Fungus‐growing termites of the subfamily Macrotermitinae together with their highly specialized fungal symbionts (Termitomyces) are primary decomposers of dead plant matter in many African savanna ecosystems. The termites provide crucial ecosystem services also by modifying soil properties, translocating nutrients, and as important drivers of plant succession. Despite their obvious ecological importance, many basic features in the biology of fungus‐growing termites and especially their fungal symbionts remain poorly known, and no studies have so far focused on possible habitat‐level differences in symbiont diversity across heterogeneous landscapes. We studied the species identities of Macrotermes termites and their Termitomyces symbionts by excavating 143 termite mounds at eight study sites in the semiarid Tsavo Ecosystem of southern Kenya. Reference specimens were identified by sequencing the COI region from termites and the ITS region from symbiotic fungi. The results demonstrate that the regional Macrotermes community in Tsavo includes two sympatric species (M. subhyalinus and M. michaelseni) which cultivate and largely share three species of Termitomyces symbionts. A single species of fungus is always found in each termite mound, but even closely adjacent colonies of the same termite species often house evolutionarily divergent fungi. The species identities of both partners vary markedly between sites, suggesting hitherto unknown differences in their ecological requirements. It is apparent that both habitat heterogeneity and disturbance history can influence the regional distribution patterns of both partners in symbiosis.
BackgroundLarge and complex mounds built by termites of the genus Macrotermes characterize 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 genus Termitomyces. 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.ObjectivesIn Tsavo Ecosystem two Macrotermes species associate with three different Termitomyces symbionts, 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.MethodsExternal dimensions were measured from 164 Macrotermes mounds and the cultivated Termitomyces species 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.ResultsMound 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.”ConclusionsOur results indicate that different Termitomyces species have different temperature requirements, and that one of the cultivated species is relatively intolerant of low temperatures. The dominant Macrotermes species 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.
Fungus-growing termites of the genus Macrotermes cultivate 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 four Macrotermes colonies 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.
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