A review of the latest research on termite biology.
Latest termite biology research
Can termites learn?
Classical conditioning, where an animal learns to associate a particular stimulus with a benefit or adverse effect, has been well studied in bees, and to a degree in ants. However, studies on classical conditioning in termites have been limited. Working with the dampwood termite, Zootermopsis angusticollis, researchers conditioned worker termites to associate an odour (maple abstract) with the reward of a sugar solution, such that after conditioning, they would show excitatory responses when exposed to the maple extract alone.1
Should this behaviour be shown in other termite species, it could impact our interpretation of a range of termite behaviours. Certainly, learned responses could impact food choice and preferences when foraging. In terms of termite control, the ability to condition termites to adverse effects, such as sub-lethal insecticide doses, may impact the termite response to termite treatments.
Trichoderma fungi trigger aggregation behaviour in Coptotermes formosanus
Trichoderma fungi are soil microbes found in close association with termites. They appear to help in protecting against infection from entomopathogenic fungi such as Metarhizium. Previous research has shown that the presence of Trichoderma triggers a strong aggregation response in Coptotermes formosanus. In addition, termites have also been shown to preferentially forage in soils containing Trichoderma,
where they will also produce significantly larger tunnels than in soils without Trichoderma. Researchers have now found that four metabolites from extracts of Trichoderma fungi also trigger the aggregation behaviour in isolation.2 The authors believe that these chemicals should be evaluated as termite attractants and for their potential use in termite baits.
Termicin secretion forms part of anti-fungal protection in termites
Protection from entomopathogenic fungi, such as Metarhizium, is essential for termite colony health. A key part of the defence mechanism is allogrooming to remove fungal spores before they infect an individual and spread to the colony. Successful removal of spores of course depends on the termites being able to detect the fungi. However, some isolates of the fungi only elicit a weak allogrooming response, making it less likely for the termites to detect their presence, making them more susceptible to infection.
However, termites have other tools to help protect against infection. Researchers have discovered that termicin, an anti-fungal component in salivary gland secretions, appears to be most effective against these difficult-to-detect isolates.3 The researchers outline an “arms race” between fungi and termites, whereby selective pressure causes the fungi to develop variants that are not detected by termites (or at least variants that elicit a weak allogrooming response) so as to successfully infect the termites. In turn this puts selection pressure on the termites to produce an anti-fungal secretion that is particularly effective against these strains that manage to escape the allogrooming procedure.
Termite soldiers are important in nest hygiene
In the higher termites, in particular in the Nasutitermitinae, soldiers are more than just the ‘muscles’ of the colony – they are also known to be important in resource selection and foraging. The latest research indicates that they also have a role to play in colony immunity. When in mixed caste groups, optimally 30% soldiers/70% workers (which is the natural ratio in the field), the groups demonstrated increased grooming behaviour and trophallaxis, with worker grooming removing spores and the soldiers producing anti-fungal volatiles.4 The mixed groups containing soldiers were the only groups to also show vibratory movements, which may be used in communicating the potential threat. These actions resulted in increased survival time for the mixed caste groups when exposed to Metarhizium anisopliae fungi and also seemed to result in a reduced level of fungi in dead termites.
Aggregation Pheromones in Termites
Aggregation pheromones are well known in cockroaches, the distant relatives of termites. It therefore makes sense to investigate the potential role of aggregation pheromones in termite foraging. Aggregation pheromones typically have an attractant component to target individuals from afar and an arrestant component to stay at the pheromone source. Researchers in Japan have identified a mixture of four fatty acids from extracts of Coptotermes formosanus workers, which appear to work at arrestants.5
Much is still unknown about food location in termites and what attracts termites to a particular food source. Given that termites utilise decaying wood as a food source, several studies have looked at whether components of rotting wood attract termites. Researchers in Japan have identified dehydroabietic acid (DAA), a component in brown-rotted Japanese red pine, as a termite attractant in trials with Reticulitermes speratus.6 DAA is also an antimicrobial compound, so its presence in decaying timber would limit the number of potentially lethal pathogens present. As a relatively soluble terpenoid it would leach into soil in the field and the concentration gradient would allow termites to find and locate the food source. Although DAA appears to be an attractant, the authors suggest future research should look at its potential arrestant activity.
Understanding the role of aggregation pheromones (attractants and arrestants) in foraging behaviour will also give rise to potential improvements in termite control products, especially in baits.
References
1 Norman, J.H et al. (2023). Odorant Classical Conditioning in the Termite Zootermopsis angusticollis. Journal of Insect Behavior, 36: 150-155.
2 Zhang, L. et al. (2023). Trichoderma metabolites trigger aggregation behavior in Formosan subterranean termites (Coptotermes formosanus). Insect Science, 30(6): 1759-1772 https://doi.org/10.1111/1744-7917.13196
3 Luitel, B. et al. (2023). Subterranean termites raise the alarm when their anti-fungal weapon falters. The Science of Nature, 111(1).
4 Ferreira, L.F. et al. (2023). Caste composition contributes to improve the social immunity in a nasute termite species exposed to entomopathogenic fungus. Ecological Entomology, 48(6): 775-784. https://doi.org/10.1111/een.13274
5 Mitaka, Y. et al. (2023). Even- and odd-numbered fatty acids used as worker arrestant aggregation pheromone components in the Formosan subterranean termite Coptotermes formosanus. Chemoecology, 34: 1–12.
6 Mitaka, Y. et al. (2024). Dehydroabietic acid, an aromatic abietane diterpenoid, attracts termite workers. Applied Entomology and Zoology,
59: 195–201.
Keeping the colony healthy
Given the warm, humid environment and large numbers of individuals inside termite nests, preventing pathogens from entering (especially fungi) is essential for keeping the colony healthy. Previous research has suggested that termites infected with a pathogen may exhibit shaking behaviour. In addition, non-infected nestmates may pick up some olfactory cues from the infested nestmate. Either way, at the early stages of infection, typically non-infected nestmates will groom infected individuals (as pictured above) to remove any spores, although if the infection has reached a lethal level, grooming is generally replaced by cannibalisation. In some cases, healthy workers have been observed to prevent infected individuals returning to the colony, a behaviour seen in other social insects where the colony tries to protect high value individuals in the nest (reproductive and brood).
Recent research from Texas A&M University took a closer look at the individual and colony behaviours towards infected Reticulitermes flavipes workers.1 The researchers infected workers with a known fungal pathogen and observed their behaviours in isolation and on return to their nestmates. The data indicated that shaking behaviours or locomotion did not change in the presence of nestmates, indicating that these behaviours did not likely play a role in communicating infection. However, they were subjected to intense inspection and grooming.
Interestingly, the infected workers were allowed to return to the central nest area, showing that at least in these laboratory trials there was no evidence of isolation of infected individuals. Although this may seem at odds with the need to protect the high value individuals from infection, the central nest area will see infected individuals subjected to more intense grooming. Meanwhile, the termite nest material exhibits strong anti-microbial activity. The researchers did acknowledge that behaviours may be different in the field with the larger number of individuals and the complexity of large nest structures.
Although shaking behaviours didn’t appear to be a trigger to stimulate grooming, clearly there must be stimuli that would trigger the pathogen avoidance behaviours. Researchers in China had a closer look at volatile chemicals released from the cuticles of Coptotermes formosanus and compared the chemicals released from termites exposed to a Metarhizium fungus to those of heathy termites.2
The results highlighted one notable difference, namely that a significantly higher level of ergosterol was released from fungus-exposed termites. When ergosterol was applied to filter paper discs, termites stayed on the filter paper significantly longer than on control discs. Furthermore, termites that were exposed to ergosterol followed by Metarhizium anisopliae conidia were allogroomed at a significantly higher frequency and for a longer duration than termites exposed to alcohol alone followed by M. anisopliae conidia. The study clearly indicates that ergosterol has a role in allogrooming and pathogen control in C. formosanus, although a lot more research needs to be carried out in this area.
In terms of the mechanics of spore removal from the cuticle, this cannot be done by soldiers, so should they become infected they are entirely reliant on workers to remove any fungal spores. Looking more closely at this grooming behaviour in Coptotermes formosanus, researchers have found that both infected and uninfected workers are involved in grooming and under normal soldier/worker ratios, there is no bias in which caste gets preferential grooming.3 However, as the number of workers in the group decreases (higher soldier/worker ratio), the workers had to work harder to remove the spores from the soldiers (fewer workers to groom more soldiers), to the detriment of their own survival rate.
Although social immunity through allogrooming is a key component for maintaining colony health, innate immunity on an individual basis is also important. Researchers compared the roles of social and innate immunity for two closely related termite species – Reticulitermes flavipes and R. virginicus – in response to infection from two species of pathogenic fungi.4
R. flavipes was very reliant on allogrooming to prevent infection, whereas R. virginicus had higher levels of innate immunity – shown by increased survival in the absence of grooming. This innate immunity was explained by the higher levels of anti-fungal activity measured with cuticular washes from R. virginicus. The researchers also detected that individual termites exposed to high levels of conidia exhibited alarm when surrounded by other termites, resulting in increased grooming, They also noted that R. flavipes, which was more reliant on allogrooming to prevent infection, demonstrated higher levels of alarm behaviour.
Moulting in the central nest – recycling nitrogen
It has been observed that termite workers return to the central nest to moult. This may be in part a self-preservation exercise; individuals will be more susceptible to predation and picking up pathogens during the moulting process. However, researchers have hypothesised that this behaviour may have additional benefits. Termites have a nitrogen-poor diet and yet nitrogen is required in order to create amino acids and protein for growth. With the exuviae (spent cuticles) containing 11% nitrogen, it would be beneficial from an evolutionary point of view for this nitrogen to be retained within the colony.
Exuviae from a Coptotermes gestroi colony were marked with immunoglobulin G (IgG) and were fed to two-year-old C. gestroi colonies.5 The IgG marker was later detected in every caste and life stage, except first-instar larvae. Workers and possibly second-star larvae would have fed on the exuviae directly while queens, kings and soldiers received the marker through trophallaxis. With exuviae containing 11% nitrogen by weight, moulting back at the central nest and recycling the nitrogen by consuming the exuviae retains the vital nitrogen within the colony.
The same group of researchers went on to assess the impact of exuviae consumption on queen oviposition and colony growth.6 Feeding different levels of exuviae to incipient termite colonies in both nitrogen-rich and nitrogen-poor environments, the performance of the colonies was assessed after six and a half months. Colonies raised in nitrogen-poor environments gained significantly more biomass (were bigger) when fed exuviae compared to colonies without access to exuviae. However, in nitrogen-rich environments the presence or absence of exuviae had no effect on colony growth. In addition, queens from colonies that had access to exuviae produced more eggs than queens without access to exuviae, especially in low nitrogen soils.
Fixing nitrogen from the air
Whilst subterranean termites access nitrogen through eating exuviae and soil, drywood termites have limited access to nitrogen as they generally do not have access to soil. However, drywood termites have the ability to fix (obtain) nitrogen from the atmosphere. Measuring nitrogenase expression as an indicator of the level of nitrogen fixation from the atmosphere, researchers found that nitrogenase expression was four times higher in the drywood termite Cryptotermes brevis than in the subterranean termite Coptotermes formosanus.7 The fixation of nitrogen is essential for drywood termites, particularly during colony growth.
Understanding the termite gut
The termite gut microbiome is a critical component to the success of termites, allowing them to eat wood, a food source that is notoriously difficult to digest, due to the lignin and cellulose it contains. The symbiotic gut microbiome includes archaea, bacteria and (in the case of lower termites) cellulolytic flagellates. Many of these microbes are only found in the termite gut and are passed between generations, vertically and horizontally, through proctodeal feeding. This is because termites are not born with gut microbes and they also lose the whole gut microbiome every time they moult.
Much of the work in understanding the termite gut microbiome has focused on the guts of the pest termite species. Researchers have now completed an in-depth study, characterising the gut microbiome of 145 species representative of termite diversity.8
The research concluded that the composition and function of the termite gut prokaryotic communities has been remarkably conserved since termites first appeared. Although there are some variations in the proportions of microbes, the gut microbiota of all termites possess similar genes for carbohydrate and nitrogen metabolism. They also observed that the current classification of termites largely matches the observed variations in gut bacterial community.
The world’s smallest bioreactor
Sustainability is a core consideration in many industries and the development of renewable biofuels is a significant area of research. Biodiesel is a renewable fuel that can be produced from a range of organic and renewable feedstock including fresh or vegetable oils, animal fats, and oilseed plants. However, there is also another waste stream with potential to be a feedstock for biofuels: lignin-based aromatic waste polymers from agriculture and the textile industry. Lignin-based materials are notoriously difficult to break down. However, termites, with their symbiotic gut microbiome, are one of the few animals to break down lignin (a key component of wood). Indeed, the termite gut has been called “the world’s smallest bioreactor” by Prof Andreas Brune from the Max Planck Institute for Terrestrial Microbiology. As a result, the termite gut microbiome is the focus of significant research in the biofuels and waste management/recycling industries.
Although much of the termite gut research has focused on bacteria, a wide range of other microbes are present, including yeast. A number of interesting discoveries have recently been made in this area. For example, researchers have isolated a number of yeasts that appear to be very efficient in converting aromatics into lipids, which are then used to produce biofuels.9
It also appears that yeasts from termite guts have the potential to solve the significant environmental issue of waste plastics. Researchers have discovered that a number of yeasts isolated from termite guts produce high levels of LDPE-degrading enzymes and appear to have potential in the biodegradation of plastics, in particular low-density polyethylene (LDPE).10
References
1 Moran, Megan & Aguero, Carlos & Eyer, Pierre-André & Vargo, Edward. (2022). Rescue Strategy in a Termite: Workers Exposed to a Fungal Pathogen Are Reintegrated Into the Colony. Frontiers in Ecology and Evolution. 10. 10.3389/fevo.2022.840223.
2 Chen, Yong & Zhao, Chongwen & Zeng, Wenhui & Wu, Wenjing & Zhang, Shijun & Zhang, Dandan & Li, Zhi-Qiang. (2022). The effect of ergosterol on the allogrooming behavior of termites in response to the entomopathogenic fungus Metarhizium anisopliae. Insect Science. 30. 10.1111/1744-7917.13055.
3 Zeng, Wenhui & Shen, Danni & Chen, Yong & Zhang, Shijun & Wu, Wenjing & Li, Zhi-Qiang. (2022). A High Soldier Proportion Encouraged the Greater Antifungal Immunity in a Subterranean Termite. Frontiers in Physiology. 13. 10.3389/fphys.2022.906235.
4 Bulmer, Mark & Franco, Bruno & Biswas, Aditi & Greenbaum, Samantha. (2023). Overcoming Immune Deficiency with Allogrooming. Insects. 14. 128. 10.3390/insects14020128.
5 Tong, Reina & Choi, Eun-Kyung & Ugarelli, Kelly & Chouvenc, Thomas & Su, Nan-Yao. (2023). Trophic Path of Marked Exuviae Within Colonies of Coptotermes gestroi (Blattodea: Rhinotermitidae). Journal of insect science (Online). 23. 10.1093/jisesa/iead007.
6 Tong, Reina & Patel, Jayshree & Gordon, Johnalyn & Lee, Sang-Bin & Chouvenc, Thomas & Su, Nan-Yao. (2023). Exuviae Recycling Can Enhance Queen Oviposition and Colony Growth in Subterranean Termites (Blattodea: Rhinotermitidae: Coptotermes). Environmental entomology. 52. 10.1093/ee/nvad009.
7 Mullins, Aaron & Scheffrahn, Rudolf & Su, Nan-Yao. (2022). Nitrogen Inventories and Nitrogenase Expression Rates of a Drywood and a Subterranean Termite. Annals of the Entomological Society of America. 115. 10.1093/aesa/saac014.
8 Arora, Jigyasa & Kinjo, Yukihiro & Šobotník, Jan & Buček, Aleš & Clitheroe, Crystal-Leigh & Stiblík, Petr & Roisin, Yves & Žifčáková, Lucia & Park, Yung Chul & Kim, Ki & Sillam-Dussès, David & Hervé, Vincent & Lo, Nathan & Tokuda, Gaku & Brune, Andreas & Bourguignon, Thomas. (2022). The functional evolution of termite gut microbiota. Microbiome. 10. 10.1186/s40168-022-01258-3.
9 Ali, Sameh & Altohamy, Rania & Mohamed, Tarek & Mahmoud, Yehia & Ruiz, Héctor & Sun, Lushan (Sarina) & Sun, Jianzhong. (2022). Could termites be hiding a goldmine of obscure yet promising yeasts for energy crisis solutions based on aromatic wastes? A critical state-of-the-art review. Biotechnology for Biofuels and Bioproducts. 15. 10.1186/s13068-022-02131-z.
10 Elsamahy, Tamer & Sun, Jianzhong & Elsilk, Sobhy & Ali, Sameh. (2023). Biodegradation of low-density polyethylene plastic waste by a constructed tri-culture yeast consortium from wood-feeding termite: Degradation mechanism and pathway. Journal of Hazardous Materials. 448. 130944. 10.1016/j.jhazmat.2023.130944.
Termite antennae
With chemical communication integral to termite behaviour, it begs the question as to whether there are any differences in the antennae between the different termite castes. Researchers have recently characterised the antennae of alates, soldiers and workers in Coptotermes formosanus.1 They determined that the antennae of alates were longer than those in soldiers and workers, had more segments and twice as many antennal sensilla (sensory receptors). There was very little difference in the sensilla composition between males and females or between workers and soldiers. However, all termite castes had the same nine types of sensilla.
The researchers related variations in the abundance of the different sensilla types to the various behaviours of the castes. For example, workers had a sensilla mix that relates to their need to be more responsive to changes in humidity and temperature. They also noted that relative to body length, the soldiers had the longest antennae, which may help them perceive information from a relatively wider range, which could be beneficial in defence behaviours.
Also, alates had a great abundance of chemosensilla at the end of their antennae, which would make them more sensitive to environmental odours. This makes sense, as they need increased sensory awareness when in the open during the alate flight and pairing. However, it is interesting to note that antennal cropping, where the ends of the antennae are intentionally removed, has been recorded in dealates. The ends of the antennae are either self-cropped or removed by their partner. It is hypothesised that this behaviour reduces pheromonal sensitivity, which would align with the lower levels of sensitivity required in the enclosed nest environment rather than in the open.
Geomagnetic orientation
Whilst many will be aware that pheromones are a key element of communication in termites, the involvement of geomagnetic fields in orientation and navigation is only just coming to light. Working with both Reticulitermes chinensis and Odontotermes formosanus, researchers have established that both species show a directional preference to the geomagnetic field under both light conditions and complete darkness.2 The researchers concluded that geomagnetic fields play an important role in termite orientation, especially when trail pheromones cannot provide a precise direction.
References
1 Castillo, Paula & Le, Nathan & Sun, Qian. (2021). Comparative Antennal Morphometry and Sensilla Organization in the Reproductive and Non- Reproductive Castes of the Formosan Subterranean Termite. Insects. 12. 576. 10.3390/insects12070576.
2 Gao, Yong & Wen, Ping & Cardé, Ring & Huan, Xu & Huang, Qiuying. (2021). In addition to cryptochrome 2, magnetic particles with olfactory co-receptor are important for magnetic orientation in termites. Communications Biology. 4. 1121. 10.1038/s42003-021-02661-6.
Further reading:
General information on termites
