Transactions of the American Fisheries Society 138:777–789, 2009
Ó Copyright by the American Fisheries Society 2009
DOI: 10.1577/T08-106.1
[Article]
Barging Effects on Sensory Systems of Chinook Salmon Smolts
MICHELE B. HALVORSEN*
Department of Biology and Center for Comparative and Evolutionary Biology of Hearing,
University of Maryland, College Park, Maryland 20742, USA
LIDIA E. WYSOCKI
Department of Behavioural Biology, University of Vienna, Vienna, Austria
CARLA M. STEHR
DAVID H. BALDWIN
AND
National Oceanic and Atmospheric Administration Fisheries, Northwest Fisheries Science Center,
Environmental Conservation Division, 2725 Montlake Boulevard East, Seattle, Washington 98112, USA
DAVID R. CHICOINE
Doctor of Chiropractic Program, New York Chiropractic College, Seneca Falls, New York 13148, USA
NATHANIEL L. SCHOLZ
National Oceanic and Atmospheric Administration Fisheries, Northwest Fisheries Science Center,
Environmental Conservation Division, 2725 Montlake Boulevard East, Seattle, Washington 98112, USA
ARTHUR N. POPPER
Department of Biology and Center for Comparative and Evolutionary Biology of Hearing,
University of Maryland, College Park, Maryland 20742, USA
Abstract.—To avoid mortality caused by passage through dam turbines and spillways, juvenile Chinook
salmon Oncorhynchus tshawytscha are annually transported downstream by barge through the federal
hydropower system on the Snake and Columbia rivers. Survival of transported fish is higher than that of inriver migrants; however, transported fish experience higher rates of postrelease mortality. Increased mortality
could result from a decrease in the ability to detect or avoid predators due to stressors associated with the
barge environment. This study examined the effects of barging on juvenile Chinook salmon olfaction and
auditory function, two sensory systems involved in predator detection. We focused on dissolved metals
known to be toxic to the salmon olfactory system and on the level of noise from the barge, which could impair
the auditory system. Experimental groups included animals collected (1) before barge loading (control group),
(2) at the Bonneville Dam bypass system (migrant fish), (3) immediately after barge transport, and (4) within
7 d postbarging and at or after 7 d postbarging. Measured concentrations of dissolved metals from the water
within the barge were below established water quality criteria for the protection of aquatic life. Moreover,
ultrastructural examination of the olfactory epithelium surface showed no evidence of injury to olfactory
sensory neurons. Noise in the barge holding tanks had levels up to 136 dB referenced to 1 lPa (root mean
square) with primary energy below 400 Hz. Auditory sensitivity was measured using the auditory-evoked
potentials (AEP) technique. We found a small but statistically significant threshold shift for fish collected
within 7 d postbarging, while in the 7-d-and-later postbarging group the AEP thresholds were similar to the
control. Our findings indicate that the olfactory systems of transported Chinook salmon are intact and
probably functional, while the auditory sensitivities are compromised with probable recovery.
Out-migrating Pacific salmon and steelhead Oncorhynchus mykiss (anadromous rainbow trout) have
been transported through the federal hydrosystem on
the Snake and Columbia rivers in the Pacific Northwest
for the past several decades. Transportation by trucking
and barging was developed as a management strategy
* Corresponding author: [email protected]
Received June 9, 2008; accepted December 5, 2008
Published online May 28, 2009
to reduce the mortality caused by turbines and
spillways at dams (Ebel 1980). Each year, smolts of
Chinook salmon O. tshawytscha and steelhead are
collected at Snake River dams and barged downstream
to a release point below Bonneville Dam. They then
migrate unimpeded to the lower Columbia River
estuary.
Ward et al. (1997) showed that survival during
hydrosystem passage is generally higher for transported fish than for in-river migrants. However, when
777
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passive integrated transponder tagged fish returned as
adults, analyses of smolt-to-adult return rates revealed
that unexpectedly often, the rates of postrelease
survival were lower among transported fish relative
to in-river migrants (Williams et al. 2005). This
suggests that transportation causes some form of latent
mortality that does not manifest until after barged fish
are released below Bonneville Dam.
Several hypotheses have been proposed to account
for the differential post-hydrosystem survival between
transported smolts and in-river migrants, termed D
(Williams et al. 2005). These include the stress of
crowding and holding in the barges (Congleton et al.
2000), co-transport with larger, more aggressive
steelhead (Wagner et al. 2004), the potential for
increased disease susceptibility (Arkoosh et al. 2006),
disrupted smoltification (Budy et al. 2002), altered time
of ocean entry (Muir et al. 2006), and lost growth
opportunity for barged fish (Muir et al. 2006). An
additional hypothesis is that the barge environment
alters the physiology and behavior of smolts in ways
that might increase their vulnerability to predators as
they transition to the lower Columbia River estuary.
The present study focused on two particular features
of the barge environment. Specifically, we assessed the
potential effects of degraded water quality and
underwater noise in the holding areas for Chinook
salmon smolts. The sensory organs of fish, including
the ear, nose (peripheral olfactory epithelium), and
lateral line, are highly sensitive to the sublethal effects
of various anthropogenic stressors. For salmon, a loss
of normal sensory function could have important
implications for the survival of fish released from
barges. This includes, for example, the ability of smolts
to detect and avoid predators in the river and estuary.
To assess a potential role of degraded water quality
in causing D, we measured concentrations of dissolved
metals at different intervals during barging. We then
assessed the effects of different passage histories
through the hydrosystem on the ultrastructural integrity
of olfactory sensory neurons in Chinook salmon
smolts. The concern was that heavy metals, which
can originate from pipes, metal fixtures, and other
materials on barges, are known to be highly toxic to
fish sensory systems. Dissolved copper, for example,
targets sensory neurons in the nose (e.g., Hansen et al.
1999) as well as the lateral line (Linbo et al. 2006).
Exposure to copper can cause the physical degeneration of olfactory neurons (Moran et al. 1992; Julliard et
al. 1996). In addition, short-term exposures to copper
(on the order of hours) at relatively low concentrations
can impair olfactory function and also render salmon
unresponsive to olfactory cues (Baldwin et al. 2003).
Moreover, copper-exposed salmon with diminished
olfactory function fail to respond to chemical predation
cues (Sandahl et al. 2007).
Assessment of salmon hearing is particularly
important since sound is a major source of environmental information for fish (e.g., Popper 2003).
Various salmonid species are able to detect sounds
from below 30 Hz to over 600 Hz (e.g., Hawkins and
Johnstone 1978; Knudsen et al. 1994; Wysocki et al.
2007). Presumably, fish use hearing to detect and
respond to environmental signals. Such environmental
sounds are produced by predators and prey and by
numerous abiotic environmental sources, such as
waves, rain, and water moving over rock. This
‘‘auditory scene’’ potentially conveys to fish environmental information beyond the visual field, thus
extending the sensory world to distances beyond the
fish (Fay and Popper 2000). Consequently, degradation
of hearing could result in decreased perception and
response to biologically relevant sounds that affect fish
health and survival.
Classically, fish have been referred to as hearing
generalists or specialists (e.g., Popper 2003). A
specialist is a fish with a morphological adaptation
that physically couples the swim bladder to the ear,
thereby aiding in its pressure detection abilities.
Traditionally, the confining definition for generalists,
which have no hearing adaptations, is that they lack
pressure sensitivity but are sensitive to particle motion.
Evidence exists for a continuum wherein nonspecialists
are primarily sensitive to particle motion and to some
extent pressure, which would depend on the distance
between the swim bladder and the inner ear (e.g.,
Chapman and Hawkins 1973; Sand and Enger 1973).
Diversity among fishes is broad, and hearing abilities
and sensitivities are quite varied. Thus, extrapolation of
data from one fish species to another in regards to
hearing should be done with utmost caution. Salmonids
lack hearing specializations and therefore will be
referred to here as nonspecialists.
To assess the potential effects of barging noise on
fish, we first assessed the degree of underwater noise
associated with normal barging operations by recording
sound spectra and pressure in holding chambers. We
then compared the hearing sensitivity of barged fish
with that of in-river migrants. This was done since it is
becoming apparent that protracted exposures to
underwater noise may cause temporary hearing loss
(often referred to as temporary threshold shift [TTS]) in
some fish species (Scholik and Yan 2001, 2002a;
Smith et al. 2004a; Popper et al. 2007). One study on
goldfish Carassius auratus reported hair-cell damage
correlated with temporary hearing loss after 48 h of
noise exposure (Smith et al. 2006).
The experimental approach allowed us to determine
BARGING EFFECTS ON SMOLT SENSORY SYSTEMS
779
whether contaminants and noise in the barge environment were potentially hazardous to transported Chinook salmon smolts. In addition, we were able to
explore whether barging impairs key sensory systems
that are critical for smolt survival.
Methods
Fish
The collection, handling, and care of hatchery
Chinook salmon were conducted in accordance with
state and federal requirements. The experimental
procedures for measuring hearing sensitivity were
approved by the University of Maryland’s Animal
Care and Use Committee. The average length and
weight of smolts used in this study were 154.7 6 0.14
mm (mean 6 SE) and 26.5 6 0.84 g, respectively. A
dip net was used to collect smolts from raceways, and a
lift net was used to remove fish from the barge holding
tanks. Fish were placed into buckets containing water
treated with a nonlethal dose of buffered tricaine
methanesulfonate (MS-222) to identify and collect
adipose fin-clipped (hatchery) Chinook salmon smolts.
All fish were revived in freshwater and maintained in
aerated water or in holding tanks with flow-through
water. All experiments took place during May 2005.
Loading and Transport of Smolts in Barges
Chinook salmon migrating down the Snake River
were collected from the bypass raceway at Lower
Granite Dam (Figure 1). Barges were loaded by
pumping smolts into holding tanks. The process took
approximately 20–24 h, and loaded barges departed
Lower Granite Dam every 24 h. Fish used in this study
spent 33.5–58.5 h on the barge during loading and
transport to Bonneville Dam (Figure 1).
The U.S. Army Corps of Engineers 8000 Series
barges were specifically constructed to transport
juvenile salmon through the federal hydropower
system. Each barge contained six holding tanks in
pairs along the barge’s length, and all tanks had topside
access. The holding tanks were filled with circulating
river water and fitted with degas exchange columns. A
tugboat moved each barge downstream. Diesel engines
located at the aft end of the barge were run constantly
during transport to maintain and control life support
systems for the fish. Fish from holding tanks that were
the closest to the diesel engines were used in the
experiments to assess the integrity of the peripheral
olfactory system as well as hearing sensitivity.
Experimental Groups
This study used several groups of hatchery Chinook
salmon smolts: (1) control fish consisted of smolts
taken from Lower Granite Dam and were not barged,
FIGURE 1.—The Columbia and Snake River basins, showing
the transport route used for the barging of Chinook salmon
smolts. Lower Granite and Bonneville dams are underlined to
show the beginning and ending, respectively, of the smolt
transportation run (east to west). This illustration is adapted
from an U.S. Army Corps of Engineers brochure and does not
include all dams within the geographical area depicted.
(2) migrant fish were smolts collected from Bonneville
Dam’s bypass system and were not barged, and (3)
barged fish consisted of smolts taken from barge
holding tanks (on two different transportation runs;
barged fish group A [BFA] and barged fish group B
[BFB]).
Control fish.—The control fish consisted of Chinook
salmon smolts collected from the raceway at Lower
Granite Dam before they were loaded onto the barge.
These fish were not exposed to any stressors associated
with the barge environment. Olfactory rosettes from 10
fish were collected at the Lower Granite Dam facility.
Twenty-four additional control fish were placed into a
cooler containing aerated raceway water and were
transported by vehicle for 5 h to the Juvenile Fish
Bypass and Monitoring Facility at Bonneville Dam.
They were subsequently maintained in flow-through
holding tanks until tests for hearing sensitivity were
performed (n ¼ 11).
Migrant fish.—Chinook salmon migrating through
the dams on the Snake and Columbia rivers (in-river
migrants) were collected from raceways at Bonneville
Dam’s Juvenile Fish Bypass and Monitoring Facility.
These fish served as an additional set of controls to
assess the potential sensory effect of transporting the
control fish by vehicle. Although these in-river migrant
Chinook salmon smolts were not barged, their passage
history in terms of encounters with bypass systems,
spillways, and turbines at one or more dams upstream
of Bonneville Dam was unknown. In-river migrants
were abundant at Bonneville Dam’s bypass facility and
were collected from raceways as needed. Olfactory
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HALVORSEN ET AL.
TABLE 1.—Concentrations of dissolved metals (lg/L; mean 6 SE; n ¼ number of samples analyzed) at the Lower Granite
Dam (LGD) bypass, in a fish barge holding tank (JDD ¼ John Day Dam; DAL ¼ the Dalles Dam), and at the Bonneville Dam
(BON) bypass (see Figure 1). Hardness-based water quality criteria use a value for hardness of 50 mg/L.
Barge holding tank
Dissolved
metal
Water quality
criteria
Nickel
Copper
Zinc
Cadmium
Lead
260
7
65
0.6
30
LGD bypass
(before barging)
n¼
0.050 6
0.530 6
0.13 6
0.0038 6
0.046 6
5
0.004
0.003
0.04
0.0002
0.002
Pre-transit
0.066
0.63
0.47
0.0052
0.06
5
6
6
6
6
6
0.008
0.03
0.08
0.0006
0.01
rosettes were collected from 10 migrant fish, and
hearing was measured on 11 fish.
Barged fish.—Transported Chinook salmon smolts
(BFA and BFB) were sampled from two different
barges that made separate trips downstream from
Lower Granite Dam to Bonneville Dam. Fish were
exposed to the barge environment for 33.5–58.5 h
(BFA) or for 38.0–58.5 h (BFB). Differences between
these intervals reflect the time required to load the
barges at Lower Granite Dam. Just before arrival at the
Bonneville Dam lock, Chinook salmon smolts were
removed from the barge holding tanks, sorted, and
placed into coolers containing aerated river water.
Approximately 80 smolts were then transported via a
10-min vehicle trip to the Juvenile Fish Bypass and
Monitoring Facility at Bonneville Dam. The fish were
maintained in holding tanks at the facility.
Olfactory rosettes were collected from 10 BFA
smolts immediately upon arrival at the monitoring
facility. To screen for a possible delayed onset of
olfactory injury, olfactory rosettes were collected from
another 10 BFA smolts that were held at the Bonneville
Dam facility for 9 d.
To evaluate hearing function in barged fish,
electrophysiological recordings were obtained from
both groups of fish (BFA: n ¼ 22; BFB: n ¼ 10). Tests
of hearing sensitivity began 1 h after the fish were
removed from the barge and continued up to a
maximum of 182 h.
Analyses for Dissolved Metals
High-density polyethylene bottles were used to
collect water samples for dissolved metals analysis.
Twenty individual water samples were collected over
four consecutive days at five different points during the
collection and transport of BFA smolts. These included
samples from (1) the raceway holding area at Lower
Granite Dam sampled just before barge loading (n ¼ 5),
(2) a barge holding tank containing smolts sampled just
before departure from Lower Granite Dam (n ¼ 5), (3)
the same barge holding tank sampled early in the transit
In transit below JDD
0.065
0.85
0.64
0.0095
0.025
2
6
6
6
6
6
0.015
0.02
0.07
0.0005
0.002
In transit below DAL
0.047
0.623
0.4
0.0093
0.023
3
6
6
6
6
6
0.007
0.003
0.1
0.0007
0.006
BON bypass
(after barging)
0.050
0.640
0.19
0.0084
0.015
5
6
6
6
6
6
0.007
0.006
0.03
0.0005
0.002
to Bonneville Dam (n ¼ 2), (4) the same barge holding
tank sampled close to the arrival to Bonneville Dam (n
¼ 3), and (5) the fish bypass system at Bonneville Dam
sampled after the arrival of BFA (n ¼ 5).
The concentrations of 12 dissolved metals (Table 1)
were determined for each sample by an outside
laboratory (Frontier Geosciences, Seattle, Washington).
Samples were filtered through a precleaned, 0.45-lm
filter unit and were preserved with 1% HNO3. Each
filtrate was analyzed separately by inductively coupled
plasma mass spectrometry (Perkin-Elmer ELAN 6000).
Statistical analyses on the concentrations were performed using one-way analysis of variance (ANOVA)
followed by Tukey’s honestly significant difference
test in JMP software version 5.1 (SAS Institute, Inc.,
Cary, North Carolina).
Ultrastructural Analysis of the Salmon Olfactory
Epithelium
Chinook salmon smolts were individually euthanized in a bucket of river water containing a lethal dose
of buffered MS-222. When gill movement ceased,
pipettes filled with fixative were inserted into each
fish’s nares. Both nares were simultaneously flooded
with about 10 mL of fixative containing 0.75%
glutaraldehyde and 3% formaldehyde in a buffer of
0.1-M sodium cacodylic acid, 5.5% sucrose, and 0.2%
CaCl2 dehydrate adjusted to pH 7.4. The upper jaw
(containing the two nares) was immediately removed
and immersed in fixative. Tissues were fixed overnight,
placed into sodium cacodylic buffer, and refrigerated
until processing. The olfactory rosettes were carefully
dissected and further washed in buffer. They were
postfixed in 2% osmium tetroxide in sodium cacodylic
buffer for 2 h, rinsed in buffer twice, and dehydrated
through a graded series of alcohols, followed by a
graded series of amyl acetate. Samples were criticalpoint dried with CO2 using a Pelco CPD2 critical-point
dryer, were mounted with silver paste on aluminum
stubs, and were sputter coated (Emitech K500x) with
gold palladium. Olfactory rosettes were examined with
BARGING EFFECTS ON SMOLT SENSORY SYSTEMS
a JEOL LSM-6360LV scanning electron microscope.
Rosettes from 10 smolts were examined for each of the
following treatment groups: control fish, migrant fish,
BFA upon arrival at Bonneville Dam, and BFA at 9 d
postbarging.
Underwater Noise Recordings from Barges
Recordings of the underwater noise from holding
tanks containing BFB smolts took place during normal
barge operations. Samples of 30-s duration were
recorded on a Marantz PMD 670 digital recorder
(Itasca, Illinois) connected to a Shure FP-11 (Evanston,
Illinois) preamplifier and an HTI-96-MIN hydrophone
(frequency response ¼ 2–30 kHz, voltage sensitivity ¼
189.9 dB referenced to [re] 1 V/lPa; High Tech, Inc.,
Gulfport, Mississippi). Noise recordings were analyzed
using Matlab version 7.0. Six underwater noise
recordings were collected; four were recorded from
an aft holding tank that was nearest to the diesel
engines. Recordings were made at the forward end and
at the aft end of this tank at depths of 0.5 and 1.0 m.
Two additional recordings were made from the middle
of a holding tank at the opposite end of the barge (the
bow), also at depths of 0.5 and 1.0 m.
Hearing Sensitivity Tests
All hearing tests took place in the Juvenile Fish
Bypass and Monitoring Facility at Bonneville Dam.
Acoustic Stimulation and Data Acquisition
The auditory-evoked potentials (AEP) technique, a
noninvasive electrophysiological measure of the synchronized brain response to auditory stimuli (e.g.,
Corwin et al. 1982; Kenyon et al. 1998), was used to
monitor the hearing sensitivity of Chinook salmon
smolts. The AEP hearing measures were obtained from
each fish one time only. Fish were lightly anesthetized
with buffered MS-222, restrained in a mesh sling, and
suspended 6 cm below the water surface in the center
of a 19-L, plastic rectangular tank. Two stainless steel
electrodes (Rochester Electro-Medical, Inc., Tampa,
Florida) were insulated with fingernail polish except at
the tips. A grounding electrode was placed in the water.
A reference electrode was inserted subcutaneously
between the nares, and a recording electrode was
inserted subcutaneously at the dorsal midline just
posterior to the cranium. During each recording
session, an HTI-96 hydrophone was affixed laterally
to the fish to record and analyze the acoustic stimulus.
Sound Stimulus
The sound stimulus was a 15-ms tone with a 2-ms
Blackman window gate. The signals were created by
SigGen software, sent to a Tucker-Davis Technologies
781
(TDT) RP2.1 analog-to-digital/digital-to-analog conversion board, amplified with a Hafler P1000 amplifier
(Hafler, Sharon, Massachusetts), and played on an
underwater speaker (UW30; Lubell Laboratories, Inc.,
Columbus, Ohio). The frequencies presented for AEP
testing were 100, 200, 400, and 600 Hz for
comparisons between different groups of fish, while
frequencies presented for measurement of entire
audiograms also included 300, 500, 700, and 800 Hz.
Sound pressure levels were recorded with an HTI-96
hydrophone (calibration sensitivity ¼ 164.0 dB re 1
V/lPa). The hydrophone was positioned 6 cm below
the water surface in the fish holder without the fish.
The hydrophone signal was amplified with a Shure FP23, and the output was measured through TDT’s
BioSig software, which calculated a root mean square
(RMS) value of the recorded sound signal. The sound
signal was also measured using an oscilloscope to
ensure that the same values were obtained.
Stimulus signals were recorded and analyzed using a
fast Fourier transform within TDT BioSig. All test
frequencies had first harmonics that were at least 30 dB
below the fundamental frequency; the exception was
100 Hz, for which the first harmonic (200 Hz) was 18
dB lower than the fundamental frequency.
Electrophysiology
The AEPs at each signal level were collected in
response to 500 averages of 15-ms tones repeated 20
times/s via a TDT Medusa RA4LI headstage, RA4PA
preamplifier, and RA16BA base station; AEPs were
digitized with TDT BioSig software and stored. The
brain signal had a gain of 100, was low-pass filtered at
3 kHz, high-pass filtered at 30 Hz, and notch filtered at
60 Hz via BioSig software.
Sound pressure levels at each frequency were
decreased in 5-dB steps until the AEP responses
disappeared. Responses were visually judged, and
detection was defined as being able to see a repeatable,
stereotypical AEP response just above background
noise. This qualitative assessment is commonly used in
AEP studies (Hall 1992; Kenyon et al. 1998) and gives
results similar to those of statistical methods (Mann et
al. 2001; Brittan-Powell et al. 2002). Therefore, AEP
threshold was defined as the lowest sound level that
gave a defined repeatable response (e.g., see Figure 5).
For technical reasons, hearing thresholds are given
in terms of sound pressure (dB re 1 lPa RMS). It is
likely that salmon are primarily sensitive to particle
motion. Thus, the thresholds presented here should not
be interpreted as absolute values for sensitivity.
Instead, our goal was to investigate whether there were
relative differences in detection; using a pressure
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HALVORSEN ET AL.
Results
Exposure to Dissolved Metals
FIGURE 2.—Scanning electron micrograph of an olfactory
rosette from a nonbarged Chinook salmon smolt collected at
Lower Granite Dam on the Snake River.
measurement is a valid approach for comparative
purposes (also see Popper et al. 2007)
Statistical Analysis
Hearing thresholds from the different treatment
groups were compared using two-factor mixed-measures ANOVA, repeated-measures multivariate ANOVA (MANOVA), and discriminant analysis (DA).
Within factors consisted of thresholds repeated across
frequency (i.e., those frequencies at which hearing was
tested) and the interaction between these factors;
between factors consisted of the experimental treatment
groups of fish (i.e., control compared with barged fish).
Due to the nature of subgroup analysis, the Bonferroni
correction was applied to the post hoc tests to maintain
the familywise error rate at 0.05. Analyses were
performed using JMP version 5.1.
Statistical comparisons include control versus migrant fish, BFA versus BFB, and control versus pooled
BFA and BFB. A comparison was then performed on
the control versus pooled barged fish sampled within 7
d postbarging or sampled at 7 d postbarging and later.
For each test, the within factor of frequency was
significant (P , 0.001). These significant differences
were expected due to the inherent J shape of these
audiograms. Moreover, for each test no significant
interactions were present in within factors or between
factors. While this is relevant, the effect of interest in
each case was the treatment groups; thus, between
factors were consequently reported.
To determine whether transported Chinook salmon
smolts are exposed to potentially toxic concentrations
of dissolved metals, water samples were collected from
(1) the bypass raceway before loading, (2) the barge
environment during transport, and (3) the bypass
facility at Bonneville Dam (posttransport). The measured levels of nickel, copper, zinc, cadmium, and lead
were low at all points sampled during downstream
transportation (Table 1). No metal exceeded 1 lg/L,
and all five were at least an order of magnitude below
the U.S. Environmental Protection Agency’s recommended water quality criteria (critical maximum
criteria, adjusted for a hardness of 50 mg/L; available
at: www.epa.gov/waterscience/criteria/wqcriteria.
html). The levels of copper and cadmium were well
below published thresholds for olfactory and lateral
line toxicity (e.g., Baker and Montgomery 2001; Linbo
et al. 2006; Sandahl et al. 2007). Measured concentrations of arsenic and selenium were also low (1.16 and
0.28 lg/L, respectively). Consequently, barges do
not appear to be significant sources of waterborne
heavy metals. Specifically, copper and cadmium in the
barge environment did not reach levels that would be
expected to cause sensory neurotoxicity in transported
smolts.
Structural Integrity of the Olfactory Epithelium
Scanning electron microscopy was used to examine
the architecture of olfactory sensory neurons in the
experimental groups. A single olfactory rosette, which
contains regions of both sensory and nonsensory
epithelium, is shown in Figure 2. There was no
evidence of structural injury to the olfactory epithelium
in fish from any of the groups with different passage
and holding histories. The integrity of both the sensory
and nonsensory epithelia was intact in all fish. An
example in Figure 3 compares the apical surfaces of
rosettes from a control (nonbarged) fish and a fish that
had been barged. In all cases, the olfactory epithelial
surfaces were intact and similar to those described
previously for other salmonids (Yamamoto and Ueda
1977; Yamamoto 1982; Thommesen 1983; Moran et
al. 1992). Consistent with the low levels of dissolved
metals in the holding tanks of barges, there was no
indication of physical injury to the olfactory system of
transported Chinook salmon.
Barge Noise
The mean RMS levels of recordings from the aft
holding tank were 132 dB re 1 lPa (0.5-m depth) and
136 dB re 1 lPa (1.0-m depth) at the aft end and 129
BARGING EFFECTS ON SMOLT SENSORY SYSTEMS
783
FIGURE 3.—Scanning electron micrographs showing (A) nonsensory olfactory epithelium of a nonbarged Chinook salmon
smolt (i.e., control fish), (B) nonsensory olfactory epithelium of a barged smolt, (C) sensory epithelium of a nonbarged smolt,
and (D) sensory epithelium of a barged smolt. No damage was evident in the surface structure of the olfactory epithelium (NS ¼
nonsensory ciliated cells, CR ¼ ciliated receptor cells, MR ¼ microvillar receptor cells).
dB re 1 lPa (0.5-m depth) and 134 dB re 1 lPa (1.0-m
depth) at the forward end. Levels measured in the
middle of the bow holding tank were 131 dB re 1 lPa
(0.5-m depth) and 135 dB re 1 lPa (1.0-m depth). The
main energy content of the noise was concentrated
below 400 Hz from all recording sites (Figure 4). The
peak energy was the spectrum level of 128 dB re 1 lPa
(corrected for filter bandwidth) at 21 Hz, and there
were additional prominent energy peaks of 124 dB re 1
lPa at 91 Hz, 122 dB re 1 lPa at 120 Hz, and 121 dB
re 1 lPa at 181 Hz. The noise had no clear harmonic
structure. Both holding tanks showed a decrease in
spectral energy levels at both recording depths (0.5 and
1.0 m) between 21 and 400 Hz. The aft holding tank,
which is closest to the diesel engines, had about a 35dB decrease, while the bow holding tank, which is
farthest from the engines, had a 45-dB decrease. The
spectrum had a region of minimum energy content
between 8 Hz and 2 kHz. Noise levels were higher
between 2 and 8 kHz but were still at least 30 dB below
peak values.
AEP Threshold
All fish auditory thresholds were recorded at 100,
200, 400, and 600 Hz (see Figure 5 for representative
AEP traces). In addition, 6 of the 10 control fish were
tested at additional frequencies to measure a complete
AEP audiogram for Chinook salmon smolts (Figure 6).
The mean AEP threshold value at each frequency for
each experimental group is presented in Table 2.
First, ANOVA and DA were used to compare the
between factor of control versus migrant fish. The null
hypothesis was that handling and holding control fish
did not have an effect on hearing. The null hypothesis
784
HALVORSEN ET AL.
FIGURE 4.—Noise spectra recorded at water depths of 0.5 and 1.0 m in the aft quarter of the fish holding tank in which
Chinook salmon smolts were transported for 38.0–58.5 h (barged fish group B; see Methods) from Lower Granite Dam on the
Snake River to Bonneville Dam on the Columbia River. The lower graphs give a detail of the noise spectra up to 1 kHz.
was not rejected (ANOVA: F1,17 ¼ 0.58, P ¼ 0.457;
DA: Wilk’s lambda ¼ 0.789, F4,14 ¼ 0.933, P ¼ 0.473),
which indicates that handling and holding did not have
an effect on hearing thresholds and that hearing
sensitivities were similar between control fish and
migrant fish.
Next, ANOVA and DA were used to compare BFA
with BFB. The null hypothesis was that thresholds
were similar in both BFA and BFB. Again, the null
hypothesis was not rejected (ANOVA: F1,28 ¼ 0.099, P
FIGURE 5.—Auditory-evoked potentials (AEP) traces from
barged Chinook salmon smolts of group B recorded at 15 h
postbarging. Stimulus was various levels of a 600-Hz tone.
The sound level (dB referenced to [re] 1 lPa) for each trace is
shown along the y-axis; amplitude and time are shown on the
inset. The threshold was 109 dB re 1 lPa.
FIGURE 6.—Audiogram based on mean (6SE) sound pressure
level (SPL) values (dB referenced to [re] 1 lPa) of control
(nonbarged) Chinook salmon smolts (n ¼ 10 for SPL values at
100, 200, 400, and 600 Hz; n ¼ 6 for SPL values at 300, 500,
700, and 800 Hz; SPL values ¼ 88 6 1.3, 104 6 1.9, 119 6 3.6,
and 126 6 2.6, respectively; see Table 2 for more details).
785
BARGING EFFECTS ON SMOLT SENSORY SYSTEMS
TABLE 2.—Mean (6SE) auditory-evoked potentials thresholds (dB) in juvenile Chinook salmon (SL¼ standard length; Wt¼
weight; BFA ¼ barged fish group A; BFB ¼ barged fish group B; Ctrl ¼ control fish; BF ¼ barged fish).
Group
n
Control fish
Migrant fish
BFA (all)
BFB (all)
All BF
Ctrl , 7 d
BF , 7 d
Ctrl 7 d
BF 7 d
10
9
20
10
30
5
13
5
17
100 Hz
97.2
97.0
98.8
100.0
99.2
95.2
99.2
99.2
99.2
6
6
6
6
6
6
6
6
6
1.57
1.27
0.84
1.33
0.71
2.06
0.94
2.2
1.05
200 Hz
89.5
89.9
91.6
92.0
91.7
89.2
90.8
89.8
92.5
6
6
6
6
6
6
6
6
6
1.57
2.04
1.05
1.33
0.82
2.35
0.99
2.33
1.23
400 Hz
97.4
99.4
100.15
100.0
100.1
94.6
99.7
100.2
100.4
¼ 0.755; DA: Wilk’s lambda ¼ 0.964, F4,25 ¼ 0.230, P
¼ 0.919). Since there was no indication of a difference
between these two groups, all barged fish were pooled
for subsequent testing, which increased the power of
these analyses.
To investigate the main subject of interest in this
experiment, MANOVA was used to compare the
factors of treatment (control versus barged fish) and
time (,7 and 7 d postbarging). For the treatment
factor, the null hypothesis was rejected (F1,36 ¼ 4.26, P
¼ 0.0463); thus, there was evidence that a significant
threshold shift occurred between control fish and
pooled barged fish (Figure 7A). In the case of the
time factor, the null hypothesis was not rejected (F1,36
¼ 3.965, P ¼ 0.0541); however, because the P-value
was near the significance level, a follow-up analysis
(post hoc) of the MANOVA was necessary to further
investigate the influence of the time factor on
treatment.
The follow-up comparison examined control fish
versus barged fish sampled within 7 d postbarging or at
7 d postbarging and later; once again, ANOVA and DA
were used. For data collected within 7 d postbarging,
the null hypothesis was rejected (ANOVA: F1,16 ¼
7.91, P ¼ 0.013, Bonferroni-corrected P ¼ 0.026; DA:
Wilk’s lambda ¼ 0.463, F4,13 ¼ 3.776, P ¼ 0.030); thus,
there is evidence that a significant TTS occurred
between control and barged fish groups during this
period (Figure 7B). The degree of TTS was 3.95 dB for
100 Hz, 1.6 dB for 200 Hz, 5.09 dB for 400 Hz, and
4.72 dB for 600 Hz. For data collected at 7 d
postbarging and later, the null hypothesis was not
rejected (ANOVA: F1,20 ¼ 0.275, P ¼ 0.606; DA:
Wilk’s lambda ¼ 0.825, F4,17 ¼ 0.899, P ¼ 0.486); thus,
there was no evidence that a significant TTS occurred
between control and barged fish during this period of
time, and fish recovery from TTS was indicated (Figure
7C).
In summary, the results show that there was no
difference between controls and migrants, thus indicating that handling did not affect hearing thresholds;
6
6
6
6
6
6
6
6
6
1.21
1.43
0.65
1.45
0.63
0.98
0.75
1.32
0.97
600 Hz
112.6
115.8
115.5
115.5
115.5
110.2
114.9
115
115.9
6
6
6
6
6
6
6
6
6
SL (cm)
1.56
1.18
0.68
1.07
0.57
2.57
0.89
1.22
0.74
13.05
13.97
13.08
13.52
13.23
12.98
13.11
13.12
13.32
6
6
6
6
6
6
6
6
6
0.23
0.51
0.11
0.21
0.11
0.29
0.15
0.39
0.15
Wt (g)
24.59
30.41
24.68
27.95
25.77
24.41
25.31
24.77
26.13
6
6
6
6
6
6
6
6
6
1.10
3.89
0.57
1.60
0.70
1.33
0.76
1.92
1.10
there was also no difference between BFA and BFB,
and these groups were pooled together. There was a
statistical difference in thresholds between controls and
barged fish sampled within 7 d postbarging, but the
hearing threshold in barged fish sampled at 7 d
postbarging and later was similar to that of the control
fish, suggesting that the barged fish had recovered.
Discussion
To investigate potential causes of latent mortality in
Chinook salmon smolts transported downstream by
barge, we considered stressors potentially associated
with the barge environment that might impair the
olfactory and the auditory systems. Water quality and
noise that occur within the confines of a barge holding
tank have the potential to affect the olfactory and
auditory systems. While basic water quality variables
(e.g., temperature, dissolved oxygen, and pH) are
continuously monitored throughout every barge transport, exposure to dissolved metals and noise might be
associated with the tank, plumbing, and water
circulation equipment.
Dissolved Metals and Olfactory Function
Barges do not appear to be a significant source of
waterborne heavy metals. The barge holding tanks are
continuously refreshed with river water, and we did not
observe an accumulation of nickel, cadmium, zinc,
copper, or lead to concentrations that might adversely
affect the health of transported salmon. We focused on
copper in this study because this metal is particularly
toxic to the peripheral sensory neurons of fish. Copper
causes the physical degeneration and death of olfactory
neurons at concentrations that exceed approximately 20
lg/L (e.g., Moran et al. 1992; Julliard et al. 1996).
These degenerative effects occur over a time scale of a
few hours in both the olfactory system (Hansen et al.
1999) and the lateral line (Linbo et al. 2006). No such
injury was observed in the olfactory system of
transported fish; this finding was consistent with the
786
HALVORSEN ET AL.
relatively low concentrations of copper and other
metals in the barge holding tanks.
Since direct measurement of olfactory function was
not performed for this study, it is possible that olfactory
impairment may have occurred without physical
evidence of sensory cell degeneration. Several studies
have shown that copper can interfere with the
physiological function of olfactory sensory neurons at
levels below those that cause physical injury to the
epithelium. For example, electrophysiological recording from both the olfactory epithelium (Baldwin et al.
2003) and the olfactory forebrain (Sandahl et al. 2004)
have shown that dissolved copper reduces the olfactory
response of salmon to natural odorants. Loss of
olfactory function occurs very quickly (i.e., within
minutes; Baldwin et al. 2003) and at relatively low
concentrations. Functional anosmia corresponds to
reductions in chemically mediated predator avoidance
behaviors for copper exposures at or above approximately 2 lg/L (Sandahl et al. 2007). However,
measured copper concentrations in the barge environment were below this threshold for neurobehavioral
toxicity. The levels of cadmium and other metals were
also well below those expected to have physiological
effects on olfactory sensory neurons (e.g., Scott et al.
2003).
Barge Noise and Hearing
FIGURE 7.—Auditory-evoked potentials thresholds (sound
pressure level [SPL], dB referenced to [re] 1 lPa) of Chinook
salmon smolts: (A) control fish compared with all barged fish
(significantly different); (B) comparison of control fish (ctrl)
and barged fish (BF) sampled within 7 d postbarging (,7 d;
significantly different); and (C) comparison of control fish and
barged fish sampled at 7 d postbarging and later (7 d; not
significantly different).
Recordings of noise levels in the barge holding tanks
resolved mean broadband RMS levels of up to 136 dB
re 1 lPa, and the maximum energy content (below 400
Hz) fell within the sensitive hearing range of salmon.
Diesel engines on the fish transport barges created
mechanical noise that contained considerable lowfrequency energy; thus, smolts were exposed to these
noise levels continuously for up to 58.5 h. The barge
holding tanks have a boundary of air between the tank
walls and the barge hull. This air boundary may
dampen the airborne engine noise from entering the
holding tanks; however, the engines are coupled to the
tanks via the metal hull, thereby mechanically feeding
vibrations into the holding tank waters.
The results for control versus barged fish sampled
within 7 d postbarging suggest that barge noise at 136
dB re 1 lPa for up to 58.5 h caused a statistically
significant TTS that can be seen in Figure 7B.
Recovery from TTS is shown by the overlapping
thresholds in Figure 7C, where control fish are
compared with barged fish sampled at 7 d postbarging
and later. Thus, the noise level and noise duration in
the barge holding tanks were sufficient to induce mild
TTS in Chinook salmon smolts, but recovery seems
likely.
Only a few studies have looked at the effects of
BARGING EFFECTS ON SMOLT SENSORY SYSTEMS
‘‘noise’’ on nonspecialist fishes (Scholik and Yan
2002b; Smith et al. 2004a; Wysocki et al. 2007). One
study using navy sonar at much higher sound levels
(e.g., 193 dB re 1 lPa RMS) reported TTS in rainbow
trout (Popper et al. 2007). In contrast, there are studies
reporting TTS in hearing specialists after exposure to
white noise for as little as 2 h (e.g., Scholik and Yan
2001, 2002a; Smith et al. 2004b, 2006).
A few studies on nonspecialist fishes are worth
noting. Wysocki et al. (2007) exposed 92-d-old
rainbow trout to a maximum aquaculture noise level
of 150 dB re 1 lPa for 8 months and found no TTS
compared with control groups. Scholik and Yan
(2002b) exposed bluegills Lepomis macrochirus to
white noise at 142 dB re 1 lPa for 24 h and found no
immediate threshold shift. However, after 6 d they
found a latent threshold shift of 5 dB or less across
tested frequencies; this shift was not significant. Their
study exposed bluegills to noise that was 6 dB louder
than noise in the barging study; however, our study
exposed Chinook salmon smolts for a longer time. The
results of the two studies are similar except for choice
of species. Smith et al. (2004a) exposed Nile tilapia
Oreochromis niloticus to white noise at 170 dB re 1
lPa for 28 d and reported an immediate threshold shift
only at 800 Hz. That study used a much longer duration
and higher intensity stimulus than our present study;
therefore, a direct comparison cannot be made between
the two studies. Moreover, most other studies involve
tests on hearing specialists, making these studies
incomparable with the present study because salmonids
are nonspecialists.
Conclusions
Overall, our results show a TTS that might put
Chinook salmon smolts at a disadvantage in terms of
detecting and avoiding predators as they migrate
through the Columbia River estuary. However, the
magnitude of TTS and the extent to which it could
affect fish (e.g., behavior, predatory avoidance, or
auditory scene interpretation) are unknown at this time.
These results warrant further investigation to determine
the ways in which TTS affects fish and ultimately their
survival.
While not examined directly in this study, a likely
cause of fish loss may be overall increases in stress that
result from decreased sensory sensitivity, even if it is
below the threshold that could be seen in the studies
performed. Indeed, smolts in the Columbia River basin
are subject to considerable avian (Schreck et al. 2006)
and aquatic predation (Muir et al. 2006). It is typically
easier for predators to capture prey when the prey have
impaired sensory functions or are in a substandard
condition because of exposure to an environmental
787
stressor (Temple 1987; Mesa et al. 1994). Handling
and transportation are well-known stressors for fish
(e.g., Scott et al. 2001; Chandroo et al. 2005;
Huntingford et al. 2006). In addition, Congleton et al.
(2000) have reported increased levels of stress
indicators in Chinook salmon smolts from barge
transportation. Thus, it is probable the barge experience
was a stressor for the fish and that this was exacerbated
by temporary hearing loss. Moreover, exposure to boat
noise has been found to increase cortisol secretion in
several species of freshwater fishes compared with
controls kept either in a quiet environment or exposed
to constant noise (Wysocki et al. 2006).
Investigations increasingly highlight the importance
of sublethal effects of stress by estimating the effects of
anthropogenic stressors on natural salmon populations
(Peterson et al. 2003). In the case of barged Chinook
salmon smolts, clear auditory effects are indicated, but
further studies must be performed to know whether
these effects lead to a substantial increase in postrelease
predation mortality (i.e., at the scale of D). It would be
important to repeat the study with more fish and to
investigate the potential for combined effects with
other stressors.
Acknowledgments
We thank the U.S. Army Corps of Engineers
(USACE) for funding this project (TPE-W-04-06)
through Normandeau Associates. We also thank Jana
Labenia (National Oceanic and Atmospheric Administration Fisheries), Derek Fryer (USACE), Melanie
Sharp (Normandeau), Adam Frankel (Marine Acoustics, Inc.), and Ed Smith (University of Maryland;
supported by P30 DC004664 from the National
Institute on Deafness and Other Communication
Disorders, National Institutes of Health) for technical
support. Jennifer Hill and David Zeddies provided
helpful discussions. Thanks to Cathy Laetz and Bill
Muir for reviewing the manuscript. Thanks also to staff
and associates from Bonneville Dam, including Dean
Ballinger and Jon Rerecich, for facility support.
Important assistance came from the scientists who
collected smolts on the barge, including Brad Ryan,
Lyle Gilbreath, and Ben Housman. Finally, thanks to
Lyle Gilbreath for lending us large holding tanks at the
monitoring facility to maintain the Chinook salmon
smolts.
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