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For whales and seals the ocean is not blue: a visual pigment loss in marine mammals*

Leo Peichl

Max‐Planck‐Institut für Hirnforschung, Deutschordenstr. 46, D‐60528 Frankfurt, Germany

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Günther Behrmann

Alfred‐Wegener‐Institut für Polar‐und Meeresforschung, Am Handelshafen 12, D‐27570 Bremerhaven, Germany

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Ronald H. H. Kröger

Lunds Universitet, Zoologiska Institutionen, Helgonavägen 3, S‐22362 Lund, Sweden.

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First published: 20 December 2001
Cited by: 81
: Dr Leo Peichl, as above.
E‐mail: peichl@mpih‐frankfurt.mpg.de

*This paper is dedicated to the late Professor Brian B. Boycott FRS (1924–2000), great scientist, teacher and friend.

Abstract

Most terrestrial mammals have colour vision based on two spectrally different visual pigments located in two types of retinal cone photoreceptors, i.e. they are cone dichromats with long‐to‐middle‐wave‐sensitive (commonly green) L‐cones and short‐wave‐sensitive (commonly blue) S‐cones. With visual pigment‐specific antibodies, we here demonstrate an absence of S‐cones in the retinae of all whales and seals studied. The sample includes seven species of toothed whales (Odontoceti) and five species of marine carnivores (eared and earless seals). These marine mammals have only L‐cones (cone monochromacy) and hence are essentially colour‐blind. For comparison, the study also includes the wolf, ferret and European river otter (Carnivora) as well as the mouflon and pygmy hippopotamus (Artiodactyla), close terrestrial relatives of the seals and whales, respectively. These have a normal complement of S‐cones and L‐cones. The S‐cone loss in marine species from two distant mammalian orders strongly argues for convergent evolution and an adaptive advantage of that trait in the marine visual environment. To us this suggests that the S‐cones may have been lost in all whales and seals. However, as the spectral composition of light in clear ocean waters is increasingly blue‐shifted with depth, an S‐cone loss would seem particularly disadvantageous. We discuss some hypotheses to explain this paradox.

Number of times cited: 81

  • , Vision, Encyclopedia of Marine Mammals, 10.1016/B978-0-12-804327-1.00266-1, (1035-1044), (2018).
  • , Scene through the eyes of an apex predator: a comparative analysis of the shark visual system, Clinical and Experimental Optometry, 101, 5, (624-640), (2018).
  • , Optic nerve, superior colliculus, visual thalamus, and primary visual cortex of the northern elephant seal (Mirounga angustirostris) and California sea lion (Zalophus californianus), Journal of Comparative Neurology, 525, 9, (2109-2132), (2017).
  • , Coping with copepods: do right whales (Eubalaena glacialis) forage visually in dark waters?, Philosophical Transactions of the Royal Society B: Biological Sciences, 372, 1717, (20160067), (2017).
  • , The Genetic and Evolutionary Drives behind Primate Color Vision, Frontiers in Ecology and Evolution, 5, (2017).
  • , Icelandic herring-eating killer whales feed at night, Marine Biology, 164, 2, (2017).
  • , Head and Senses, Anatomy of Dolphins, 10.1016/B978-0-12-407229-9.00005-1, (133-196), (2017).
  • , Cetacean Sensory Systems, Encyclopedia of Animal Cognition and Behavior, 10.1007/978-3-319-47829-6_939-1, (1-9), (2017).
  • , The Retina of Asian and African Elephants: Comparison of Newborn and Adult, Brain, Behavior and Evolution, 10.1159/000464097, 89, 2, (84-103), (2017).
  • , Evolutionary loss of cone photoreception in balaenid whales reveals circuit stability in the mammalian retina, Journal of Comparative Neurology, 524, 14, (2873-2885), (2016).
  • , Eye Histology and Ganglion Cell Topography of Northern Elephant Seals (irounga angustirostris), The Anatomical Record, 299, 6, (798-805), (2016).
  • , Inactivation of Cone-Specific Phototransduction Genes in Rod Monochromatic Cetaceans, Frontiers in Ecology and Evolution, 4, (2016).
  • , Adaptations of Cetacean Retinal Pigments to Aquatic Environments, Frontiers in Ecology and Evolution, 4, (2016).
  • , Visual Matched Filtering in Vertebrates, The Ecology of Animal Senses, 10.1007/978-3-319-25492-0_7, (169-203), (2015).
  • , Rod-cone based color vision in seals under photopic conditions, Vision Research, 125, (30), (2016).
  • , CHARACTERIZATION OF ANTERIOR SEGMENT OPHTHALMOLOGIC LESIONS IDENTIFIED IN FREE-RANGING DOLPHINS AND THOSE UNDER HUMAN CARE, Journal of Zoo and Wildlife Medicine, 47, 1, (56), (2016).
  • , Sensory Perception in Cetaceans: Part I—Current Knowledge about Dolphin Senses As a Representative Species, Frontiers in Ecology and Evolution, 4, (2016).
  • , Sharks senses and shark repellents, Integrative Zoology, 10, 1, (38-64), (2015).
  • , Integumentary and Sensory Systems, Marine Mammals, 10.1016/B978-0-12-397002-2.00007-7, (169-210), (2015).
  • , How Elasmobranchs Sense Their Environment, Physiology of Elasmobranch Fishes: Structure and Interaction with Environment, 10.1016/B978-0-12-801289-5.00002-X, (19-99), (2015).
  • , Advances in understanding the molecular basis of the first steps in color vision, Progress in Retinal and Eye Research, 49, (46), (2015).
  • , Spectral shifts of mammalian ultraviolet-sensitive pigments (short wavelength-sensitive opsin 1) are associated with eye length and photic niche evolution, Proceedings of the Royal Society B: Biological Sciences, 282, 1819, (20151817), (2015).
  • , No rainbow for grey bamboo sharks: evidence for the absence of colour vision in sharks from behavioural discrimination experiments, Journal of Comparative Physiology A, 10.1007/s00359-014-0940-0, 200, 11, (939-947), (2014).
  • , Preliminary evidence for color stimuli discrimination in the Asian small-clawed otter (Aonyx cinerea), Learning & Behavior, 42, 2, (176), (2014).
  • , S cones: Evolution, retinal distribution, development, and spectral sensitivity, Visual Neuroscience, 10.1017/S0952523813000242, 31, 02, (115-138), (2013).
  • , On the perception, production and function of blue colouration in animals, Journal of Zoology, 289, 4, (229-242), (2012).
  • , Brightness discrimination in the South African fur seal (Arctocephalus pusillus), Vision Research, 84, (26), (2013).
  • , Vision, The Biology of Sea Turtles, Volume III, 10.1201/b13895-3, (31-58), (2013).
  • , The conflict between the southern right whale and coastal fisheries on the southern coast of Brazil, Marine Policy, 38, (428), (2013).
  • , Anatomic features of the cetacean globe, Veterinary Ophthalmology, 16, (52-63), (2013).
  • , Losses of functional opsin genes, short-wavelength cone photopigments, and color vision—A significant trend in the evolution of mammalian vision, Visual Neuroscience, 30, 1-2, (39), (2013).
  • , Nocturnal Light Environments Influence Color Vision and Signatures of Selection on the OPN1SW Opsin Gene in Nocturnal Lemurs, Molecular Biology and Evolution, 30, 6, (1420), (2013).
  • , Why become speckled? Ontogeny and function of speckling in Shark Bay bottlenose dolphins (Tursiops sp.)1, Marine Mammal Science, 28, 2, (295), (2012).
  • , Changes in the colour of light cue circadian activity, Animal Behaviour, 10.1016/j.anbehav.2012.01.035, 83, 5, (1143-1151), (2012).
  • , Functional significance of the taper of vertebrate cone photoreceptors, The Journal of General Physiology, 10.1085/jgp.201110692, 139, 2, (159-187), (2012).
  • , Behavioral responses of minke whales (Balaenoptera acutorostrata) to experimental fishing gear in a coastal environment, Journal of Experimental Marine Biology and Ecology, 413, (13), (2012).
  • , Estimated absorbance spectra of the visual pigments of the North Atlantic right whale (Eubalaena glacialis), Marine Mammal Science, 27, 4, (E321-E331), (2011).
  • , Is colour cognitive?, Optics & Laser Technology, 43, 2, (251), (2011).
  • , Behavioural evidence of dichromacy in a species of South American marsupial, Animal Behaviour, 81, 5, (1049), (2011).
  • , Microspectrophotometric evidence for cone monochromacy in sharks, Naturwissenschaften, 98, 3, (193), (2011).
  • , Anatomy of the California sea lion globe, Veterinary Ophthalmology, 13, (63-71), (2010).
  • , The Verriest Lecture 2009: Recent progress in understanding mammalian color vision, Ophthalmic and Physiological Optics, 30, 5, (422-434), (2010).
  • , Diversity of Color Vision: Not All Australian Marsupials Are Trichromatic, PLoS ONE, 5, 12, (e14231), (2010).
  • , Phylogenetic analyses in cetacean species of the family Delphinidae using a short wavelength sensitive opsin gene sequence, Fisheries Science, 76, 4, (571), (2010).
  • , Overview of comparative cognitive studies of dolphins in Japan, Japanese Psychological Research, 51, 3, (168-176), (2009).
  • , Aerial visual acuity in harbor seals (Phoca vitulina) as a function of luminance, Journal of Comparative Physiology A, 195, 7, (643), (2009).
  • , Basic mechanisms in pinniped vision, Experimental Brain Research, 199, 3-4, (299), (2009).
  • , Vision, Encyclopedia of Marine Mammals, 10.1016/B978-0-12-373553-9.00275-3, (1200-1211), (2009).
  • , Visual Ecology, The Senses: A Comprehensive Reference, 10.1016/B978-012370880-9.00337-6, (211-245), (2008).
  • , Effect of animal-borne camera and flash on the diving behaviour of the female Antarctic fur seal (Arctocephalus gazella), Deep Sea Research Part I: Oceanographic Research Papers, 55, 9, (1179), (2008).
  • , Brightness discrimination in the harbor seal (Phoca vitulina), Vision Research, 48, 1, (96), (2008).
  • , Evolution of vertebrate visual pigments, Vision Research, 48, 20, (2022), (2008).
  • , The Causes and Consequences of Color Vision, Evolution: Education and Outreach, 1, 4, (476), (2008).
  • , Mammalian Photopigments, The Senses: A Comprehensive Reference, 10.1016/B978-012370880-9.00257-7, (247-268), (2008).
  • , Nocturnal activity by mammal‐eating killer whales at a predation hot spot in the Bering Sea, Marine Mammal Science, 24, 4, (990-999), (2008).
  • , Adaptive features of aquatic mammals' eye, The Anatomical Record, 290, 6, (701-715), (2007).
  • , SPECTRAL SENSITIVITY IN TWO SPECIES OF PINNIPEDS (PHOCA VITULINA AND OTARIA FLAVESCENS), Marine Mammal Science, 22, 1, (156-166), (2006).
  • , Visual pigments of marine carnivores: pinnipeds, polar bear, and sea otter, Journal of Comparative Physiology A, 192, 8, (833), (2006).
  • , Corneal topography, refractive state, and accommodation in harbor seals (Phoca vitulina), Vision Research, 46, 6-7, (837), (2006).
  • , Integumentary and Sensory Systems, Marine Mammals, 10.1016/B978-012088552-7/50008-4, (132-II), (2006).
  • , Effect of water turbidity on the visual acuity of harbor seals (Phoca vitulina), Vision Research, 46, 11, (1777), (2006).
  • , Diversity of mammalian photoreceptor properties: Adaptations to habitat and lifestyle?, "The Anatomical Record Part A: Discoveries in Molecular, Cellular, and Evolutionary Biology", 287A, 1, (1001-1012), (2005).
  • , Cone visual pigments of aquatic mammals, Visual Neuroscience, 22, 06, (873), (2005).
  • , Discrimination of achromatic colors in a bottlenose dolphin, Japanese Journal of Animal Psychology, 55, 2, (59), (2005).
  • , Photoreceptors and photopigments in a subterranean rodent, the pocket gopher (Thomomys bottae), Journal of Comparative Physiology A, 191, 2, (125), (2005).
  • , Recovery of Underwater Visibility and Structure by Polarization Analysis, IEEE Journal of Oceanic Engineering, 30, 3, (570), (2005).
  • , Unusual cone and rod properties in subterranean African mole‐rats (Rodentia, Bathyergidae), European Journal of Neuroscience, 19, 6, (1545-1558), (2004).
  • , Ancestral Loss of Short Wave-Sensitive Cone Visual Pigment in Lorisiform Prosimians, Contrasting with Its Strict Conservation in Other Prosimians, Journal of Molecular Evolution, 58, 3, (314), (2004).
  • , Photopic Spectral Sensitivity of Green and Loggerhead Sea Turtles, Copeia, 2004, 4, (908), (2004).
  • , Animal colour vision — behavioural tests and physiological concepts, Biological Reviews, 78, 1, (81-118), (2007).
  • , Comparative Psychology of Vision, Handbook of Psychology, (47-70), (2003).
  • , Colors of primate pelage and skin: Objective assessment of conspicuousness, American Journal of Primatology, 59, 2, (67-91), (2003).
  • , Historical contingency in the evolution of primate color vision, Journal of Human Evolution, 44, 1, (25), (2003).
  • , MONITORING THE PREY‐FIELD OF MARINE PREDATORS: COMBINING DIGITAL IMAGING WITH DATALOGGING TAGS, Marine Mammal Science, 18, 3, (680-697), (2006).
  • , Adaptive loss of ultraviolet‐sensitive/violet‐sensitive (UVS/VS) cone opsin in the blind mole rat (Spalax ehrenbergi), European Journal of Neuroscience, 16, 7, (1186-1194), (2002).
  • , Spectral sensitivity and Color Vision in the Bottlenose Dolphin (Tursiops Truncatus), Marine and Freshwater Behaviour and Physiology, 35, 3, (129), (2002).
  • , Trichromatic Color Vision in Primates, Physiology, 17, 3, (93), (2002).
  • , A mouse-like retinal cone phenotype in the Syrian hamster: S opsin coexpressed with M opsin in a common cone photoreceptor, Brain Research, 929, 1, (139), (2002).
  • , Short and mid‐wavelength cone distribution in a nocturnal Strepsirrhine primate (Microcebus murinus), Journal of Comparative Neurology, 438, 4, (490-504), (2001).
  • , Rod Monochromacy and the Coevolution of Cetacean Retinal Opsins, PLoS Genetics, 10.1371/journal.pgen.1003432, 9, 4, (e1003432), (2013).
  • , Retinal photoreceptor and ganglion cell types and topographies in the red fox () and Arctic fox (), Journal of Comparative Neurology, , (2018).