Communication In Termites Research Articles

Termite exocrine systems: a review of current knowledge

AbstractIn this review, we summarize the 22 exocrine glands hitherto described for termites (Isoptera), highlighting their distribution, morphological features, and likely function. The secretion from such glands displays a very important role in termite communication, but is also attributed to many other activities performed by these insects, including defense, building, and foraging, as well as physiological processes such as the synthesis of digestive enzymes, and antiseptic and lubricant compounds. Here, glands are divided into those associated with termite mouthparts and other head appendages, tegumentary glands with epithelial arrangement, those related to the reproductive apparatus, and glands which do not fit into these divisions. The exocrine systems in termites may be composed of classes 1, 2, and 3 secretory cells, which differ in how the glandular secretion is released. Moreover, they may exhibit a varied composition of secretory cell classes. Different glands may be involved in specific tasks and therefore produce specific compounds, although there are cases in which the same content is secreted by different glands, suggesting a functional plasticity. The chemical nature of these secretions and their role are well known for some glands, such as the frontal, salivary, tergal, and sternal ones. On the other hand, such aspects remain speculative or completely unknown for other glands. The number of termite exocrine glands is extremely low when compared to those described for eusocial Hymenoptera, and is a likely consequence of the higher diversity of species and chemical communication in the latter group. Moreover, vibroacoustic signals represent an important type of communication in termites. Further studies are encouraged to provide new insights into the occurrence and function of the exocrine systems in termites and how they modulate the different activities displayed by them.

Conserved orthology in termite chemosensory gene families

Termites are eusocial insects known to use a variety of pheromones in tasks necessary for maintenance of their societies. As such, olfaction and pheromone communication in termites has been an object of intense study; trail-following pheromones (TFPs) and sex-pairing pheromones (SPPs), for example, have been identified in many termite species. In contrast, the molecular basis of olfactory detection is understudied in the group. Here, we present chemosensory genes of three species of termites belonging to three distinct lineages, Neotermes cubanus (Kalotermitidae), Prorhinotermes simplex (Rhinotermitidae), and Inquilinitermes inquilinus (Termitidae). Using antennal transcriptome screening of termite workers, we identified the chemosensory genes, which allowed us to perform phylogenetic analysis. We found a comparatively large repertoires of odorant receptors (ORs), gustatory receptors (GRs), ionotropic receptors (IRs), odorant binding proteins (OBPs), chemosensory proteins (CSPs), and sensory neuron membrane proteins (SNMPs). The evolutionary analysis of termite chemosensory genes revealed Isoptera-specific expansions with a 1:1 orthologous pattern, indicating the existence of conserved olfactory functions. Our findings on basal eusocial insects will further enhance our understanding of the molecular underpinnings of eusociality and the evolution of olfactory communication in termites.

Comparative Antennal Morphometry and Sensilla Organization in the Reproductive and Non-Reproductive Castes of the Formosan Subterranean Termite.

Simple SummaryInsects use antennae to perceive the chemical environment, and olfaction (the sense of smell) is essential for a variety of behavioral responses. Termites are social insects that display a division of labor based on an elaborate caste system consisting of reproductive (queen and king) and non-reproductive individuals (workers and soldiers). Whether these castes have different senses of smell is poorly understood. In this study, we characterized the morphology of antennae in alates (winged reproductives), workers, and soldiers in the Formosan subterranean termite, Coptotermes formosanus, and further analyzed the diversity and abundance of the antennal sensilla (sensory receptors) in each caste. We found that both female and male alates had longer antennae and greater numbers of sensilla than workers and soldiers, but all castes possessed the same nine types of antennal sensilla. Each type of sensilla had a specific spatial distribution along the antenna. The quantitative composition of sensilla differed between the reproductive and non-reproductive castes, but few differences were found between female and male alates or between worker and soldier castes. These results suggest that the olfactory morphology is associated with the reproductive division of labor in subterranean termites.Antennae are the primary sensory organs in insects, where a variety of sensilla are distributed for the perception of the chemical environment. In eusocial insects, colony function is maintained by a division of labor between reproductive and non-reproductive castes, and chemosensation is essential for regulating their specialized social activities. Several social species in Hymenoptera display caste-specific characteristics in antennal morphology and diversity of sensilla, reflecting their differential tasks. In termites, however, little is known about how the division of labor is associated with chemosensory morphology among castes. Using light and scanning electron microscopy, we performed antennal morphometry and characterized the organization of sensilla in reproductive (female and male alates) and non-reproductive (worker and soldier) castes in the Formosan subterranean termite, Coptotermes formosanus Shiraki. Here, we show that the antennal sensilla in alates are twice as abundant as in workers and soldiers, along with the greater number of antennal segments and antennal length in alates. However, all castes exhibit the same types of antennal sensilla, including basiconicum, campaniformium, capitulum, chaeticum I, chaeticum II, chaeticum III, marginal, trichodeum I, and trichodeum I. The quantitative composition of sensilla diverges between reproductive and non-reproductive castes, but not between female and male alates or between worker and soldier castes. The sensilla display spatial-specific distribution, with basiconicum exclusively and capitulum predominantly found on the ventral side of antennae. In addition, the abundance of chemosensilla increases toward the distal end of antennae in each caste. This research provides morphological signatures of chemosensation and their implications for the division of labor, and suggests future neurophysiological and molecular studies to address the mechanisms of chemical communication in termites.

Dataset on Substrate-Borne Vibrations of Constrictotermes cyphergaster (Blattodea: Isoptera) Termites

Here we present data on distinct stimuli as elicitors of substrate-borne vibrations performed by groups of termites belonging to the species Constrictotermes cyphergaster (Blattodea: Isoptera: Termitidae: Nasutitermitinae). The study consisted of assays where termite workers and soldiers were exposed to different airborne stimuli and the vibrations thereby elicited were captured by an accelerometer attached under the floor of the arena in which the termites were confined. A video camera was also used as a visual complement. The data provided here contribute to fill a gap currently existing in published datasets on termite communication.

Key physical wood properties in termite foraging decisions.

As eusocial and wood-dwelling insects, termites have been shown to use vibrations to assess their food, to eavesdrop on competitors and predators and to warn nest-mates. Bioassay choice experiments used to determine food preferences in animals often consider single factors only but foraging decisions can be influenced by multiple factors such as the quantity and quality of the food and the wood as a medium for communication. A statistical analysis framework is developed here to design a single bioassay experiment to study multifactorial foraging choice ( Pinus radiata) in the basal Australian termite species Coptotermes ( C.) acinaciformis (Isoptera: Rhinotermitidae). By employing a correlation analysis, 17 measured physical properties of 1417 Pinus radiata veneer discs were reduced to five key material properties: density, moisture absorption, early wood content, first resonance frequency and damping. By applying a fuzzy c-means clustering technique, these veneer discs were optimally paired for treatment and control trials to study food preference by termites based on these five key material properties. A multifactorial analysis of variance was compared to a permutation analysis of the results indicating for the first time that C. acinaciformis takes into account multiple factors when making foraging decisions. C. acinaciformis prefer denser wood with large early wood content, preferably humid and highly damped. Results presented here have practical implications for food choice experiments and for studies concerned with communication in termites as well as their ecology and coevolution with trees as their major food source.

A lipocalin protein, Neural Lazarillo, is key to social interactions that promote termite soldier differentiation.

Social communication among castes is a crucial component of insect societies. However, the genes involved in soldier determination through the regulation of inter-individual interactions are largely unknown. In an incipient colony of the damp-wood termite Zootermopsis nevadensis, the first larva to develop into a third instar always differentiates into a soldier via frequent trophallactic feeding from the reproductives. Here, by performing RNA-seq analysis of third instar larvae, a homologue of Neural Lazarillo (named ZnNLaz1) was found to be the most differentially expressed gene in these soldier-destined larvae, compared with worker-destined larvae. This gene encodes a lipocalin protein related to the transport of small hydrophobic molecules. RNAi-induced knockdown of ZnNLaz1 significantly inhibited trophallactic interactions with the queen and decreased the soldier differentiation rates. This protein is localized in the gut, particularly in the internal wall, of soldier-destined larvae, suggesting that it is involved in the integration of social signals from the queen through frequent trophallactic behaviours. Based on molecular phylogenetic analysis, we suggest that a novel function of termite NLaz1 has contributed to social evolution from the cockroach ancestors of termites. These results indicated that a high larval NLaz1 expression is crucial for soldier determination through social communication in termites.

Gene expression and molecular phylogenetic analyses of beta-glucosidase in the termite Reticulitermes speratus (Isoptera: Rhinotermitidae)

Beta-glucosidase (BG) is known as a multifunctional enzyme for social maintenance in terms of both cellulose digestion and social communication in termites. However, the expression profiles of each BG gene and their evolutionary history are not well understood. First, we cloned two types of BG homologs (RsBGI and RsBGII) from the termite Reticulitermes speratus (Kolbe). Gene expression analyses showed that RsBGI expression levels of primary queens and kings from 30 to 100days after colony foundation were high, but those of reproductives dropped after day 400. Extremely low gene expression levels of RsBGI were observed in eggs, whereas workers had significantly higher expression levels than those of soldiers and other colony members. Consequently, RsBGI gene expression levels changed among each developmental stage, and RsBGI was shown to be involved in cellulose digestion. On the other hand, the RsBGII gene was consistently expressed in all castes and developmental stages examined, and notable expression changes were not observed among them, including in eggs. It was indicated that RsBGII is a main component involved in social communication, for example, the egg-recognition pheromone shown in this species previously. Finally, we obtained partial gene homologs from other termite and cockroach species, including the woodroach (genus Cryptocercus), which is the sister group to termites, and performed molecular phylogenetic analyses. The results showed that the origin of the BG gene homologs preceded the divergence of termites and cockroaches, suggesting that the acquisition of multifunctionality of the BG gene also occurred in cockroach lineages.

Intracolony vibroacoustic communication in social insects

Vibrations and sounds, collectively called vibroacoustics, play significant roles in intracolony communication in termites, social wasps, ants, and social bees. Modalities of vibroacoustic signal production include stridulation, gross body movements, wing movements, high-frequency muscle contractions without wing movements, and scraping mandibles or tapping body parts on resonant substrates. Vibroacoustic signals are perceived primarily via Johnston’s organs in the antennae and subgenual organs in the legs. Substrate vibrations predominate as vibroacoustic modalities, with only honey bees having been shown to be able to hear airborne sound. Vibroacoustic messages include alarm, recruitment, colony activation, larval provisioning cues, and food resource assessment. This review describes the modalities and their behavioral contexts rather than electrophysiological aspects, therefore placing emphasis on the adaptive roles of vibroacoustic communication. Although much vibroacoustics research has been done, numerous opportunities exist for continuations and new directions in vibroacoustics research.

Worker aggression of ant Lasius japonicus enhanced by termite soldier–specific secretion as an alarm pheromone of Reticulitermes speratus

AbstractThe subterranean termite Reticulitermes speratus usually nests in rotten wood trunks, which may also be occupied by the Japanese garden ant Lasius japonicus. Few battles were observed between them under ordinary circumstances because they inhabit separate nesting sites. However, once the termite nesting sites were artificially broken, the ant workers invaded and hunted the termites, although the termite soldiers fought against the ants. This study aims to confirm intra‐ and inter‐specific chemical interactions between the termite and ant. Solid phase microextraction–gas chromatograph (SPME‐GC) analyses revealed that R. speratus soldiers secreted caste‐specific sesquiterpene hydrocarbon when they were irritated. Both the hexane extract of the soldiers and its hydrocarbon fraction, as well as the crushed soldier bodies, attracted the soldiers but dispersed the workers when presented on the trails. We also confirmed that the soldier chemicals enhanced aggressiveness of L. japonicus, which rushed around the odor sources and hunted any termites that were present. These findings suggest that: (i) the soldier–specific secretion might serve as an alarm pheromone in termite chemical communication, in which components recruit soldiers and also warn the other colony members away; and (ii) termite communication is eavesdropped on by L. japonicus workers to locate and hunt the termites.

Chemical communication in termites: syn-4,6-dimethylundecan-1-ol as trail-following pheromone, syn-4,6-dimethylundecanal and (5 E)-2,6,10-trimethylundeca-5,9-dienal as the respective male and female sex pheromones in Hodotermopsis sjoestedti (Isoptera, Archotermopsidae)

The trail-following pheromone and sex pheromones were investigated in the Indomalayan termite Hodotermopsis sjoestedti belonging to the new family Archotermopsidae. Gas chromatography coupled to mass spectrometry (GC–MS) after solid phase microextraction (SPME) of the sternal gland secretion of pseudergates and trail-following bioassays demonstrated that the trail-following pheromone of H. sjoestedti was syn-4,6-dimethylundecan-1-ol, a new chemical structure for termite pheromones. GC–MS after SPME of the sternal gland secretion of alates also allowed the identification of sex-specific compounds. In female alates, the major sex-specific compound was identified as (5 E)-2,6,10-trimethylundeca-5,9-dienal, a compound previously identified as the female sex pheromone of the termite Zootermopsis nevadensis. In male alates, the major sex-specific compound was identified as syn-4,6-dimethylundecanal, a homolog of syn-4,6-dimethyldodecanal, which has previously been confirmed as the male sex pheromone of Z. nevadensis. The presence of sex-specific compounds in alates of H. sjoestedti strongly suggests for this termite the presence of sex-specific pairing pheromones which were only known until now in Z. nevadensis. Our results showed therefore a close chemical relationship between the pheromones of the taxa Hodotermopsis and Zootermopsis and, in contrast, a clear difference with the taxa Stolotermes and Porotermes, which is in total agreement with the recent creation of the families Archotermopsidae and Stolotermitidae as a substitute for the former family Termopsidae.

Sex Pheromone and Trail Pheromone of the Sand Termite Psammotermes hybostoma

Within the complex network of chemical signals used by termites, trail pheromones and sex pheromones are among the best known. Numerous recent papers map the chemical identity and glandular origin of these pheromones in nearly all major isopteran taxa. In this study, we aimed to describe the sex pheromone and the trail pheromone of a poorly known sand termite, Psammotermes hybostoma. We identified (3Z,6Z,8E)-dodeca-3,6,8-trien-1-ol (dodecatrienol) as the sex pheromone released by tergal and sternal glands of female imagos and, at the same time, as the trail pheromone secreted from the sternal gland of workers. We conclude that chemical communication in Psammotermes does not differ from that of most other Rhinotermitidae, such as Reticulitermes, despite the presence of a diterpene as a major component of the trail pheromone of Prorhinotermes to which Psammotermes is presumed to be phylogenetically close. Our findings underline once again the conservative nature of chemical communication in termites, with dodecatrienol being a frequent component of pheromonal signals in trail following and sex attraction and, at the same time, a tight evolutionary relationship between the trail following of working castes and the sex attraction of imagos.

Sex pheromones and trail-following pheromone in the basal termites Zootermopsis nevadensis (Hagen) and Z. angusticollis (Hagen) (Isoptera: Termopsidae: Termopsinae)

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.

Identification of multi-component trail pheromones in the most evolutionarily derived termites, the Nasutitermitinae (Termitidae)

In the present study, trail pheromone blends are identified for the first time in termites. In the phylogenetically complex Nasutitermitinae, trail-following pheromones are composed of dodecatrienol and neocembrene, the proportions of which vary according to species, although neocembrene is always more abundant than dodecatrienol (by 25–250-fold). Depending on species, termites were more sensitive to dodecatrienol or to neocembrene but the association of both components always elicited significantly higher trail following, with a clear synergistic effect in most of the studied species. A third component, trinervitatriene, was identified in the sternal gland secretion of several species, but its function remains unknown. The secretion of trail pheromone blends appears to be an important step in the evolution of chemical communication in termites. The pheromone optimizes foraging, and promotes their ecological success.

Termites assess wood size by using vibration signals

Contrary to the common perception that termites are indiscriminant eaters, termites choose their food carefully; however, the methods by which they choose food are not well understood. Using choice experiments and recordings of termites feeding on wooden blocks of different sizes, we show that worker drywood termites (Cryptotermes domesticus) use the resonant frequency of a block of wood to assess its size. Drywood termites showed differences in their response to vibration recordings of termites compared with artificially generated signals, suggesting that they can discriminate the source of vibration. Furthermore, fewer workers matured into neotenic reproductives when recorded termite signals were played, suggesting that vibration signals play an important role in termite communication.