Nest sanitation through defecation: antifungal properties of wood cockroach feces

Abstract

The wood cockroach Cryptocercus punctulatus nests as family units inside decayed wood, a substrate known for its high microbial load. We tested the hypothesis that defecation within their nests, a common occurrence in this species, reduces the probability of fungal development. Conidia of the entomopathogenic fungus, Metarhizium anisopliae, were incubated with crushed feces and subsequently plated on potato dextrose agar. Relative to controls, the viability of fungal conidia was significantly reduced following incubation with feces and was negatively correlated with incubation time. Although the cockroach's hindgut contained abundant β-1,3-glucanase activity, its feces had no detectable enzymatic function. Hence, these enzymes are unlikely the source of the fungistasis. Instead, the antifungal compound(s) of the feces involved heat-sensitive factor(s) of potential microbial origin. When feces were boiled or when they were subjected to ultraviolet radiation and subsequently incubated with conidia, viability was "rescued" and germination rates were similar to those of controls. Filtration experiments indicate that the fungistatic activity of feces results from chemical interference. Because Cryptocercidae cockroaches have been considered appropriate models to make inferences about the factors fostering the evolution of termite sociality, we suggest that nesting in microbe-rich environments likely selected for the coupling of intranest defecation and feces fungistasis in the common ancestor of wood cockroaches and termites. This might in turn have served as a preadaptation that prevented mycosis as these phylogenetically related taxa diverged and evolved respectively into subsocial and eusocial organizations.

Symbiont-derived β-1,3-glucanases in a social insect: mutualism beyond nutrition

“…The benefits derived from harboring an intact gut microbiome (along with the functional β-1,3GLUs) can be also appreciated at the communal level. Because termites use their liquid and solid feces in nest construction (Rosengaus et al, 1998b) and given that the liquid feces have β-1,3GLU activity [ Figure 1A , but not the fecal pellets (Rosengaus et al, 2013)], the excretion and incorporation of β-1,3GLUs from the liquid feces into the termite’s nest structure likely expands mycosis protection to the entire colony. Although previous research has demonstrated that termite feces have potent antifungal properties (Rosengaus et al, 1998b; Chouvenc et al, 2013) and that Actinobacteria may be responsible for such negative effects (Chouvenc et al, 2013), no information exists on whether microbes colonizing the termite fecal pellets produce β-1,3GLUs.…”

“…Cryptocercus punctulatus, the closest extant roach relative of termites (Nalepa and Bandi, 2000; Lo and Eggleton, 2011), also contains β-1,3GLU activity in its hindgut (Bulmer et al, 2012) and its liquid feces (Rosengaus et al, 2013). They also share many of the same gut microbiota with termites (Brune, 2014).…”

Social immunity and the evolution of group living in insects

“…Table adapted from Cremer et al [7], which also contains information on whether these defences are prophylactic or induced. References of frass as nest material has been shown to limit parasite development [46,47,[49][50][51]. The maintenance of frass in the nest may also provide immune benefits by allowing exchanges of endosymbionts and other immune factors among group members.…”

Probiotic Enterococcus mundtii Isolate Protects the Model Insect Tribolium castaneum against Bacillus thuringiensis

“…Birds can transfer their microbes via the eggshell or regurgitation (Godoy-Vitorino et al, 2010; Ruiz-De-Castañeda et al, 2011; Kohl, 2012), and insects can transfer beneficial microbes by trophallaxis or coprophagy (Koch and Schmid-Hempel, 2011; Engel and Moran, 2013; Brune and Dietrich, 2015). Insect feces are not only relevant for microbial transmission but they also fulfill a protective function (Rosengaus et al, 2013; Diehl et al, 2015). This is particularly relevant in the case of storage pests, which defecate and live in the same environment.…”