Social insects nesting in soil environments are in constant contact with entomopathogens but have evolved a range of defence mechanisms, resulting in both individual and social immunity that reduce the chance for epizootics in the colony, as in the case of subterranean termites. Coptotermes formosanus uses its faeces as building material for its nest structure that result into a ‘carton material’, and here, we report that the faecal nest supports the growth of Actinobacteria which provide another level of protection to the social group against entomopathogens. A Streptomyces species with in vivo antimicrobial activity against fungal entomopathogens was isolated from the nest material of multiple termite colonies. Termite groups were exposed to Metarhizium anisopliae, a fungal entomopathogen, during their foraging activity and the presence of Streptomyces within the nest structure provided a significant survival benefit to the termites. Therefore, this report describes a non-nutritional exosymbiosis in a termite, in the form of a defensive mutualism which has emerged from the use of faecal material in the nesting structure of Coptotermes. The association with an Actinobacteria community in the termite faecal material provides an extended disease resistance to the termite group as another level of defence, in addition to their individual and social immunity.

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Subterranean termites such as Coptotermes formosanus Shiraki inhabit underground nests consisting of a complex network of galleries resulting in a highly modified environment relative to the surrounding soils. A healthy colony can maintain homeostatic conditions within the nest, limiting opportunities for pathogens, parasites, and predators to exploit the termite colony as a resource. However, a stressed or senescent colony can display a lack of nest maintenance, leading to the colonization of the nest as an opportunistic niche by other organisms. In this study, we described the nest colonization by microbes and arthropods during the collapse of three dying C. formosanus laboratory colonies. The carton nest and the tunnel lining that are mostly made out of termite fecal material were invaded by a variety of fungi, and Acari and Collembolan populations quickly increased during the senescence phase of the termite colony, presumably scavenging on the fungal material. Finally, the carton colonized by fungal mycelia hosted numerous larvae of a sciarid fly, Bradysia sp. (Diptera). This fungus gnat used the decomposing carton material as a breeding site, and numerous adults of this fly were found hovering above the dying termite colony. Bradysia larvae also showed infestation by parasitic nematodes, suggesting the presence of multiple trophic levels in the resource utilization of the nest of a declining termite colony. We concluded that a dying subterranean colony represents a resource opportunity for scavenging organisms and that the nest structure represents an opening niche that initiates an ecological succession.

Subterranean termites live in large groups in underground nests where the pathogenic pressure of the soil environment has led to the evolution of a complex interaction among individual and social immune mechanisms in the colonies. However, groups of termites under stress can show increased susceptibility to opportunistic parasites. In this study, an isolate of Aspergillus nomius Kurtzman, Horn & Hessltine was obtained from a collapsed termite laboratory colony. We determined that it was primarily a saprophyte and, secondarily, a facultative parasite if the termite immunity is undergoing a form of stress. This was determined by stressing individuals of the Formosan subterranean termite Coptotermes formosanus Shiraki via a co-exposure to the virulent fungal parasite Metarhizium anisopliae (Metch.) Sorokin. We also examined the dynamics of a mixed infection of A. nomius and M. anisopliae in a single termite host. The virulent parasite M. anisopliae debilitated the termite immune system, but the facultative, fast growing parasite A. nomius dominated the mixed infection process. The resource utilization strategy of A. nomius during the infection resulted in successful conidia production, while the chance for M. anisopliae to complete its life cycle was reduced. Our results also suggest that the occurrence of opportunistic parasites such as A. nomius in collapsing termite laboratory colonies is the consequence of a previous stress, not the cause of the stress.