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Title of Journal: Anim Cogn

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Abbravation: Animal Cognition

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Springer Berlin Heidelberg

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DOI

10.1007/s10832-007-9078-6

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1435-9456

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Why do seals have cones Behavioural evidence for

Authors: Christine Scholtyssek Almut Kelber Guido Dehnhardt
Publish Date: 2014/12/02
Volume: 18, Issue: 2, Pages: 551-560
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Abstract

All seals and cetaceans have lost at least one of two ancestral cone classes and should therefore be colourblind Nevertheless earlier studies showed that these marine mammals can discriminate colours and a colour vision mechanism has been proposed which contrasts signals from cones and rods However these earlier studies underestimated the brightness discrimination abilities of these animals so that they could have discriminated colours using brightness only Using a psychophysical discrimination experiment we showed that a harbour seal can solve a colour discrimination task by means of brightness discrimination alone Performing a series of experiments in which two harbour seals had to discriminate the brightness of colours we also found strong evidence for purely scotopic rodbased vision at light levels that lead to mesopic rod–conebased vision in other mammals This finding speaks against rod–conebased colour vision in harbour seals To test for colourblindness we used a cognitive approach involving a harbour seal trained to use a concept of same and different We tested this seal with pairs of isoluminant stimuli that were either same or different in colour If the seal had perceived colour it would have responded to colour differences between stimuli However the seal responded with “same” providing strong evidence for colourblindnessSeeing the world in colour allows for reliable object detection and recognition under variable illumination For an animal to see colour its retina has to contain at least two spectrally distinct photoreceptor types whose signals are compared in colour opponent mechanisms Kelber et al 2003 Most terrestrial mammals possess two spectral classes of cones SWS1 shortwavelengthsensitive and LWS longwavelengthsensitive Jacobs 2009 Kelber et al 2003 Peichl 2005 A few nocturnal species lack SWS1 cones and are therefore LWS monochromats Deegan and Jacobs 1996 Jacobs 2013 Jacobs et al 1996 Peichl and Moutairou 1998 Peichl and Pohl 2000 What seems to be an exception among terrestrial mammals has evolved to be the rule in the two largest groups of marine mammals All cetaceans and seals that have been investigated have lost their SWS1 cones and hence the basis of conebased colour vision Crognale et al 1998 Fasick et al 1998 Levenson and Dizon 2003 Levenson et al 2006 Newman and Robinson 2005 Peichl and Moutairou 1998 Some species of whales Balaenidae Balaenopteroidea the Sowerby’s beaked whale Mesoplodon bidens the giant sperm whale Physeter macrocephalus and the pygmy sperm whale Kogia breviceps have even lost both cone types and are therefore rod monochromats Meredith et al 2013 These findings suggest that a secondarily aquatic lifestyle in contrast to a terrestrial lifestyle favours colourblindness The reason could be the narrow spectra of light that whales and seals encounter when foraging in coastal waters or at greater depth Jerlov 1951 If the spectral bandwidth is too small to ensure colour constancy benefits of colour vision—such as facilitated object detection and recognition—are lost Furthermore colour vision compromises sensitivity and considering the small amount of light that is left for most whales or seals during foraging colour vision may have been lost in favour of the absolute sensitivity of the visual systemSurprisingly early behavioural investigations seem to have demonstrated that marine mammals see colour Wartzok and McCormick 1978 showed that one of two Bering Sea spotted seals Phoca largha discriminated blue from orange light Other behavioural studies investigated colour discrimination in South African fur seals Arctocephalus pusillus South American fur seals Arctocephalus australis California sea lions Zalophus californianus and a bottlenose dolphin Tursiops truncatus Busch and Dücker 1987 Griebel and Schmid 1992 2002 The general conclusion of all studies was that these cone monochromats see colour and the hypothesis arose that marine mammals may have colour vision mediated by an opponent mechanism contrasting neural signals from LWS cones and rods Crognale et al 1998 However those studies underestimated the sensitivity for brightness differences in these animals Scholtyssek and Dehnhardt 2013 Scholtyssek et al 2008 and therefore did not control sufficiently for the relative brightness of the stimuli that the animals were trained to discriminate Hence it cannot be excluded that the demonstration of colour discrimination in previous studies was based on brightness discrimination rather than colour vision Furthermore for a rod–conebased colour vision mechanism rods and cones need to be active at the same time mesopic vision Flicker photometric electroretinograms ERGs in the California sea lion and the harbour seal failed to find any contribution of the LWS cones to the spectral sensitivity of the eye Crognale et al 1998 Levenson et al 2006 Instead the spectral sensitivity functions resembled those of the rods even at an ambient luminance of 495 lx which leads to photopic vision in humans van Hateren and Snippe 2007The goal of our study was to shed light on the paradox of anatomical and physiological findings that suggest colourblindness and behavioural experiments that suggest colour vision in marine mammals by performing a series of psychophysical experiments with harbour seals In Experiment 1 we used a classical approach to test for colour vision We trained a harbour seal to discriminate between stimuli that appear blue or green to humans The brightness of blue and green was chosen in such a way that we could determine whether the seal used brightness or colour to solve the discrimination task Since the contrasts between blue and green differ for scotopic rodbased and photopic conebased vision we could also determine which photoreceptors mediated brightness perception in the harbour sealWith a classical approach like the one used in Experiment 1 it is hard to prove colourblindness since the animal could have failed to learn the discrimination but still see colour To overcome this problem we used a cognitive approach to test for colour vision in Experiment 2 which involved a harbour seal that had learned to form a concept of sameness and difference in a previous study Scholtyssek et al 2013 That study demonstrated that the seal could use this concept to judge whether completely unfamiliar stimuli were same or different irrespective of the dimension in which they differed shape brightness or pattern In the present study we confronted the harbour seal with stimuli that differed only in colour blue vs green and tested whether it would perceive them as “same” or as “different” This way we found convincing evidence for colourblindnessThe experimental animal was a 12yearold male harbour seal named Nick He was housed with eight conspecifics and one fur seal in the opensea enclosure of the Marine Science Center in Rostock Germany Nick was experienced in learning and performing visual discriminationsTo ensure a constant state of adaptation all experiments were conducted in a lighttight experimental chamber 2 m wide 3 m long and 22 m high On command of the experimenter the seal could enter the chamber through a sliding door a picture of the chamber can be found in Scholtyssek et al 2013 Illumination was provided by white LEDs Conrad Telux LED TLWW 7600 spectral bandwidth 400–800 nm powered by an adjustable constant current source Voltcraft type 3610 that produced a wellcontrolled and evenly distributed illumination of 09 lx in the area surrounding the experimental apparatus This is equivalent to a luminance of 05 cd/m2 measured with a Minolta luminance meter This luminance corresponds to the lower range of mesopic vision in mammals including humans whose mesopic range falls between 0001 and 10 cd/m2 Hammod and James 1971 Virsu et al 1987


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