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Sex-pairing pheromone of Ancistrotermes dimorphus (Isoptera: Macrotermitinae)

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... In most cases, the sex-pairing pheromones were identified as singlecomponent pheromones; however, the modern techniques used in the recent studies allowed detection of minor components in several species, suggesting that the sex-pairing pheromones may be more complex than previously thought (e.g. Wen et al. 2012Wen et al. , 2015. ...
... c Shortrange bioassays with serial dilutions of DDE compared to a solvent control. The data shows means ±95% confidence intervals, calculated from a transformed Preference Index macrotermitines Ancistrotermes dimorphus (Wen et al. 2015) and Odontotermes formosanus (Wen et al. 2012). Behavioral roles of DE are controversial. ...
... Behavioral roles of DE are controversial. Long-range attraction of males was suggested in O. formosanus (Wen et al. 2012), while no effect on attraction or species-specific female discrimination was reported in C. silvestrii , and A. dimorphus (Wen et al. 2015). Even though our results indicate an eventual role of the compound as a minor component in the pheromone of S. minutus, the example of E. neotenicus adds to the doubts about its biological significance. ...
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Termite colonies are almost always founded by a pair of winged dispersers, in spite of the high costs and low success rates inherent in independent colony foundation. The dispersal flights of imagoes from natal colonies are followed by mate search, mediated by sex-pairing pheromones. Here, we studied the chemistry of sex-pairing pheromones and the related aspects of mate search in winged imagoes of two facultatively parthenogenetic species, Embiratermes neotenicus and Silvestritermes minutus, and an additional species from the same subfamily, Silvestritermes heyeri. All three species are widespread in the Neotropics, including the rainforests of French Guiana. After the dispersal flight and spontaneous loss of wings, females expose their hypertrophied tergal glands situated under abdominal tergites VIII – X. The females are attractive to males and, upon direct contact, the two sexes form characteristic tandems. Chemical analyses indicated that the females secrete species-specific combinations of unbranched, unsaturated C12 primary alcohols from the tergal glands, (3Z,6Z,8E)-dodeca-3,6,8-trien-1-ol (approx. 200 pg per female) and (3Z)-dodec-3-enol (185 pg) in E. neotenicus, (3Z,6Z)-dodeca-3,6-dien-1-ol (3500 pg) in S. heyeri, and (3Z,6Z)-dodeca-3,6-dien-1-ol (300 pg) and (3Z)-dodec-3-enol (50 pg) in S. minutus. (3Z,6Z,8E)-Dodeca-3,6,8-trien-1-ol and (3Z,6Z)-dodeca-3,6-dien-1-ol act as major pheromone components in the respective species and mimic the function of female tergal gland extracts in electrophysiological and behavioral experiments. Biologically relevant amounts of the third compound, (3Z)-dodec-3-enol, elicited non-significant reactions in males of E. neotenicus and S. minutus, and slight synergistic effects in males of S. minutus when tested in combination with the major component.
... Sex pheromones have independently evolved from multiple glandular sources in insects 21 such as ants 22 , bees 22 , and termites 23,24 . Bumble bees 25 and eusocial halictine bees 26 can produce sex pheromones in their cuticular hydrocarbons. ...
... In the termites (Isoptera), some species evidently produce sex pheromone in their sternal glands 23,24 . However, to our knowledge, prior studies have not shown that any Hymenoptera can produce sex pheromones in their sternal glands, although Hymenoptera are known to produce sex pheromones in their mandibular [42][43][44] and venom 11,12,16,28 glands. ...
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The Asian hornet, Vespa velutina, is an invasive, globally-distributed predator of European honey bees and other insects. To better under its reproductive biology and to find a specific, effective, and low-impact control method for this species, we identified and tested the key compounds in V. velutina sex pheromone. Virgin gynes (reproductive females) produced this sex pheromone in the sixth intersegmental sternal glands of their abdomens. The active compounds were 4-oxo-octanoic acid (4-OOA, 10.4 μg bee−1) and 4-oxo-decanoic acid (4-ODA, 13.3 μg bee−1) at a 0.78 ratio of 4-OOA/4-ODA. We synthesized these compounds and showed that male antennae were highly sensitive to them. Moreover, males were only strongly attracted to a 4-OOA/4-ODA blend at the natural ratio produced by gynes. These results provide the first demonstration of an effective way to lure V. velutina males, and the first chemical identification of a sex pheromone in the eusocial hornets.
... In order to reinforce the alarm signal secretion by the soldiers, legs of termite soldiers from a different colony or from a different species were placed into the vials. DOE and DDE were synthesized as described in Wen et al. [34] and the different concentrations were made by diluting the solutions with hexane. The number of ants that chose each vial was recorded and analysed. ...
... However, if the trails contained higher levels of DDE it indicated a larger group of termites with high likelihood of soldiers. Surprisingly, higher DDE may also show the presence of imagos as DDE is the dominant female sex pheromone component in O. yunnanensis and A. dimorphus [34,40,41]. Trails with high DDE content may represent higher returns due to the high abundance of individuals, but the likely presence of soldiers means that the predator would be subjected to higher risk. ...
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Predators may eavesdrop on their prey using innate signals of varying nature. In regards to social prey, most of the prey signals are derived from social communication and may therefore be highly complex. The most efficient predators select signals that provide the highest benefits. Here, we showed the use of eusocial prey signals by the termite-raiding ant Odontoponera transversa. O. transversa selected the trail pheromone of termites as kairomone in several species of fungus-growing termites (Termitidae: Macrotermitinae: Odontotermes yunnanensis, Macrotermes yunnanensis, Ancistrotermes dimorphus). The most commonly predated termite, O. yunnanensis, was able to regulate the trail pheromone component ratios during its foraging activity. The ratio of the two trail pheromone compounds was correlated with the number of termites in the foraging party. (3Z)-Dodec-3-en-1-ol (DOE) was the dominant trail pheromone component in the initial foraging stages when fewer termites were present. Once a trail was established, (3Z,6Z)-dodeca-3,6-dien-1-ol (DDE) became the major recruitment component in the trail pheromone and enabled mass recruitment of nest-mates to the food source. Although the ants could perceive both components, they revealed stronger behavioural responses to the recruitment component, DDE, than to the common major component, DOE. In other words, the ants use the trail pheromone information as an indication of suitable prey abundance, and regulate their behavioural responses based on the changing trail pheromone component. The eavesdropping behaviour in ants therefore leads to an arms race between predator and prey where the species specific production of trail pheromones in termites is targeted by predatory ant species.
... The former is the trail-following pheromone in all Kalotermitidae species studied (Sillam-Dussès et al. 2009b), as well as some Macrotermitinae (Peppuy et al. 2001a, b;Wen et al. 2014), while the latter is the trail-following pheromone of some Syntermitinae and Macrotermitinae species (Bordereau and Pasteels 2011;Sillam-Dussès 2011). Both compounds are also used as sex pheromones by some species (Robert et al. 2004;Wen et al. 2012Wen et al. , 2015. The chemical economy of termite pheromones has been previously highlighted (Bordereau and Pasteels 2011) and contrasts with the richness of defensive compounds. ...
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Pheromones play a crucial role in the ecology of dispersal and foraging in termites. Sex-pairing pheromones possess a double role of long-range attraction to unite sexual partners and a short-range or contact attraction to maintain the pair during the tandem behaviour. Sex-pairing pheromones most often comprise a single compound capable of eliciting both behavioural effects. They appear very conservative in their evolution, and their role in the reproductive isolation of sympatric species greatly varies according to species. Species-specific sex-pairing pheromones consist of different major compounds or of a common major compound with species-specific minor components. Foraging is a collective behaviour mainly regulated by trail-following pheromones secreted from only one glandular source, the sternal gland. Trail-following pheromones may be also used by “one-piece” termites to colonise additional food sources. Although trail-following pheromones of termites have a double role of orientation and recruitment, they appear most often composed of only one compound. An alternative hypothesis is given to the postulated existence of a volatile ephemeral compound of recruitment and a long-lasting compound of orientation. Trail-following pheromones appear highly conserved in their chemical evolution (only 8 different pheromones for 60 species), even if a clear separation is observed between basal termites and more derived termites. The major ecological event of the external foraging was not related to a chemical evolutionary step of the trail-following pheromones. Pheromonal parsimony (the utilisation of a same molecule for multiple functions) is common in termites in the behavioural context of dispersal and foraging. The same molecule is used in many species as a sex-pairing pheromone and a trail-following pheromone, depending upon the pheromone concentration and the caste involved.
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Article
Trail-following pheromones were studied in four fungus-growing termites from northern Vietnam: Macrotermes annandalei, M. barneyi, Odontotermes hainanensis and O. maesodensis. From bioassays, we suggest that trail pheromones of these species are composed of a common or anonymous signal, as well as species-specific signals. The anonymous signal has been identified by GC-MS as (Z)-dodec-3en-1-ol for each species from extracts of sternal glands and from solid phase microextraction of the surface of their sternal gland. This compound is secreted in much higher quantities (up to 1.4 ng/worker) than dodecatrienol, another anonymous signal of trail-following in termites. (Z)-dodec-3-en-1-ol is an anonymous signal of trail-following for numerous fungusgrowing termites, including African termites M. bellicosus and M. subhyalinus, but is not ubiquitous for all Macrotermitinae. Trail specificity is much more pronounced between species of different genera than between congeners. Speciesspecific compounds were not identified.
Chapter
Pheromones, secreted by exocrine glands, play a key role in all of the social activities of termites. Sex pheromones are usually released by one of the imago to attract the opposite sex, whereas trail pheromones are used by workers to mark their path to food. The sternal glands are undoubtedly involved in the secretion of a trail pheromone, unlike the tergal glands and the posterior sternal glands, which are known to produce a sex pheromone. In some species, the sternal gland secretes a sex pheromone. These pheromones mainly consist of a single compound, which may be used as the trail pheromone and sex pheromone in termites of the same species, depending on the concentration released and the caste involved. Many species from the same family or even from different families often use the same compound as a trail pheromone or a sex pheromone. Consequently, in termites, these pheromones are highly conservative in their chemical evolution and only seven compounds have been identified as a major or minor component of the trail pheromone or the sex pheromone of more than sixty species. These few pheromone compounds identified do not reflect the very large diversity observed in the nature and organization of the glands involved in their secretion. Even close species may differ greatly in the number of these glands, their shape or their cell composition and organization. Since many termite species are known to damage buildings and crops, the systems involving pheromone compounds have been considered for pest control, but the real potential of these pheromones in pest management has yet to be demonstrated.
Book
Pheromones, secreted by exocrine glands, play a key role in all of the social activities of termites. Sex pheromones are usually released by one of the imago to attract the opposite sex, whereas trail pheromones are used by workers to mark their path to food. The sternal gland is undoubtedly involved in the secretion of a trail pheromone, unlike the tergal glands and the posterior sternal glands, which are known to produce a sex pheromone. This new book presents and discusses information regarding trail pheromones and sex pheromones in termites.
Article
In the context of an evolutionary study of the chemical communication in termites, sex pheromones and trail-following pheromones were investigated in two Termopsidae, Zootermopsis nevadensis and Z. angusticollis. In these species, in which the presence of sex-specific pheromones has been demonstrated previously, the chemical structure of the female sex pheromone has now been identified as (5E)-2,6,10-trimethylundeca-5,9-dienal and the male sex pheromone as (+)- or (−)-syn-4,6-dimethyldodecanal. The amount of sex pheromone was estimated at 5–10 ng per individual in females and 2–5 ng in males. Because these two sympatric species do not differ in their pheromonal chemical composition, reproductive isolation is probably mediated chiefly by differences in dispersal flight chronology. The trail-following pheromone was shown to be composed of the same compound as the male sex pheromone, that is syn-4,6-dimethyldodecanal. The compound syn-4,6-dimethyldodecanal was 10 times more active than the racemic (+/−)-syn + (+/−)-anti-4,6-dimethyldodecanal in eliciting trail-following. The amount of syn-4,6-dimethyldodecanal was estimated at 0.1–0.5 ng per pseudergate. Regarding the phylogenetic aspects, the nature of the female sex pheromone of Zootermopsis is structurally akin to the trail-following pheromone of Mastotermes darwiniensis of Mastotermitidae and Porotermes adamsoni and Stolotermes victoriensis of Termopsidae. Interestingly, the nature of the trail-following pheromone of the Termopsinae Zootermopsis is clearly different from that of the Porotermitinae P. adamsoni and the Stolotermitinae S. victoriensis, which mirrors recent molecular data on the paraphyly of Termopsidae. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100, 519–530.
Article
The sex-pairing pheromone of the black winged subterranean termite, Odontotermes formosanus (Shiraki) (Isoptera, Termitidae), was investigated using headspace-SPME, GC-MS, GC-EAD, and attraction bioassays. Females secrete the pheromone from their sternal gland to attract males. The sex-pairing pheromone is composed of (Z,Z)-dodeca-3,6-dien-1-ol and (Z)-dodec-3-en-1-ol, estimated at 9 to 16.64 ng and 0.2 to 0.54 ng, respectively. Both short- and long-distance sex attraction bioassays were employed to show that these compounds act in synergy at long distance, but only (Z,Z)-dodeca-3,6-dien-1-ol is active at short distance. The pheromone may be useful in efforts to control this pest, which is considered one of the most harmful termite species in Southeast Asia.
Article
The species-specificity of pairing has been studied in three sympatric Neotropical termites: Cornitermes bequaerti, Cornitermes cumulans and Cornitermes silvestrii (Termitidae, Syntermitinae). Bioassays showed that sex attraction was highly species-specific between C. bequaerti and C. cumulans but not between C. cumulans and C. silvestrii. The sex-pairing pheromone of the three species is secreted by the tergal glands of female alates. It consists of a common compound (3Z,6Z,8E)-dodeca-3,6,8-trien-1-ol. In C. bequaerti, this polyunsaturated alcohol is the only compound of the sex-pairing pheromone, whereas it is associated with the oxygenated sesquiterpene (E)-nerolidol in C. cumulans, and with (E)-nerolidol and (Z)-dodec-3-en-1-ol in C. silvestrii. (3Z,6Z,8E)-Dodeca-3,6,8-trien-1-ol is responsible for sexual attraction, whereas (E)-nerolidol, which is inactive in eliciting attraction of male alates, is responsible for the species-specificity of the attraction. This is the first time that a multicomponent sex-pairing pheromone has been identified in termites. The role of (Z)-dodec-3-en-1-ol present on the surface of the tergal glands of the female alates of C. silvestrii could not be definitively determined, but it is suggested that this compound could be involved in the species-specificity of sex attraction with other sympatric species of Cornitermes. Our study shows that the reproductive isolation in termites is due to a succession of factors, as the chronology of dispersal flights, the species-specificity of sex-pairing pheromones and the species-specific recognition.
Article
(Z)-dodec-3-en-1-ol was isolated and identified by GC-MS as the major component of the trail-following pheromone from whole body and sternal gland extracts of workers of the fungus-growing termite, Macrotermes annandalei (Silvestri) (Termitidae, Macrotermitinae). For the first time, this trail pheromone was also identified by using solid phase microextraction from the surface of the secretory sternal gland of workers. Bioassays showed that synthetic dodecenol induced both orientation and recruitment behavioral effects. The activity threshold of (Z)-dodec-3-en-1-ol in eliciting trail-following is similar to that of (3Z,6Z,8E)-dodeca-3,6,8-trien-1-ol in the Rhinotermitidae, but amounts of dodecenol secreted are 100 times higher than those of dodecatrienol. There is about 1 ng of (Z)-dodec-3-en-1-ol per worker. Artificial trails made of synthetic dodecenol are able to compete with natural trails in the field. The activity duration of synthetic (Z)-dodec-3-en-1-ol trails is shorter than that of trails made from whole sternal secretion of workers. Observations showed that (Z)-dodec-3-en-1-ol is probably the only major component of the trail-following pheromone of M. annandalei and that it could be associated with other compounds in a pheromonal blend providing specificity and/or stability to trails.
Article
Thirty-nine species belonging to different families of termites are studied to give a comprehensive view of the evolution of the sternal glands. Several modifications occurring at cuticular and cytological levels are described in neuter castes. The outer epicuticle is always pierced by epicuticular pores. In advanced termites the epicuticular filaments greatly increase in number and length creating a thick layer. The pore canals gradually enlarge while the cuticle changes into a lattice structure lining an extracellular space in which the secretion is stored. Two classes of cells are present in basal termites (Mastotermitidae, Hodotermitidae, Termopsidae and Kalotermitidae) but their glandular structures greatly differ between families. A more complex organization with three classes of cells is found in the Serritermitidae and Rhinotermitidae. A regressive evolution occurs in the Termitidae where only two classes of cells are present. A dual nervous control (campaniform sensilla and neurosecretory fibers) is found in lower termites, except for the Hodotermitidae which have mechanosensory bristles. In the other families, neurosecretory fibers are lacking. A comparison with phylogenetic data is given. A more versatile role of sternal glands in neuter castes is hypothesized.
The abdominal epidermal glands of termites and their phylogenetic significance
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