otto Schencksucceeded in synthesizing cantharidin as early as 1941.[49][50]The preparation of pheromones requires the use of highlychemo-,regio- andstereoselective syntheses.In the 1970s,asymmetric synthesisusing theSAMPmethod succeeded in producing various pheromones enantiomerically pure.[51]Furthermore, chemists used asymmetricepoxidation,asymmetricdihydroxylation,biocatalysis,olefin metathesis,and many other stereoselective reactions to synthesize pheromones.[52]TheWittig reactionis suitable for thechemical synthesisof pheromones with (Z)-olefinicdouble bonds.[53]

Genetically modified tobacco plants can also produce sex pheromones. The fatty alcohols obtained from them by extraction are subsequentlyacetylatedto obtain the respective target sex pheromones. This semisynthetic route of production produces insect pheromones in relatively large quantities and with high purity.[54]

Properties

[edit]
Chamaesphecia empiformison pheromone dispenser

Chemical communication between living beings by means of pheromones follows the same principles as technicaldata transmission.Atransmitter,for example theglandof a female insect, emits the signal in the form of a chemicalsubstance.Both the chemical structure of themoleculesand their quantity ratio determine theinformation contentand serve as amodel of communicationfor the species. The physical properties of the substances, such asvapor pressure,determine the function of their molecules as short- or long-range information transmitters.[55]

The insect pheromone is transmitted by direct contact or via a medium such as water or air. From thereceiver,for example thepheromone receptorsin theantennaof a male insect, the substance is received and triggers a behavioral response. The term antenna was first used to refer to the antennae of insects and subsequently in engineering.[56]Insect pheromones have a highly species-specific effect, meaning that they elicit the desired behavioral response only inbiological specificitybut not in individuals of other species. For example, although the chemical compounds that act as sex pheromones in butterflies may be the same in different species, the composition of the pheromone cocktail is different in all species.[55]In addition, pheromone cocktails often contain substances that act as behavioral inhibitors for other species, such as significantly reducing the rate of approach of males of alien species to an attracting female.[56]The pheromone cocktail is a highly effective means of inhibiting the behavior of males of other species.

Physico-chemical properties

[edit]

The pheromones are usually produced as a liquid and are either transmitted by direct contact or released into the environment as a liquid orvapor.They can be either heavy orlight volatile.Diffusivity significantly affects the function of the pheromone.[57]Alarm pheromones are often highly volatile to spread quickly bydiffusion.Therefore, they are often short-chain substances with relatively high vapor pressure and low complexity.[40]There is no high requirement for species-specificcodingeffect as in sex pheromones. Sex pheromones have a higher complexity than most alarm pheromones, but a lower molar mass than marker pheromones, which permanently indicate an area.[58]

In the case of flying insects - such as butterflies - the pheromone as a molecule must not be too large, otherwise thevapor pressureand volatility are too low. Thus, over 200 identified sex pheromones of butterfly species are mono- and bis-olefinicfatty aldehydes,fatty alcohols and their acetates with chains of 10 to 18 carbon atoms.[40]

Depending on the function, there are different emission and reception scenarios. Ants, for example, emit alarm pheromones intermittently or continuously in the usually windless environment of the anthill. Trace pheromones are emitted by an ant as a moving source. Silkmoth sex pheromones are emitted in discrete scent threads in an air stream.[57]

Monarch butterfly malewith clearly visible scent scales pockets

Male monarch butterflies do not emit volatile pheromones, but pheromone-ladennanoparticlescalled pheromone transfer particles, which they use to transfer arrestants or aphrodisiac pheromones to females. The pheromone transfer particles position the males on their brush hairs and scatter them during courtship flight. The nanoparticles adhere to the antennae of the females, which are equipped with pheromone receptors, where they slowly release the pheromones, resulting in a long-lasting stimulus for the female.[59]

Females of theArctiinaePyrrharctia isabellaemit anaerosolconsisting exclusively of sex pheromone droplets. The amount of pheromone released in this process is much greater than in other known female moths. The apparent wastefulness of the sex pheromone is explained by the short amount of time an adult has to find a reproductive partner due to the short Arctic spring.[60]

Recipients usually perceive pheromones in an environment characterized by the presence of many other chemicals. To ensure specific perception, the pheromone chemical must either be so complex that it does not occur more than once in nature, or the correct ratio of several individual components must trigger the stimulus. However, it has been shown that only in exceptional cases does a single substance convey the message. Often, amixtureof substances must be present in very precise proportions that, in addition to the chemical structure of the individual pheromones, determine the informational content of the pheromone cocktail.[40]

Periplanon B

The chemical structure of pheromones is directly related to their signaling function andsignaling environment.Pheromones released into the air often have acarbon chainof 5 to 20 atoms and amolar massof about 80 to 300 g-mol-1. With a carbon chain of less than five carbon atoms, the number of possible isomers is small and targeted species-specific coding is difficult.[58]With longer carbon chains, the number of possible isomers increases rapidly.

Periplanon B,the sex pheromone of theAmerican cockroach,is an example of a complex single substance to which males respond at extremely low levels of 10−5nanograms.[61][62]

Biological properties

[edit]
Antenna of aLasiocampidae

The sex pheromone cocktail emitted by a female insect spreads downwind. In the recipient male, the molecules strike the antennae, where reception of the pheromones takes place by means of olfactory cells on the olfactory hairs orsensilla.The antennae adsorb about 30% of the pheromone molecules contained in an airstream.[56]The remaining molecules hit the outerexoskeletonwhere they are enzymatically degraded.

The pheromone molecules first reach thecuticleof the olfactory hairs and diffuse through pores into a pore cone and from there intotubules.From there, the molecules diffuse further to thedendritic membrane.[40]This membrane has receptors that, when a pheromone is received, cause a change in electrical resistance via the opening ofion channels,creating anelectrical resistancethat results in aperception.[40]Even a single pheromone molecule can trigger a nerve impulse.[59] However, the recognition of a specific pheromone cocktail requires a certain level of excitation of differentcell typesof varyingspecificity.[56]It is assumed that the characteristic excitations received from the different receptors in thecentral nervous systemare modulated there into an excitation pattern. If this excitation pattern, which depends on the quantitative ratio of the received pheromone molecules, matches the coding of an innatebehavioral pattern,this leads to the triggering of a corresponding behavioral response, such as the headwind approach to a pheromone source.[55]

Pheromone species

[edit]

According to their effect, two classes of pheromones can be distinguished, the primer and the releaser pheromones. Under certain conditions, certain pheromones act as both releaser and primer pheromones.[63]

Releaserpheromone

[edit]

Releaser pheromones have a brief, immediate behavior-controlling effect. The first pheromone discovered, bombycol, is an example. Releaser pheromones typically include aggregation pheromones, dispersal pheromones, alarm pheromones, tracking pheromones, and marking pheromones, among others, in addition to the well-known sex pheromones.[63]

Aggregation pheromones

[edit]
Aggregation ofPentatomidae

Aggregation pheromones are produced by both sexes and are used for the sex-nonspecific attraction of individuals of the same species. These are known, for example, in thebark beetleand other beetle species,bipeds,hemipteraandgrasshoppers.Insects use aggregation pheromones for defense against predators, inmate choice,and to overcomehost plantresistance to mass attack. A group of individuals at a site is referred to as anaggregation,regardless of sex.[64]Aggregation pheromones, in addition to sex attractants, play a significant role in the development of pheromone traps for selective pest control.[65]

Studies usingelectroantennogram techniquesshowed that aggregation pheromones elicited relatively high receptor potentials in a sex-nonspecific manner, whereas sex pheromones elicited high receptor potentials in only one sex. Aggregation pheromones may therefore be evolutionary precursors of sex pheromones.[35]

Sex pheromones

[edit]
See also:List of insect sex pheromones
Copulatingpoplar hawk moth pair

Sex pheromones signal the female animal's readiness tomating.Male animals also emit pheromones; they contain information about sex andgenotype.Many insects release sex pheromones; some butterfly species still perceive the pheromone at a distance of 10 kilometers. The sensory cell response in the male silkmoth begins at a concentration of about 1000 molecules per cubic centimeter of air.[56]The scent signal of a female, as soon as a certain concentration threshold is exceeded, initially triggers an oriented headwind flight in the silkmoth male.[56]In other species such as thecodling moth,on the other hand, the male tests thestereochemical purityof the attractant molecule. As soon as a small admixture of another stereoisomer is present in the pheromone cocktail, the approach to the source stops.[56]In this case, the other stereoisomer acts as arepellent.[40]In addition to the main components, some species release so-called short-range components in small amounts, which influence the behavioral response.[56]In addition to the main components, some species release so-called short-range components in small amounts.

Fouraginghoney bees spread the scent of (Z)-11-eicosen-1-ol.European bee wolvesare guided by this scent to prey on honey bees. Male bee wolves use this component, and thus the existing sensory preference of females for bee scent, as part of their sex pheromone cocktail to attract them.[66]

Aphrodisiac apheromones

[edit]
Olean- the aphrodisiac apheromone of the olive fruit fly (Bactrocera oleae).

Aphrodisiacpheromones stimulate the readiness to mate. Thespiroacetalolean,for example, is the aphrodisiac pheromone of theolive fruit fly(Bactrocera oleae). Only the (R)enantiomeris effective on males; the (S) enantiomer is ineffective on them. The female produces theracemate,responds to (R)- and (S)-olean, and also stimulates herself with it.[67]

So-called anti-aphrodisiacs have exactly the opposite effect.Bedbugnymphsprotect themselves with such a pheromone, which has a specific mi xing ratio of the aldehydes(E)-2-hexenal,(E)-2-octenaland4-oxo-(E)-2-hexenal,against mating attempts by male bedbugs. The latter directly drills a hole into the abdomen of sexually mature female bedbugs and injects its sperm there (traumatic insemination). For mated nymphs, however, such injury can be fatal.[68]

Alarm pheromones

[edit]

Some insect species emit alarm pheromones when attacked. These trigger either flight or increased aggression. In bees, for example, two alarm pheromone mixtures are known. One is released by the Koshevnikov gland near the sting and contains more than 40 different compounds, such asisoamyl acetate,already described by Butler in its effect, besidesbutyl acetate,1-Hexanol,1-Butanol,1-Octanol,hexyl acetate,octyl acetateand2-Nonanol.These components have lowmolar mass,are volatile, and are the most non-specific of all pheromones. Alarm pheromones are released when a bee stings another animal to attract and entice other bees to attack.Smokesuppresses the effect of alarm pheromones, which is exploited by beekeepers.[69]

The other alarm pheromone of the honey bee contains mainly2-Heptanone,another volatile substance released by the mandibular glands.[70]This component has a repellent effect onpredatoryinsects. The alarm pheromone cocktail of the bedbug contains unsaturated witch and octenaldehydes, which are perceived as a characteristic sweetish odor in bedbug-infested rooms.[71][72]

Marking and dispersion pheromones

[edit]

Certain insects, such as thecherry fruit fly,mark their oviposition sites in such a way that other females of the same species avoid the site and lay their eggs elsewhere to avoid competition for food among the offspring.[73]Territorial social insects, such as colonies of ants, also mark territories they claim with pheromones.[74]

The marking pheromones include the dispersion pheromones, with which, for example, bark beetles prevent overcolonization of a tree.[75]The females and nymphs of the German cockroach transmit dispersion pheromones in direct contact via their saliva. In the nymphal stage, these serve to deter adult cockroaches and thus protect againstcannibalism.In adults, they prevent the translocation of a habitat.[76]

Trace pheromones

[edit]
Fire antsuse track pheromones to mark the path from the colony to feeding sites.

Trace pheromones are mainly known in insects living incolonies,which mark their paths with low-volatile substances such as higher molecular weighthydrocarbons.Ants in particular often mark the path from a food source to the nest in this way.[77]As long as the food source exists, the trail is renewed. When the food source dries up, the ants spray over the trail pheromone with a repellent pheromone.[78]In 1921, the U.S. naturalistCharles William Beebereported on theant millphenomenon, which trace pheromones can trigger inarmy ants:If the animals are separated from the main trail of the colony, the blind ants follow the pheromone trails of ants running in front of them. These run in large circles until complete exhaustion or death, without finding their way back to the colony.[79]

Recruitment pheromones

[edit]

Recruitment pheromones are widely used as an element of chemical communication in social insects and have been demonstrated for bees,termites,and ants. These pheromones are used by insects to stimulate other members of the colony to forage at a food source.[63]Bumblebeesperform a dance similar to thewaggle danceprimarily to distribute recruitment pheromones.[80]

Primerpheromones

[edit]

The orderHymenopteracontains the largest group of eusocial insects, including manybees,especially of the subfamilyApinae,ants, and some species ofvespidae,especially of the subfamily ofVespidaes.Characteristics often include the presence of a reproductive queen andcasteswith specializedworkers beesand soldiers. Termites form the second major group of eusocial insects. Colonies are divided into distinct castes, with a queen and king as reproductive individuals, workers, and soldiers defending the colony.[81]Primer pheromones have a major influence on the organization ofhymenopteran statesformed by Hymenoptera and of termite colonies. These pheromones influence the hormonal system of the recipient; they often interfere withmetabolismvia asignaling cascadeor activate proteins that can bind toDNA.In contrast to the releaser pheromones, the primer pheromones are less well studied. For a long time, only one primer pheromone, 9-ODA, was known.

Primer pheromones of bees

[edit]

A well-known example of primer pheromones are the queen bee pheromones.[82]These pheromones control social behavior, comb maintenance, swarming, and ovary formation of worker bees. The components arecarboxylic acidsandaromatic compounds.(E)-9-oxo-dec-2-enoic acid (9-ODA), for example, suppresses further breeding of queens and inhibits development of ovaries of worker bees. It is also a potent sex pheromone fordronesonnuptial flight.[83]

Brood recognition pheromones are emitted by larvae andpupaeand discourage worker bees from leaving the hive while there are still offspring to be cared for. Furthermore, they suppress the formation of ovaries in worker bees. The pheromones consist of a mixture of tenfatty acid esters,includingglyceryl 1,2-dioleate-3-palmitate.[84]Worker pupae contain 2 to 5, drone pupae about 10 and queen pupae 30microgramsof the pheromone.

Older, fouraging worker bees releaseoleic acid ethyl ester,which inhibits the development of nurse bees and makes them care for brood longer.[85]The oleic acid ester acts as a primer pheromone and stabilizes the ratio of brood-caring and food-producing bees. The foragers produce it fromnectarmixed with traces ofethanol,which they feed to the nurse bees. This delays their development until the number of older foragers decreases and with it theexposureof nurse bees to ethyl oleate.

Caste determinant pheromones

[edit]

TheReticulitermes flavipesusesterpenessuch asγ-cadineneand γ-cadinenal as caste-stimulating or -inhibiting primerpheromones. These assist the juvenile hormone in determining the position oftotipotentworkers in the caste system.[86]In ants, female larvae possessbipotentialityfor some time and thus the possibility of developing as either queens or workers. At some point in larval development, continued feeding determines the fate of the larva. If the juvenile hormone titer is raised above a certain threshold,gynomorphsdevelop; otherwise, workers develop. Control of larval feeding is governed by a primerpheromone of the queen ant.[87]

Application

[edit]

In the 19th century,Lymantria disparescaped from entomologistÉtienne Léopold TrouvelotinMassachusettsand spread throughout the United States by the mid-20th century, becoming one of the most fearedpeststoday. As early as 1898, Edward Forbush and Charles Fernald made attempts to control the population of the gypsy moth by luring males into traps set with attractant females.[88]The United States Department of Agriculturecontinued these attempts in the 1930s, using extracts of female abdominal spikes to attract male moths.[89]The United States Department of Agriculture was the first to use this method. The application of insect pheromones inpest controlhas been intensively studied, especially since the first syntheses, with the aim of developing environmentally friendly methods to controlpopulation dynamics.[90]

Insect trapforbark beetles

In pest control, the use of pheromones inattractanttraps to control insects is common practice. This can involve attracting the insects to kill them with aninsecticideor physically to trap them or formonitoring.Bark beetlesare attracted with aggregation pheromones to trap them. The attractant is usually released when drilling into spruce wood, signaling that the tree can be colonized. The bark beetle trap is an important tool for controlling bark beetles.[91]However, the use of attractant traps poses the problem that the pheromone may act as akairomoneand thus attract predatory insects. By reducing the population of natural predators of the bark beetle, the pheromone trap has a counterproductive effect in this case.[92]Monitoring by means of attractant traps, such aswindow traps,is used for the quantitative detection of pests to control them more specifically with insecticides depending on the activity detected. In addition, they are used in the identification of new species.[93]

Trap beetleswork on the same principle as attractant traps. The bark beetles of the initial infestation attract further conspecifics by aggregation pheromones. Windthrow is suitable as trap beetles, which can be equipped withpheromone dispensersto enhance the attraction effect. Trees prepared in this way divert approaching bark beetles from the stand and bind them to controllable stems. The use of trap trees requires regular inspection of the trees. When larval galleries appear, the trees are debarked and larvae and pupae dry out. If necessary, the infested tree may be treated with insecticides or burned to prevent escape of the next generation.[94]

Egg-laying-preventing marking pheromones are widely used in the insect world. Various experiments have demonstrated the possibility of controlling population dynamics by these pheromones.[95]Application of the oviposition-preventing marking pheromone ofRhagoletis cerasi,which cannot be controlled withyellow boards,for example, reduced infestations of cherries by 90%.[96]

Another application is the confusion method or mating disruption. Here, a high substance concentration of artificially produced pheromones is applied. This makes it impossible for the males to follow the pheromones of the females, thus hindering the reproduction of the pest. The confusion method has a species-specific effect.[97]It is usually successful with respect to one species if sufficient dispensers are applied, but in some cases related species occupy theecological nichethat is released.

Bees use theNasanov pheromoneto guide worker bees back to the hive. The pheromone contains terpenes such asgeraniolandcitral.Beekeepers use a man-made product to attract bees to an unused hive.[98]The process is suitable for trappingAfricanized honey beesin trap boxes.[99]

Toxicology

[edit]

Toxicological studies were mainly carried out in connection with the approval of pheromone traps and dispensers. A health hazard cannot be generally assessed due to the large chemical diversity of pheromones, but is usually excluded because only small amounts are emitted. However, in higher doses, orally administered pheromones such ascantharidincause death in rare cases.[100]

Evidence

[edit]
Recording of anelectroantennogramas a function of scent current concentration.

Commercial application in crop protection intensified the study of pheromones and led to the development of highly sensitiveanalytical methods.[32]The identification of a pheromone proceeds through several steps. First, an extract of the pheromone is obtained. This is done by the method already used by Butenandt of extracting glands or whole animals with an easily evaporatedsolvent,ideally at the time of high pheromone production. Alternatively, the pheromone isadsorbedonactivated carbonfrom the gas phase and an extract is obtained with little solvent.[101]For very small traces,solid-phase microextractionis suitable. For identification, the extracts or the solid-phase microextraction samples are analyzed bygas chromatography-mass spectrometry.[101]

The electroantennogram technique is suitable for studying thebiological activityof insect pheromones.[55][102]In this technique, anelectrodeinserted into the antenna main stem and an antenna branch measures the change inelectrical voltageas a function of theconcentrationof pheromone molecules impinging on the antenna, which are transported to the antenna in a defined manner by an air current. [58] By varying the pheromone molecule, the influence of certainfunctional groupsinteracting with thechiralelements of the receptors can be determined.[55]

The coupling ofgas chromatographyand electroantennogram allows the biological activity of the compounds present in an extract to be verified.[55]The shape of the electroantennogram depends on the fragrance component in the air stream, and the amplitude increases with the concentration and flow velocity of the air.[103]

References

[edit]
  1. ^Gossauer, Albert (2006).Struktur und Reaktivität der Biomoleküle.Zurich: Helvetica Chimica Acta. p. 134.ISBN978-3-906390-29-1.
  2. ^Karlson, Peter; Butenandt, Adolf (1959). "Pheromones (Ectohormones) in Insects".Annual Review of Entomology.4:39–58.doi:10.1146/annurev.en.04.010159.000351.
  3. ^abKarlson, Peter; Lüscher, Martin (1959). "Pheromones: a New Term for a Class of Biologically Active Substances".Nature.183(4653): 55–56.Bibcode:1959Natur.183...55K.doi:10.1038/183055a0.PMID13622694.S2CID4243699.
  4. ^Gemoll, Wilhelm (2006).Griechisch-Deutsches Schul- und Handwörterbuch. Neubearbeitung.Munich: Oldenbourg Schulbuchverlag.ISBN3-637-00234-5.
  5. ^Karlson, Peter; Lüscher, Martin (1959)."The Proposed Biological Term" Pheromone ".Nature.183(4678): 1835.Bibcode:1959Natur.183.1835K.doi:10.1038/1831835b0.
  6. ^abcdBethe, Albrecht (1932). "Vernachlässigte Hormone".Die Naturwissenschaften.20(11): 177–181.Bibcode:1932NW.....20..177B.doi:10.1007/BF01504737.S2CID40051319.
  7. ^Nordlund, D. A.; Jones, R. L.; Lewis, W. J. (1981).Semiochemicals: Their Role in Pest Control.New York: Wiley. pp. 13–28.ISBN0-471-05803-3.
  8. ^Karlson, Peter; Lüscher, Martin (1959). "Pheromone".Die Naturwissenschaften.46(2): 63–64.Bibcode:1959NW.....46...63K.doi:10.1007/BF00599084.
  9. ^abWilson, Edward O. (1962). "Chemical communication among workers of the fire ant Solenopsis saevissima (Fr. Smith) 1. The Organization of Mass-Foraging".Animal Behaviour.10(1–2): 134–147.doi:10.1016/0003-3472(62)90141-0.
  10. ^abWilson, Edward O.; Bossert, William H. (1963). "Chemical communication among animals".Recent Progress in Hormone Research.19:673–716.PMID14284035.
  11. ^Dethier, Vincent G.; Browne, Barton L. (1960). "The Designation of Chemicals in Terms of the Responses They Elicit from Insects 1".Journal of Economic Entomology.53(1): 134–136.doi:10.1093/jee/53.1.134.
  12. ^Sakuma, Masayuki; Fukami, Hiroshi (1993). "Aggregation arrestant pheromone of the German cockroach, Blattella germanica (L.) (Dictyoptera: Blattellidae): Isolation and structure elucidation of blattellastanoside-A and -B".Journal of Chemical Ecology.19(11): 2521–2541.Bibcode:1993JCEco..19.2521S.doi:10.1007/BF00980688.PMID24248708.S2CID37967410.
  13. ^Bonnie Blaimer:Zur Struktur und Funktion der androconialen Organe und Sekrete bei Brassolini (Lepidoptera).Retrieved April 23rd, 2014.
  14. ^Pankiw, T.; Huang, Z-Y.; Winston, M. L.; Robinson, G. E. (1998). "Queen mandibular gland pheromone influences worker honey bee (Apis mellifera L.) foraging ontogeny and juvenile hormone titers".Journal of Insect Physiology.44(7–8): 685–692.Bibcode:1998JInsP..44..685P.doi:10.1016/S0022-1910(98)00040-7.PMID12769952.
  15. ^Nordlund, Donald A.; Lewis, W. J. (1976). "Terminology of chemical releasing stimuli in intraspecific and interspecific interactions".Journal of Chemical Ecology.2(2): 211–220.Bibcode:1976JCEco...2..211N.doi:10.1007/BF00987744.S2CID20085075.
  16. ^Free, J. B.; Simpson, J. (1968). "The alerting pheromones of the honeybee".Zeitschrift für Vergleichende Physiologie.61(3): 361–365.doi:10.1007/BF00428008.S2CID34252989.
  17. ^Raven, Charles E. (1950).John Ray, Naturalist: His Life and Works.Cambridge University Press. p. 395.
  18. ^abcButenandt, Adolf (1962). "Fettalkohole als Sexual-Lockstoffe der Schmetterlinge".Fette, Seifen, Anstrichmittel.64(3): 187–192.doi:10.1002/lipi.19620640302.
  19. ^Maeterlinck, Maurice (1901-05-01). "The Life of the Bee".Projekt Gutenberg.
  20. ^Bayliss, W. M.; Starling, E. H. (1906). "Die chemische Koordination der Funktionen des Körpers".Ergebnisse der Physiologie.5:664–697.doi:10.1007/BF02321027.
  21. ^Butenandt, Adolf; Beckmann, Rüdiger; Stamm, D. (1959). "Über den Sexuallockstoff des Seidenspinners".Zeitschrift für Naturforschung B.14:283–284.
  22. ^Butenandt, Adolf; Hecker, Erich; Hopp, Manfred; Koch, Wolfgang (1962). "Über den Sexuallockstoff des Seidenspinners, IV. Die Synthese des Bombykols und der cis-trans-Isomeren Hexadecadien-(10.12)-ole-(1)".Justus Liebigs Annalen der Chemie.658:39–64.doi:10.1002/jlac.19626580105.
  23. ^Butenandt, Adolf; Beckmann, Rüdiger; Hecker, Erich (1961). "Über den Sexuallockstoff des Seidenspinners, I. Der biologische Test und die Isolierung des reinen Sexuallockstoffes Bombykol".Hoppe-Seyler's Zeitschrift für physiologische Chemie.324:71–83.doi:10.1515/bchm2.1961.324.1.71.PMID13689417.
  24. ^Wilson, Edward O. (1958)."A Chemical Releaser of Alarm and Digging Behavior in the Ant Pogonomyrmex Badius (Latreille)".Psyche: A Journal of Entomology.65(2–3): 41–51.doi:10.1155/1958/57483.
  25. ^Butler, C. G.; Callow, R. K.; Johnston, N. C. (1962). "The Isolation and Synthesis of Queen Substance, 9-oxodec-trans-2-enoic Acid, a Honeybee Pheromone".Proceedings of the Royal Society B: Biological Sciences.155(960): 417–432.Bibcode:1962RSPSB.155..417B.doi:10.1098/rspb.1962.0009.S2CID86183254.
  26. ^Kasang, Gerhard; Kaißling, Karl Ernst; Vostrowsky, Otto; Bestmann, Hans Jürgen (1978). "Bombykal, eine zweite Pheromonkomponente des Seidenspinners Bombyx mori L".Angewandte Chemie.90(1): 74–75.Bibcode:1978AngCh..90...74K.doi:10.1002/ange.19780900132.
  27. ^Raina, Ashok K.; Klun, Jerome A. (1984). "Brain Factor Control of Sex Pheromone Production in the Female Corn Earworm Moth".Science.225(4661): 531–533.Bibcode:1984Sci...225..531R.doi:10.1126/science.225.4661.531.PMID17750856.S2CID40949867.
  28. ^Löfstedt, C. (1989)."No linkage between genes controlling female pheromone production and male pheromone response in the European corn borer, Ostrinia nubilalis Hübner (Lepidoptera; Pyralidae)".Genetics.123(3): 553–556.doi:10.1093/genetics/123.3.553.PMC1203827.PMID2599367.
  29. ^10 facts on malaria.WHO.int.März 2014, retrieved July 9th, 2014
  30. ^Mao, Y.; Xu, X.; Xu, W.; Ishida, Y.; Leal, W. S.; Ames, J. B; Clardy, J. (2010)."Crystal and solution structures of an odorant-binding protein from the southern house mosquito complexed with an oviposition pheromone".Proceedings of the National Academy of Sciences.107(44): 19102–19107.Bibcode:2010PNAS..10719102M.doi:10.1073/pnas.1012274107.PMC2973904.PMID20956299.
  31. ^Boppre, Michael; Schneider, Dietrich (1985). "Pyrrolizidine alkaloids quantitatively regulate both scent organ morphogenesis and pheromone biosynthesis in male Creatonotos moths (Lepidoptera: Arctiidae)".Journal of Comparative Physiology A.157(5): 569–577.doi:10.1007/BF01351351.S2CID26225408.
  32. ^abAttygalle, Athula B.; Morgan, E. David (1988). "Pheromones in Nanogram Quantities: Structure Determination by Combined Microchemical and Gas Chromatographic Methods [New Analytical Methods (35)]".Angewandte Chemie International Edition in English.27(4): 460–478.doi:10.1002/anie.198804601.
  33. ^Kaissling, K. E.; Kasang, G.; Bestmann, H. J.; Stransky, W.; Vostrowsky, O. (1978). "A new pheromone of the silkworm moth Bombyx mori".Naturwissenschaften.65(7): 382–384.Bibcode:1978NW.....65..382K.doi:10.1007/BF00439702.S2CID35272625.
  34. ^Kasang, Gerhard; Kaissling, Karl Ernst; Vostrowsky, Otto; Bestmann, Hans Jürgen (1978). "Bombykal, a Second Pheromone Component of the Silkworm MothBombyx mori L".Angewandte Chemie International Edition in English.17:60.doi:10.1002/anie.197800601.
  35. ^abcLevinson, Hermann; Levinson, Anna (2008-10-10). "Zu Struktur und Wirkungsweise der Pheromondrüsen vorratsschädlicher Insektenarten – Nachtrag 2008".Forschungsarbeiten über Insekten und andere Gliedertiere sowie deren Kulturgeschichte.
  36. ^Butler, C. G.; Calam, D. H. (1969). "Pheromones of the honey bee – The secretion of the Nassanoff gland of the worker".Journal of Insect Physiology.15(2): 237–244.Bibcode:1969JInsP..15..237B.doi:10.1016/0022-1910(69)90271-6.
  37. ^Naumann, Ken; Winston, Mark L.; Slessor, Keith N.; Prestwich, Glenn D.; Webster, Francis X. (1991). "Production and transmission of honey bee queen (Apis mellifera L.) mandibular gland pheromone".Behavioral Ecology and Sociobiology.29(5): 321–332.Bibcode:1991BEcoS..29..321N.doi:10.1007/BF00165956.S2CID44951006.
  38. ^Tillman, Julie A.; Seybold, Steven J.; Jurenka, Russell A.; Blomquist, Gary J. (1999). "Insect pheromones – an overview of biosynthesis and endocrine regulation".Insect Biochemistry and Molecular Biology.29(6): 481–514.Bibcode:1999IBMB...29..481T.doi:10.1016/S0965-1748(99)00016-8.PMID10406089.
  39. ^Roelofs, Wendell L. (1995)."Chemistry of sex attraction".Proceedings of the National Academy of Sciences.92(1): 44–49.Bibcode:1995PNAS...92...44R.doi:10.1073/pnas.92.1.44.PMC42814.PMID7816846.
  40. ^abcdefghBestmann, Hans Jürgen; Vostrowsky, Otto (1993). "Chemische Informationssysteme der Natur: Insektenpheromone".Chemie in unserer Zeit.27(3): 123–133.doi:10.1002/ciuz.19930270304.
  41. ^Carde, R. T.; Minks, A. K. (1997).Insect Pheromone Research: New Directions.Springer. p. 5.ISBN978-0-412-99611-5.
  42. ^Cusson, Michel; Tobe, Stephen S.; McNeil, Jeremy N. (1994). "Juvenile hormones: Their role in the regulation of the pheromonal communication system of the armyworm moth, Pseudaletia unipuncta".Archives of Insect Biochemistry and Physiology.25(4): 329–345.doi:10.1002/arch.940250408.
  43. ^Tea, Yi-Kai; Soong, Jonathan Wei; Beaver, Ethan P.; Lohman, David J. (2021). "Kleptopharmacophagy: Milkweed butterflies scratch and imbibe from Apocynaceae-feeding caterpillars".Ecology.102(12): e03532.Bibcode:2021Ecol..102E3532T.doi:10.1002/ecy.3532.PMID34496059.S2CID237454762.
  44. ^Meinwald, Jerrold (1990)."Alkaloids and isoprenoids as defensive and signalling agents among insect".Pure Appl. Chem.62(7): 1325–1328.doi:10.1351/pac199062071325.S2CID97197919.
  45. ^Reddy, Gadi V. P.; Guerrero, Angel (2004). "Interactions of insect pheromones and plant semiochemicals".Trends in Plant Science.9(5): 253–261.Bibcode:2004TPS.....9..253R.doi:10.1016/j.tplants.2004.03.009.PMID15130551.
  46. ^Boppré, Michael (1977). "Pheromonbiologie am Beispiel der Monarchfalter (Danaidae)".Biologie in unserer Zeit.7(6): 161–169.doi:10.1002/biuz.19770070604.S2CID85126060.
  47. ^Boppré, Michael; Schneider, Dietrich (1985). "Pyrrolizidine alkaloids quantitatively regulate both scent organ morphogenesis and pheromone biosynthesis in male Creatonotos moths (Lepidoptera: Arctiidae)".Journal of Comparative Physiology A.157(5): 569–577.doi:10.1007/BF01351351.S2CID26225408.
  48. ^Boppré, Michael (1995). "Pharmakophagie: Drogen, Sex und Schmetterlinge".Biologie in unserer Zeit.25:8–17.doi:10.1002/biuz.19950250103.
  49. ^Ziegler, Karl; Schenck, Günther Otto; Krockow, E. W. (1941). "Synthese des Cantharidins".Die Naturwissenschaften.29(26): 390–391.Bibcode:1941NW.....29..390Z.doi:10.1007/BF01479894.S2CID46621694.
  50. ^Eiden, Fritz (2006)."Cantharidin: Hochzeitsgabe, Schutz- und Lockstoff, Blasenzieher und Enzymhemmer".Chemie in unserer Zeit.40:12–19.doi:10.1002/ciuz.200600354.
  51. ^Enders, Dieter; Eichenauer, Herbert (1979). "Asymmetrische Synthese von Ameisen-Alarmpheromonen – α-Alkylierung von acyclischen Ketonen mit praktisch vollständiger asymmetrischer Induktion".Angewandte Chemie.91(5): 425–427.Bibcode:1979AngCh..91..425E.doi:10.1002/ange.19790910512.
  52. ^Mori, Kenji; Tashiro, Takuya (2004). "Useful Reactions in Modern Pheromone Synthesis".Current Organic Synthesis.1:11–29.doi:10.2174/1570179043485466.
  53. ^Bestmann, Hans Jürgen; Vostrowsky, Otto (1983). "Selected topics of the wittig reaction in the synthesis of natural products".Wittig Chemistry.Topics in Current Chemistry. Vol. 109. Springer, Berlin/Heidelberg. pp. 85–163.doi:10.1007/BFb0018057.ISBN0-387-11907-8.{{cite book}}:CS1 maint: location missing publisher (link)
  54. ^Ding, Bao-Jian; Hofvander, Per; Wang, Hong-Lei; Durrett, Timothy P.; Stymne, Sten; Löfstedt, Christer (2014)."A plant factory for moth pheromone production".Nature Communications.5:1–7.Bibcode:2014NatCo...5.3353D.doi:10.1038/ncomms4353.PMC3948062.PMID24569486.
  55. ^abcdefBestmann, Hans Jürgen (1985). "Synthese und Wirkungsweise von Pheromonen".Information und Kommunikation. Naturwissenschaftliche, medizinische und technische Aspekte.Stuttgart: Wissenschaftliche Verlagsgesellschaft mbH: 301–316.ISBN3-8047-0814-5.
  56. ^abcdefghPriesner, Ernst (1985). "Pheromone als Sinnesreize".Information und Kommunikation. Naturwissenschaftliche, medizinische und technische Aspekte.Stuttgart: Wissenschaftliche Verlagsgesellschaft mbH: 207–226.ISBN3-8047-0814-5.
  57. ^abBossert, William H.; Wilson, Edward O. (1963). "The analysis of olfactory communication among animals".Journal of Theoretical Biology.5(3): 443–469.Bibcode:1963JThBi...5..443B.doi:10.1016/0022-5193(63)90089-4.PMID5875169.
  58. ^abWyatt, Tristram D. (2003).Pheromones and Animal Behaviour. Communication by Smell and Taste.Cambridge University Press. p. 13.ISBN0-521-48526-6.
  59. ^Boppré, Michael (1976). "Pheromon-Transfer-Partikel auf einem Duftpinselhaar eines Monarchfalters (Danaus formosa)".Naturwissenschaftliche Rundschau.29(9).
  60. ^Krasnoff, Stuart B.; Roelofs, Wendell L. (1988). "Sex pheromone released as an aerosol by the moth Pyrrharctia isabella".Nature.333(6170): 263–265.Bibcode:1988Natur.333..263K.doi:10.1038/333263a0.S2CID4339228.
  61. ^Cardé, Ring (2011).Advances in Insect Chemical Ecology.Cambridge University Press. p. 190.ISBN978-0-521-18893-7.
  62. ^Okada, Kentaro; Mori, Masataka; Shimazaki, Kazuko; Chuman, Tatsuji (1990). "Behavioral responses of male Periplaneta americana L. to female sex pheromone components, periplanone-A and periplanone-B".Journal of Chemical Ecology.16(9): 2605–2614.Bibcode:1990JCEco..16.2605O.doi:10.1007/BF00988072.PMID24264316.S2CID30323914.
  63. ^abcRegnier, Fred E.; Law, John H. (1968)."Insect pheromones".Journal of Lipid Research.9(5): 541–551.doi:10.1016/S0022-2275(20)42699-9.PMID4882034.
  64. ^Foster, S. P.; Harris, M. O. (1997). "Behavioral manipulation Methods for Insect Pest-Management".Annual Review of Entomology.42:123–146.doi:10.1146/annurev.ento.42.1.123.PMID15012310.
  65. ^Vite, Jean Pierre; Francke, Wittko (1985). "Waldschutz gegen Borkenkäfer: Vom Fangbaum zur Falle".Chemie in unserer Zeit.19:11–21.doi:10.1002/ciuz.19850190103.
  66. ^Herzner, Gudrun; Schmitt, Thomas; Linsenmair, K. Eduard; Strohm, Erhard (2005). "Prey recognition by females of the European beewolf and its potential for a sensory trap".Animal Behaviour.70(6): 1411–1418.doi:10.1016/j.anbehav.2005.03.032.S2CID53269076.
  67. ^Schäfer, Bernd (2007).Naturstoffe in der chemischen Industrie.Spektrum Akademischer. pp. 522–524.ISBN978-3-8274-1614-8.
  68. ^Harraca, Vincent; Ryne, Camilla; Ignell, Rickard (2010)."Nymphs of the common bed bug (Cimex lectularius) produce anti-aphrodisiac defence against conspecific males".BMC Biology.8:121.doi:10.1186/1741-7007-8-121.PMC2944131.PMID20828381.
  69. ^Visscher, P. Kirk; Vetter, Richard S.; Robinson, Gene E. (1995). "Alarm pheromone perception in honey bees is decreased by smoke (Hymenoptera: Apidae)".Journal of Insect Behavior.8(1): 11–18.Bibcode:1995JIBeh...8...11V.doi:10.1007/BF01990966.S2CID45575468.
  70. ^Shearer, D. A.; Boch, R. (1965)."2-Heptanone in the Mandibular Gland Secretion of the Honey-bee".Nature.206(4983): 530.Bibcode:1965Natur.206..530S.doi:10.1038/206530a0.
  71. ^Levinson, Hermann; Levinson, Anna (2008-07-06)."Die Bettwanze, ein Ektoparasit der Fledermaus und des Menschen in eiszeitlichen Höhlen und zeitgemäßen Wohnstätten".Forschungsarbeiten über Insekten und andere Gliedertiere sowie deren Kulturgeschichte.Retrieved July 1st, 2014
  72. ^Klasen, Jutta; Schrader, Gabriele (2011-03-23)."Bettwanzen, Biologie des Parasiten und Praxis der Bekämpfung.(PDF) ".Umweltbundesamt FG IV 1.4 Gesundheitsschädlinge und ihre Bekämpfung.Retrieved July 1st, 2014
  73. ^Boller, E. F.; Aluja, M. (1992). "Oviposition deterring pheromone in Rhagoletis cerasi L".Journal of Applied Entomology.113(1–5): 113–119.doi:10.1111/j.1439-0418.1992.tb00644.x.S2CID84768250.
  74. ^Hölldobler, Bert; Wilson, Edward O. (1977)."Colony-specific territorial pheromone in the African weaver ant Oecophylla longinoda (Latreille)".Proceedings of the National Academy of Sciences.74(5). USA: 2072–2075.Bibcode:1977PNAS...74.2072H.doi:10.1073/pnas.74.5.2072.PMC431076.PMID266729.
  75. ^Koleva, Petia (2012). "Untersuchungen zur Effizienz von insektizidbehandelten Fanghölzern gegen den Buchdrucker Ips typographus (Coleoptera, Curculionidae)".Forstschutz Aktuell.54:16–21.
  76. ^Faulde, M.; Fuchs, M. E. A.; Nagl, W. (1990). "Further characterization of a dispersion-inducing contact pheromone in the saliva of the German cockroach, Blattella germanica L. (Blattodea: Blattellidae)".Journal of Insect Physiology.36(5): 353–359.Bibcode:1990JInsP..36..353F.doi:10.1016/0022-1910(90)90017-A.
  77. ^Breed, M. D.; Bennett, B. (1985). "Mass recruitment to nectar sources in Paraponera clavata: A field study".Insectes Sociaux.32(2): 198–208.doi:10.1007/BF02224233.S2CID8111724.
  78. ^Robinson, E. J. H.; Green, K. E.; Jenner, E. A.; Holcombe, M.; Ratnieks, F. L. W. (2008)."Decay rates of attractive and repellent pheromones in an ant foraging trail network"(PDF).Insectes Sociaux.55(3): 246–251.doi:10.1007/s00040-008-0994-5.S2CID27760894.
  79. ^Franks, N. R.; Gomez, N.; Goss, S.; Deneubourg, J. L. (1991). "The blind leading the blind in army ant raid patterns: Testing a model of self-organization (Hymenoptera: Formicidae)".Journal of Insect Behavior.4(5): 583–607.Bibcode:1991JIBeh...4..583F.doi:10.1007/BF01048072.S2CID14928826.
  80. ^Mena Granero, Angeles; Guerra Sanz, Jose M.; Egea Gonzalez, Francisco J.; Martinez Vidal, Jose L.; Dornhaus, Anna; Ghani, Junaid; Roldan Serrano, Ana; Chittka, Lars (2005)."Chemical compounds of the foraging recruitment pheromone in bumblebees".Naturwissenschaften.92(8): 371–374.Bibcode:2005NW.....92..371G.doi:10.1007/s00114-005-0002-0.PMID16049691.S2CID24317856.
  81. ^Costa-Leonardo, Ana-Maria; Haifig, Ives (2014). "Termite Communication During Different Behavioral Activities".Biocommunication of Animals.Springer Netherlands. pp. 161–190.doi:10.1007/978-94-007-7414-8_10.ISBN978-94-007-7413-1.{{cite book}}:CS1 maint: location missing publisher (link)
  82. ^Hoover, Shelley E. R.; Keeling, Christopher I.; Winston, Mark L.; Slessor, Keith N. (2003). "The effect of queen pheromones on worker honey bee ovary development".Naturwissenschaften.90(10): 477–480.Bibcode:2003NW.....90..477H.doi:10.1007/s00114-003-0462-z.PMID14564409.S2CID22875850.
  83. ^Wanner, K. W.; Nichols, A. S.; Walden, K. K. O.; Brockmann, A.; Luetje, C. W.; Robertson, H. M. (2007)."A honey bee odorant receptor for the queen substance 9-oxo-2-decenoic acid".Proceedings of the National Academy of Sciences.104(36): 14383–14388.Bibcode:2007PNAS..10414383W.doi:10.1073/pnas.0705459104.PMC1964862.PMID17761794.
  84. ^Koeniger, N.; Veith, H. J. (1984)."Spezifität eines Brutpheromons und Bruterkennung bei der Honigbiene (Apis Mellifera L.)".Apidologie.15(2): 205–210.doi:10.1051/apido:19840208.
  85. ^Leoncini, I.; Le Conte, Y.; Costagliola, G.; Plettner, E.; Toth, A. L.; Wang, M.; Huang, Z.; Becard, J.-M.; Crauser, D.; Slessor, K. N.; Robinson, G. E. (2004)."Regulation of behavioral maturation by a primer pheromone produced by adult worker honey bees".Proceedings of the National Academy of Sciences.101(50): 17559–17564.doi:10.1073/pnas.0407652101.PMC536028.PMID15572455.
  86. ^Tarver, Matthew R.; Schmelz, Eric A.; Scharf, Michael E. (2011). "Soldier caste influences on candidate primer pheromone levels and juvenile hormone-dependent caste differentiation in workers of the termite Reticulitermes flavipes".Journal of Insect Physiology.57(6): 771–777.Bibcode:2011JInsP..57..771T.doi:10.1016/j.jinsphys.2011.02.015.PMID21356212.
  87. ^Vargo, Edward (1998). "Primer pheromones in ants".Pheromone Communication in Social Insects: Ants, Wasps, Bees, and Termites:293–313.
  88. ^Forbush, Edward Howe; Fernald, Charles Henry (1896).Gypsy moth. Porthetria dispar (Linn.).: A Report of the Work of Destroying the Insect in the Commonwealth of Massachusetts together with an Account of its History and Habits both in Massachusetts and in Europe.Boston: Wright & Potter. p. 339.ISBN0-405-10393-X.
  89. ^Collins, Charles Walter; Potts, Samuel Frederick (1932). "Attractants for the flying gipsy moths as an aid in locating new infestations".Technical Bulletin No. 336.U.S. Department of Agriculture.
  90. ^Levinson, H. Z. (1975). "Possibilities of using insectistatics and pheromones in pest control".Die Naturwissenschaften.62(6): 272–282.Bibcode:1975NW.....62..272L.doi:10.1007/BF00608953.PMID1105200.S2CID35982749.
  91. ^Klimetzek, D.; Schlenstedt, L. (1991). "Waldschutz gegen Borkenkäfer: Der Beitrag von Duftstoffmeteorologie und Populationsdynamik".Anzeiger für Schädlingskunde Pflanzenschutz Umweltschutz.64(7): 121–128.doi:10.1007/BF01906002.S2CID21132323.
  92. ^Wigger, H. (1993). "Ökologische Bewertung von Räuber-Beifängen in Borkenkäfer-Lockstoffallen".Anzeiger für Schädlingskunde Pflanzenschutz Umweltschutz.66(4): 68–72.doi:10.1007/BF01903073.
  93. ^Pühringer, Franz; Ryrholm, Nils (2000-12-31). "Pheromonanflug europäischer Glasflügler (Lepidoptera, Sesiidae)".Mitteilungen der Entomologischen Arbeitsgemeinschaft Salzkammergut:65–72 (zobodat.at[PDF; Retrieved May 12nd, 2014]).
  94. ^Borkenkäfer – Vorbeugung und Bekämpfung.(2009)(PDF; 1,5 MB) (No longer available online.)Waldverband.at.Archived from the original on July 14, 2014; retrieved April 12, 2018.
  95. ^Kachigamba, Donald L.; Ekesi, Sunday; Ndung'u, Mary W.; Gitonga, Linus M.; Teal, Peter E. A.; Torto, Baldwyn (2012)."Evidence for Potential of Managing Some African Fruit Fly Species (Diptera: Tephritidae) Using the Mango Fruit Fly Host-Marking Pheromone".Journal of Economic Entomology.105(6): 2068–2075.doi:10.1603/EC12183.PMID23356072.S2CID15244235.
  96. ^Katsoyannos, B. I.; Boller, E. F. (1980). "Second field application of oviposition-deterring pheromone of the European cherry fruit fly, Rhagoletis cerasi L. (Diptera: Tephritidae)".Zeitschrift für Angewandte Entomologie.89(1–5): 278–281.doi:10.1111/j.1439-0418.1980.tb03467.x.
  97. ^Welter, Stephen C.; Pickel, Carolyn; Millar, Jocelyn; Cave, Frances; Van Steenwyk, Robert A.; Dunley, John (2005)."Pheromone mating disruption offers selective management options for key pests".California Agriculture.59:16–22.doi:10.3733/ca.v059n01p16.S2CID51802541.
  98. ^Danka, R. G.; Williams, J. L.; Rinderer, T. E. (1990)."A bait station for survey and detection of honey bees".Apidologie.21(4): 287–292.doi:10.1051/apido:19900403.
  99. ^Rowell, G. A.; Makela, M. E.; Villa, J. D.; Matis, J. H.; Labougle, J. M; Taylor, O. R. (1992). "Invasive dynamics of africanized honeybees in North America".Naturwissenschaften.79(6): 281–283.Bibcode:1992NW.....79..281R.doi:10.1007/BF01175399.S2CID44359661.
  100. ^Polettini, A.; Crippa, O.; Ravagli, A.; Saragoni, A. (1992). "A fatal case of poisoning with cantharidin".Forensic Science International.56(1): 37–43.doi:10.1016/0379-0738(92)90144-L.PMID1398375.
  101. ^abSchulz, Stefan (2011). "Auf der Spur der chemischen Sprache der Tiere".Nachrichten aus der Chemie.59(7–8): 704–709.doi:10.1002/nadc.201173368.
  102. ^Schneider, Dietrich (1957). "Elektrophysiologische Untersuchungen von Chemo- und Mechanorezeptoren der Antenne des Seidenspinners Bombyx mori L".Zeitschrift für Vergleichende Physiologie.40:8–41.doi:10.1007/BF00298148.S2CID6168639.
  103. ^Dietrich Schneider:Insect pheromone research: some history and 45 years of personal recollections.(PDF) Retrieved April 23, 2014.

Bibliography

[edit]
[edit]
Wikimedia Commons has media related toPheromone.

Collection of images, videos and audio data

Look upPheromonein Wiktionary, the free dictionary.

Meaning explanations, word origin, synonyms, translations

Retrieved from "https://en.wikipedia.org/w/index.php?title=Insect_pheromones&oldid=1240591243"