Eye structure, activity rhythms, and visually-driven behavior are tuned to visual niche in ants.

Ayse Yilmaz,Yilmaz Camlitepe,Martin Giurfa,Volkan Aksoy

doi:10.3389/fnbeh.2014.00205

Abstract

Insects have evolved physiological adaptations and behavioral strategies that allow them to cope with a broad spectrum of environmental challenges and contribute to their evolutionary success. Visual performance plays a key role in this success. Correlates between life style and eye organization have been reported in various insect species. Yet, if and how visual ecology translates effectively into different visual discrimination and learning capabilities has been less explored. Here we report results from optical and behavioral analyses performed in two sympatric ant species, Formica cunicularia and Camponotus aethiops. We show that the former are diurnal while the latter are cathemeral. Accordingly, F. cunicularia workers present compound eyes with higher resolution, while C. aethiops workers exhibit eyes with lower resolution but higher sensitivity. The discrimination and learning of visual stimuli differs significantly between these species in controlled dual-choice experiments: discrimination learning of small-field visual stimuli is achieved by F. cunicularia but not by C. aethiops, while both species master the discrimination of large-field visual stimuli. Our work thus provides a paradigmatic example about how timing of foraging activities and visual environment match the organization of compound eyes and visually-driven behavior. This correspondence underlines the relevance of an ecological/evolutionary framework for analyses in behavioral neuroscience.

Highlights

Social insects constitute an established model for the study of visual perception and learning and have contributed important insights into the principles of vision and visual cognition (Menzel and Backhaus, 1991; Dafni et al, 1997; Giurfa and Menzel, 1997; Briscoe and Chittka, 2001; Srinivasan, 2010; Avarguès-Weber et al, 2011; Dyer, 2012; Zhang et al, 2012)
In the case of F. cunicularia and C. aethiops minors, activity increased during the morning, but peaks of activity differed: while F. cunicularia exhibited maximal activity around 12:00 h, C. aethiops minors reached a maximum around 10:00 AM, after which activity dropped significantly
At the time when F. cunicularia was most active, which corresponded to a great increase in illumination levels (Figures 2C,D), C. aethiops minors were less active

Summary

Introduction

Social insects constitute an established model for the study of visual perception and learning and have contributed important insights into the principles of vision and visual cognition (Menzel and Backhaus, 1991; Dafni et al, 1997; Giurfa and Menzel, 1997; Briscoe and Chittka, 2001; Srinivasan, 2010; Avarguès-Weber et al, 2011; Dyer, 2012; Zhang et al, 2012). Ant species may differ in their visual niches and light conditions and experience different selective pressures on their visual systems As a consequence, their compound eyes may exhibit adaptations to specific life styles (Greiner et al, 2007; Narendra et al, 2011) where trade-offs between spatial resolution and sensitivity are expected (Kirschfeld, 1976; Land, 1997). We studied two sympatric ant species in the northwest of Turkey, which possess apposition eyes but differ in the characteristics of their visual environments: Formica cunicularia ants are considered to be diurnal, while Camponotus aethiops ants are reported to be rather crepuscular and nocturnal (Figure 1A)

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