CHEMO-BIOLOGICAL ASPECTS OF PHEROMONES IN ANT AND TERMITES

ABSTRACT

Pheromones are a mode of chemical communication in eusocial insects including ants and termites. The pheromones correspondent distinct social communication or activities such as counting, foraging, building, mating, and nestmate recognition. Various studies have been conducted on different types of pheromones present in ants and termites and their chemical nature. However, a lack of literature is available on the combined study of ant and termite pheromones and how pheromones of one insect affect the other. Hence, this review will be a consolidated analysis of the trail-following pheromone of the termites and ants, their chemical nature and the involvement of pheromones in ant-termite interaction. This article also discusses the different biological and commercial importance of the chemical compounds of pheromones. Such a study will give a new outlook towards ant-termite interaction and the pheromones associated with it and also help in finding other important functions of pheromone associated compounds.

АННОТАЦИЯ

Феромоны представляют собой способ химической коммуникации у эусоциальных насекомых, включая муравьев и термитов. Феромоны соответствуют различным социальным коммуникациям или действиям, таким как подсчет, поиск пищи, строительство, спаривание и распознавание товарищей по гнезду. Были проведены различные исследования различных типов феромонов, присутствующих в муравьях и термитах, и их химической природы. Однако недостаточно литературы по совместному изучению феромонов муравьев и термитов и тому, как феромоны одного насекомого влияют на другое. Таким образом, этот обзор будет представлять собой сводный анализ феромонов, следующих по следам термитов и муравьев, их химической природы, а также участия феромонов во взаимодействии муравьев и термитов. В этой статье также обсуждается различное биологическое и коммерческое значение химических соединений феромонов. Такое исследование даст новый взгляд на взаимодействие муравьев и связанных с ними феромонов, а также поможет выявить другие важные функции соединений, связанных с феромонами.

Keywords: Pheromones, trail-following pheromone, sex pheromone. 

Ключевые слова: Феромоны, феромон следования, половой феромон.

1. Introduction

Pheromones are a common form of intraspecies communication throughout the animal kingdom from insects to vertebrates (Dusses, 2010). These are the chemicals secreted by exocrine glands in eusocial insects (Meer and Alonso, 1998). Pheromones have been evolved from hormones, chemicals released on injury, host plant odors or waste products (Wyatt, 2005).  These pheromones play a variety of functions in social insects (especially ants and termites) such as trail laying for foraging, in defence against predators and in social communication (Vander Meer et al., 2019; Jaffe et al., 2012; Prestwich, 1979). Of these trail pheromones play very important role as they not only guide social insects from one point to another but also helps in regulating foraging activity in the colony via either positive or negative feedback (Czaczkes et al., 2015). Especially in the case of eusocial insects such as termites and ants, a huge set of informative chemicals are required, to maintain the intricate community interactions (Fewell, 2003; Fukao et al., 2007; Richard and Hunt, 2013; Costa and Haifig, 2014; Van et al., 2014).  In these insects, the chemically transferred information plays a very important role in kin and nestmate recognition (Richard and Hunt, 2013; Costa-Leonardo et.al., 2009; Hölldobler and Wilson, 1990).

Termites are known to orient themselves through trail-following pheromones. These pheromones secreted from their sternal glands triggers the nestmates to leave the nest and orient themselves to the food source (Cristaldo 2018; Stuart 1961, 1981). The chemical nature of trail pheromones is well studied in various termite species (Cristaldo 2018; Bordereau and Pasteels 2011; Sillam-Dusses 2010; Costa-Leonardo et.al.2009). However, besides trail pheromones other types of pheromones are also present in termites including alarm pheromones, sex pheromones and defensive pheromones (Bordereau et al., 2010; Stuart, 1981; Kirchner et al., 1994). Termite species such as subterranean termites use aggregation pheromones for expanding their nesting areas as they regulate the process of foraging in such termites (Mitaka et al., 2020). Moreover, termites also use faecal cement that contain cement pheromones to deposit the soil pellets and helps in pillar formation of termite chambers (Hill and Bullock, 2015). Hence, various types of pheromones present in termites perform distinct functions and play important role in their survival and reproduction.

In contrast, the trail following process in ants begins when they return to the nest after feeding. Ants leave a variety of chemical signals either through antennal contact, mandibular gland secretions, regurgitation, jerking movements or odor emission, recruiting other workers to leave the nest (Sasaki et al., 2014; Morgan, 2009). Trail following by worker ants and recruitment of workers comprises a combined study of entomologists and chemists that led to the study of the chemical nature of such pheromones. Pheromones may contain a single compound (foraging pheromones) or a blend of various compounds (sex pheromones), comprising the secretions from one or more glands (Morgan, 2009; Francke et al., 1985; Evershed et al., 1982). Hence, it is clear that both organisms use pheromones as a part of chemical communication within their community. However, these pheromones also play an important role in the interaction between ants and termites.

Besides the specific roles of ant and termites in their communities, they perform a range of ecological functions and their interaction is necessary for various ecosystem processes such as interacts with each-other due to their prey-predator relationship (DelToro et al., 2012; Philpott and Armbrecht, 2006; Bignell and Eggleton, 2000). Ant and termites frequently encounter each other in nature due to their high abundance, species richness and biomass in the same ecosystem (Dial et al., 2006). Hence, termites produce some counter-attack compounds such as repellents, toxins, anti-healing metabolites and sticky secretions from their exocrine glands that function to fight the predatory ants (Lubin and Montgomery, 1981; Sobotnik et al., 2010a). Various studies have been conducted on pheromone associated chemical compounds and their functions in ants and termites separately. However, there is a dearth of available literature on the combined study of pheromones in ant and termites and the way these pheromones affect the interaction between the two social insects. Therefore, this review focuses on various ant and termite pheromones, the chemical compounds present in these pheromones and the mechanism in which pheromones of both the insects manipulate each-others lifestyle. This study is unique because it also states different commercial and biological properties of the pheromone associated compounds present in ant and termites.

2. Ant pheromones and their functions:

Ant colonies use multiple signals to communicate and coordinate specific tasks such as nest defence, brood care and foraging (Hölldobler and Wilson, 1990). The first compound identified from trails pheromone was 4-methylpyrrole-2-carboxylate found in the venom gland of Atta texana however, this compound was also identified later in other ant species (Cross et al., 1982; Riley et al., 1974; Tumlinson et al., 1972). Various classes of chemical compounds are present in trail pheromones belonging to amines, hydrocarbons, alcohols and ketones (Cerda et al., 2014). Among them, volatile pyrazines (amines) are commonly used for food gathering and alarming behaviors in different ant species (Silva et al., 2018). For example, an alarm pheromone in ant Temnothorax rugatulus elicits different behavior in ants depending on the context. When this ant was tethered in an unfamiliar nest, it secreted a pheromone (2,5-dimethyl pyrazine) from its mandibular gland which signals other ants for nest rejection presumably to avoid the danger. However, when the same pheromone was presented near the familiar nest ants got attracted to it apparently to respond to a danger to the colony (Sasaki et al., 2014). Volatile compounds associated with pheromones may play similar or different roles in a variety of ant species.

Trail pheromones identified in six species of ants were named as six-species trail pheromone blend (6-TPB) and all of them are involved in foraging in these ants. These ant species are of two types sympatric and allopatric, based on that ant species responded differently towards the identified pheromones. The pheromones produced by allopatric species are hetero-specific for sympatric species and those produced by their own are con-specific (Meer and Alonso, 1998; Hölldobler and Wilson; 1990). Sympatric species involves Camponotus modoc, Lasius niger, Myrmica rubra and allopatric species involves Tetramorium caespitum, Novomessor albisetosus, Linepithema humilis (Chalissery et al., 2019).  L. niger contains trail pheromone 3,4-Dihydro-8-hydroxy-3-7-trimethylisocoumarin (isocoumarin) (Bestmann et al., 1992), C. modoc contains hexanolide (Renyard et al., 2019), M. rubra contains 3-Ethyl-2,5-dimethylpyrazine (Evershed et al., 1982). In T. caespitum, N. albisetosus, L. humilis the observed trail pheromones were 2,5-dimethylpyrazine (Attygalle and Morgan, 1983), 4-Methyl-3-heptanone (Hölldobler et al., 1995), (Z)-9-Hexadecenal (Key et al., 1982) respectively. In Camponotus modoc (2S,4R,5S)-2,4-dimethyl-5-hexanolide is the key trail pheromone component that also helps in foraging by attracting foragers and mediating their orientation to trail. Moreover, other compounds including 2,4- dimethylhexanoic acid, pentadecane, dodecanoic acid and 3,4-dihydro-8-hydroxy-3,5,7- trimethyl isocoumarin were found in hindgut extract of C. modoc (Renyard et al., 2019). When 6-TPB was provided to ants it showed induced trail following behaviour in C. modoc and L. niger indicated that C. modoc followed trails for both 6-TPB and its own pheromones to similar distances though L. niger followed 6- TPB for longer distances then their  own pheromone (Chalissery et al., 2019). Hence, it indicates that different ant species behaved in a diverse way to 6-TPB showing that ant community members eavesdrop on each-others trail pheromones.

3. Termite pheromones and their functions

In termites, only 9 chemicals have been identified till date, from  7 families (66 species) including basal termites (such as Mastotermitidae, Archotermopsidae, Stolotermitidae, Kalotermitidae, Rhinotermitidae, Serritermitidae) and advanced termites (Termitidae) family. The identified compounds belong  to alcohols, aldehydes, hydrocarbons and ketones. In terms of acquiring their food from outside or inside the nest, these species are distinguished for different ecological live type, namely “separated” (e.g. Termopsidae and Kalotermitidae), “intermediate” (e.g. Mastotermitidae, Rhinotermitidae) and “one-piece” (e.g. Hodotermitidae, some Rhinotermitidae and almost all Termitidae), all life types termites possess trail-pheromones, even “one-piece” life type species use it to recruit workers for defence or nest moving and orientation system is not desired (KlauseJafee et.al 2011). The pheromone such as (give example here) in “one-piece” type may be engaged in alarm communication, in which a trail laid by termite from the point of disturbance reaches to its nestmates to defend and repair disturbance point (Sillam-Dusses 2010). Evolution of life type of termite triggers to evolve chemical nature of trail-pheromone. Even with low difference, certain phylogenetic trends can be deduced from the distribution of trail following pheromones on the tree of life.

Basal termites differ from higher termites due to their  flagellated Protozoan symbiont, which is correlated with a special type of trophallaxis, that help in  exchange of proctodaeal feeding (Ch.NOIROT 1985). Basal termite species possess branched C₁₃, C₁₄ or C₁₈ aliphatic aldehydes and alcohols, present in their trail pheromones. One such example is E-2,6,10-trimethyl-5,9-undecadien-1-ol, which is present trail pheromone of Mastotermes darwiniensis (Mastotermitidae). This pheromone exists in two species of the family Termopsidae, namely Porotermes adamsoni (Porotermitinae) and Stolotermes victoriensis (Stolotermitinae) (Sillam-Dusses et al.2007). Similarly, another trail pheromone present in Zotermopsis angusticollis and Z. Nevadensis is syn 4,6-dimethyldodecanal (Bordereau et.al.2010). However, in higher termite, various substances including unbranched mono, di- or tri-unsaturated alcohols with 12 carbon atoms were identified as trail-following pheromones. Similarly, in some cases these atoms along with a mixture of diterpene hydrocarbons such asneocembrene or trinervitatriene were also found. The trail pheromones in higher termite family Termitidae differ between subfamilies. For example, (Z, Z)-dodeca-3,6 dien-1-ol was identified as trail pheromones in subfamily Macrotermitinae of termite Ancistrotermes sp. Similarly, (Z)-dodec-3-en-1-ol was identified in Macrotermes and Odontotermesspecies although, (3Z,6Z,8E)-dodeca-3,6,8-trien-1-ol was identified in Psammotermes and Pseudacanthotermes species. Trail pheromone of subfamily Termitinaeand Syntermitinaeis mixture of two chemicals have two type of chemicals namely dodecatrienol and neocembrene although one species of subfamily Syntermitinae namely Syntermes possess only dodecatrienol. Similarly, in the case of subfamily Nasutitermitinae the trail pheromones a mixture of dodecatrienol (3Z,6Z,8E)-dodeca-3,6,8-trien-1-ol) and neocembrene in Constrictrotermes species while in the case of Nasultitermes the trail pheromone is a combination of dodecatrienol, neocembrene and trinervitat. However, Cubitermes, Drepanotermes and Termes possess only one trail pheromone which isdodecatrienol (3Z,6Z,8E)-dodeca-3,6,8-trien-1-ol).

4.Types of interactions between ants and termites

Signals through trail pheromones are used particularly for foraging. The most elaborated form of chemical communication is the odor trail system (Morgan, 2009).  Foraging is a common activity found in both ant and termites during which the risk of predation is very high. Therefore, secretion of trail-following pheromone, foraging pheromone (Czaczkes et al., 2015; Wen et al., 2014; Jaffe et al., 2012; Bordereau and Pasteels, 2010), alarm pheromones and communication for the recognition of nest-mate for precise defensive behavior are important (Kirchner et al., 1994; Evans et al., 2009; Van et al., 2014). For example, ant species such as Odontoponera transversa (termite raiding ant) track and attack termites by following the pheromones released by termites (Wen et al., 2017).

Ants often use their sting to paralyze their prey as in the case of Neoponera marginata (Aili et al., 2014; Leal and Oliveira, 1995). The worker ants use their sting during an attack to paralyze the termites and then store them in the ant nest as food reserve (Leal and Oliveira, 1995). Ant species such as Dorylus performs regular assault on termite colonies showing effective predation (Tuma et al., 2020; Abe and Darlington, 1985; Bodot, 1961).  Another communication system is through alarm pheromones which is more sophisticated and provides information according to the threatening situation (Jackson and Morgan, 1993; Sasaki et al., 2014). Counterattacking in termites is also recruited by the use of alarm pheromones. The specific defensive glands (labial or frontal) of termites are evolved to produce toxic compounds as well as alarm pheromones (Sobotnik et al., 2010b; Deligne et al., 1981; Prestwich et., 1977; Wood et al., 1975;). Alarming signals can also be produced for other colony members by the vibration of the termite body (Deligne and Blum, 1981; Prestwich, 1984; Sobotnik et al., 2010a). Alarm pheromones have dual roles to play in some cases as they attract soldiers to the site of the strike during the attack on the colony and simultaneously protecting the workers who are vulnerable (Sobotnik et al., 2010a). However, in the species with a low soldier to worker ratios workers are known to bite the invading ants and slowing them down till the time other workers bung the passage to termite nest for ants (Sheppe, 1970; Eisner and Aneshansley, 1976; Ishikawa and Miura, 2012).

How one species affects other?

The most studied interaction between ants and termites is their predator-prey relationship. Prey communication is one of the riskiest activities as it provides specific cues for predators. Some prey communicates using chemical or vocal signals to avoid the predatory attack. However, predators still use these signals through eavesdropping (Lichtenberg et al., 2014) as they are equipped with special sensors to detect unique prey signals (Magnhagen, 1991; Labarrere et al., 2011; Moreno-Rueda, 2017). One such example is the detection of termite trail odor, colony odor and alarm pheromones by their predatory ant species (Trong and Akino, 2012). Ants not only regulate termite populations as predators but also affect their environment such as decreasing the decomposition rate of wood, litter and organic matter in the soil. It ultimately affects plant growth conditions (Tuma et al., 2020).   As these two groups of social insects have intricate effects on biotic and abiotic factors of the ecosystem hence, they are considered as ecosystem engineers (Jouquet et al., 2006). To avoid the risk of predators, prey species use a variety of chemical, behavioral, mechanical and combination of defensive adaptations (Krebs and Davies, 2009). The trail may composeof multiple pheromones with different properties containing information to form a trail network (Jackson et al., 2004; Robinsonet al., 2005; Jackson and Ratnieks, 2006; Dussutour et al., 2009). Predators also use a variety of signals which are innate to earwig on their prey. In the case of social prey such as termites, most of the signals derived from social communication are highly complex (Wen et al., 2017). Trail following can work in both ways either synergistic or complementary to the other sources of information such as the memory of the individual (Czaczkes et al., 2015).

4. Other properties of chemical compounds in pheromones

Table 1.

Values

Reference:

1. David Morgan, E. (2009). Trail pheromones of ants. Physiological entomology, 34(1), 1-17.
2. Wen, X. L., Wen, P., Dahlsjö, C. A., Sillam-Dussès, D., &Šobotník, J. (2017). Breaking the cipher: ant eavesdropping on the variational trail pheromone of its termite prey. Proceedings of the Royal Society B: Biological Sciences, 284(1853), 20170121.
3. Choe DH, Villafuerte DB, Tsutsui ND. Trail pheromone of the Argentine ant, Linepithemahumile (Mayr) (Hymenoptera: Formicidae). PLoS One. 2012;7(9):e45016. doi:10.1371/journal.pone.0045016
4. Evershed, R. P., Morgan, E. D., & Cammaerts, M. C. (1982). 3-Ethyl-2, 5-dimethylpyrazine, the trail pheromone from the venom gland of eight species of Myrmica ants. Insect Biochemistry, 12(4), 383-391.
5. Francke, W., Borchert, J., & Klimetzek, D. (1985). Volatile constituents of the red wood ant Formica rufa L.(Hymenoptera: Formicidae). Zeitschrift für Naturforschung C, 40(9-10), 661-664.
6. Prestwich, G. D. (1979). Chemical defense by termite soldiers. Journal of Chemical Ecology, 5(3), 459-480.
7. Vander Meer, R. K., & Alonso, L. E. (1998). Pheromone directed behavior in ants. Pheromone communication in social insects, 159-192.
8. Jaffe, K., Issa, S., & Sainz-Borgo, C. (2012). Chemical recruitment for foraging in ants (Formicidae) and termites (Isoptera): a revealing comparison. Psyche, 2012, 694910.
9. Vander Meer, R. K., Breed, M. D., Winston, M., & Espelie, K. E. (2019). Pheromone communication in social insects: ants, wasps, bees, and termites. CRC Press.
10. Wyatt, T. D. (2005). Pheromones: convergence and contrasts in insects and vertebrates. In Chemical Signals in Vertebrates 10 (pp. 7-19). Springer, Boston, MA.
11. Aili, S. R., Touchard, A., Escoubas, P., Padula, M. P., Orivel, J., Dejean, A., & Nicholson, G. M. (2014). Diversity of peptide toxins from stinging ant venoms. Toxicon, 92, 166-178.
12. Arunpanichlert, J., Rukachaisirikul, V., Sukpondma, Y., Phongpaichit, S., Tewtrakul, S., Rungjindamai, N., &Sakayaroj, J. (2010). Azaphilone and isocoumarin derivatives from the endophytic fungus Penicillium sclerotiorum PSU-A13. Chemical and Pharmaceutical Bulletin, 58(8), 1033-1036.
13. Ololade, Z. S., Olatunde, O. Z., Oyelese, O. J., Olaoye, O. O., &Odewande, R. A. (2014). Total Phenolic Content, Free Radical Inhibition, Antioxidant and Antibacterial Potentials of the Medicinal Organic Compounds in the Fruit of Terminalia catappa Linn. Nat Sci, 12(2), 46-50.
14. Devienne, K. F., Raddi, M. G., Coelho, R. G., &Vilegas, W. (2005). Structure–antimicrobial activity of some natural isocoumarins and their analogues. Phytomedicine, 12(5), 378-381.
15. Silva-Junior, E. A., Ruzzini, A. C., Paludo, C. R., Nascimento, F. S., Currie, C. R., Clardy, J., &Pupo, M. T. (2018). Pyrazines from bacteria and ants: convergent chemistry within an ecological niche. Scientific reports, 8(1), 1-7.
16. Hill, N., & Bullock, S. (2015, July). Modelling the role of trail pheromone in the collective construction of termite royal chambers. In Artificial Life Conference Proceedings 13 (pp. 43-50). One Rogers Street, Cambridge, MA 02142-1209 USA journals-info@ mit. edu: MIT Press.
17. Chalissery, J. M., Renyard, A., Gries, R., Hoefele, D., Alamsetti, S. K., &Gries, G. (2019). Ants sense, and follow, trail pheromones of ant community members. Insects, 10(11), 383.
18. Burkholder, W. E., Phillips, J. K., Walgenbach, C. A., & Klein, J. A. (1986). U.S. Patent No. 4,584,193. Washington, DC: U.S. Patent and Trademark Office.
19. National Center for Biotechnology Information. PubChem Database (2011). 3-Ethyl-2,5-dimethylpyrazine, CID=25916, https://pubchem.ncbi.nlm.nih.gov/compound/3-Ethyl-2_5-dimethylpyrazine.
20. Cerda, X., Van Oudenhove, L., Bernstein, C., & Boulay, R. R. (2014). A list of and some comments about the trail pheromones of ants. Natural product communications, 9(8), 1934578X1400900813.
21. Matsui, T., Guth, H., & Grosch, W. (1998). A comparative study of potent odorants in peanut, hazelnut, and pumpkin seed oils on the basis of aroma extract dilution analysis (AEDA) and gas chromatography‐olfactometry of headspace samples (GCOH). Lipid/Fett, 100(2), 51-56.
22. Richard, F. J., & Hunt, J. H. (2013). Intracolony chemical communication in social insects. Insectes sociaux, 60(3), 275-291.
23. Mitaka, Y., Matsuyama, S., Mizumoto, N., Matsuura, K., & Akino, T. (2020). Chemical identification of an aggregation pheromone in the termite Reticulitermes speratus. Scientific Reports, 10(1), 1-10.
24. Walgenbach, C. A., Phillips, J. K., Burkholder, W. E., King, G. G., Slessor, K. N., & Mori, K. (1987). Determination of chirality in 5-hydroxy-4-methyl-3-heptanone, the aggregation pheromone ofSitophilusoryzae (L.) andS. zeamaisMotschulsky. Journal of chemical ecology, 13(12), 2159–2169. https://doi.org/10.1007/BF01012564
25. Hölldobler, B., & Wilson, E. O. (1990). The ants. Harvard University Press.
26. Sudd, J. H. (1959). Interaction between ants on a scent trail. Nature, 183(4675), 1588-1588.
27. Semmelroch, P., Laskawy, G., Blank, I., & Grosch, W. (1995). Determination of potent odourants in roasted coffee by stable isotope dilution assays. Flavour and fragrance journal, 10(1), 1-7.
28. Sherwood, C. L., & Boitano, S. (2016). Airway epithelial cell exposure to distinct e-cigarette liquid flavorings reveals toxicity thresholds and activation of CFTR by the chocolate flavoring 2, 5-dimethypyrazine. Respiratory research, 17(1), 1-11.
29. Bordereau, C., &Pasteels, J. M. (2010). Pheromones and chemical ecology of dispersal and foraging in termites. In Biology of termites: a modern synthesis (pp. 279-320). Springer, Dordrecht.
30. Jaffe, K., Issa, S., &Sainz-Borgo, C. (2012). Chemical recruitment for foraging in ants (Formicidae) and termites (Isoptera): a revealing comparison. Psyche, 2012, 694910.
31. Kirchner, W. H., Broecker, I., & TAUTZ, J. (1994). Vibrational alarm communication in the damp‐wood termite Zootermopsisnevadensis. Physiological Entomology, 19(3), 187-190.
32. Evans, T. A., Inta, R., Lai, J. C., Prueger, S., Foo, N. W., Fu, E. W. E., & Lenz, M. (2009). Termites eavesdrop to avoid competitors. Proceedings of the Royal Society B: Biological Sciences, 276(1675), 4035-4041.
33. van Wilgenburg, E., Felden, A., Choe, D. H., Sulc, R., Luo, J., Shea, K. J., ... &Tsutsui, N. D. (2012). Learning and discrimination of cuticular hydrocarbons in a social insect. Biology letters, 8(1), 17-20.
34. Tuma, J., Eggleton, P., &Fayle, T. M. (2020). Ant‐termite interactions: an important but under‐explored ecological linkage. Biological Reviews, 95(3), 555-572.
35. Bignell, D. E., &Eggleton, P. (2000). Termites in ecosystems. In Termites: evolution, sociality, symbioses, ecology (pp. 363-387). Springer, Dordrecht.
36. Del Toro, I., Ribbons, R. R., & Pelini, S. L. (2012). The little things that run the world revisited: a review of ant-mediated ecosystem services and disservices (Hymenoptera: Formicidae). Myrmecological News, 17, 133-146.
37. Jouquet, P., Dauber, J., Lagerlöf, J., Lavelle, P., & Lepage, M. (2006). Soil invertebrates as ecosystem engineers: intended and accidental effects on soil and feedback loops. Applied soil ecology, 32(2), 153-164.
38. Philpott, S. M., &Armbrecht, I. (2006). Biodiversity in tropical agroforests and the ecological role of ants and ant diversity in predatory function. Ecological entomology, 31(4), 369-377.
39. Dial, R. J., Ellwood, M. D., Turner, E. C., & Foster, W. A. (2006). Arthropod abundance, canopy structure, and microclimate in a Bornean lowland tropical Rain forest 1. Biotropica, 38(5), 643-652.
40. Lubin, Y. D., & Montgomery, G. G. (1981). Defenses of Nasutitermes termites (Isoptera, Termitidae) against Tamandua anteaters (Edentata, Myrmecophagidae). Biotropica, 66-76.
41. Šobotník, J., Jirošová, A., &Hanus, R. (2010a). Chemical warfare in termites. Journal of Insect Physiology, 56(9), 1012-1021.
42. Deligne, J., Quennedey, A., & Blum, M. S. (1981). Social Insects, Vol. II (Herman, H. R., ed.).
43. Prestwich, G. D. (1984). Defense mechanisms of termites. Annual review of entomology, 29(1), 201-232.
44. Šobotník, J., Sillam-Dussès, D., Weyda, F., Dejean, A., Roisin, Y., Hanus, R., & Bourguignon, T. (2010b). The frontal gland in workers of Neotropical soldierless termites. Naturwissenschaften, 97(5), 495-503.
45. Sheppe, W. (1970). Invertebrate predation on termites of the African savanna. InsectesSociaux, 17(3), 205-218.
46. Eisner, T., Kriston, I., &Aneshansley, D. J. (1976). Defensive behavior of a termite (Nasutitermesexitiosus). Behavioral Ecology and Sociobiology, 1(1), 83-125.
47. Ishikawa, Y., & Miura, T. (2012). Hidden aggression in termite workers: plastic defensive behaviour dependent upon social context. Animal Behaviour, 83(3), 737-745.
48. Renyard, A., Alamsetti, S. K., Gries, R., Munoz, A., &Gries, G. (2019). Identification of the trail pheromone of the carpenter ant Camponotusmodoc. Journal of Chemical Ecology, 45(11-12), 901-913.
49. Bestmann, H. J., Kern, F., Schäfer, D., &Witschel, M. C. (1992). 3, 4‐dihydroisocoumarins, a new class of ant trail pheromones. AngewandteChemie International Edition in English, 31(6), 795-796.
50. Evershed, R. P., Morgan, E. D., &Cammaerts, M. C. (1982). 3-Ethyl-2, 5-dimethylpyrazine, the trail pheromone from the venom gland of eight species of Myrmica ants. Insect Biochemistry, 12(4), 383-391.
51. Dussutour, A., Nicolis, S. C., Shephard, G., Beekman, M., & Sumpter, D. J. (2009). The role of multiple pheromones in food recruitment by ants. Journal of Experimental Biology, 212(15), 2337-2348.
52. Jackson DE, Ratnieks FLW. 2006. Communication in ants. Curr. Biol. 16(15):R570–74
53. Robinson, E. J., Jackson, D. E., Holcombe, M., &Ratnieks, F. L. (2005). ‘No entry’signal in ant foraging. Nature, 438(7067), 442-442.
54. Jackson, D. E., Holcombe, M., &Ratnieks, F. L. (2004). Trail geometry gives polarity to ant foraging networks. Nature, 432(7019), 907-909.
55. Attygalle, A. B., & Morgan, E. D. (1984). Identification of trail pheromone of the antTetramoriumcaespitum L.(Hymenoptera: Myrmicinae). Journal of chemical ecology, 10(10), 1453-1468.
56. Hölldobler, B., Oldham, N. J., Morgan, E. D., & König, W. A. (1995). Recruitment pheromones in the ants Aphaenogasteralbisetosus and A. cockerelli (Hymenoptera: Formicidae). Journal of insect physiology, 41(9), 739-744.
57. Key, S. V. V., & Baker, T. C. (1982). Trail-following responses of the Argentine ant, Iridomyrmex humilis (Mayr), to a synthetic trail pheromone component and analogs. Journal of Chemical Ecology, 8(1), 3-14.
58. Bodot, P. (1961). Destruction of the nests of termites, BellicositermesnatalensisHav., by an ant, Dorylus (Typhlopone) dentifronsWasmann. Comptesrendushebdomadaires des seances de l'Academie des sciences, 253, 3053.
59. ABE, T. (1985). Distribution and abundance of a mound-building termite, Macrotermesmichaelseni, with special reference to its subterranean colonies and ant predators. Physiol. Ecol. Japan, 22, 59-74.
60. Leal, I. R., & Oliveira, P. S. (1995). Behavioral ecology of the neotropical termite-hunting ant Pachycondyla (= Termitopone) marginata: colony founding, group-raiding and migratory patterns. Behavioral ecology and sociobiology, 37(6), 373-383.
61. Lichtenberg, E. M., Zivin, J. G., Hrncir, M., &Nieh, J. C. (2014). Eavesdropping selects for conspicuous signals. Current Biology, 24(13), R598-R599.
62. Moreno‐Rueda, G. (2017). Preen oil and bird fitness: a critical review of the evidence. Biological Reviews, 92(4), 2131-2143.
63. Magnhagen, C. (1991). Predation risk as a cost of reproduction. Trends in Ecology & Evolution, 6(6), 183-186.
64. Labarrere, C. A., Woods, J. R., Hardin, J. W., Campana, G. L., Ortiz, M. A., Jaeger, B. R., ... & Pitts, D. E. (2011). Early prediction of cardiac allograft vasculopathy and heart transplant failure. American Journal of Transplantation, 11(3), 528-535.
65. TRONG NGUYEN, T., &Akino, T. (2012). Worker aggression of ant Lasius japonicus enhanced by termite soldier–specific secretion as an alarm pheromone of Reticulitermes speratus. Entomological Science, 15(4), 422-429.
66. Krebs, J. R., & Davies, N. B. (Eds.). (2009). Behavioural ecology: an evolutionary approach. John Wiley & Sons.
67. Costa-Leonardo, A. M., &Haifig, I. (2014). Termite communication during different behavioral activities. In Biocommunication of animals (pp. 161-190). Springer, Dordrecht.
68. Czaczkes, T. J., Grüter, C., &Ratnieks, F. L. (2015). Trail pheromones: an integrative view of their role in social insect colony organization. Annual review of entomology, 60.
69. Fukao, T., Fukuda, Y., Kiga, K., Sharif, J., Hino, K., Enomoto, Y., ... & Tanabe, M. (2007). An evolutionarily conserved mechanism for microRNA-223 expression revealed by microRNA gene profiling. Cell, 129(3), 617-631.
70. Fewell, J. H. (2003). Social insect networks. Science, 301(5641), 1867-1870.
71. Van Oystaeyen, A., Oliveira, R. C., Holman, L., van Zweden, J. S., Romero, C., Oi, C. A., ... & Millar, J. G. (2014). Conserved class of queen pheromones stops social insect workers from reproducing. Science, 343(6168), 287-290.
72. Sasaki, T., Hölldobler, B., Millar, J. G., & Pratt, S. C. (2014). A context-dependent alarm signal in the ant Temnothoraxrugatulus. Journal of Experimental Biology, 217(18), 3229-3236.
73. Jackson, B. D., & Morgan, E. D. (1993). Insect chemical communication: pheromones and exocrine glands of ants. Chemoecology, 4(3-4), 125-144.
74. Prestwich, G. D., Bierl, B. A., Devilbiss, E. D., & Chaudhury, M. F. B. (1977). Soldier frontal glands of the termiteMacrotermessubhyalinus: Morphology, chemical composition, and use in defense. Journal of Chemical Ecology, 3(5), 579-590.
75. Deligne, J. E. A. N., Quennedey, A. N. D. R. E., & Blum, M. S. (1981). The enemies and defense mechanisms of termites. Social insects, 2, 1-76.
76. David Sillam-Dusses 2010 Trail-Pheromones and Sex Pheromones in termites.Nova Science Publishers/Novinka, 2010, 79
77. Costa-Leonardo, A. M., Casarin, F. E., and Lima, J. T. (2009). Chemical communication inIsoptera. Neotrop. Entomol. 38, 1–6
78. Paulo F. Cristaldo (2018) Trail Pheromones in Termites. Termites and Sustainable Management,volume 1, 145-158
79. Stuart, A. M. (1961). Mechanism of trail-laying in two species of termites. Nature, 189, 419.
80. Stuart, A. M. (1981). The role of pheromones in the initiation of foraging, recruitment and defence by the soldiers of a tropical termite, Nasutitermescorniger (Motschulsky). Chemical Senses, 6, 409–420.
81. Reinhard, J., &Kaib, M. (2001). Trail communication during foraging and recruitment in the subterranean termite Reticulitermessantonensis De Feytaud (Isoptera, Rhinotermitidae). Journal of Insect Behavior, 14, 157–171.
82. Cristian Bordereau and Jacques M.Pasteels.  Pheromone and chemical ecology of dispersal and foraging in termites 2011, Biology of Termites: a Modern Synthesis, 279-311
83. Sillam-Dussès, D., Semon, E., Lacey, M. J., Robert, A., Lenz, M., & Bordereau, C. (2007). Trail-following pheromones in basal termites, with special reference to Mastotermesdarwiniensis. Journal of Chemical Ecology, 33, 1960–1977.
84. Bordereau, C., Lacey, M., Sémon, E., Braekman, J. C., Ghostin, J., Robert, A., Sherman, J. S., &Sillam-Dussès, D. (2010). Sex pheromones and trail-following pheromone in the basal termites Zootermopsisnevadensis(Hagen) and Z. angusticollis(Hagen) (Isoptera: Termopsidae: Termopsinae). Biological Journal of the Linnean Society, 100, 519–530.
85. Lacey, M. J., Sémon, E., Krasulová, J., Sillam-Dussés, D., Robert, A., Cornette, R., Hoskovec, M., Žáček, M., Valterová, I., & Bordereau, C. (2011). Chemical communication in termites: Syn-4,6-dimethylundecan-1-ol as trail-following pheromone, syn-4,6-dimethylundecanal and (5E)-2,6,10-trimethylundeca-5,9-dienal as the respective male and female sex pheromones in Hodotermopsissjoestedti(Isoptera). Journal of Insect Physiology, 57, 1585–1591.
86. Sillam-Dussès, D., Semon, E., Robert, A., & Bordereau, C. (2009). (Z)-Dodec-3-en-1-ol, a common major component of the trail-following pheromone in the termites Kalotermitidae.Chemoecology, 19, 103–108.
87. Robert, A., Peppuy, A., Semon, E., Boyer, F. D., Lacey, M. J., & Bordereau, C. (2004). A new C12 alcohol identified as a sex pheromone and a trail-following pheromone in termites: The diene (Z,Z)-dodeca-3,6-dien-1-ol. Naturwissenschaften, 91, 34–39.
88. Deng, X. J., Zhang, J. M., JF, H., Yang, J. F., YY, H., & Zheng, Q. (2002). Biological activity of a synthetic trail-pheromone analogue of the black-winged subterranean termite, OdontotermesformosanusShiraki. Acta EntomologicaSinica, 45, 739–742.
89. Hanus, R., Šobotník, J., Krasulová, J., Jiroš, P., Žáček, M., Dolejšová, K., Cvačka, J., Bourguigon, T., Roisin, Y., Lacey, M. J., &Sillam-Dussès, D. (2012). Nonadecadienone, a new termite trail-following pheromone identified in Glossotermesoculatus (Serritermitidae). Chemical Senses, 37, 55–63.
90. Matsumura, F., Coppel, H., & Tai, A. (1968). Isolation and identification of termite trail-following pheromone. Nature, 219, 963–964.
91. Tai, A., Matsumura, F., &Coppel, H. C. (1969). Chemical identification of the trail-following pheromone for a southern subterranean termite. The Journal of Organic Chemistry, 34, 2180–2182.
92. Tokoro, M., Takahashi, M., Tsunoda, K., & Yamaoka, R. (1989). Isolation and primary structure of  trail pheromone of the termite, CoptotermesformosanusShiraki (Isoptera: Rhinotermitidae). Wood Research, 29–38.
93. Tokoro, M., Takahashi, M., Tsunoda, K., Yamaoka, R., &Hayashiya, K. (1991). Isolation and identification of the trail pheromone of the subterranean termite Reticulitemessperatus (Kolbe) (Isoptera: Rhinotermitidae). Wood Research, 78, 1–14.
94. Bordereau, C., Robert, A., Laduguie, N., Bonnard, O., Le Quéré, J. L., & Yamaoka, R. (1993). Detection du (Z,Z,E)-3,6,8-dodecatrien-1-ol par les ouvriers et les essaimants de deux especes de termites champignonnistes: Pseudacanthotermesspinigeret P. militaris(Termitidae, Macrotermininae). Actes des ColloquesInsectesSociaux, 8, 145–149.
95. Laduguie, N., Robert, A., Bonnard, O., Vieau, F., Le Quere, J. L., Sémon, E., & Bordereau, C. (1994). Isolation and identification of (3Z,6Z,8E)-3,6,8-Dodecatrien-1-ol in Reticulitermes santonensisFeytaud (Isoptera, Rhinotermitidae): Roles in worker trail-following and in alate sex-attraction behavior. Journal of Insect Physiology, 40, 781–787.
96. Wobst, B., Farine, J.-P., Ginies, C., Sémon, E., Robert, A., Bonnard, O., Connétable, S., & Bordereau, C. (1999). (Z, Z, E)-3,6,8-Dodecatrien-1-ol, a major component of trail-following pheromone in two sympatric termite species Reticulitermes lucifugusgrasseiand R. santonensis. Journal of Chemical Ecology, 25, 1305–1318.
97. Sillam-Dussès, D., Robert, A., Semon, E., Lacey, M., & Bordereau, C. (2006). Trail-following pheromones and phylogeny in termites. In: Proc XV Congr IUSSI. Washington DC, pp 100–101.
98. Bordereau, C., &Pasteels, J. M. (2011). Pheromones and chemical ecology of dispersal and foraging in termites. In E. D. Bignell, Y. Roisin, & N. Lo (Eds.), Biology of termites: A modern synthesis (pp. 279–320). Dordrecht: Springer.
99. Sillam-Dussès, D., Hanus, R., El-Latif, A. O., Jiroš, P., Krasulová, J., Kalinová, B., Valterová, I., &Šobotník, J. (2011). Sex pheromone and trail pheromone of the sand termite Psammotermeshybostoma. Journal of Chemical Ecology, 37, 179–188.
100. Wen, P., Ji, B. Z., &Sillam-Dussès, D. (2014). Trail communication regulated by two trail pheromone components in the fungus-growing termite Odontotermesformosanus(Shiraki). PLoSOne, 9, e90906.
101. Cristaldo, P. F., DeSouza, O., Krasulová, J., Jirošová, A., Kutalová, K., Lima, E. R., Šobotník, J., &Sillam-Dussès, D. (2014). Mutual use of trail-following chemical cues by a termite host and  its inquiline. PLoS One, 9, e85315.
102. Moore, B. P. (1966). Isolation of the scent-trail pheromone of an Australian termite. Nature, 211,746–747.
103. Birch, A. J., Brown, W. V., Corrie, J. E. T., & Moore, B. P. (1972). Neocembrene-A, a termite trail pheromone. Journal of the Chemical Society, Perkin Transactions, 1, 2653–2658.
104. McDowell, P. G., &Oloo, G. W. (1984). Isolation, identification, and biological activity of trail-following pheromone of termite Trinervitermesbettonianus (Sjostedt) (Termitidae: Nasutitermitinae). Journal of Chemical Ecology, 10, 835–851.
105. Klaus Jaffe, Solange Issa, and Cristina Sainz-Borgo (2011) Chemical Recruitment for Foraging in Ants (Formicidae) and Termites (Isoptera): A Revealing Comparison. Psyche A Journal of Entomology 11(0033-2615)
106. Cross, J. H., West, J. R., Silverstein, R. M., Jutsum, A. R., & Cherrett, J. M. (1982). Trail pheromone of the leaf-cutting ant, Acromyrmex octospinosus (Reich), (Formicidae: Myrmicinae). Journal of chemical ecology, 8(8), 1119-1124.
107. Riley, R. G., Silverstein, R. M., Carroll, B., & Carroll, R. (1974). Methyl 4-methylpyrrole-2-carboxylate: a volatile trail pheromone from the leaf-cutting ant, Atta cephalotes. Journal of insect physiology, 20(4), 651-654.
108. Tumlinson, J. H., Moser, J. C., Silverstein, R. M., Brownlee, R. G., & Ruth, J. M. (1972). A volatile trail pheromone of the leaf-cutting ant, Atta texana. Journal of Insect physiology, 18(5), 809-814.
109. Ch.NOIROT  (1985) Pathways of caste development in the lower termites. Caste Differentiation in Social Insects, Pages 41-57, p-41-57
110. Kurt Bauer, Dorothea Garbe, Horst Surburg (2002) Common Fragrance and Flavor Materials: Preparation, Properties and Uses, pages 300
111. James Kirby a , Minobu Nishimoto a , J. Genevieve Park a , Sydnor T. Withers a,d , Farnaz Nowroozi a,e , Dominik Behrendt a , Elizabeth J. Garcia Rutledge a , Jeffrey L. Fortman a,g , Holly E. Johnson b , James V. Anderson c , Jay D. Keasling a,d,e,f,g, * Cloning of casbene and neocembrene synthases from Euphorbiaceae plants and expression in Saccharomyces cerevisiae, Phytochemistry Volume 71, Issue 13, September 2010, Pages 1466-1473
112. US patent 2004/0029918 A1