Nematode-free agricultural system of a fungus-growing termite

Abstract

Fungus-growing termites forage dead plant materials from the field to cultivate symbiotic Termitomyces fungi in the nest. Termite foraging behavior and the entry of symbiotic arthropod inquilines may transfer nematodes into a nest and adversely affect fungus production. To test whether nematodes were transferred to fungus gardens by termites and inquilines, we examined the occurrence of nematodes in fungus gardens, five termite castes, and nine species of inquilines of a fungus-growing termite, Odontotermes formosanus . Our results revealed that nematodes were commonly carried by foraging termites and beetle inquilines. Numerous nematodes were found under the beetle elytra. No nematodes were found on termite larvae, eggs, and wingless inquilines. In addition, nematodes rarely occurred in the fungus garden. By observing the response of nematodes to three species of Termitomyces spp. and the fungus gardens, we confirmed that the fungus and fungus gardens are not actually toxic to nematodes. We suggest that nematodes were suppressed through grooming behavior and gut antimicrobial activity in termites, rather than through the antimicrobial activity of the fungus.

Area‐population control of fungus‐growing termite, Odontotermes formosanus, using hexaflumuron durable baits

“…66 In addition, more than 12 species of invertebrates, including minute bark beetles, rove beetles (Order: Coleoptera), fungus gnats, phorid flies (Order: Diptera), and silverfishes (Order: Thysanura), were reported to rely on the nutrition from O. formosanus or their fungus gardens. 67,68 Predictably, population suppression of fungus-growing termites would lead to the following consequences: (i) reduction of the decomposition rates of litters, and (ii) reduction of diversity of vertebrates and invertebrates in the forest ecosystem. We suggest avoiding applying termite control practices in natural forests.…”

Multipartite symbioses in fungus‐growing termites (Blattodea: Termitidae, Macrotermitinae) for the degradation of lignocellulose

“…Many symbiotic termitophiles and inquilines are also found inside termite nests (Carrijo et al ., 2012; Kanzaki et al ., 2019), especially beetles (Costa & Vanin, 2010), ants (Diehl et al ., 2005), spiders (DeVisser et al ., 2008), other termite species (da Cunha & Morais, 2010; Darlington, 2012), caterpillars, flies, mites, bugs, and millipedes (Cai et al ., 2017; Kanzaki et al ., 2019). However, the dependence of these associations may range from facultative to obligatory (Cristaldo et al ., 2012).…”

“…Recently, Kanzaki et al . (2019) assumed that the entry of symbiotic arthropods may transfer nematodes into the termite colony and affect the production of the fungus garden. Specifically, they tested the nine species of termitophiles of the fungus‐growing termite Odontotermes formosanus and found that numerous nematodes were present under the beetle elytra.…”

“…Some of the most common examples among insects include the cultivation of Polysiphonia algae by damselfish (Hata & Kato, 2006), the facilitation of invasive mealy bugs by the invasive fire ant Solenopsis invicta (Helms & Vinson, 2002), the symbiotic association between plant sap‐feeding aphids and Buchnera aphidicola (Hansen & Moran, 2011), the cultivation of fungus by ants in their colonies (Henrik et al ., 2014; Khadempour et al ., 2016; Khadempour, 2018), and the symbiotic association between mountain pine beetles, fungi, and bacteria (Boone et al ., 2013; Wang et al ., 2013). Termites are also known to have symbiotic relationships with fungi and gut microbiota (Bastien et al ., 2013; Brune, 2014; Poulsen et al ., 2014) and in some cases with other arthropods (Kanzaki et al ., 2019).…”

“…Indeed, fungus‐growing termites can degrade more than 90% of plant biomass in some areas within half an hour (Bastien et al ., 2013; Li et al ., 2017) and thus have a major impact on carbon cycling (Bonachela et al ., 2015; Pennisi, 2015). Central to the success of these termites is their mutual symbiotic association with eukaryotic and prokaryotic microorganisms (Bastien et al ., 2013; Poulsen et al ., 2014; Bourguignon et al ., 2018) as well as their commensalistic association with termitophiles/inquilines (Krikken, 2008; Kanzaki et al ., 2019). The symbiotic microbes help the host to degrade highly complex plant polysaccharides, alleviate the effect of plant defense compounds, and improve the quality of their nutrient‐poor diet (Hansen & Moran, 2014; Poulsen et al ., 2014; Pennisi, 2015).…”