Dissemination of Fusarium proliferatum by mealworm beetle Tenebrio molitor

Abstract

BackgroundPlant pathogenic fungi of the genus Fusarium infect a wide array of crops and produce numerous health-threatening mycotoxins. Recently, we found that larvae of the common pest of stored products Tenebrio molitor preferably fed on grains colonized with Fusarium proliferatum. We draw the hypothesis that the increased attractiveness of infected grains for mealworms facilitates dispersal of the fungus. In this work we examined the dissemination of F. proliferatum and further Fusarium spp. by adults of T. molitor.ResultsMealworm beetle Tenebrio molitor transmitted Fusarium species F. avenaceum, F. culmorum, F. poae, and F. proliferatum to wheat grains with varying efficiency. F. proliferatum was disseminated most efficiently: 20 days after feeding on Fusarium cultures, the beetles still transmitted F. proliferatum to most grains exposed to feeding. The transmission of F. culmorum gradually declined over time and the transmission of the other Fusarium spp. ceased completely 20 d after beetles feeding of fungal cultures. Propagules of F. proliferatum and F. culmorum were traceable in beetles' feces for 20 days while no colonies of F. poae and F. avenaceum were detectable after 5 days. Because F. proliferatum was transmitted by mealworms most efficiently, this species was further investigated. Mealworm beetles T. molitor preferred feeding on grains colonized with F. proliferatum as compared to uninfected grains. Male beetles infected with F. proliferatum transmitted the fungus by copulation.ConclusionsEfficient dissemination of F. proliferatum by mealworm beetle together with the feeding preference of the beetle for grains colonized with F. proliferatum show that the chemical phenotype of the fungus responsible for the enhanced attractiveness of infected grains is subjected to positive selection. This indicates that adaptation of F. proliferatum to transmission by insects involved an alteration of insects' feeding preferences.

A Systematic Review of the Behavioral Responses by Stored-Product Arthropods to Individual or Blends of Microbially Produced Volatile Cues

“…A positive association was found between the survival rate of R. dominica and S. oryzae in grain and aflatoxin levels [ 57 ]. Propagules of F. proliferatum and F. culmorum were traceable in T. molitor feces 20 days after feeding [ 45 ]. Even the ham mite, T. putrescentiae, was found to disseminate Fusarium spp.…”

“…For example, there may be innate attraction or repulsion to some compounds [27], learning of habitat cues from the natal environment [44], or physiological constraints in the response of a given taxon to a particular MVOC. In the possible behavioral manipulation of stored-product arthropods by microbes, others have hypothesized that T. molitor may be preferentially attracted to infected kernels with Fusarium, because it facilitates dispersal of the fungus, and the chemical phenotype in the fungus responsible for attraction was found to be under positive selection [45]. Further studies should determine how widespread possible behavioral manipulation of stored-product arthropods is by microbes found on grain.…”

Products Derived from Buchenavia tetraphylla Leaves Have In Vitro Antioxidant Activity and Protect Tenebrio molitor Larvae against Escherichia coli-Induced Injury

“…These samples were selected to be evaluated in a model of stress induced by heat-killed E. coli in T. molitor larvae. This insect has been used as a model organism in studies of microbial pathogenesis and drug development (antimicrobial, antivirulence, and immunomodulator agents) [27][28][29]. Several factors have supported the use of this animal.…”

Feeding study for the mycotoxin zearalenone in yellow mealworm (Tenebrio molitor) larvae—investigation of biological impact and metabolic conversion

“…In turn, the increased feeding preference might be due to the specific capability of Fusarium strains to actively attract T. molitor . The larvae have been shown to enhance the dissemination of F. proliferatum by carrying the fungus in the digestive tract or adherent to the larval body (Guo et al 2018). Our study is also in line with van Broekhoven et al (2017) who could show that not the spiked mycotoxin alone but only naturally contaminated grain material possesses additional attractiveness for the larvae (Van Broekhoven et al 2017).…”