Transactions of the American Fisheries Society 130:46–52, 2001 q Copyright by the American Fisheries Society 2001
R
USSELL
W. P
ERRY
, 1 N
OAH
S. A
DAMS
,*
AND
D
ENNIS
W. R
ONDORF
U.S. Geological Survey, Biological Resources Division,
Western Fisheries Research Center, Columbia River Research Laboratory,
5501A Cook-Underwood Road, Cook, Washington 98605, USA
Abstract.—We investigated the effect of two different sizes of surgically implanted transmitters on the buoyancy compensation of juvenile chinook salmon Oncorhynchus tshawytscha. We determined buoyancy by measuring the density of fish with a filled air bladder in graded salinity baths.
In addition, we examined the effect of pressure changes on buoyancy by measuring the pressure reduction (P
R
) at which fish became neutrally buoyant. We found no significant difference between the density of control and tagged groups, indicating that fish were able to compensate for the transmitter by filling their air bladders. However, both groups of tagged fish had significantly lower P
R than control fish. Regression analysis of fish density on P
R indicated that density of the tagged groups changed at a higher rate than that of the controls. As a result, tagged fish attained neutral buoyancy with less pressure reduction even though the tagged and control groups exhibited similar densities. This relation was confirmed by using Boyle’s law to simulate buoyancy changes with change in depth. Although fish compensated for the transmitter, changes in depth affected the buoyancy of tagged fish more than that of untagged fish. Reduced buoyancy at depth may affect the behavior and physiology of tagged juvenile salmonids, and researchers should be aware of this potential bias in telemetry data. In addition, there was little difference in P
R of the density
2
P
R or the slope regression lines between tagged groups. This was caused by the small difference in excess mass (i.e., weight in water) of the two transmitters. Thus, although two transmitters may not weigh the same, their effects on buoyancy may be similar depending on the excess mass.
Biotelemetry has been used extensively to monitor the activities of avian, terrestrial, and aquatic animals. Because fish are difficult to observe visually in the wild, biotelemetry allows researchers to gather data on fish movements that would otherwise be unobtainable. However, the validity of using this information to make inferences about an entire population hinges on the assumption that fish movements are unaffected by transmitters. To legitimately make this assumption, however, requires knowledge of whether the transmitter affects fish physiology and behavior.
Many studies have examined the effects of transmitters on physiological indicators such as growth and swimming performance (McCleave and Stred 1975; Mellas and Haynes 1985; Greenstreet and Morgan 1989; Moser et al. 1990; Adams et al. 1998a, 1998b). However, little research has investigated a transmitter’s effect on buoyancy compensation. Gallepp and Magnuson (1972) found that induced negative buoyancy owing to weight insertion caused bluegills Lepomis macro-
* Corresponding author: noah p adams@usgs.gov
1 Present address: School of Resources and Environmental Management, Simon Fraser University, Burnaby,
British Columbia V5A 1S6, Canada.
Received December 29, 1999; accepted July 6, 2000
chirus to increase pectoral fin movements. Pectoral fin movements decreased as fish filled their air bladders to compensate for the additional weight.
Fried et al. (1976) found that smolts of Atlantic salmon Salmo salar increased buoyancy over time after insertion of a dummy transmitter and that fish denied access to air could not increase buoyancy.
Both Gallepp and Magnuson (1972) and Fried et al. (1976) concluded that fish were able to compensate for the weight of a transmitter by filling their air bladders.
Increasing air bladder volume to compensate for added weight is advantageous for fish. A neutrally buoyant fish will expend little energy to maintain its station in the water column. A negatively buoyant fish must constantly swim to keep from sinking. For a fish to be neutrally buoyant, its density must match the density of its environment. Tissue and bone are denser than water, so most fish use their air bladder as a hydrostatic organ to decrease their density. Because salt water is denser than freshwater, a typical freshwater fish has an air bladder that occupies about 7% of its total volume, while that of a typical marine fish occupies about
5% (Jones and Marshall 1953; Alexander 1966).
Thus, the density of a fish’s tissue and bone and the density of its environment determine the air bladder volume required to achieve neutral buoy-
46

BUOYANCY COMPENSATION OF SALMON 47 ancy. Because implanting a transmitter increases a fish’s density, a tagged fish must increase its air bladder volume to compensate for the transmitter.
A fish’s air bladder is also subject to changes in pressure. The air bladders of most fish change volume in close accordance with Boyle’s law (Jones
1951; Alexander 1966). A neutrally buoyant fish is in a state of equilibrium. If it ascends, however, its air bladder will expand, its density will fall below that of its environment, and it will become positively buoyant. Conversely, if the fish descends, its air bladder will be compressed, its density will increase, and it will become negatively buoyant. Thus, a fish is neutrally buoyant and its density equal to that of its environment at only one depth unless the quantity of gas in the air bladder is altered.
Our interest was in juvenile chinook salmon On-
corhynchus tshawytscha, a physostomous species that can only effect substantial changes in air bladder volume by gulping air at the water’s surface
(Tait 1959; Harvey et al. 1968; Fried et al. 1976).
If a transmitter affects buoyancy, then information obtained via radiotelemetry may not be representative of the population. Hence, the objective of this study was to determine how transmitter implantation affects the buoyancy of juvenile chinook salmon. Specifically, we tested two hypotheses. First, we examined whether fish filled their air bladder to compensate for the mass of the transmitter. Second, we investigated whether changes in pressure affected the buoyancy of tagged fish differently from that of untagged fish.
Methods
We used juvenile chinook salmon weighing between 11.0 and 54.0 g (mean
5
27.0 g) and measuring between 100 and 164 mm in fork length
(mean
5
131 mm) from the Little White Salmon
National Fish Hatchery, Washington. Fish were held in circular fiberglass tanks (1.5 m in diameter and 0.9 m deep; 1,400 L) that were located outdoors, subjected to the natural photoperiod, and supplied with 9–11 8 C well water. Fish were fed
Biomoist feed pellets (Bioproducts, Warrendale,
Oregon) ad libitum 3–5 times daily.
We used two different sizes of dummy transmitters, representing 3.2–9.4% of the body weight of tagged fish. The ratios between tag weight and body weight were higher than the generally recommended 2–5% for field telemetry studies (Winter 1983; Adams et al. 1998a, 1998b). However, we incorporated a large range of fish sizes to determine how fish size affects buoyancy compen-
T
ABLE
1.—Physical properties of dummy transmitters used in buoyancy tests.
Transmitter
Small
Large
Dimensions
(mm)
7 3 18
9 3 22
Weight
(g)
1.2
1.7
Volume
(mL)
0.5
0.8
Excess mass (g)
0.7
0.9
sation. The small transmitter (manufactured by Lotek Engineering, Newmarket, Ontario) was cylindrical and consisted of functional components encased in an inert resin. The large transmitter
(manufactured by Advanced Telemetry Systems,
Isanti, Minnesota) was also cylindrical and consisted of lead shot encased in an inert resin (Table
1). The excess mass (also referred to as ‘‘weight in water’’) presented in Table 1 is the difference between the mass of an object and the mass of the water it displaces (Gallepp and Magnuson 1972).
External flexible antennas were deliberately left off the dummy transmitters because preliminary buoyancy tests indicated that the antennas interfered with accurate measures of neutral buoyancy.
Thus, the dummy transmitters more closely represented ultrasonic transmitters, which lack an antenna. However, these results can also be applied to radio transmitters because an antenna’s effect on buoyancy will simply be the additional excess mass.
Fish were randomly assigned to one of three treatments: handled but not tagged (the control group), surgical implantation of large transmitters
(hereafter referred to as large-tag fish), and surgical implantation of small transmitters (hereafter referred to as small-tag fish). Transmitters were surgically implanted following techniques described by Adams et al. (1998a) but modified slightly for implantation of transmitters without an antenna. We implanted 21 fish with the small transmitter, 25 fish with the large transmitter, and treated 35 as controls. We incorporated more controls into the study design because preliminary studies indicated that a higher proportion of control fish expelled air prior to buoyancy measurements. Immediately following surgical implantation, five to six fish each were placed in 125-L holding containers and allowed 24 h to recover from tagging.
We determined buoyancy by measuring the density of fish with a filled air bladder. Density was measured by subjecting fish to a graded series of salinity baths (sodium chloride solutions) ranging in density from 1.001 g/mL to 1.015 g/mL in increments of 0.001 g/mL (Harvey 1963). The density of the fish was considered equal to the density

48 PERRY ET AL.
of the bath in which the fish just floated off the bottom (i.e., neutral buoyancy). The saline baths were kept at the same temperature as the fish holding containers and were tested with a hydrometer just prior to density measurements. In addition, the baths were filled to the same approximate height as the buoyancy chamber and holding containers so that fish were subjected to the same hydrostatic pressure.
We measured the effect of pressure changes on buoyancy using the methods of Saunders (1965).
An anesthetized fish was placed in a sealed cylindrical Plexiglas pressure chamber (30 cm in height and 25 cm in diameter) filled to a height of 26 cm with a 70-mg/L solution of tricaine methanesulfonate (MS-222). The pressure was gradually reduced by a vacuum pump and monitored with a pressure gauge. We recorded the pressure reduction (P
R
) at which fish became neutrally buoyant, which was defined as the pressure reduction (mm
Hg) at which the fish’s entire body just began to float off the bottom of the pressure chamber.
Changes in atmospheric pressure affect the total pressure on the air bladder and thus buoyancy. For measurements to be comparable for different atmospheric pressures, P
R must be subtracted from the total atmospheric plus hydrostatic pressure in the pressure chamber. This corrected measure is termed the ‘‘pressure of neutral buoyancy’’ (P
NB
;
Saunders 1965). However, we did not correct for atmospheric pressure because P
R provides a more intuitive measure of the pressure required to effect neutral buoyancy. The closer a fish is to neutral buoyancy, the smaller the pressure reduction (P
R
) required to achieve it. Because atmospheric pressure remained constant for the duration of our study, using P
R to make comparisons between fish is valid. Our measurements can be made comparable to those of other studies (Saunders 1965;
Pinder and Eales 1969; Fried et al. 1976) simply by subtracting P
R from the atmospheric pressure
(738 mm Hg) plus the hydrostatic pressure (19 mm
Hg).
After the 24-h recovery period, the five to six fish in each 125-L holding container were anesthetized simultaneously with 70 mg/L MS-222.
Shortly after the anesthetic was introduced, a screen was placed just below the water’s surface to prevent fish from swallowing air prior to the buoyancy tests. Multiple fish were anesthetized simultaneously to minimize the stress associated with handling and netting, which can cause salmonids to expel air (Harvey 1963). Both pressure and density measurements were taken on each fish.
First, P
R was measured in the buoyancy chamber; immediately following that, the fish’s density was determined in the saline baths. Any fish that expelled air before or during the buoyancy measurements was excluded from the analysis.
Measuring both the P
R and density of each fish allowed us to test a number of hypotheses and examine the relation between pressure change and buoyancy. We used a single-factor analysis of variance (ANOVA) on density measurements to test the null hypothesis that fish compensated for the transmitter by filling their air bladders. We also used a single-factor ANOVA on P
R to test the null hypothesis that changes in pressure affected the buoyancy of tagged fish in the same way as that of untagged fish. Multiple comparisons were made using Tukey’s Studentized range test. Additionally, we used linear models to test the null hypothesis that the rate of change in density with pressure
(i.e., the slope of the density
2
P
R regression line) was the same between treatments (SAS Institute
1994).
Because the air bladders of most fish change volume in close accordance with Boyle’s law, we used Boyle’s law to simulate the effect of fish size and changes in depth on the buoyancy of tagged and untagged fish. Boyle’s law states that a volume of gas (i.e., the air bladder) is inversely proportional to the pressure applied. We estimated air bladder volume by modifying an equation from
Alexander (1993) to include the physical properties of the transmitter, that is,
V b
5 [(W 1 W )/d ] 2 (V 1 V ), where V b is air bladder volume, W t and V t are the weight and volume of the transmitter, W and V are the weight and the volume of the fish without the air bladder, and d b a filled air bladder.
is the density of the fish with
Calculating the volume of the fish without the air bladder (V) required an estimate of tissue density. Published measurements of tissue density for juvenile salmonids ranged from 1.060 g/mL to
1.072 g/mL (Harvey 1963; Pinder and Eales 1969;
Sosiak 1982). We used a value of 1.065, the midway point in the range of values. Although the range of densities represents a 20% difference in the absolute air bladder volume, the difference in the relative (% volume) air bladder volume between tagged and untagged fish remains unchanged. Therefore, our conclusions would remain the same regardless of the tissue density estimate used in the calculations.

BUOYANCY COMPENSATION OF SALMON
T
ABLE
2.—Mean density and pressure reduction (P
R for buoyancy test treatment groups, with standard devia-
) tions in parentheses. Means with the same small letter were not significantly different.
Treatment group
Control
Small tag
Large tag
Sample size
25
16
24
Mean density
(g/mL)
1.003 (0.0015) z
1.002 (0.0015) z
1.003 (0.0017) z
Mean P
R
(mm Hg)
47 (20) z
30 (16) y
29 (18) y
49
Results
Density measurements were obtained for 25 controls, 24 large-tag fish, and 16 small-tag fish.
Measurements of P
R were obtained for 26 controls,
25 large-tag fish, and 16 small-tag fish. Nine controls and five small-tag fish expelled air before or during P
R measurements; one control and one large-tag fish expelled air during density measurements. These fish were not included in the analysis. Controls and tagged fish exhibited slight negative buoyancy but were close to neutral buoyancy (Table 2).
There was no significant difference in density among treatments (P
5
0.6882; Table 2), which suggests that tagged fish were able to compensate for the transmitter by filling their air bladders.
However, there were significant differences in P
R
(P
5
0.0027), with both tagged groups having significantly lower P
R than the control group (P ,
0.05; Table 2). Regression of fish density on P
R for each treatment resulted in a significant relationship in each case (P
5
0.0001 and r 2
.
0.89
F
IGURE
2.—Simulation of the effect of fish size and depth change on the density of (A) untagged fish and
(B) fish implanted with the large transmitter.
F
IGURE
1.—The relationship between fish density and
P
R for control fish (diamonds and alternating-size dash line; r 2
5
0.92, P
5
0.0001), small-tag fish (triangles and solid line; r 2 5
0.91, P
5
0.0001), and large-tag fish (squares and single-size dash line; r 2 5
0.89, P
5
0.0001).
for all; Figure 1). However, a test for homogeneity of slopes revealed significant differences between the slopes of the regression lines (P 5 0.0001).
These results indicate that in response to pressure, the density of tagged fish changed at a higher rate than that of controls. The change in density per unit change in pressure averaged 5.9
3 10 –5 g/mL per mm Hg for control fish, 7.9
3
10 –5 g/mL per mm Hg for small-tag fish, and 8.7
3 10 –5 g/mL per mm Hg for large-tag fish. These higher rates of change caused tagged fish to attain neutral buoyancy with less pressure reduction even though the density of tagged and untagged fish was similar.
Simulations based on Boyle’s law confirmed our empirical observation that the buoyancy of tagged fish is affected by changes in pressure more than the buoyancy of untagged fish (Figure 2). In addition, these simulations indicate that the size of tagged fish also affects the rate of density change.

50 PERRY ET AL.
F
IGURE
3.—Relative air bladder volume expressed as
(A) a percentage of body weight and (B) the percentage increase in air bladder volume (bottom panel) for control fish (diamonds), small-tag fish (triangles), and large-tag fish (squares).
To compensate for a transmitter, a fish must fill its air bladder by a constant amount equal to the excess mass of the transmitter (Gallepp and Magnuson 1972). Therefore, as fish size decreases, the relative air bladder volume of tagged fish increases
(Figure 3). We found a significant correlation between the rate of density change and the relative air bladder volume of tagged fish (r
5
0.41, P
5
0.008).
Discussion
Research has shown that fish fill their air bladder to compensate for the excess mass of a transmitter
(Gallepp and Magnuson 1972; Fried et al. 1976; this study). In addition, Jones (1951, 1952) and
Alexander (1966) found that the change in density in response to pressure is dependent on the relative size of the air bladder. By comparing species of fish that naturally have different relative air bladder volumes, both Jones (1951, 1952) and Alexander (1966) showed that the rate of change in buoyancy is proportional to the percentage volume of the air bladder. However, little research has applied these basic physical principles to the effects of a transmitter on buoyancy. Intraspecific differences in relative air bladder volume vary little, but transmitter implantation alters this relation (Figure
3). Our research has shown that the increase in air bladder volume caused by the presence of a transmitter will affect the buoyancy of tagged fish more than that of untagged fish.
Because the rate of buoyancy change, the relative air bladder volume, and pressure are proportional, the percentage increase in air bladder volume provides a direct estimate of the magnitude of the transmitter’s effect on buoyancy. For field studies, recent research has recommended that the maximum tag:fish weight ratio should be no greater than 5.0% (Adams et al. 1998b). For the large and small transmitters used in this study, this ratio corresponds to fish weighing 34 and 24 g and experiencing 45% and 50% increases in air bladder volume, respectively (at an average density of
1.003 g/mL). This is a substantial increase in air bladder volume. Thus, the rate of change in density for these tagged fish would be 1.45 and 1.50 times
(i.e., 45% and 50% greater than) that of equivalent untagged fish. Minimizing the tag:fish weight ratio and the increase in relative air bladder volume will reduce the effect of pressure change on buoyancy.
Although it is clear that fish increase air bladder volume to compensate for the transmitter, we believe that diffusion of gases into the air bladder plays a negligible role in buoyancy compensation for juvenile salmonids. Fried et al. (1976) found that juvenile Atlantic salmon implanted with transmitters recovered more than 85% of their buoyancy within 3 h if allowed access to air. However, tagged fish denied access to air did not increase buoyancy after 24 h. Harvey et al. (1968) found that juvenile sockeye salmon Oncorhynchus nerka that expelled air and were subsequently denied access to air did not increase their air bladder volume after 8 d. In addition, rainbow trout Oncorhynchus
mykiss and brown trout Salmo trutta that were denied access to air lost air bladder gas in experiments lasting 10 2 18 d (Tait 1959). While diffusion of gases into the air bladder does occur in physostomes (Jones and Marshall 1953; Alexander
1966), filling of the air bladder via diffusion requires an extremely long time. Thus, this mechanism appears to play a minor role in hydrostatic regulation by salmonids.
If tagged fish are unable to maintain the same buoyancy as untagged fish, then the physiology and behavior of tagged fish may be affected. Most fish respond to a decrease in buoyancy with com-

BUOYANCY COMPENSATION OF SALMON 51 pensatory swimming movements to maintain their position in the water column, increasing such movements as density increases (Jones 1952;
Brawn 1962; Harvey 1963; Gallepp and Magnuson
1972). Therefore, tagged juvenile chinook salmon that are less buoyant than untagged fish will expend more energy. Alternatively, reduced buoyancy may cause a tagged juvenile salmonid to reside at a shallower depth than an untagged fish in order to reduce energy expenditure and remain in a suitable range of buoyancy. Underwater antenna arrays (Adams et al. 1999; Johnson et al. 2000), pressure sensitive transmitters (Beeman et al.
1998), and ultrasonic systems (Arnold and Walker
1992; Cote et al. 1998) are increasingly being used by researchers to determine the depth location of fish. Researchers should be aware of the potential bias in relation to the vertical distribution of tagged fish caused by the increased rate of buoyancy change with depth.
The tag:fish weight ratio is the most common index for assessing the effect of a transmitter on the study subject. However, Brown et al. (1999) recommended the use of transmitter volume and weight in water (i.e., excess mass) as alternative measures. We provide quantitative evidence that excess mass may be a more appropriate measure than the tag:fish weight ratio for assessing the effects of a transmitter. Excess mass represents the additional weight in water that a fish must carry.
In our study, this was 0.9 g for the large transmitter and 0.7 g for the small transmitter. Although there is a 0.5-g difference between the actual weight of the two transmitters, there is only a 0.2-g difference in excess mass. This small difference was reflected in our findings of no significant difference in P
R lines of P
R and little difference in the regression and density between the tagged groups
(Figure 1). Thus, two transmitters may not weigh the same, but their effects on buoyancy may be similar depending on the excess mass.
For some species of fish, development of a neutrally buoyant transmitter may be beneficial. For instance, if a ‘‘pocket’’ of air equal in volume to the excess mass of the transmitter could be incorporated, the transmitter would be neutrally buoyant and a fish would not have to compensate by air bladder inflation. The pocket of air must be encapsulated in a rigid container so that the volume does not change with changes in pressure. This would maintain the neutral buoyancy of the transmitter at any depth.
Production of a neutrally buoyant transmitter would require increasing its volume, and the transmitter would therefore occupy more space in the body cavity. However, we have shown that fish in this study filled their air bladder by an amount equal to the excess mass of the transmitter. Thus, the total increase in volume of the body cavity would remain the same regardless of whether compensation for excess mass occurred in the air bladder or in the transmitter. Transmitter volume may be a limiting factor for use in some species (e.g., laterally compressed fish). However, the advantage of using a neutrally buoyant transmitter is that the relative air bladder volume of a tagged fish would not change. Thus, the rate of buoyancy change for tagged fish would be similar to that of untagged fish.
Acknowledgments
We thank J. Plumb, M. Novick, and I. Jezorek for laboratory assistance. We are grateful to John
Beeman and David Welch for insightful comments on the manuscript. Funding for this study was provided by the U.S. Army Corps of Engineers, Walla
Walla District, Walla Walla, Washington (contract
E-8693015). The use of trade names does not imply endorsement of commercial products.
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