Links Between Feeding Preferences and Electroantennogram Response Profiles in Dung Beetles: The Importance of Dung Odor Bouquets

Abstract

The detection of dung odors is a crucial step in the food-searching behavior of dung beetles (Coleoptera: Scarabaeoidea). Yet, whether certain compounds characteristic of a given dung type contribute to a ‘choosy generalism’ behavior proposed for this taxonomic group is unknown. To address this, we analyzed the chemical composition of three types of dung (cow, horse, and rabbit) and conducted behavioral and electroantennogram (EAG) bioassays on 15 species of dung beetles using 19 volatile organic compounds representing the three dung samples. Chemical analyses revealed substantial qualitative and quantitative differences among dung types. When offered these food options in an olfactometer, 14 species exhibited a feeding preference. Surprisingly, all 19 compounds used in the EAG assays elicited antennal responses, with species displaying different olfactory profiles. The relationship between behavioral preferences and electrophysiological profiles highlighted that species with different food preferences had differences in antennal responses. Moreover, a specific set of EAG-active compounds (nonanal, sabinene, acetophenone, ρ-cresol, 2-heptanone, 1H-indole, and 6-methyl-5-hepten-2-one) were the strongest drivers in the distinct sensory profiles of the trophic preference groups. Our results point to the importance of the whole bouquet of dung-emanating compounds in driving food-searching behavior, but specific volatiles could aid in determining highly marked trophic preferences in certain species.

Analysing the effect of ivermectin on the volatile organic compounds of dung and its possible influence on attraction to dung beetles

“…Considering the important chemosensory interaction that dung beetles have with an ephemeral resource like dung via their olfactory system (Cortez et al, 2016;Inouchi et al, 1988;Riffell, 2012), the absence of a significant difference in T A B L E 2 Chemical profiles of dung volatile emissions of different dung types analysed by gas chromatography-mass spectrometry. the chemical profile of the volatile compounds emitted by the treatments with IVM would explain the similar behavioural responses exhibited by the model species (Urrutia et al, 2022). In at least half of the studies analysed in Table 1, no concrete difference in attraction was verified between cattle dung from treated and non-treated animals, despite the diverse methods of IVM application and methodologies employed in their observations.…”

“…The olfactometer bioassays demonstrated that no significant differences in the attraction of the dung beetle A. cicatricosus to the different dung samples from untreated cattle (control), treated cattle and IVM‐spiked occur. Considering the important chemosensory interaction that dung beetles have with an ephemeral resource like dung via their olfactory system (Cortez et al, 2016; Inouchi et al, 1988; Riffell, 2012), the absence of a significant difference in the chemical profile of the volatile compounds emitted by the treatments with IVM would explain the similar behavioural responses exhibited by the model species (Urrutia et al, 2022). In at least half of the studies analysed in Table 1, no concrete difference in attraction was verified between cattle dung from treated and non‐treated animals, despite the diverse methods of IVM application and methodologies employed in their observations.…”

“…It is important to note that some of the VOCs identified in these chemical profiles have been previously observed. For example, p‐cresol, skatole, phenol and 1H‐indole are some of the most frequently cited dung volatile compounds in olfactory studies on dung beetles (Dormont et al, 2010; Frank et al, 2018; Inouchi et al, 1988; Stavert et al, 2014; Urrutia et al, 2022; Wurmitzer et al, 2017). This result supports the hypothesis that IVM does not modify the VOCs emitted by cattle dung, coinciding with some results observed in other studies (see Table 1).…”

“…However, chemical analyses of the dung types have not been performed to ascertain whether a marked difference was found and whether this difference could explain the observed results in attraction. What is probable is that a difference in attraction between the dung types could be associated with a difference in their chemical makeup that would provide the beetles with the necessary cues on the type and condition of the resource (Dormont et al, 2010; Frank et al, 2018; Urrutia et al, 2022; Wurmitzer et al, 2017). Likewise, in studies that have found mixed results in attraction (Dadour et al, 1999; Floate, 2007; Römbke et al, 2010), the absence of a chemical analysis of the dung types utilised prevents a clear answer to this important question.…”

“…Unfortunately, to date, none of the hypotheses has been tested by appropriate methodologies that truly analyse dung beetle attraction and selection behaviour. It is for this reason that the need to discover if IVM causes a change in the chemical composition of dung volatile emissions is a crucial step to understanding the complex chemosensory interaction that dung beetles have with their trophic resource (Dormont et al, 2010;Inouchi et al, 1987Inouchi et al, , 1988Shibuya & Inouchi, 1982;Urrutia et al, 2022;Weithmann et al, 2020) and how this natural form of information processing could be altered by the application of an endectocide that is known for its detrimental effects at various scales.…”