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The Scotopic Visual Sensitivity of Four Species of Trout: a Comparative Study

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The Scotopic Visual Sensitivity of Four Species of Trout: a Comparative Study Western North American Naturalist 67(4), © 2007, pp. 524–537 THE SCOTOPIC VISUAL SENSITIVITY OF FOUR SPECIES OF TROUT: A COMPARATIVE STUDY Russell B. Rader1,2, Timberley Belish1,3, Michael K. Young1,4, and John Rothlisberger5 ABSTRACT.—We compared the maximum scotopic visual sensitivity of 4 species of trout from twilight (mesotopic) to fully dark-adapted vision. Scotopic vision is the minimum number of photons to which a fully dark-adapted animal will show a behavioral response. A comparison of visual sensitivity under controlled laboratory conditions showed that brown trout (Salmo trutta) and brook trout (Salvelinus fontinalis) had maximum scotopic thresholds (1.1 × 10–4 μmol ⋅ m–2s–1, ~0.005 lux) 2 times lower than rainbow trout (Oncorhyncus mykiss) and Snake River cutthroat trout (Oncorhynchus clarki bouvieri), which did not differ from each other (2.1 × 10–4 μmol ⋅ m–2s–1, ~0.01 lux). A literature review tended to corroborate these results in that brown trout and brook trout were reported to be more active during the night and at twilight than cutthroat trout and rainbow trout. We also measured light intensity within open versus shaded reaches during the day, dusk, and night in 3 Rocky Mountain streams. The scotopic sensitivity of brown trout and brook trout was sufficient to allow foraging during all twilight periods and under average nighttime light intensities in open and shaded reaches, whereas the scotopic sensitivity of rainbow trout and cutthroat trout may restrict their foraging to rela- tively bright nocturnal conditions (twilight or a moonlit night). Native cutthroat trout restoration efforts may have greater success in open versus shaded stream reaches in the Rocky Mountains and elsewhere. Key words: light sensitivity, scotopic vision, cutthroat restoration, salmonids. Three attributes of light can affect trout electrophysiological studies, although valuable, vision: (1) intensity (photons ⋅ area–1time–1), were not reliable indicators of the response of (2) spectral composition (wavelength [nm]), and the whole animal: “Only behavioural (psycho - (3) polarization (the major plane of vibration in physical) studies can tell us what the animal’s which most photons oscillate). Recent research visual system is truly capable of achieving.” has demonstrated that representatives of the Photoreceptor cells (rods and cones) respond major extant clades of Salmoninae (i.e., rainbow to the number of photons striking the retina. trout, cutthroat trout, brook trout, brown trout, Scotopic vision is not possible until sufficient and Atlantic salmon) are able to detect polarized photons have struck the retina to excite a ner- light (Coughlin and Hawryshyn 1995, Novales- vous impulse (e.g., Partridge 1990). Maximum Flamarique and Hawryshyn 1997, Parkyn and sensitivity to dim light has been defined as the Hawryshyn 2000) and can see light of varying minimum number of photons to which a fully irradiance and spectral composition, including dark-adapted animal will show a behavioral ultraviolet, blue, green, yellow, and red (e.g., response (Douglas and Hawryshyn 1990). Dark- Douglas 1982, Bowmaker and Kunz 1987, adapted scotopic vision is produced by a num- Hawryshyn et al. 1989, Deutschlander et al. ber of electrophysiological and biomechanical 2001). Most of these studies have examined changes in the retina (e.g., Bowmaker 1990, the mechanisms underlying trout vision at the Wagner 1990). Photopic vision occurs during cellular/physiological level using isolated tissues the day, whereas mesotopic vision is interme- or induced immobilization of whole organisms diate between photopic and scotopic vision. (e.g., Hawryshyn and McFarland 1987, Haw - Twilight periods span the transition from pho- ryshyn et al. 1989), whereas far fewer studies topic to scotopic vision. We compared the have examined the behavioral effects of these maximum scotopic sensitivity of 4 species of physiological differences in trout vision. Dou- trout from twilight (mesotopic) to fully dark- glas and Hawryshyn (1990) emphasized that adapted vision. Maximum scotopic sensitivity 1USDA Forest Service, Rocky Mountain Research Station, 222 South 22nd Street, Laramie, WY 82070. 2Present address: Department of Integrative Biology, Brigham Young University, Provo, UT 84602-5181. E-mail: [email protected] 3Present address: Parsons Environmental Consulting, 1700 Broadway, Suite 900, Denver, CO 80290. 4Present address: Rocky Mountain Research Station, Forestry Sciences Laboratory, 800 East Beckwith, Box 8089, Missoula, MT 59807. 5University of Notre Dame, Department of Biological Sciences, Box 369, Notre Dame, IN 46556. 524 2007] SCOTOPIC SENSITIVITY OF TROUT 525 in dark-adapted specimens of 4 species of trout determine the maximum amount of time dif- was determined by the earliest commencement ferent species can forage in different reach of visual behavior during a simulated dawn. types. In the Rocky Mountains, introduced brook Our objectives were to (1) experimentally trout, brown trout, and rainbow trout (common compare the scotopic visual sensitivity of brook names follow Nelson et al. 2004) have displaced trout, brown trout, fine-spotted Snake River native cutthroat trout, reducing their distribu- cutthroat trout, and rainbow trout, (2) measure tion to a small fraction of their historic range light intensity within open versus shaded (e.g., Young et al. 1996). Introduced trout may reaches during the day, dusk, and night in 3 grow faster and achieve a greater reproductive high-elevation mountain streams, and (3) review output than native cutthroat trout if they can the literature on the diel activity of trout. feed longer because of a greater scotopic sen- sitivity. Thus, scotopic sensitivity may partially METHODS explain the ability of introduced trout to exclude native cutthroat trout. Laboratory Tests of Scotopic Sensitivity We are aware of only 3 behavioral studies All fish used in this study, as in other studies using whole organisms to compare the scotopic on trout vision (e.g., Allen et al. 1973), were vision of different salmonid species. Henderson raised in fish hatcheries (2 in Wyoming and 1 in and Northcote (1985) found that lake popula- Colorado) because differences in the rearing tions of Dolly Varden (Salvelinus malma) for- environment in a natural setting might have led aging under dim light were better at detecting to variation in sco topic sensitivity. We selected prey than cutthroat trout (Oncorhynchus clarki hatcheries with similar temperatures (12°– clarki). Similarly, Robinson and Tash (1979) 15°C), water depths, water quality, food type, found that brown trout (Salmo trutta) were and structure (open raceways) to minimize more efficient at eating brine shrimp at lower environmental effects on differences in sco- light levels (starlight > 0.001 lux) than Apache topic vision. None of the hatcheries were trout (Oncorhynchus gilae apache). These data shaded. We selected fish of each species within indicate that at least 1 species of brook trout and the same size range (25–30 cm) because the brown trout have greater scotopic sensitivity number of visual receptors (rods and cones) than cutthroat trout. Confer et al. (1978) found and the concentration of scotopic pigments that the reaction distance of lake trout (Salmo (rhodopsin and porphyropsin) increase as trout namaycush) and brook trout (Salmo fontinalis) to grow, making larger fish more sensitive to dim planktonic prey was similar at illuminances light than smaller fish (e.g., Allen et al. 1982). equal to 1.0 lux, suggesting that different We determined the scotopic sensitivity of 30 species in the same genus may have similar adult fish from each of the 4 salmonid species scotopic sensitivity. by recording the intensity of light at which in - Thus, we hypothesized that the scotopic dividual fish first responded to a hand breaking vision of brown trout and brook trout would the path of light directly overhead or to food be more sensitive than that of fine-spotted floating at the surface of the water (hatchery Snake River cutthroat trout (Oncorhynchus pellets, Purina Trout Chow). Fish appeared to clarki bouvieri). However, we had no basis for be startled by hand waving, which creates a predicting possible differences in the scotopic shadow over the entire retina that can be per- sensitivity among rainbow trout (Oncorhynchus ceived without highly acute vision. This startle mykiss), fine-spotted Snake River cutthroat response to hand waving should occur at lower trout, brown trout, and brook trout, because of light levels than a response that requires some the absence of previous research. Similarly, level of acuity, such as the detection and loca- there are no studies documenting 24-hour fluc - tion of drifting food. Also, trout may fail to re - tuations in light intensity in stream ecosystems spond to food after visual detection, even when (day, twilight, and night). Field measurements, they are starved, because of differences in in - combined with laboratory experiments to deter- dividual behavior, whereas hand waving will mine the scotopic sensitivity of these trout, al - elicit a consistent reaction, as if to a predator, lowed us to determine the percentage of time and should provide a less variable signal of the that light levels are greater than scotopic threshold number of photons striking the retina thresholds for each species. These percentages to excite vision and a subsequent response. 526 WESTERN NORTH AMERICAN NATURALIST [Volume 67 Fig. 1. Laboratory set-up for determining the maximum
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