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Home , Photopic vision, Scotopic vision

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. 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 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 . 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). 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 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 scotopic 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 ( 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 scotopic sensitivity of brook trout (Salvelinus fontinalis), brown trout (Salmo trutta), fine-spot Snake River cutthroat trout (Oncorhynchus clarki bouvieri), and rainbow trout (Oncorhynchus mykiss).

These experiments were conducted in an under complete darkness with the aid of a hand- oval recirculating laboratory stream (Frigidunits held infrared flashlight (1000 nm–0.01 cm) and Inc., Toledo, OH, www.frigidunits.com; Fig. 1). nightscope (model 260, ITT G3 Night Mariner The experimental and nonexperimental sections Binoculars, www.ittnv.com) that magnified light were layered with natural gravels obtained from ranging from 400 nm to 0.01 cm to 50,000 times Nash Fork Creek in Wyoming. Water depth brighter than ambient. Fish cannot see in the was 30 cm, current velocity 10 cm ⋅ s–1, and infrared spectrum (Ali 1961) and thus are not temperature 13°–15°C. The stream was housed disturbed when observed with infrared radia- in a large room enclosed in a warehouse to tion (Fraser et al. 1993). block extraneous light. A window was blocked We connected 2 custom-made dim-light with three layers of black plastic during exper- sensors (Skye Instruments Ltd., Wales, U.K., imental observations. The laboratory stream, www.skyeinstruments.com), 1 that measured including the tent where we stood to make total illuminance and 1 that measured total irra- observations, was also enclosed in 3 layers of diance, to a data logger (LI-COR 1000, www black plastic (Fig. 1). Observers were sepa- .licor.com) and positioned them 5 cm above the rated from the experimental section of the art - water’s surface to record the light intensity at ificial stream by 3 additional layers of black which fish first responded to hand waving or plastic with a cutout viewing port (25 × 40 cm). food. The irradiance sensor had a flat spectral Fish were observed and instruments were read response across the entire range of detectable 2007] SCOTOPIC SENSITIVITY OF TROUT 527 wavelengths (400–720 nm) and a sensitivity of 3 pieces of neutral shade cloth. The light 2.0 × 10–5 μmol ⋅ m–2s–1 to 1.6 μmol ⋅ m–2s–1, inten sity of the bulb was controlled by a com- whereas the illuminance sensor had a sensitivity puter-operated rheostat (Solar 1000, Niche Engi- of 0.0001–80 lux with a bell-shaped spectral neering) that gradually increased the voltage response curve across the range of wave- and the irradiance at the specified rate. A sim- lengths in this study (400–720 nm). This range ilar method of gradually increasing light inten- from blue (400 nm) to deep red (720 nm) was sity to simulate a natural sunrise has been pre- appropriate for this study because trout cannot viously designed for a variety of laboratory see infrared radiation (approximately >720 nm) uses (Allen 1980). and because there is very little light <400 nm We used an SR9000 spectroradiometer (Ma - (UV) in the natural environment during twi- cam Photometrics, www.macam.com) to com- light or at night after the sun has dropped below pare the spectral composition of our incandes- the horizon (e.g., Williamson 1995, Rader per- cent bulb to the natural spectrum at dawn, sonal observation). This is also the range of light dusk, and night at 3 levels of intensity: 2.0 × most available at twilight and at night and is 10–3 w ⋅ m–2nm–1 (~0.5 lux), 3.8 × 10–4 w ⋅ thus the most important range in dim-light m–2nm–1 (~0.1 lux), and 1.89 × 10–4 w ⋅ studies. m–2nm–1 (~0.05 lux). A decrease in voltage at We decided to report part of our results in bright intensities can cause the spectrum of in- lux because (1) the lux sensor allowed us to candescent bulbs to change, progressively pro - compare our results with previous behavioral ducing smaller proportions of blue light. How- studies on the visual response of salmonids (e.g., ever, decreasing the voltage from dim light to Robinson and Tash 1979, Mazur and Beau - lower intensities of dim light did not change the champ 2003), (2) data from both sensors were spectrum, which was skewed toward a greater highly correlated and provided similar results proportion of red light (Fig. 2). over the range of wavelengths used in this study We decided to use an incandescent bulb (400–720 nm), and (3) illuminance allowed us rather than a full-spectrum fluorescent light to compare our lab results with our field mea- because we could gradually increase the inten- surements, which were recorded with lux sen- sity of the incandescent bulb using the com- sors during the daylight hours. The critical in - puter-operated rheostat to simulate a natural formation (the maximum scotopic sensitivity dawn. The intensity of full-spectrum is of these species) will be reported as both irra- often controlled with a wedge-shaped neutral diance and illuminance. density optic filter (e.g., Sontag 1971). However, Each trial began in complete darkness and this requires immobilizing an animal and re - light levels were gradually increased at a rate straining it to a specific area, thus precluding of 22.0 × 10–4 μmol ⋅ m–2min–1 (0.005 lux ⋅ behavioral analyses. Also, a preliminary exercise min–1). We collected preliminary data during 2 showed that adding or removing single layers of sunrises under clear skies in June 1997 to dup- fine shade cloth from a full-spectrum light pro - licate in the laboratory the natural rate at which vided a step-wise increase in light intensity that light increases. We used our custom-made dim- was too coarse for our objectives. light sensors to record light intensity every Each species was tested separately during second for 90 minutes before the sun crested the same time of year because previous research the horizon. Values varied between 6.1 × 10–5 has shown that trout scotopic visual pigments μmol ⋅ m–2min–1 (0.003 lux ⋅ min–1), during increase during the winter and that this increase the early transition from dark to light, to 2.5 × is associated with an increase in nocturnal 10–2 μmol ⋅ m–2min–1 (1.2 lux ⋅ min–1), as the behavior (e.g., Allen et al. 1982, Rimmer and sky grew progressively lighter. We used the Paim 1989). Cutthroat trout and brook trout average rate of increase during the 1st and trials were completed during August and Sep- darkest half of the transition from dark to light, tember 1997, and rainbow and brown trout tri- which is also consistent with the natural rate als were completed in August and September of change measured at early twilight (dusk and 1999. Fish were transported from the hatcheries dawn) by Fraser and Metcalfe (1997). To dupli - to our laboratory within 24 hours in a 3000-L cate the natural rate of irradiance increase in aerated tank. Thirty individuals of each species the laboratory, it was necessary to wrap the light were tested over a 10-day period (3 fish per source (15-watt incandescent tungsten bulb) in day). All fish were tested from 09:00 to 16:00 528 WESTERN NORTH AMERICAN NATURALIST [Volume 67

Fig. 2. Spectral composition of our laboratory light source (incandescent bulb) at 3 levels of intensity: 2.0 × 10–3 w ⋅ m–2nm–1, ~0.5 lux (A); 3.8 × 10–4 w ⋅ m–2nm–1, ~0.1 lux (B); and 1.89 × 10–4 w ⋅ m–2nm–1, ~0.05 lux (C). during each trial. Before a trial, each fish was minutes and 6 feeding possibilities, the smell of starved for 72 hours and dark-adapted for 8 food should have initiated a feeding response as hours. All fish were exposed to a diel cycle of the light levels increased. The fish had 15 sec- 12 hours of night and 12 hours of day under onds to locate the food during each 30-second full-spectrum fluorescent lights for at least 7 interval before the pellet exited the experi- days prior to being dark-adapted. Under com- mental section. Every 30 seconds a hand was plete darkness, we removed a single fish from waved 4 times, without touching the water, the holding section, placed it in the observation directly above the fish. At the 4th minute, irra- area, and provided a 40-minute acclimation diance began to increase (22.0 × 10–4 μmol ⋅ period (Fig. 1). Trials did not begin until each m–2min–1, 0.005 lux ⋅ min–1), and food additions fish was calm and facing upstream. Examining and waving continued at 30-second intervals for each fish alone eliminated the effects of intra - 20 minutes. After 20 minutes irradiance reached specific interactions on their behavior, which 0.04 μmol ⋅ m–2s–1 (0.1 lux), which is the ap- could cause some fish to fail to respond to a proximate irradiance of a clear night with a full visual signal. moon (Contor and Griffith 1995). We used a We also needed to determine if these fish nightscope to record the light level when a fish could respond to food pellets by olfaction with - first responded to either hand waving or when out a visual cue. Therefore, a trial began by ad- it first oriented toward and responded to food. ding 2 food pellets every 30 seconds upstream In order to prevent disturbing the fish, waving from the experimental section for 3 minutes stopped after the 1st response; however, food under complete darkness to ensure that fish was added every 30 seconds throughout the 20- could not locate pellets by olfaction. Also, after 3 minute trial. If a fish failed to respond, it was 2007] SCOTOPIC SENSITIVITY OF TROUT 529 replaced with another fish and the trial was period at each station, and nighttime intensity rerun. was measured during each phase of the lunar cycle (no moon, part moon, or full moon). Sen- Field Light Measurements sors were leveled in the same position on the We measured light intensity in a shaded bank 0.5 m from the surface of the water at reach and in an open reach in 3 Rocky Moun- each station on each sampling date. These tain streams during the day, dusk, and night to cylindrical sensors primarily detect light from estimate the amount of time different species directly overhead, which was appropriate can forage in different reach types. West St. because light arriving directly from its source Louis Creek is a 2nd-order tributary of St. Louis (moon and stars) constitutes the majority of Creek, which is a 3rd-order mountain stream the total intensity at night (Endler 1993). draining the USDA Fraser Experimental Forest The averages of flow, width, percent shade, in Grand County, Colorado (latitude 39°53N, gradient, and maximum pool depth were cal- longitude 105°54W). Nash Fork Creek is a 3rd- culated for each reach in each stream. Average order stream draining the eastern slope of the percent shading was digitally calculated using Medicine Bow Mountains in Albany County, photographs taken from the same height (1.83 65 km west of Laramie, Wyoming (latitude m) in the middle of the stream with a wide- 41°21N, longitude 106°13W). Riparian vege- angle lens aimed directly overhead into the can - tation along shaded stream reaches consisted opy at 6 locations in each reach. of lodgepole pine (Pinus contorta), spruce (Picea Literature Review on the spp.), and fir (Abies lasiocarpa), but vegetation Diel Activity of Trout along reaches with an open canopy was domi- nated by low-growing willows (Salix spp.) and We reviewed the literature describing the grasses. All reaches were located at similar ele- diel activity of trout because differences in the vations (~2800 m asl), and the open reaches time at which fish are most active should reflect were downstream from and adjacent to the differences in scotopic visual sensitivity. For steeper, shaded reaches. each study we recorded the primary period(s) We used our custom-made low light sensors of activity and indicated the strength of evi- (lux and μmol ⋅ m–2min–1) to measure dim lev- dence supporting the conclusions. Results from els of light (last part of dusk and night) and a casual or haphazard observational data were standard bright-light lux sensor (LI-210, LI- less conclusive than systematic 24-hour obser- COR Biosciences, www.licor.com) to measure vations, day versus night gut analyses, tracking illumination during the day and the 1st part of of 24-hour activity patterns using radioteleme- dusk. Although we were interested in dim-light try, or laboratory experimental data. differences in light intensity, the bright-light Statistical Analysis lux sensors (400–720 nm) were included to show relative differences between shaded and A 1-way ANOVA and Tukey’s multiple open reaches. Thus, dim and bright readings comparison tests (SAS Institute, Inc. 1997) were expressed in lux because we only had lux with 4 levels (salmonid species) were used to sensors for bright light. compare the average light intensity of the 1st We evaluated light intensity with respect to response of individual fish to either hand wav- (1) time of day, (2) cloudiness, (3) the lunar ing or food in our laboratory experiment. Tests cycle, and (4) shading by riparian vegetation. for normality and homoscedasticity indicated Light intensity was measured during day that the data were skewed for 2 of the 4 (11:00–18:00), dusk (19:30–21:30), and night species. Therefore, analyses were run after a (23:00–02:00) once a week for 7 weeks (July and loge transformation. August 1999) at 3 stations in the shaded reaches and 3 in the open reaches in each RESULTS stream. The mean, minimum, and maximum light intensity was recorded at each station Laboratory Tests of Scotopic every 5 seconds for six 15-second intervals Visual Sensitivity evenly spaced over a 20-minute period during No fish responded to food (or waving) during the times indicated above. The weather (e.g., the 3-minute dark phase at the beginning of cloudy versus clear) was noted during each each trial. This indicated that subsequent 530 WESTERN NORTH AMERICAN NATURALIST [Volume 67

TABLE 1. Physical attributes of shaded and open reaches in 3 Rocky Mountain streams.

______St. Louis Creek ______West St. Louis Creek ______Nash Fork Creek Shaded Open Shaded Open Shaded Open Mean flow (m3 ⋅ s–1) 0.093 0.098 0.039 0.055 0.072 0.068 Mean bankfull width (cm) 687 1740 273 320 635 830 Mean percent shade410700640 Mean gradient (%) 2.1 1.5 3.1 1.7 3.6 0.6 Mean maximum pool depth (cm) 51 59 29 45 34 63

0.025 ~0.0054 lux) and brook trout (9.4 × 10–5 μmol ⋅ m–2s–1, ~0.0047 lux) was approximately half 0.020 that of cutthroat trout (2.5 × 10–4 μmol ⋅ m–2s–1, ~0.013 lux) and rainbow trout (2.2 × –4 –2 –1 0.015 10 μmol ⋅ m s , ~0.012 lux). The brightest in tensity at which brook trout first responded × –4 μ ⋅ –2 –1 0.010 (1.5 10 mol m s , ~0.0068 lux) was less than the dimmest intensity at which cut- throat trout (1.9 × 10–4 μmol ⋅ m–2s–1, ~0.01 Light Intensity (lux) 0.005 lux) and rainbow trout (1.9 × 10–4 μmol ⋅ m–2s–1, ~0.01 lux) first responded (Fig. 3). 0.000 Also, brown trout’s first response was at a dim- S. trutta S. fontinalis O. clarki O. mykiss mer light level (2.36 × 10–4 μmol ⋅ m–2s–1, Species ~0.00012 lux) than for any of the other ’ first responses, whereas cutthroat trout’s first Fig. 3. Differences in the mean maximum scotopic sen- response was at the brightest (4.2 × 10–4 μmol ⋅ sitivity of 4 species of trout. Bars represent 1 standard m–2s–1, ~0.02 lux). error about the mean, and stars are the extreme high and low responses of individual trout within each species. The spectral composition of our lab light was shifted toward longer wavelengths: orange and especially red (Fig. 2). Blue and green wave- re sponses as light intensity increased were lengths were poorly represented. Thus, differ- visual and not olfactory. Twelve fish (2 cutthroat ences in dim-light sensitivity between the 4 trout, 4 brown trout, and 6 brook trout) out of species in this study are based primarily on 120 failed to respond during this experiment, their response to light with longer wavelengths. and each was replaced by another fish. As expected, all 4 species were startled and reacted Field Light Measurements first to waving rather than food. Thirty-eight As expected, shading and light intensity var - percent of the fish did not feed at any point dur- ied by stream and time of day (Fig. 4). St. Louis ing a trial, although 21% rose to a floating pellet Creek was the largest stream and had the least with out actually feeding. Because of this varia- shade, whereas West St. Louis Creek and Nash tion we did not analyze their response to food as Fork Creek were smaller with a dense canopy a reliable indication of the maximum dim-light over the shaded reaches (Table 1). Pool depth intensities at which these species could first is important because most trout in these streams detect food floating at the surface. However, the (brook trout) reside in pools and because light dim-light threshold showing a startle response can rapidly attenuate with an increase in water was consistent across each species. Thus, the depth (e.g., Wetzel 2001). However, there were startle response was the basis for our dim-light no pools deeper than 75 cm in any of the comparisons in this study. reaches, and most were <60 cm deep. Thus, The irradiance at which fish first reacted to our light sensors, which were positioned just waving was significantly lower (F3, 116 = 64, P above the surface of the water, provided a good < 0.0001) for brown trout and brook trout than estimate of the relative differences in the light for cutthroat trout and rainbow trout (Fig. 3). available to fish in the different reaches. The average light intensity of the 1st response Light intensity varied 9 orders of magnitude of brown trout (1.1 × 10–4 μmol ⋅ m–2s–1, between extreme conditions: a clear sunny day 2007] SCOTOPIC SENSITIVITY OF TROUT 531

Fig. 4. Mean differences in light intensity during the day, dusk, and night between reaches with a closed (A) and open (B) canopy in 3 mountain streams. Bars represent 1 standard error about the mean, and stars are the extreme high and low values for each period. The line is a generalized curve for a 24-hour period. in the open versus a clear moonless night in the As expected, cloudiness greatly reduced irra- shade. However, the level of starlight on a clear diance in both open and shaded reaches. Con- moonless night in the shade was below the de - trary to expectations, however, average light tection limit of our dim-light sensors. Average intensities at night were similar in the open and irradiance at dusk and the brightest nighttime shaded reaches (1.61 × 10–4 μmol ⋅ m–2s–1, conditions (clear, full moon) were both 5 times ~0.008 lux and 1.47 × 10–4 μmol ⋅ m–2s–1, greater in the open than in the shade (Fig. 4). ~0.007 lux, respectively) because, by chance, 532 WESTERN NORTH AMERICAN NATURALIST [Volume 67 we made more nighttime measurements under orange and especially red at all of the dim- cloudy conditions in the open than in the shade. light intensities used in this study. Thus, in Our results are consistent with the summary order to place these findings in their correct provided by Contor and Griffith (1995) in which environmental context, we need to discuss the the intensity of starlight and moonlight in the availability of light with longer wavelengths open can vary between 0.0005 lux and 0.001 lux under dim-light conditions in the natural en - and between 0.05 lux and 1.0 lux, respectively. vironment. That is, the application of our lab results to a natural setting depends on whether Trout Diel Activity the predominant wavelengths in the field We found 28 studies that reported the diel under dim light (twilight, moonlight, starlight) activity of brown trout, 23 for cutthroat trout are often skewed toward longer wavelengths, and rainbow trout, and 10 for brook trout (Table especially red. 2). Brown trout and brook trout had the most Although longer wavelengths attenuate rap - frequent occurrence of activity under dim-light idly with increasing water depth (Wetzel 2001), conditions. Seventy-five percent of the studies red light should be plentiful in most mountain reported twilight and/or nocturnal activity for streams because fish habitats (pools and runs) brown trout, 70% for brook trout, and 39% for are often <50 cm deep. In distilled water, 50% cutthroat trout + rainbow trout. Also, brown of red light remains at approximately 1 m in trout had the highest percentage of reported depth (Wetzel and Likens 1991). Thus, 75% or nighttime activity (64%) followed by brook trout more of the ambient red light should remain (30%) and cutthroat trout + rainbow trout after attenuation in most pool habitats in these (13%). streams. During twilight as the sun approaches and DISCUSSION initially drops below the horizon the spectrum is skewed towards red and blue light with a We have shown that the maximum scotopic 33% reduction in green, yellow, and orange light threshold of brown trout and brook trout was (Johnson et al. 1966, McFarland and Munz more sensitive than that of cutthroat trout and 1976). However, as the sun continues to drop rainbow trout. Confounding factors did not below the horizon, red light decreases and the compromise these results because all of these spectrum becomes increasingly blue because fish were (1) raised in hatcheries under similar blue light is the dominant color of skylight. light conditions, (2) similar in size, and (3) tested Thus, early twilight is dominated by red light during the same season at the same tempera- directly from the sun and blue skylight, and late tures. Also, these results were generally sup- twilight is dominated by blue skylight unless ported by our literature review in that a greater there are clouds overhead. Reddish light from percentage of studies reported dim-light activity the setting sun will reflect off of the undersur- for brown trout and brook trout than for cut- face of clouds onto the surface of a stream, throat trout and rainbow trout, which were prolonging the period when wavelengths are primarily diurnal. Brook trout and brown trout skewed toward red (Endler 1993). Clouds pro- had average scotopic thresholds near 1.0 × duce a flat, white spectrum on the surface of a 10–4 μmol ⋅ m–2s–1 (~0.005 lux), whereas stream only if the sun shines through them from Snake River cutthroat trout and rainbow above (McFarland and Munz 1976, Endler trout had average thresholds near 2.0 × 10–4 1993). μmol ⋅ m–2s–1 (~0.01 lux). These thresholds Although the moon reflects sunlight and has underestimated the scotopic sensitivity of a fairly flat spectrum, it is enriched in red wave - these fish because in tensity was measured lengths relative to full sunlight (McFarland and near the surface of the water and not in the Munz 1976). Also, when the moon is low on the water where the fish were swimming. How- horizon, its light must pass through more of the ever, actual thresholds should be only slightly Earth’s atmosphere, causing an additional shift lower because the water in our experimental towards the red end of the spectrum. The spec- stream was shallow, clear, and pro duced a mini- trum of starlight is also skewed toward red mum amount of attenuation. wavelengths (Munz and McFarland 1973). Ad - The light source in our laboratory experi- ditionally, McFarland and Munz (1976) mea- ment was skewed toward longer wavelengths of sured the daylight spectrum of Carrabelle River 2007] SCOTOPIC SENSITIVITY OF TROUT 533

TABLE 2. Literature review of the diel activity of several salmonid species. Strength of evidence is recorded in the last column (1 = haphazard observational data, 3 = systematic observational data / diel gut analysis, 5 = telemetry/ experimental data). Species Diel periodicity Citation Evidence Oncorhynchus apache Diurnal Robinson and Tash 1979 5 Oncorhynchus clarki Diurnal Griffith 1974 1 O. clarki Diurnal Edmundson et al. 1968 1 O. clarki pleuriticus Diurnal Young et al. 1997a 5 O. clarki clarki Nocturnal Schutz and Northcote 1972 5 Oncorhynchus mykiss Crepuscular Newman 1956 1 O. mykiss Crepuscular Elliott 1970 3 O. mykiss Crepuscular Elliott 1973 3 O. mykiss Crepuscular Douglas 1982 5 O. mykiss Crepuscular Jenkins et al. 1970 5 O. mykiss Crepuscular Landless 1976 5 O. mykiss Diurnal Edmundson et al. 1968 1 O. mykiss Diurnal Eggers 1977 1 O. mykiss Diurnal Hoar 1953 1 O. mykiss Diurnal Angradi and Griffith 1990 3 O. mykiss Diurnal Tippets and Moyle 1978 3 O. mykiss Diurnal Campbell and Neuner 1985 3 O. mykiss Diurnal Young et al. 1997a 5 O. mykiss Diurnal Bisson 1978 5 O. mykiss Diurnal Boujard and Leatherland 1992 5 O. mykiss Fed at light levels >0.035 lux Tanaka 1970 5 O. mykiss Nocturnal Elliott 1973 3 O. mykiss Nocturnal Jenkins 1969 5 Salvelinus alpinus Nocturnal Dervo et al. 1991 3 Salvelinus fontinalis Crepuscular Newman 1956 1 S. fontinalis Crepuscular Boisclair 1992 3 S. fontinalis Crepuscular Hoar 1942 5 S. fontinalis Crepuscular Gibson and Keenleyside 1966 5 S. fontinalis Diurnal Griffith 1974 1 S. fontinalis Diurnal/crepuscular Allan 1981 3 S. fontinalis Continuously active Rader unpublished data 3 Salvelinus malma Diurnal Edmundson et al. 1968 1 S. malma Nocturnal Schutz and Northcote 1972 5 Salmo salar Crepuscular Hoar 1942 5 S. salar Diurnal Fraser et al. 1993 5 S. salar Diurnal Gibson and Keenleyside 1966 5 Salmo trutta Continuously active Tuša 1968 1 S. trutta Continuously active McIntosh and Townsend 1995 5 S. trutta Continuously active Oswald 1978 5 S. trutta Crepuscular Eriksson 1978 1 S. trutta Crepuscular McCormack et al. 1989 5 S. trutta Diurnal Bachman 1984 3 S. trutta Diurnal Borja et. al 1990 5 S. trutta Diurnal/crepuscular Swift 1962 3 S. trutta Diurnal/crepuscular Swift 1964 3 S. trutta Diurnal/crepuscular Elliott 1970 3 S. trutta Nocturnal Brynildson et al. 1963 1 S. trutta Nocturnal Butler and Hawthorne 1968 1 S. trutta Nocturnal Jenkins 1969 1 S. trutta Nocturnal Lewis 1969 1 S. trutta Nocturnal Dervo et al. 1991 3 S. trutta Nocturnal Shuler et al. 1994 3 S. trutta Nocturnal Chaston 1968 3 S. trutta Nocturnal Chaston 1969 3 S. trutta Nocturnal Elliott 1967 3 S. trutta Nocturnal Elliott 1973 3 S. trutta Nocturnal Young et al. 1997b 5 S. trutta Nocturnal Clapp et al. 1990 5 S. trutta Nocturnal Schutz and Northcote 1972 5 S. trutta Nocturnal Robinson and Tash 1979 5 534 WESTERN NORTH AMERICAN NATURALIST [Volume 67 in Florida and found that there was no light 1984, McIntosh et al. 1994). The ability of brook with a wavelength shorter than 600 nm during trout and brown trout to feed longer over a 24- the day in this blackwater river. This redshift is hour period may allow them to sustain or even caused by plant leachates (e.g., tannins) that are increase this initial size advantage, which allows often abundant in the groundwater associated them to maintain a greater overall fitness than with stream ecosystems. Thus, the prevalence of cutthroat trout. This fitness advantage may be a red-shifted spectrum in streams may also de - the best explanation for how introduced trout pend on the concentration of plant leachates in (brook trout and brown trout) can cause the the groundwater and the amount of ground- local extirpation of native cutthroat trout. water inflow. Overall, this information suggests Native cutthroat trout may be better able to that dim-light conditions in streams are often compete with introduced trout in open reaches skewed toward red wavelengths. Thus, our lab because brighter light intensities may reduce results do represent differences in sensitivity the foraging advantage of brook trout and between these species under frequent natural brown trout. Light intensities from mid-twilight conditions. However, we cannot eliminate the to a moonless, starlit night were about 5 times possibility that the variation in scotopic sensitiv- greater in open reaches than in shaded reaches ity among these species could change if similar of this study. In open reaches, cutthroat trout lab studies were conducted with predominantly may be able to forage longer with greater effi- blue light. ciency during the growing season than in Trout are visual predators, and light is one of darker, shaded reaches. This suggestion is con- the most important factors determining prey sistent with the observation that coastal cut- detection (e.g., Wilzbach et al. 1986, Forrester throat trout foraging efficiency and abundance et al. 1994). Over a 24-hour period, trout with were greater in logged headwater streams of sensitive scotopic vision will be able to forage the Oregon Cascades than in reaches shaded longer than trout with poor scotopic sensitivity. by stands of mature riparian vegetation (Hawk- Species with better dim-light vision could have ins et al. 1983, Wilzbach and Cummins 1986). If higher 24-hour rates of consumption. Because so, native cutthroat trout restoration efforts may food may limit trout populations (Chapman have greater success in open versus shaded 1966, Richardson 1993), higher rates of con- stream reaches in the Rocky Mountains and sumption could produce faster growth and elsewhere. greater fecundity. The light intensity necessary Future research should extend the applica- to invoke a startle response was 2 times lower tion of our results on the scotopic sensitivity of in brown trout and brook trout than in Snake Snake River cutthroat trout to all cutthroat lin- River cutthroat trout and rainbow trout. Our eages. It should examine the underlying phys- literature review showed that cutthroat trout iological mechanisms explaining differences in and rainbow trout were primarily active during scotopic sensitivity among these species. Also, the day, which suggests that cutthroat trout as future research should explore the relation- a group may have poorer scotopic vision than ship between the maximum scotopic threshold brook trout or brown trout. If so, these 2 species of cutthroat trout, their foraging efficiency, and may be able to forage longer over a 24-hour their overall fitness versus that of introduced period and during the course of a growing sea- trout in open and shaded reaches. son than most, if not all, cutthroat lineages. This may partially explain how brook trout and ACKNOWLEDGMENTS brown trout exclude most cutthroat trout pop- ulations in many mountain streams of the west- We are grateful for the dedication of our ern United States (e.g., Behnke 1992). undergraduate research assistants—Ken Ayres, Adult brook trout and brown trout spawn in Galen Cook, Andy Davis, and Valerie Mason— the fall, and young fish hatch early in the spring, in helping to gather the field light data. Clinton giving them a size advantage over the fry of R. Rader donated numerous hours of volunteer cutthroat trout, which spawn during the spring work. William N. McFarland made helpful com- and hatch later in the summer (e.g., Behnke ments at the outset of this study, and Robert 1992). For a variety of reasons, large body size is R. McDougal (U.S. Geological Survey) pro- an important factor in determining differences vided spectral analysis of our laboratory light in the fitness of stream salmonids (e.g., Fausch source. This work was sponsored by the Rocky 2007] SCOTOPIC SENSITIVITY OF TROUT 535

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