Compass Cue Integration and Its Relation to the Visual Ecology of Three Tribes of Ball-Rolling Dung Beetles

Abstract

To guide their characteristic straight-line orientation away from the dung pile, ball-rolling dung beetles steer according to directional information provided by celestial cues, which, among the most relevant are the sun and polarised skylight. Most studies regarding the use of celestial cues and their influence on the orientation system of the diurnal ball-rolling beetle have been performed on beetles of the tribe Scarabaeini living in open habitats. These beetles steer primarily according to the directional information provided by the sun. In contrast, Sisyphus fasciculatus, a species from a different dung-beetle tribe (the Sisyphini) that lives in habitats with closely spaced trees and tall grass, relies predominantly on directional information from the celestial pattern of polarised light. To investigate the influence of visual ecology on the relative weight of these cues, we studied the orientation strategy of three different tribes of dung beetles (Scarabaeini, Sisyphini and Gymnopleurini) living within the same biome, but in different habitat types. We found that species within a tribe share the same orientation strategy, but that this strategy differs across the tribes; Scarabaeini, living in open habitats, attribute the greatest relative weight to the directional information from the sun; Sisyphini, living in closed habitats, mainly relies on directional information from polarised skylight; and Gymnopleurini, also living in open habitats, appear to weight both cues equally. We conclude that, despite exhibiting different body size, eye size and morphology, dung beetles nevertheless manage to solve the challenge of straight-line orientation by weighting visual cues that are particular to the habitat in which they are found. This system is however dynamic, allowing them to operate equally well even in the absence of the cue given the greatest relative weight by the particular species.

Weighted cue integration for straight-line orientation

“…Furthermore, when the two cues were returned to their original positions, the beetles recovered their initial bearing (see STAR Methods, Quantification and statistical analysis - Cue conflict between an ersatz sun and wind ), suggesting that this new random bearing we see is actually an effect of the integration strategy and not a permanent re-set of the bearing. Similarly, Khaldy et al. (2021) showed that the ball-rolling dung beetles Garreta unicolor and Garreta nitens appeared disoriented when subjected to a conflict produced by simultaneous manipulation of a sun cue and the pattern of polarized light.…”

“…Cue integration is the process whereby an agent combines multiple sensory estimates of the world to perform a single action ( Ernst and Bülthoff, 2004 ). Most explorations of cue integration stem from human psychophysical experiments ( Ernst and Banks, 2002 ; Alais and Burr, 2004 ), but many examples of cue integration have been found throughout the animal kingdom from monkeys ( Fetsch et al., 2012 ), to rodents ( Knight et al., 2014 ), to insects ( Legge et al., 2014 ; Wystrach et al., 2015 ; Hoinville and Wehner, 2018 ; Dreyer et al., 2018 ; Dacke et al., 2014 , 2019 ; Müller and Wehner, 2007 ; Collett, 2012 ; Khaldy et al., 2021 ; Wehner et al., 2016 ).…”

Varieties of visual navigation in insects

“…A third tribe, Gymnopleurini , also lives in open habitats but weights sun and polarised light equally. In a comparative study, Khaldy et al ( 2021 ) collected beetles from these three tribes and tested their orientation strategies. Individuals within each tribe showed similar cue weighting but the tribes differed from each other and matched the patterns seen in their respective natural habitats.…”

Weighted cue integration for straight-line orientation

“…Furthermore, when the two cues were returned to their original positions, the beetles recovered their initial bearing (see STAR Methods, Quantification and statistical analysis -Cue conflict between an ersatz sun and wind), suggesting that this new random bearing we see is actually an effect of the integration strategy and not a permanent re-set of the bearing. Similarly, Khaldy et al (2021) showed that the ball-rolling dung beetles Garreta unicolor and Garreta nitens appeared disoriented when subjected to a conflict produced by simultaneous manipulation of a sun cue and the pattern of polarized light. However, upon returning the cues to their original positions, these animals recovered their initial bearings.…”

“…Cue integration is the process whereby an agent combines multiple sensory estimates of the world to perform a single action (Ernst and Bu ¨lthoff, 2004). Most explorations of cue integration stem from human psychophysical experiments (Ernst and Banks, 2002;Alais and Burr, 2004), but many examples of cue integration have been found throughout the animal kingdom from monkeys (Fetsch et al, 2012), to rodents (Knight et al, 2014), to insects (Legge et al, 2014;Wystrach et al, 2015;Hoinville and Wehner, 2018;Dreyer et al, 2018;Dacke et al, 2014Dacke et al, , 2019Mu ¨ller and Wehner, 2007;Collett, 2012;Khaldy et al, 2021;Wehner et al, 2016).…”