«Appendix J - 1 The Visual System of Dolphins 1 A Review by James T. Fulton J.1 Introduction The visual system of the dolphin, particularly the ...»
Appendix J - 1
The Visual System of Dolphins 1
A Review by James T. Fulton
The visual system of the dolphin, particularly the bottle-nosed dolphin, Tursiops truncatus, has been observed
extensively in the field from a behavioral aspect. However, from a physiological perspective, Pryor quoted one
researcher as follows2. “Compared to our knowledge of vision in terrestrial animals, our fundamental knowledge of
the cetacean’s highly evolved and very different eye is ‘pathetic.’” This situation appears to be largely unchanged in
2009. There are many unresolved questions that prevent a detailed description of the performance of the dolphin visual system. As a result, the literature of dolphin vision should be considered largely exploratory rather than descriptive.
Three major compilations have appeared relating to the sensory abilities of marine mammals; Thomas & Kastelein in 19903, Thomas, Kastelein & Supin in 19924 and Supin, Popov & Mass in 20015. As noted by a long time participant in the field, the investigators “are biologists and tank cleaners.” They may be described a bit more precisely as behavioral anthropologists with undergraduate backgrounds in biology–and tank cleaners. Very few specialists in histology, neurology or physiology have made a career in this field.
Due to this situation, concepts have crept into the literature that are perplexing. The dolphin eye when fully light adapted has been described as analogous to a pin hole camera. However, a pin hole camera does not have a lens behind the pin hole, it is defined as a camera that is refraction free (although it is limited by diffraction)–all optical rays pass straight through the aperture of a pin hole camera. The resulting image covers a very wide field of view that is not limited to the area around a chief ray. The dolphin eye when fully light adapted is a conventional eye with a fully developed lens system and a very effective aperture stop. It is not a pin hole camera by definition. It can be described in optical science as a conventional camera with a pin hole aperture in front of the lens. A pin hole aperture mask is frequently used in optometry where it is called a Hartmann mask. It may consist of one pin hole or an array of pin holes. If each pin hole in the array is turned into an interferometer, the resultant instrument becomes a Shack-Hartmann interferometer. This instrument is very useful for measuring the properties of the lens system of a camera. A simpler variant of a Hartmann mask based instrument is described below by Cronin, Fasic & Howland.
The dolphin eye has been described repeatedly as exhibiting two fovea based on a novel criteria, that the concentration of large ganglion neurons at two locations on the neural portion of the retina define two fovea.
Rivamonte described this dual fovea configuration along with the unusual operculum as constituting a bifocal visual system6. The dolphin retina, like all mammalian retinas is reversed (Section 1.7). All of the neural tissue of the retina is in the optical path leading to the photoreceptors. The hallmark of a fovea is there are NO neural cells in the optical path leading to that fovea, ganglion or otherwise. In fact, the fovea is characterized by an absence of vascularization, as well as neurons, in this “area centralis.” The photoreceptors are supported by diffusion of blood plasma through the non-neural tissue and even more importantly from the retinal pigment epithelium layers on the Released: December 12, 2009 Pryor, K. (1990) Concluding comments on vision, tactition, and chemoreception In Thomas, J. & Kastelein, R. eds Sensory abilities of cetaceans. NY: Plenum Press pp561-569, pg 565 Thomas, J. & Kastelein, R. eds Sensory abilities of cetaceans. NY: Plenum Press Thomas, J. Kastelein, R. & Supin, A. eds Marine Mammal Sensory Systems. NY: Plenum Press Supin, A. Popov, V. & Mass, A. (2001) The Sensory Physiology of Aquatic Mammals. London: Kluwer Academic Rivamonte, L. (2009) Bottlenose dolphin (Tursiops truncatus) double-slit pupil asymmetries enhance vision Aquatic Mammals vol 35(2), pp 269-280 2 Processes in Animal Vision scleral side of the retina. Surveys of the cetacean retina by conventional retinoscopic imaging have not reported any fovea in Cetacea.
The spectral performance of the dolphin visual system has been investigated primarily from the behavioral and coarse psychophysical perspectives (Madsen, 1976). The Madsen (1976) color vision study boiled down to a visibility spectrum study when, after more than 15,000 trials under several different behavioral protocols, the single subject continued to respond to perceived target brightness and failed to take advantage of spectral color cues presented. It exhibited a visual luminosity function similar to other mammals. In field studies, “a peak quantum corrected dim light sensitivity at 487.4 nm (495 nm energy-based) and a peak bright light sensitivity at 493.4 nm (500 nm energy-based)” were observed. Needless to say, the response of dolphin eyes is photon-based and should be expressed in quantum-based and not energy-based units.
Thomas, Kastelein & Supin have provided a phylogenic tree of the cetacean families. Supin, Popov & Mass give a brief but informative textual discussion of the major families of cetacea (pg 3). Leatherwood & Reeves provide a more extensive phylogenic discussion of cetacea7.
Cetacea have greatly evolved from their presumed ungulate ancestor to match the requirements of their new ecological niche. Both the performance and physiology of their visual and auditory capabilities have changed remarkably and their olfactory capability is believed to be vestigial at best.
The eyes of dolphins have evolved from those of the typical ungulate to share many of the features of more predatory families and species. The eyes share a set of six muscles with other mammals but their tasks appear to have been modified. Dolphin eyes are not known to exhibit torsional motion (rotation around the optical axis).
Additional adaptations may have occurred to satisfy ecological needs. The sclera is particularly thick and the intraocular pressure (relative to the environment) is known to be very high compared to terrestrial mammals (Dawson et al., 1992). The non spherical shape of their sclera limits eye rotation up and down and left and right about the center of the sclera or choroid.
A major void in the current literature is a definitive discussion of the location of the eyes of Tursiops truncatus relative to the skull and the outer conformation of the animal. There is reasonably broad agreement in the literature that the eyes move in ways other than simple rotation of the globe within a fixed spherical eye socket. It is likely this motion is coordinated with the skin conformation to provide optimum conditions for alternately high speed swimming and analytical examination of rostral targets at minimal speed swimming. While the eye is not spherical and able to rotate in a spherical socket like a human eye, the socket itself may be under muscular control (in conjunction with the contour of the skin. Cranford et al. have been active in computer aided tomography of the dolphins head, but with most attention focused on its acoustic properties8. They have defined a set of horizontal, vertical and transverse planes and illustrated their coordinates with a transverse plane passing through the eyes of the dolphin. Their dorsal schematic in figure 3 suggests the optical axis of the eye of Delphinus delphis is 75 degrees from the long axis of the body but a higher precision measurement is required under a variety of in-vivo conditions.
As a phylogenic family, the dolphins do not depend on vision as their primary sensory facility. Their acoustic sensing is far more important in their ecological niche. This fact is demonstrated by the so-called river dolphins who have evolved to the point they are functionally blind, although they have lived with this characteristic for millennia.
Rivamonte reviewed much of the work in the field in 2009, and focused on one of the outstanding dichotomies.
How does the dolphin see clearly in both air and water when “the dolphin eye has no obvious means to compensate for the large difference in refractive power of the cornea between air and water?” This question will be examined below.
Kroger & Kirschfeld (1993) provided a schematic of the eyes of Phocoena phocoena relative to the long axis of the body. They show the optical axis of the eyes at equal angles of less than 45 degrees from the body axis (compare to 75 degrees in Cranford). No angular dimensions are provided and no stereo vision is suggested. However, stereooptic vision could be obtained in the real system for optical axes less than 30 degrees from the body axis. As seen in Figure J.1.1-1, the dolphin may exhibit better stereooptic vision in air than in water because of the change in index of refraction of the medium. Kastelein et al. noted this possibility in 1990 (page 477). The performance of the cetacean eyes are significantly degraded at an angle of 60° from the optical axis; the angle of maximum resolving Leatherwood, S. & Reeves, R. (1990) The Bottlenose Dolphin. NY: Academic Press Cranford, T., Amundin, M. & Norris, K. (1996) functional morphology and homology in the odotocete nasal complex: implications for sound generation J Morphol vol 228, pp 223-285 Appendix J - 3 power proposed by some investigators Except for the motions of the eyes, the dolphin visual system appears to be typically mammalian except for one peculiar adaptation believed to be shared with octopus and possibly other shallow water marine species. It exhibits an operculum that is much more effective than the typical circular or oval mammalian iris. Whereas the human iris operates over a range from 8 to 2 mm in diameter giving a brightness control at the retina on the order of 16:1, the dolphin iris/operculum is able to achieve a brightness control range exceeding 100:1. Dawson et al. have provided data suggesting the time constants of the iris/operculum are similar to those of human and operate at similar light levels9.
The dolphins literal habitat involves a very large illumination range, from the depths of the ocean (down to several hundred feet) to bright direct sunlight during periods of breathing and even intermittent aerial flight. The iris/operculum appears to be maximally closed at light levels on the order of 15,000 lux (15,000 lumens/m2 or 1400 foot-candles).
While the literature tends to negate the importance of the cornea under water, Litwiler & Cronin take a different and possibly more informed view10. They summarized current knowledge in this area. “The cornea, however, may also contribute to image formation even underwater. Unlike the terrestrial cornea, which is relatively thin throughout, the dolphin cornea is thicker at the periphery than at the center, being more strongly curved on the posterior surface than the anterior surface (Kroger and Kirschfeld 1994). In addition, the periphery of the cornea has a higher refractive index than the center (Kroger and Kirschfeld 1992). Together, these result in an unusual optical system in which the cornea acts as a diverging lens and contributes negative refractive power to the overall optics of the eye11.
The negative power of the cornea may compensate for the excessive refractive power of the lens, and correct the optics of the eye to near emmetropia in water. Several hypotheses have been suggested to account for this aerial acuity, including a constricted pupil (Herman et al. 1975, Rivamonte 1976, Dawson et al. 1987, Kroger and Kirschfeld 1993), localized flattening of the cornea (Dawson et al. 1987, Kroger 1989), variation in focal position with direction of view (Dral 1972, Pack and Herman 1995), and a fine, continuous accommodative mechanism, such as movement of the lens within the eye (Dral 1972, Mass 1997). While some of these hypotheses are supported by experimental results (e.g., corneal flattening, Kroger 1989; variation with direction of view, Dral 1972), researchers have questioned the validity of others (e.g., lenticular accommodation, Dawson 1980; constricted pupil, Murphy and Howland 1991; Rivamonte 1976).” Litwiler & Cronin go on, “In general, there is a lack of observations and data on the accommodative capacity of the dolphin visual system.” “Our results are inadequate to demonstrate whether or not dolphins accommodate in air, but they strongly suggest that these animals lack the ability to adjust the focus of the eye underwater.” While the literature leans to no method of accommodation in the bottlenose dolphin eye, this is short-sighted. Living biological systems require largely automatic methods of optimization, the eyes cannot be pre-aligned and prefocused at the factory like a man-made camera. Effective imaging requires the optical image be brought to focus within 15–25 microns (0.015–0.025 millimeters) of the entrance aperture of the photoreceptors for an F/3 optical system. This quality of adjustment must be maintained through out the life of the animal (including periods of growth) and over the entire retina operating at optimal resolution. A mechanism or protocol is required to achieve this goal in any mammal. Dral, a histologist with a veterinarial bent, described the fields of view of the bottle nose dolphin under a variety of light conditions in 197512. As noted by Dral, “a mechanism for accommodation, which is lacking in the ciliary body, might be present in the iridial musculature.” These combined tissues are sometimes labeled the trabecular matrix. West et al. have explored the relevant tissue recently13.
Maintaining focus may be a demanding requirement in the bottlenose and other animals attempting to maintain high Dawson, W. Adams, C. Barris, M. & Litzkow, C. (1979) Static and kinetic properties of the dolphin pupil Am J Physiol Regul Integr Comp Physiol vol 237, pp R301-R305 Litwiler, T. & Cronin, T. (2001) No Evidence of Accommodation in the eyes of the Bottlenose Dolphin, Tursiops truncatus, Marine Mam Sci vol 17(3), pp 508-525 Kroger, R. & Kirschfeld, K. (1992) The cornea as an optical element in the cetacean eye In Thomas, J.
Kastelein, R. & Supin, A. eds. Marine Mammal Sensory Systems. NY: Plenum pp 97-142, page 105 Dral, A. (1975) Vision in Cetacea J Zoo Animal Med vol 6 West, J. Sivak, J. Murphy, C. & Kovaks, K. (1991) A comparative study of the iris and ciliary body in aquatic mammals Can J Zool vol 69, pp 2594-2607 4 Processes in Animal Vision acuity over a wide field of view. Humans are only required to maintain optimum focus over the central 1.2 degree diameter of the fovea.