Termite mound architecture regulates nest temperature and correlates with species identities of symbiotic fungi

BACKGROUND: Large 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. OBJECTIVES: In 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. METHODS: External 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. 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 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.