Termite Colonies Research Articles

Termites have wider thermal limits to cope with environmental conditions in savannas.

The most diverse and abundant family of termites, the Termitidae, evolved in African tropical forests. They have since colonised grassy biomes such as savannas. These open environments have more extreme conditions than tropical forests, notably wider extremes of temperature and lower precipitation levels and greater temporal fluctuations (of both annual and diurnal variation). These conditions are challenging for soft‐bodied ectotherms, such as termites, to survive in, let alone become as ecologically dominant as termites have.Here, we quantified termite thermal limits to test the hypothesis that these physiological limits are wider in savanna termite species to facilitate their existence in savanna environments.We sampled termites directly from mound structures, across an environmental gradient in Ghana, ranging from wet tropical forest through to savanna. At each location, we quantified both the Critical Thermal Maxima (CTmax) and the Critical Thermal Minima (CTmin) of all the most abundant mound‐building Termitidae species in the study areas. We modelled the thermal limits in two separate mixed‐effects models against canopy cover at the mound, temperature and rainfall, as fixed effects, with sampling location as a random intercept.For both CTmax and CTmin, savanna species had significantly more extreme thermal limits than forest species. Between and within environments, areas with higher amounts of canopy cover were significantly associated with lower CTmax values of the termite colonies. CTmin was significantly positively correlated with rainfall. Temperature was retained in both models; however, it did not have a significant relationship in either. Sampling location explained a large proportion of the residual variation, suggesting there are other environmental factors that could influence termite thermal limits.Our results suggest that savanna termite species have wider thermal limits than forest species. These physiological differences, in conjunction with other behavioural adaptations, are likely to have enabled termites to cope with the more extreme environmental conditions found in savanna environments and facilitated their expansion into open tropical environments.

INSIGHTS OF CASTE DETERMINATIONS IN SOCIAL INSECTS

Eusocial insects display caste structures in which reproductive ability is possessed by a single or a few queens while all other colony members act as workers. In social insects like ants, bees, and termites, vital physiological processes are regulated at the colony scale. Females in social insects have at least one reproductive caste and one nonreproductive caste; many termites have at least two male castes. The castes have considerable anatomical, physiological, and behavioural differences in higher social insects. Organismal systems, such as pheromone sensing, hormone signaling, and brain signaling pathways, are deployed in novel circumstances to impact nestmate and colony behaviours due to physiological decentralization over evolutionary time. Significant morphogenesis with region-specific cellular proliferation and degradation occurs during soldier development through two moulting via a presoldier stage in termite. JH action has been developed, in which a high JH titer causes soldier differentiation and a low JH titer causes alate differentiation. A monogamous pair of primary reproductives (one king and one queen) generated from alates normally establishes termite colonies (winged adults). The nymph-alate pathway (sexual pathway) or the worker pathway differentiates larvae in Reticulitermes termites (neuter pathway). Haplo-diploid sex determination controls the first developmental transition, in which unfertilized (haploid) embryos become males and fertilized (diploid) embryos become females in the case of Cataglyphis ant genus. The queen’s mandibular gland secretion, a mix of fatty acids and aromatic chemicals, is critical for maintaining the reproductive division of labour in honeybees (Apis mellifera), suppressing ovary growth in workers. Besides this, the brood produced by the queen also inhibits ovary development in workers by emitting two pheromones: the brood pheromone (BP), mainly composed of esters, and the highly volatile E-b-ocimene.

Mate finding in a mimetic termitophile amidst its host termites

AbstractA frequently overlooked cost can be involved in mimetic termitophily: excess resemblance to the model may compromise intraspecific recognition lowering fitness for the mimic. We address this problem, inspecting mate‐finding behavioural strategies used by Corotoca spp. rove beetles (Staphylinidae: Aleocharinae) which obligatorily cohabit the termitaria of Constrictotermes cyphergaster (Termitidae: Nasutitermitinae). In a bioassay, we show that whole‐body chemical extracts of these rove beetles (i) elicit behavioural activity, (ii) are perceivable by contact, (iii) can be used by Corotoca spp. to disguise themselves as a termite, and (iv) elicit a trail‐following behaviour similar to the "innate" one elicited by termites on themselves. In another bioassay using a Y‐shaped olfactometer, we show that beetles, despite disguising themselves, preserve their identity by employing long‐range signals to find mates amidst a termite crowd. Our data suggest that Corotoca beetles have developed different strategies (i) to bypass the nestmate recognition performed by termites (mimicking short‐range signals) and (ii) to preserve the ability to encounter their beetle conspecifics (perceiving long‐range signals). In conclusion, our results indicate that termitophiles such as Corotoca spp, while highly integrated in termite colonies, are still able to perform conspecific recognition.

Species- and Caste-Specific Gut Metabolomes in Fungus-Farming Termites.

Fungus-farming termites host gut microbial communities that contribute to the pre-digestion of plant biomass for manuring the fungal mutualist, and potentially to the production of defensive compounds that suppress antagonists. Termite colonies are characterized by complex division of labor and differences in diet between termite size (minor and major) and morphological (worker and soldier) castes, and this extends to the composition of their gut microbial communities. We hypothesized that gut metabolomes should mirror these differences and tested this through untargeted LC-MS/MS analyses of three South African species of fungus-farming termites. We found distinct metabolomes between species and across castes, especially between soldiers and workers. Primary metabolites dominate the metabolomes and the high number of overlapping features with the mutualistic fungus and plant material show distinct impacts of diet and the environment. The identification of a few bioactive compounds of likely microbial origin underlines the potential for compound discovery among the many unannotated features. Our untargeted approach provides a first glimpse into the complex gut metabolomes and our dereplication suggests the presence of bioactive compounds with potential defensive roles to be targeted in future studies.

Termitophily Documented in Earwigs (Dermaptera)

Simple SummaryIn the current report, we describe a new earwig species, Spirolabia kaja Kočárek, sp. nov. found in an association with the wood-boring termite in a dipterocarp rain forest in Borneo. To evaluate the level of association with termites we documented termite–earwig interactions in the laboratory. We found that earwigs and termites mutually communicate by antennation, and we observed no form of aggressive behavior. The earwigs responded to the proximity of an experimentally irritated termite soldier by the feigning of death (thanatosis), which seems to be a defensive reaction. The occurrence of earwig adults together with the nymphs in the galleries termite strongly suggests that the earwig reproduces inside the termite colony. Spirolabia kaja Kočárek, sp. nov. is the first earwig species for which termitophily has been demonstrated.Based on behavioral observations, we report termitophily by the earwig Spirolabia kaja Kočárek, sp. nov. (Spongiphoridae: Labiinae). The new species was found in association with the wood-boring termite Schedorhinotermes sarawakensis (Holmgren, 1913) in a dipterocarp rain forest in Borneo; in addition to being observed in the galleries, termite–earwig interactions were subsequently documented in the laboratory. We found that earwigs and termites communicate by antennation, and we observed no form of targeted mutual or unilateral aggressive behavior. The earwigs responded to the proximity of an experimentally irritated termite soldier by conflict-avoidance behavior based on thanatosis, which seems to be a defensive reaction that may reduce the chance of being attacked by an irritated termite. Based on the analysis of gastrointestinal tract contents, we conclude that S. kaja sp. nov. is an omnivorous species that feeds mainly on plant tissues and fungi but occasionally on arthropod remains. The occurrence of S. kaja sp. nov. adults together with the nymphs (2nd to 4th instars) in the galleries of S. sarawakensis strongly suggests that the earwig can reproduce inside the termite colony. Spirolabia kaja Kočárek, sp. nov. is the first earwig species for which termitophily has been demonstrated.

Soil organic matter is essential for colony growth in subterranean termites

Intrinsic dinitrogen (N2) fixation by diazotrophic bacteria in termite hindguts has been considered an important pathway for nitrogen acquisition in termites. However, studies that supported this claim focused on measuring instant N2 fixation rates and failed to address their relationship with termite colony growth and reproduction over time. We here argue that not all wood-feeding termites rely on symbiotic diazotrophic bacteria for colony growth. The present study looks at dietary nitrogen acquisition in a subterranean termite (Rhinotermitidae, Coptotermes). Young termite colonies reared with wood and nitrogen-rich organic soil developed faster, compared to those reared on wood and inorganic sand. More critically, further colony development was arrested if access to organic soil was removed. In addition, no difference of relative nitrogenase expression rates was found when comparing the hindguts of termites reared between the two conditions. We therefore propose that subterranean termite (Rhinotermitidae) colony growth is no longer restricted to metabolically expensive intrinsic N2 fixation, as the relationship between diazotrophic bacteria and subterranean termites may primarily be trophic rather than symbiotic. Such reliance of Rhinotermitidae on soil microbial decomposition activity for optimal colony growth may also have had a critical mechanistic role in the initial emergence of Termitidae.

Macro-symbiosis triggered by a defence-reproduction tradeoff in a social insect

Symbiotic associations underlie hierarchical evolutionary transitions being crucial to understanding biological complexity. But which proximate triggers promote the first successful contact between guests and their hosts? We tackle this problem, studying the macro-symbiotic model system comprised by two termite species (Blattodea: Isoptera) cohabiting termitaria as a host and its obligatory inquiline. We tested the hypothesis that ergonomic adjustments in resource allocation force termite colonies to trade current defence for future reproduction, thence easing inquiline infiltration. To do so, we combined mathematical modelling and field bioassays. Initially, we created a dynamic model to inspect colony’s resource allocation as a result of the competition between a physical “defence specialist” caste (soldiers) competing for resources with a reproductive caste (alates) and with a physical resource-gatherer specialist caste (workers). This model differs from Oster & Wilson’s “bang–bang” model by the explicit inclusion of solders as a physical defence specialist. Then, we sought empirical support for the end results of our model (i) censusing the population and (ii) measuring the patrolling efforts by soldiers, in 154 mature field termite colonies along a year-long reproductive season. Finally, we verified in the field whether reproducing termite colonies would be more likely to house inquilines than colonies still not at reproductive stage. Modelling and field results matched closely, supporting our hypothesis. Inquiline termites (Inquilinitermes microcerus) sneaked into nests of host termites (Constrictotermes cyphergaster) as these latter colonies undergone a defence-reproduction tradeoff. As the host colony entered reproduction, their soldier numbers and patrolling waned, enhancing the proneness of infiltration by obligatory inquilines. Our results indicate that defence-reproduction tradeoffs, more than a strategy to optimise resource use, can be important initiators of symbioses by loosening self/non-self discrimination and enhancing tolerance. We speculate that, if changes in the internal stasis of an organism or superorganism can enhance tolerance, it could be invoked to explain why symbioses are frequently enhanced by stress and disturbance.

Subterranean termite colony elimination can be achieved even when only a small proportion of foragers feed upon a CSI bait

Subterranean termite colony elimination can be achieved even when only a small proportion of foragers feed upon a CSI bait

Queen Egg Laying and Egg Hatching Abilities are Hindered in Subterranean Termite Colonies When Exposed to a Chitin Synthesis Inhibitor Bait Formulation.

Subterranean termite control methods using chitin synthesis inhibitors (CSIs) aim at eliminating colonies that feed upon a bait formulation. Several benzoylurea active ingredient formulations are currently commercially available as alternative termite management strategies to liquid termiticides. Individual workers need to molt on a regular basis and CSIs interfere with such molting process, allowing sufficient time for the acquisition of a colony-wide lethal dose prior to widespread mortality. As workers progressively die, the colony eventually collapses, leaving only soldiers and primary reproductives that starve to death. One common observation is that young workers often die early owing to their relatively short molting cycle. However, the absence of brood in dying colonies raises questions about the potential fate of eggs laid by the queen. This study aims to determine if CSI baits also terminate the ability of a colony to produce a new cohort of workers by disabling the ongoing brood development. Incipient termite colonies were used to test the impact of noviflumuron on the queen's ability to lay eggs and on the eggs' ability to hatch. Our results showed that queens in colonies exposed to CSI not only initially laid less eggs than the control queens, but eggs also did not develop and were progressively cannibalized, eventually leading to colony establishment failure. This result implies that queens of mature colonies exposed to CSI would lose the ability to lay viable eggs as the colony collapses, leading to an absence of worker replacement, aiding in colony elimination.

Queen Harems of Higher Termites are Regulated by Queen Pheromone

Colonies of higher termites (Termitidae) are usually headed by one king and one queen. Striking exceptions have recently been described in several species, whose founding queens prematurely die and are replaced by harems of up to hundreds of neotenic queens, arising from unfertilized eggs. This complex breeding system calls for the presence of a mechanism which would control the onset of the harem and its size. Here we show in one of such species, Embiratermes neotenicus, that the sesquiterpenoid (3R,6E)-nerolidol, emitted by queens and eggs, delays the development of new neotenic queens. We prove its effect as an airborne signal and demonstrate its olfactory detection. We conclude that (3R,6E)-nerolidol acts as a queen pheromone which may ensure the correct timing of the founding queen’s replacement and optimize the harem size according to colony population and fitness of reigning queen(s), being thus the key regulatory element of the harem breeding system.

Characterization of cellulose-degrading microbiota from the eastern subterranean termite and soil

Background: While there have been a lot of studies on the termite gut microbiota, there has been very little research directly on the cellulose-degrading microbiota in termites or their soil environment. This study addresses this problem by profiling cellulose-degrading bacteria and archaea in the selective cellulose cultures of two samples of the eastern subterranean termite (Reticulitermes flavipes) and one soil sample collected at the same location as one of the termite samples. Methods: All the cultures were examined for cell concentration and remaining cellulose after the culture was completed. The 16S rRNA pyrotag sequencing method was used to identify the prokaryotic microbiota for the three cultures and one termite colony without culture. The MOTHUR, SSU-ALIGN, RDPTools, phyloseq, and other R packages were used for sequence and statistical analyses. Results: Biochemical analyses of the cultures suggested high efficiency of cellulose degradation. Comparative analyses between the cultured and uncultured termite gut microbiota revealed a significant difference. Proteobacteria and Firmicutes were found to be the two most abundant phyla of cellulose-degrading bacteria from the three cultures, but different classes within each phylum dominated the different samples. Shared and sample-specific cellulose-degrading taxa, including a core set of taxa across all the cultures, were identified. Conclusions: Our study demonstrates the importance of using selective cellulose culture to study the cellulose-degrading microbial community. It also revealed that the cellulose-degrading microbiota in the eastern subterranean termite is significantly influenced by the microbiota in the surrounding soil environment. Biochemical analyses showed that the microbial communities enriched from all the selective cultures were efficient in degrading cellulose, and a core set of bacteria have been identified as targets for further functional analyses.

A beneficial relationship: associated trees facilitate termite colonies (Macrotermes michaelseni) in Namibia

AbstractIn many tropical ecosystems, termites are important ecosystem engineers. Mound‐building termite species often contribute to topographical landscape heterogeneity, and the associated accumulation of soil moisture and nutrients affects the spatial distribution of plant communities. Plants that grow next to the termite mound are known to benefit from the provided nutrients and water storage. The other way around, protection against erosion and cooling effects on the microclimate of the mounds imposed by associated trees have been described. However, little is known regarding the influence of tree parameters and the long‐term effects on colony development. In an interval of 12 yr, we studied all Macrotermes michaelseni mounds occurring within one square kilometer of Namibian thornbush savanna in terms of morphology, life history, and associated plants, with a focus on the role of associated trees which grow directly adjacent to the termite mounds. Here, we present the results of a combined analysis of the character states recorded at the termite mound and the associated trees. More than 50% of all 345 recorded termite mounds were associated with a tree. Mounds with associated trees showed increased activity, growth, and height. Mound growth within the study period was correlated positively with the canopy coverage by the associated tree, while total mound heights were correlated non‐linear with medium canopy coverage of about 40%. Mounds with a tree covering the sun's average zenith (north) were taller, grew most within 12 yr, and were more likely to be active than those with no northern canopy coverage. Mounds associated with the evergreen Boscia albitrunca attained highest average height (195.06 ± 11.76 cm). We conclude that vital parameters like growth, size, and activity of the termite colonies are facilitated by shading associated trees. These benefits were shown to take significant effect within the span of 12 yr. This indicates a proper long‐term mutualism, not a loose alliance and not an obligative eu‐symbiosis. Therefore, we propose to use the term “partner tree” for trees associated with M. michaelseni mounds.

A Review of Ectoparasitic Fungi Associated With Termites

AbstractTermites and ectoparasitic fungi have been at odds for millions of years. Surprisingly, fungi rarely kill their host and termites are continuously parasitized, albeit at low rates. ‘Termitophilous’ fungi have succeeded in the difficult task of infiltrating the ecological fortress of social immunity that is the termite colony. Here we review 34 definitive ectoparasitic fungal species from nine genera specialized to infest the cuticle of 50 + termite species. In general, reports of fungal ectoparasites on termites are underestimated and the actual prevalence of infestation is likely much greater in nature. In this review, we synthesize >120 yr of reports and studies on ectoparasitic fungi and their termite hosts to present an update to where our knowledge rests and where the proceeding steps should be focused. In reviewing this material, we aim to unite knowledge from two disciplines, entomology and mycology, creating a literary source useful for entomologists and mycologists alike. We provide a comprehensive summary of all fungal genera, illustrations showing morphological distinctions and development on the termite host, a glossary of mycological terminology, and an updated chart of the biogeography of these groups. Additionally, we provide a phylogenetic summary of parasite lineages and their known hosts as well as the first review of molecular evidence obtained from these fungal species.

The role of termite CH<sub>4</sub> emissions on the ecosystem scale: a case study in the Amazon rainforest

Abstract. The magnitude of termite methane (CH4) emissions is still an uncertain part of the global CH4 budget and current emission estimates are based on limited field studies. We present in situ CH4 emission measurements of termite mounds and termite mound subsamples performed in the Amazon rainforest. Emissions from five termite mounds of the species Neocapritermes brasiliensis were measured by use of a large flux chamber connected to a portable gas analyser measuring CH4 and CO2. In addition, the emissions of mound subsamples were measured, after which the termites were counted so that a termite CH4 and CO2 emission factor could be determined. Mound emissions were found to range between 17.0 and 34.8 nmol mound−1 s−1 for CH4 and between 1.1 and 13.0 µmol mound−1 s−1 for CO2. A termite emission factor of 0.35 µmol CH4 gtermite-1 h−1 was found, which is almost twice as high as the only other reported value for the Amazon. By combining mound emission measurements with the termite emission factor, colony sizes could be estimated, which were found to range between 55–125 thousand individuals. Estimates were similar to literature values, and we therefore propose that this method can be used as a quick non-intrusive method to estimate termite colony size in the field. The role of termites in the ecosystem's CH4 budget was evaluated by use of two approaches. Termite mound emission values were combined with local mound density numbers, leading to an estimate of 0.15–0.71 nmol CH4 m−2 s−1, on average, emitted by termite mounds. In addition, the termite CH4 emission factor from this study was combined with termite biomass numbers, resulting in an estimate of termite-emitted CH4 of ∼1.0 nmol m−2 s−1. Considering the relatively low net CH4 emissions previously measured at this ecosystem, we expect that termites play an important role in the CH4 budget of this terra firme ecosystem.

Subterranean Termite (Coptotermes gestroi (Blattodea: Rhinotermitidae)) Colony Elimination Through Exposure to a Novaluron CSI Bait Formulation in Laboratory.

The development of baits for subterranean termite control over the past 25 yr has provided cost-effective alternatives to liquid termiticide treatments. Current bait products use one of the few available benzoylurea chitin synthesis inhibitors (CSIs) labeled for subterranean termites. These insecticides are used because of their nonrepellency, their slow-acting mode of action, and their dose-independent lethal time. Although many studies have provided ample evidence of the efficacy of CSI baits for subterranean termite colony elimination, most have focused on hexaflumuron and noviflumuron. However, bait products using alternative CSIs have not received the same level of scrutiny, limiting the amount of evidence proving their efficacy. One such compound is novaluron, the active ingredient currently used in the Trelona ATBS-Advance Termite Baiting System bait product. The current study independently tested the efficacy of this commercially available bait formulation against whole colonies of Coptotermes gestroi (Wamann) (~63,910 workers) in the laboratory, using an extended experimental setup to simulate a 15-m foraging distance from the central part of the nest to the bait, while having access to alternative food sources. Treated colonies progressively ceased to feed on wood items within 45 d after being provided access to the novaluron bait formulation, with a subsequent progressive collapse of the population, leading to colony elimination by 91 d. This study therefore confirms the efficacy of novaluron baits against subterranean termites, and currently remains one of the few CSIs that can be applied for the successful control of Coptotermes infestations.

Regulatory Mechanisms Underlying the Differentiation of Neotenic Reproductives in Termites: Partial Release From Arrested Development

Eusocial insects exhibit reproductive division of labor, in which only a part of colony members differentiates into reproductives. In termite colonies, the division of labors is performed among multiple types of individuals (i.e., castes), such as reproductives, workers, and soldiers to organize their society. Caste differentiation occurs according to extrinsic factors, such as social interactions, leading to developmental modifications during postembryonic development, and consequently, the caste ratio in a colony is appropriately coordinated. In particular, when the current reproductives die or become senescent, some immature individuals molt into supplementary reproductives, also known as “neotenics,” that take over the reproductive task in their natal colony. Neotenics exhibit variety of larval features, such as winglessness, and thus, immature individuals are suggested to differentiate by a partial release from arrested development, particularly in the reproductive organs. These neotenic features, which have long been assumed to develop via heterochronic regulation, provide us opportunities to understand the developmental mechanisms and evolutionary origin of the novel caste. This article overviews the accumulated data on the physiological and developmental mechanisms that regulate the neotenic differentiation in termites. Furthermore, the evolutionary trajectories leading to neotenic differentiation are discussed, namely the acquisition of a regulatory mechanism that enable the partial release from a developmentally arrested state.

Limited evidence of C4 plant consumption in mound building Macrotermes termites from savanna woodland chimpanzee sites.

Stable isotope analysis is an increasingly used molecular tool to reconstruct the diet and ecology of elusive primates such as unhabituated chimpanzees. The consumption of C4 plant feeding termites by chimpanzees may partly explain the relatively high carbon isotope values reported for some chimpanzee communities. However, the modest availability of termite isotope data as well as the diversity and cryptic ecology of termites potentially consumed by chimpanzees obscures our ability to assess the plausibility of these termites as a C4 resource. Here we report the carbon and nitrogen isotope values from 79 Macrotermes termite samples from six savanna woodland chimpanzee research sites across equatorial Africa. Using mixing models, we estimated the proportion of Macrotermes C4 plant consumption across savanna woodland sites. Additionally, we tested for isotopic differences between termite colonies in different vegetation types and between the social castes within the same colony in a subset of 47 samples from 12 mounds. We found that Macrotermes carbon isotope values were indistinguishable from those of C3 plants. Only 5 to 15% of Macrotermes diets were comprised of C4 plants across sites, suggesting that they cannot be considered a C4 food resource substantially influencing the isotope signatures of consumers. In the Macrotermes subsample, vegetation type and caste were significantly correlated with termite carbon values, but not with nitrogen isotope values. Large Macrotermes soldiers, preferentially consumed by chimpanzees, had comparably low carbon isotope values relative to other termite castes. We conclude that Macrotermes consumption is unlikely to result in high carbon isotope values in either extant chimpanzees or fossil hominins.

Dynamic protozoan abundance of Coptotermes kings and queens during the transition from biparental to alloparental care

An incipient termite colony initially functions as a biparental family unit. The emergence of the first workers initiates the transition from biparental to alloparental care within a colony. During this transition, the number of protozoa harbored by Reticulitermes speratus (Kolbe) kings and queens is dynamic. In Coptotermes gestroi (Wasmann), the transition to alloparental care is completed by 150 days after colony foundation. In the present study, we quantified the protozoan abundance of C. gestroi and Coptotermes formosanus Shiraki kings and queens at ten time points during the transition from biparental to alloparental care (0–400 days post colony foundation). The protozoan abundance of C. gestroi and C. formosanus kings and queens peaked on either day 35 or 60 during the biparental care period, and then progressively decreased during the remainder of the study. By day 400 the protozoan abundance of kings and queens was either similar to or less than the abundance observed within unmated dealates. Both C. gestroi and C. formosanus kings and queens still harbored protozoa at day 150 even though the transition to alloparental care was completed by this time. On days 250 and 400 for C. formosanus, and on day 400 for C. gestroi, the protozoan abundance of kings was greater than the abundance of queens. These results indicate that alloparental care can become set within a colony prior to the loss of protozoa within the royal pair, and that queens lose their protozoa earlier than kings during incipient colony development.

Royal presence promotes worker and soldier aggression against non-nestmates in termites

Many eusocial insects can distinguish nestmates from non-nestmate conspecifics, which ensures that altruistic behavior is directed toward close relatives. In termites, however, colonies exhibit various responses to non-nestmates: from killing to accepting as a colony member. Why and how termite colonies adopt closed versus open societies remain largely unknown, while it is presumably related to not only genetic but also social-environmental factors. Here, we show that kings and queens play a key role in maintaining high aggression levels of workers and soldiers toward non-nestmate intruders in the subterranean termite Reticulitermes speratus. The level of aggression toward non-nestmate conspecifics was significantly lower in “royal-absent” colonies compared to “royal-present” colonies. In addition, the proportion of workers and soldiers exhibiting aggressive behaviors toward non-nestmates decreased in the absence of kings and queens. Our results demonstrate that social conditions, including royal presence, can influence intercolonial interactions, and may explain why previous studies of termite aggression have reported contradictory findings. This study provides important new insights into nestmate recognition and colony defense in eusocial insects.

A Review of Termite Pheromones: Multifaceted, Context-Dependent, and Rational Chemical Communications

Termite colonies, composed of large numbers of siblings, develop an important caste-based division of labor; individuals in these societies interact via intra- or intercaste chemical communications. For more than 50 years, termites have been known to use a variety of pheromones to perform tasks necessary for maintenance of their societies, similar to eusocial hymenopterans. Although trail-following pheromones have been chemically identified in various termites, other types of pheromones have not been elucidated chemically or functionally. In the past decade, however, chemical compositions and biological functions have been successfully identified for several types of termite pheromones; accordingly, the details of the underlying pheromone communications have been gradually revealed. In this review, we summarize both the functions of all termite pheromones identified so far and the chemical interactions among termites and other organisms. Subsequently, we argue how termites developed their sophisticated pheromone communication. We hypothesize that termites have diverted defensive and antimicrobial substances to pheromones associated in caste recognition and caste-specific roles. Furthermore, termites have repeatedly used a pre-existing pheromone or have added supplementary compounds to it in accordance with the social context, leading to multifunctionalization of pre-existing pheromones and emergence of new pheromones. These two mechanisms may enable termites to transmit various context-dependent information with a small number of chemicals, thus resulting in formation of coordinated, complex, and rational chemical communication systems.