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BMC Ecology Biomed Central BMC Ecology BioMed Central Research article Open Access Visual ecology of the Australian lungfish (Neoceratodus forsteri) Nathan S Hart*1, Helena J Bailes1,2, Misha Vorobyev1,3, N Justin Marshall1 and Shaun P Collin1 Address: 1School of Biomedical Sciences, The University of Queensland, Brisbane, QLD 4072, Australia, 2Faculty of Life Sciences, The University of Manchester, Oxford Road, Manchester, M13 9PL, UK and 3Department of Optometry and Vision Science, The University of Auckland, Private Bag 92019, Auckland, New Zealand Email: Nathan S Hart* - [email protected]; Helena J Bailes - [email protected]; Misha Vorobyev - [email protected]; N Justin Marshall - [email protected]; Shaun P Collin - [email protected] * Corresponding author Published: 18 December 2008 Received: 27 August 2008 Accepted: 18 December 2008 BMC Ecology 2008, 8:21 doi:10.1186/1472-6785-8-21 This article is available from: http://www.biomedcentral.com/1472-6785/8/21 © 2008 Hart et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. 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 (λmax) at 540 nm. Four spectrally distinct single cone photoreceptors contain visual pigments with λmax 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. Page 1 of 14 (page number not for citation purposes) BMC Ecology 2008, 8:21 http://www.biomedcentral.com/1472-6785/8/21 Background drum. The eyes of lungfishes are small relative to body Lungfishes (Dipnoi) diverged from the main vertebrate size when compared with other vertebrates [12-14] and stock in the early Devonian (ca. 390 MYA) [1] and have low spatial resolving power [15,16]. Moreover, together with coelancanths and the extinct osteolepimor- behavioural studies of both captive and wild populations phs comprise the Sarcopterygii (lobe-finned fish). While it of Neoceratodus suggest that, except during the breeding is generally agreed that tetrapods evolved from sarcoptery- season, they are predominantly crepuscular or nocturnal gian fish, phylogenetic relationships within the Sarcop- in habit [7,17]. Nevertheless, the retina of Neoceratodus terygii have been the subject of considerable debate [2,3]. has at least three morphologically distinct cone photore- A recent consensus, based on the analysis of nuclear DNA ceptor types, some of which contain brightly coloured oil [4] mitochondrial DNA [5] and ribosomal RNA gene droplets or spectral filters [15,18], and expresses multiple sequences [6], is that lungfishes rather than coelacanths visual pigment opsin genes [19]. Coloured oil droplets/ are the closest living relatives of the tetrapods. spectral filters (combined with multiple spectral subtypes of cone photoreceptor) are characteristic of strongly diur- Worldwide, there are six extant species of lungfishes: four nal (and generally terrestrial) non-mammalian verte- in Africa, one in South America and one in Australia. All brates, such as birds, turtles and lizards [10] and are African (Protopterus sp.) and South American (Lepidosiren) thought to improve colour vision by tuning the spectral lungfishes belong to the Lepidosirenidae; the Australian sensitivity functions of the cones [20,21]; densely pig- lungfish (Neoceratodus forsteri; Fig. 1) is the only surviving mented spectral filters are generally absent from nocturnal species in the Ceratodontidae [4,7]. Compared with the or crepuscular species [10] because they absorb light and other species of lungfishes, which have paired lungs, reduce absolute sensitivity. Neoceratodus has a single lung and uses predominantly gill respiration, only breathing air during periods of increased Thus, the polychromatic visual system of the lungfish is at activity or when water quality is poor [7]. Based on this odds with its known behavioural characteristics and raises and other morphological, molecular and palaeontologi- a number of interesting questions with regard to the neu- cal evidence, Neoceratodus is considered to be the more roethology of the lungfish, the function and utility of col- primitive lungfish species [8,9]. oured oil droplets and the evolution of the tetrapod visual system. To investigate these issues, we have measured Although originally considered to be rather degenerate some of the most important parameters of the visual ecol- [10] and of little behavioural importance [11], the visual ogy of Neoceratodus forsteri: the spectral absorption charac- system of the lungfish represents something of a conun- teristics of the visual pigments and spectral filters (pigmented oil droplets and diffuse pigment in the ellip- soid and paraboloid regions) of the retinal photorecep- tors, the spectral transmittance of the ocular media, the spectral distribution of the ambient light in a typical lung- fish habitat and the spectral reflectance of relevant objects in its environment. Using these data, we have modelled the performance of the lungfish visual system with respect to its ability to distinguish both real and theoretical col- oured objects. Results Photoreceptor visual pigments, spectral filters and spectral sensitivity The retina of the Australian lungfish is duplex, containing both rod and cone photoreceptors. Microspectrophotom- etry showed that juvenile lungfish possess four types of single cone photoreceptor with visual pigments maxi- AsteriFigure juvenile 1 (TL = 25 cm) Australian lungfish, Neoceratodus for- mally sensitive to ultraviolet (UVS, λ 366 nm), short- A juvenile (TL = 25 cm) Australian lungfish, Neocera- max todus forsteri. Note the strong dorso-ventral countershad- (SWS, λmax 479 nm), medium- (MWS, λmax 558 nm) and ing and pale belly colouration. Scale bar = 1 cm. This long-wavelengths (LWS, λmax 623 nm; Table 1 and Fig. photograph, taken by HJB and NJM, appeared as a cover 2A) and, therefore, have the potential for tetrachromatic image in the British Journal of Ophthalmology (Vol. 90, colour vision. UVS cones are the only photoreceptor type number 7) and is reproduced with kind permission from the not found in the retina of the adult lungfish. The retinae BMJ Publishing Group. of both juveniles and adults also contain a single type of MWS rod (λmax 540 nm). We did not observe double Page 2 of 14 (page number not for citation purposes) BMC Ecology 2008, 8:21 http://www.biomedcentral.com/1472-6785/8/21 Table 1: Summary of spectral and morphological characteristics of retinal photoreceptors in juvenile and adult Australian lungfish (Neoceratodus forsteri). Rods Cones UVS SWS MWS LWS Visual pigments Mean λmax of prebleach spectra (nm) 539.8 ± 1.1 366.3 ± 2.2 479.2 ± 2.9 558.2 ± 4.8 623.2 ± 3.3 λmax of mean prebleach spectrum (nm) 539.7 366.5 478.8 558.5 623.6 Mean λmax of difference spectra (nm) 542.9 ± 1.4 367.6 ± 2.1 480.5 ± 4.0 558.8 ± 4.4 623.4 ± 2.3 λmax of mean difference spectrum (nm) 542.8 367.6 479.1 557.7 623.3 Mean transverse (decadic) absorbance at λmax of difference 0.137 ± 0.029 0.023 ± 0.004 0.023 ± 0.007 0.037 ± 0.010 0.037 ± 0.010 spectrum Mean outer
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