The properties of the visual system in the Australian desert ant Melophorus bagoti

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Abstract

The Australian desert ant Melophorus bagoti shows remarkable visual navigational skills relying on visual rather than on chemical cues during their foraging trips. M. bagoti ants travel individually through a visually cluttered environment guided by landmarks as well as by path integration. An examination of their visual system is hence of special interest and we address this here. Workers exhibit distinct size polymorphism and their eye and ocelli size increases with head size. The ants possess typical apposition eyes with about 420–590 ommatidia per eye, a horizontal visual field of approximately 150° and facet lens diameters between 8 and 19 μm, depending on body size, with frontal facets being largest. The average interommatidial angle Δϕ is 3.7°, the average acceptance angle of the rhabdom Δρrh is 2.9°, with average rhabdom diameter of 1.6 μm and the average lens blur at half-width Δρl is 2.3°. With a Δρrhϕ ratio of much less than 2, the eyes undersample the visual scene but provide high contrast, and surprising detail of the landmark panorama that has been shown to be used for navigation.

Highlights

► Compound eye and ocelli size increases with head size. ► Number of ommatidia ranges between 420 and 590 per compound eye. ► Horizontal visual field of approximately 150°. ► The average interommatidial angle of each compound eye is 3.7°. ► Compound eyes provide sufficient detail of landmark panorama for navigation.

Introduction

The most common mechanisms by which ants find their way to food sites or back to the nest are by following a scent trail, by relying on path integration and/or on landmark guidance. The primary means of navigation for ants that live in landmark-poor desert environments is path integration, a strategy that allow ants to take the shortest possible path back home after a circuitous foraging trip (Collett and Collett, 2000, Wehner, 2003). In landmark-rich environments ants rely more heavily on visual landmark information (Beugnon et al., 2001, Fukushi, 2001, Narendra, 2007b, Bregy et al., 2008). Visual landmarks are used to locate specific goals (Wehner and Räber, 1979, Collett, 1992, Macquart et al., 2006), to follow routes (Collett et al., 1992, Graham et al., 2003, Narendra, 2007b, Wystrach et al., 2010) and to determine compass directions. For both path integration and landmark guidance ants make use of a variety of compass cues: the pattern of the polarised skylight (Duelli and Wehner, 1973), the position of the sun (Wehner and Müller, 2006), the landmark panorama (Fukushi, 2001, Graham and Cheng, 2009a, Graham and Cheng, 2009b), the pattern of the canopy (Hölldobler, 1980) and possibly also the direction of the magnetic field (Çamlitepe and Stradling, 1995, Riveros and Srygley, 2008).

Foragers of the Australian desert ant Melophorus bagoti scavenge mainly for other arthropods that have fallen victim to the heat of the desert sun (Muser et al., 2005, Schultheiss et al., 2010). Individual ants leave their nest for relatively long foraging trips and locate the nest on their return with high precision. M. bagoti are visually guided ants that localise goals using landmarks (Narendra et al., 2007), follow landmark-defined routes (Kohler and Wehner, 2005, Narendra, 2007b) and use the distant landmark panorama as a compass cue (Graham and Cheng, 2009a). The extent to which they rely on visual landmarks depends on their familiarity with a scene (Narendra, 2007a, Narendra, 2007b).

Little is known, however, about the properties of the visual system in M. bagoti. As we show here, the ants possess apposition compound eyes, which are typical for insects with diurnal lifestyle (Land and Nilsson, 2002). In apposition compound eyes, light reaches the fused rhabdom to which all photoreceptor cells contribute through one individual corneal lens. The number, arrangement and dimensions of ommatidia determine the visual field and the resolution (acuity) of compound eyes.

In this study we analyse the behaviourally relevant properties of the compound eyes of M. bagoti as far as resolving power is concerned, the distribution of facet size across the eye and note the unusual presence and the external dimensions of the ocelli.

Section snippets

Materials and methods

Melophorus bagoti (Lubbock) foragers were collected from different nests about 10 km south of Alice Springs, NT. Head width, compound eye and ocelli size were measured from photographs taken with a dissection Zeiss microscope (8-32×). To determine the exact number and size distribution of facet lenses, we covered compound eyes with a thin layer of colourless nail polish to produce cornea replicas (Ribi et al., 1989). Once dry, the cornea replicas were carefully removed and flattened on a

Overview

There is a clear size polymorphism among workers of M. bagoti, with head width measuring 1.7 mm in smallest and 3.2 mm in largest workers (Christian and Morton, 1992). Workers possess two compound eyes and three ocelli. The left and right compound eye are of equal size (anterior–posterior axis: t test, p = 0.15; dorsal–ventral axis: t test, p = 0.46). However, eye size increases with head size (anterior–posterior axis: Pearson correlation test, r = 0.930, p < 0.001; dorsal–ventral axis: Pearson

Discussion

M. bagoti ants possess typical apposition compound eyes. The presence of a biconvex corneal lens, the arrangement of crystalline cones, primary and secondary pigment cells and retinula cells, which form the fused rhabdom, all resemble the basic structure of apposition compound eyes in hymenoptera (Varela and Porter, 1969, Land and Fernald, 1992, Brunnert and Wehner, 1973).

There is a distinct worker size polymorphism in M. bagoti and the dimensions of compound eyes as well as the median ocellus

Acknowledgements

We are grateful for facilities provided by the Centre for Advanced Microscopy at The Australian National University, Canberra and the ARC Centre of Excellence in Vision Science. SS was supported by a Macquarie University graduate scholarship, Sydney. AN was supported by a postdoctoral fellowship from The Australian Research Council (DP0986606). AN and JZ acknowledge additional support from the ARC Centre of Excellence in Vision Science. We thank Antoine Wystrach for providing us with the

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