Risto Vesala

Termites are pivotal ecosystem engineers in African savanna ecosystems where they significantly contribute to nutrient cycling and facilitate the success of many other organisms. Termites can also introduce atmospheric nitrogen into terrestrial cycling via symbiotic nitrogen‐fixing gut bacteria and potentially through fungus gardens maintained by the fungus‐growing (Macrotermitinae) species. In termite fungus gardens, a variety of microorganisms, including the symbiotic Termitomyces fungus and various bacteria, break down lignocellulose and recycle organic nitrogen from dead plant matter. However, the specific roles of these fungal and bacterial symbionts in the nutrition of termite hosts are not yet fully understood. Here, we investigate nutritional interactions between Kenyan Macrotermes michaelseni termites and their symbiotic fungi and bacteria using compound‐specific stable isotope analyses (δ¹³C and δ¹⁵N) of amino acids (CSIA‐AA). Microbial resource utilization varies across termite castes. Essential amino acids (EAAs) in eggs and larvae primarily originate from fungi (50%–67%), whereas bacterial contributions are most pronounced in workers (22%) and soldiers (16%–24%). The amino acid δ¹⁵N patterns indicate that biological nitrogen fixation occurs in both termite guts and their fungus gardens, and the fixed nitrogen heavily affects the amino acid δ¹⁵N values, especially in eggs and larvae. Concurrently, the relatively modest proportion of bacterially synthesized EAAs in the eggs and larvae (<11%) suggests that the fixed ammonium is largely assimilated into amino acids within fungal or termite host cells. These findings underscore the intricate collaborative interactions among bacterial, fungal and insect metabolisms that support the protein supply within this symbiotic system. These interactions may have broader implications for introducing novel atmospheric nitrogen into nutrient‐deficient savanna ecosystems. Read the free Plain Language Summary for this article on the Journal blog.

Termites are a significant natural source of greenhouse gases (GHGs), but quantifying emissions especially from large termite mounds is problematic as they rarely fit in measurement chambers. Predicting fluxes based on internal and atmospheric concentrations could provide an indirect way to assess mound emissions, but developing such models necessitates better understanding of the concentration levels and their variance. We used gas chromatography to measure carbon dioxide (CO ₂ ), methane (CH ₄ ) and nitrous oxide (N ₂ O) concentrations within nests of two co‐occurring species of fungus‐growing termites in both dry and wet seasons in Kenya, with termite Macrotermes michaelseni building mounds with a closed and Macrotermes subhyalinus with an open ventilation system. Gas concentrations were 3–100 times higher in mounds than the global averages in atmosphere, implying that termite mounds are sources of all three GHGs. Carbon dioxide concentrations were higher in closed than in open mounds. Methane concentrations remained constant in open mounds, whereas closed mounds exhibited considerable variation between nests and across seasons. Concentrations of both CH ₄ and N ₂ O correlated positively with mound volume during the wet season, whereas interactions with mound size were not observed in CO ₂ concentrations or during the driest sampling period. These findings underline that among fungus‐growing termites, mound size, ventilation type and precipitation affect nest gas concentrations and with this likely the magnitude of mound GHG emissions. Potential reasons behind the observed relationships are discussed, including differences in population size, biomass of fungus gardens and CH ₄ oxidation.

Fungus‐growing termites and their symbiotic Termitomyces fungi are critically important carbon and nutrient recyclers in arid and semiarid environments of sub‐Saharan Africa. A major proportion of plant litter produced in these ecosystems is decomposed within nest chambers of termite mounds, where temperature and humidity are kept optimal for the fungal symbionts. While fungus‐growing termites are generally believed to exploit a wide range of different plant substrates, the actual diets of most species remain elusive. We studied dietary niches of two Macrotermes species across the semiarid savanna landscape in the Tsavo Ecosystem, southern Kenya, based on carbon (C) and nitrogen (N) stable isotopes in Termitomyces fungus combs. We applied Bayesian mixing models to determine the proportion of grass and woody plant matter in the combs, these being the two major food sources available for Macrotermes species in the region. Our results showed that both termite species, and colonies cultivating different Termitomyces fungi, occupied broad and largely overlapping isotopic niches, indicating no dietary specialization. Including laser scanning derived vegetation cover estimates to the dietary mixing model revealed that the proportion of woody plant matter in fungus combs increased with increasing woody plant cover in the nest surroundings. Nitrogen content of fungus combs was positively correlated with woody plant cover around the mounds and negatively correlated with the proportion of grass matter in the comb. Considering the high N demand of large Macrotermes colonies, woody plant matter seems to thus represent a more profitable food source than grass. As grass is also utilized by grazing mammals, and the availability of grass matter typically fluctuates over the year, mixed woodland‐grasslands and bushlands seem to represent more favorable habitats for large Macrotermes colonies than open grasslands.

Fungus-growing termites of the genusMacrotermescultivate symbiotic fungi (Termitomyces) in their underground nest chambers to degrade plant matter collected from the environment. Although the general mechanism of food processing is relatively well-known, it has remained unclear whether the termites get their nutrition primarily from the fungal mycelium or from plant tissues partly decomposed by the fungus. To elucidate the flows of carbon and nitrogen in the complicated food-chains within the nests of fungus-growing termites, we determined the stable isotope signatures of different materials sampled from fourMacrotermescolonies in southern Kenya. Stable isotopes of carbon revealed that the termite queen and the young larvae are largely sustained by the fungal mycelium. Conversely, all adult workers and soldiers seem to feed predominantly on plant and/or fungus comb material, demonstrating that the fungal symbiont plays a different nutritional role for different termite castes. Nitrogen stable isotopes indicated additional differences between castes and revealed intriguing patterns in colony nitrogen cycling. Nitrogen is effectively recycled within the colonies, but also a presently unspecified nitrogen source, most likely symbiotic nitrogen-fixing bacteria, seems to contribute to nitrogen supply. Our results indicate that the gut microbiota of the termite queen might be largely responsible for the proposed nitrogen fixation.

Background: Large and complex mounds built by termites of the genusMacrotermescharacterize many dry African landscapes, including the savannas, bushlands, and dry forests of the Tsavo Ecosystem in southern Kenya. The termites live in obligate symbiosis with filamentous fungi of the genusTermitomyces. The insects collect dead plant material from their environment and deposit it into their nests where indigestible cell wall compounds are effectively decomposed by the fungus. Above-ground mounds are built to enhance nest ventilation and to maintain nest interior microclimates favorable for fungal growth.Objectives: In Tsavo Ecosystem twoMacrotermesspecies associate with three differentTermitomycessymbionts, always with a monoculture of one fungal species within each termite nest. As mound architecture differs considerably both between and within termite species we explored potential relationships between nest thermoregulatory strategies and species identity of fungal symbionts.Methods: External dimensions were measured from 164Macrotermesmounds and the cultivatedTermitomycesspecies were identified by sequencing internal transcribed spacer (ITS) region of ribosomal DNA. We also recorded the annual temperature regimes of several termite mounds to determine relations between mound architecture and nest temperatures during different seasons.Results: Mound architecture had a major effect on nest temperatures. Relatively cool temperatures were always recorded from large mounds with open ventilation systems, while the internal temperatures of mounds with closed ventilation systems and small mounds with open ventilation systems were consistently higher. The distribution of the three fungal symbionts in different mounds was not random, with one fungal species confined to “hot nests.”Conclusions: Our results indicate that differentTermitomycesspecies have different temperature requirements, and that one of the cultivated species is relatively intolerant of low temperatures. The dominantMacrotermesspecies in our study area can clearly modify its mound architecture to meet the thermal requirements of several different symbionts. However, a treacherous balance seems to exist between symbiont identity and mound architecture, as the maintenance of the thermophilic fungal species obviously requires reduced mound architecture that, in turn, leads to inadequate gas exchange. Hence, our study concludes that while the limited ventilation capacity of small mounds sets strict limits to insect colony growth, in this case, improving nest ventilation would invariable lead to excessively low nest temperatures, with negative consequences to the symbiotic fungus.