Visual ecology of the Australian lungfish (Neoceratodus forsteri)

Abstract

Background: The transition from water to land was a key event in the evolution of vertebrates that occurred over a period of 15-20 million years towards the end of the Devonian. Tetrapods, including all land-living vertebrates, are thought to have evolved from lobe-finned (sarcopterygian) fish that developed adaptations for an amphibious existence. However, while many of the biomechanical and physiological modifications necessary to achieve this feat have been studied in detail, little is known about the sensory adaptations accompanying this transition. In this study, we investigated the visual system and visual ecology of the Australian lungfish Neoceratodus forsteri, which is the most primitive of all the lungfish and possibly the closest living relative to the ancestors of tetrapods.

Results: Juvenile Neoceratodus have five spectrally distinct retinal visual pigments. A single type of rod photoreceptor contains a visual pigment with a wavelength of maximum absorbance (lambdamax) at 540 nm. Four spectrally distinct single cone photoreceptors contain visual pigments with lambdamax at 366 (UVS), 479 (SWS), 558 (MWS) and 623 nm (LWS). No double cones were found. Adult lungfish do not possess UVS cones and, unlike juveniles, have ocular media that prevent ultraviolet light from reaching the retina. Yellow ellipsoidal/paraboloidal pigments in the MWS cones and red oil droplets in the LWS cones narrow the spectral sensitivity functions of these photoreceptors and shift their peak sensitivity to 584 nm and 656 nm, respectively. Modelling of the effects of these intracellular spectral filters on the photoreceptor colour space of Neoceratodus suggests that they enhance their ability to discriminate objects, such as plants and other lungfishes, on the basis of colour.

Conclusion: The presence of a complex colour vision system based on multiple cone types and intracellular spectral filters in lungfishes suggests that many of the ocular characteristics seen in terrestrial or secondarily aquatic vertebrates, such as birds and turtles, may have evolved in shallow water prior to the transition onto land. Moreover, the benefits of spectral filters for colour discrimination apply equally to purely aquatic species as well as semi-aquatic and terrestrial animals. The visual system of the Australian lungfish resembles that of terrestrial vertebrates far more closely than that of other sarcopterygian fish. This supports the idea that lungfishes, and not the coelacanth, are the closest living relatives of the ancestors of tetrapods.

Figure 1

A juvenile (TL = 25 cm) Australian lungfish, Neoceratodus forsteri. Note the strong dorso-ventral countershading and pale belly colouration. Scale bar = 1 cm. This photograph, taken by HJB and NJM, appeared as a cover image in the British Journal of Ophthalmology (Vol. 90, number 7) and is reproduced with kind permission from the BMJ Publishing Group.

Figure 2

Spectral characteristics of retinal photoreceptors and ocular media in juvenile and adult Australian lungfish (Neoceratodus forsteri). (A) Normalized absorbance spectra of cone photoreceptor visual pigments. UVS, SWS, MWS and LWS refer to the pigments found in the ultraviolet-, short-, medium- and long-wavelength-sensitive cones, which have wavelengths of maximum absorbance (λ_max) at 366, 479, 558 and 623 nm, respectively. The absorbance spectrum of the rod pigment (λ_max 540 nm) is not shown. All pigments are found in juvenile lungfish (j), but the UVS cones are absent from adults (a). (B) Absorptance spectra of intracellular organelles and spectral filters. R, E and C refer to the red oil droplets, yellow ellipsoid pigment and colourless oil droplets in the LWS, MWS and SWS/UVS cones (spectra pooled), respectively. The absorptance spectrum of the yellow paraboloid pigment in the MWS cones of adult Neoceratodus (not shown) is almost identical to that of the ellipsoidal pigment in juveniles. (C) Normalized transmittance spectra of the combined ocular media (lens, cornea, etc.) of adult and juvenile lungfish. Note the increased absorption of shorter wavelength light by the ocular media of the adult. (D) Calculated quantal spectral sensitivities of the 4 cone types in juveniles and 3 cone types in adults, taking into account the spectral filtering effects of the intracellular spectral filters and ocular media on the absorption of light by the visual pigment in each cone type

Figure 3

Object colour solids of juvenile and adult lungfish. The volume of the object colour solid was calculated for juvenile (A, B) and adult (C, D) lungfish, both with (A, C) and without (B, D) the filtering effects of the yellow ellipsoidal and red oil droplet spectral filters in the MWS and LWS cones. The tetrachromatic colour space of the juvenile lungfish (A, B) is shown by two different projections of the spaces defined by the quantum catches of the UVS, SWS and MWS cones and also the SWS, MWS and LWS cones. Note the increase in the volume of the object-colour solid (and consequently the number of discriminable colours) in both juveniles (B) and adults (D) with spectral filters, relative to the situation without the effects of spectral filters. See Fig. 2 for explanation of abbreviations. Projections were generated using Mathematica software (Wolfram Research, Inc., Champaign, IL, USA).

Figure 4

Habitat irradiance and reflectance spectra of objects of potential importance to the visual ecology of lungfish. (A) Downwelling spectral irradiance at increasing depths in a typical lungfish habitat, the Mary River, Queensland, Australia. Note the rapid attenuation of ultraviolet wavelengths with increasing depth compared to longer wavelengths. (B) Reflectance spectra of lungfish body colours compared to sandy riverbed substrate against which they might be viewed. (C) Reflectance spectra of typical macrophytes found in a typical lungfish habitat, some of which (e.g. Vallisneria spiralis) are eaten or used as spawning sites.

Figure 5

Chromaticity diagrams of lungfish cone photoreceptor colour space. Calculations were made for juvenile (A, B) and adult (C, D) lungfish, both with (A, C) and without (B, D) the filtering effects of the yellow ellipsoidal and red oil droplet spectral filters in the MWS and LWS cones. The black star in each diagram is the achromatic point. Large spheres/circles are the body colours (brown, orange, red), rocks and sand substrate (grey) and macrophytes (green) shown in Figs. 4B, C. Small circles represent monochromatic loci at 5nm intervals across the lungfish-visible spectrum. Note the increased separation of the object reflectance spectra and the displacement of the monochromatic loci towards the vertices in both juveniles (B) and adults (D) with spectral filters, relative to the situation without the effects of spectral filters. See Fig. 2 for explanation of abbreviations.