Effects of rapid experimental temperature increases on acute physiological stress and behaviour of stream dwelling juvenile chinook salmon

ARTICLE IN PRESS

Journal of Thermal Biology 31 (2006) 429–441 www.elsevier.com/locate/jtherbio

Effects of rapid experimental temperature increases on acute physiological stress and behaviour of stream dwelling juvenile chinook salmon Jason T. Quigleya,, Scott G. Hinchb,c a

Fisheries and Oceans Canada, 200-401 Burrard Street, Vancouver, BC, Canada b Department of Forest Sciences, University of British Columbia, Canada c Institute for Resources, Environment and Sustainability, University of British Columbia, 2424 Main Mall, Vancouver, BC, Canada Received 15 November 2005; accepted 14 February 2006

Abstract We experimentally heated small streams in summer and investigated the short-term behavioural changes and physiological stress responses of juvenile chinook salmon (Oncorhynchus tshawytscha). We rapidly raised temperatures
1–4 1C for 1.5 h above ambient levels of
7–15 1C in groundwater fed tributary streams and
19–23 1C in side-channel streams. Juvenile chinook rearing in groundwater fed tributaries were generally unaffected behaviourally; however, we found that temperature increase caused fish in the tributary trials to be physiologically stressed (elevations in mean cortisol concentrations ranged from 116% to 253%). Side-channel trials caused some mortality of juvenile chinook and a stronger display of behaviours indicative of stress and avoidance such as erratic swimming, abnormal posture, and aggregative behaviour. Foraging rates increased over 56 times in response to heating in side-channel trials. Cortisol levels did not increase in side-channel trials, but rather showed a trend to levels below control values suggesting an impaired stress response possibly due to chronic stress. Our results may reflect conservative responses in terms of what we may find with other salmonid species since juvenile chinook have been described as the most tolerant of the Pacific salmon species to elevated temperatures. r 2006 Elsevier Ltd. All rights reserved. Keywords: Juvenile chinook; Temperature; Field experiment; Physiological stress; Cortisol; Avoidance; Foraging

1. Introduction Water temperature has been called the ‘‘master ecological factor’’ (Brett, 1971) in terms of fish growth and survival. For stenothermic fish such as salmonids, temperature influences spatial distribution (Brett, 1971; Levy, 1992; Glova and Mason, 1977), behaviour (Glova and Mason, 1977), and metabolic processes (Brett, 1995). The primary mechanism for body temperature regulation is through behavioural changes (Levy, 1992). Indeed, salmonids display considerable behavioural plasticity when faced with water temperatures that deviate from their preferred Corresponding author. Current address: Canadian Environmental Assessment Agency, 320-757 West Hastings Street, Vancouver, BC, Canada V6C 1A1. Tel.: +1 604 666 6989; fax: +1 604 666 6990. E-mail address: [email protected] (J.T. Quigley).

0306-4565/$ - see front matter r 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.jtherbio.2006.02.003

range and have been documented to avoid and/or select habitats based on thermal regimes and to compete for locales with favourable temperatures (Beitinger et al., 2000). Over certain temperature ranges, increases in temperature can stimulate feeding and growth. Increases beyond species- or age-specific metabolically optimal temperatures can, however, result in weight loss because of high metabolic costs. Rapid increases in temperature of 7–15 1C can cause dispersal (Gray, 1990), increase vulnerability to predation (Sylvester, 1972; Coutant, 1973), advance ageing and skin deterioration (Iger et al., 1995), elevate levels of heat shock proteins and cause hypercortisolemia (Thomas et al., 1986), and cause acute thermal shock (Sylvester, 1972). Furthermore, physiological stress caused by rapid increases beyond optimal temperatures can be exacerbated by other environmental features which may

ARTICLE IN PRESS 430

J.T. Quigley, S.G. Hinch / Journal of Thermal Biology 31 (2006) 429–441

be altered themselves by increasing temperatures (i.e. dissolved oxygen levels, water pollution; Nolan et al., 2003). While rapid temperature change can be a natural phenomenon encountered by fish during migration or dispersal life stages, there are several anthropogenic causes of rapid temperature change (e.g. thermal discharges from industrial cooling water, reservoir outlets, river level fluctuations from operations at hydroelectric dams, streamside logging) which can affect fish during all stages of life. Most research focusing on the effects of rapid temperature increases on fish behaviour and physiology has primarily relied on experiments in laboratory settings or in artificial streams (Brett, 1952, 1970; Bisson and Davis, 1976; Coutant, 1973; Linton et al., 1999). Field studies can provide the ecological realism (Adams, 1990; Waldichuk, 1993) lacking in laboratory settings, but because rapid thermal changes occur simultaneously with changes in other environmental characteristics such as stream flow or suspended sediment loads, few have isolated thermalspecific effects. Needed are studies that thermally manipulate natural streams in order to confirm previous lab and field results. Furthermore, a large component of the past research has focussed on examining acute effects of relatively large changes in temperature (e.g. Sylvester, 1972; Coutant, 1973; Wedemeyer, 1973; Thomas et al., 1986; Mesa et al., 2002; temperature changes in those studies ranged from 6.5 to 30 1C with an average change of 11.4 1C). While such temperature changes may occur naturally, or as a result of anthropogenic influences, smaller changes are likely a much more common phenomenon and deserve more careful attention. There have been no field experiments to examine how fish respond, behaviourally and physiologically, explicitly to short-term thermal manipulations. We manipulated thermal conditions of small streams through rapid artificial heating and investigated short-term effects of modest temperature increases to juvenile chinook salmon (Oncorhynchus tshawytscha). Temperature increases above ambient levels ranged among trials from
1 to 4 1C. We conducted experiments in summer in two thermally different, though physically similar, natural environments in which juveniles routinely rear. Groundwater fed streams are relatively cool during summer periods whereas side-channel streams are fed from mainstem rivers which are relatively warm during summer periods. For groundwater streams, we predicted that rapid temperature increases, provided these entered into or remained within the species preferred thermal range (12–14 1C for juvenile chinook; Brett, 1952) would not lead to physiological stress but may result in increased activity and feeding levels because of increases to fish metabolism. For side-channel streams, whose temperatures are naturally elevated well above the upper preferred temperature, we predicted that temperature increases would cause physiological stress and lead to behaviours indicative of dispersal provided we did not exceed upper thermal maximum levels (
26–29 1C for most juvenile

salmonids, Beitinger et al., 2000; 25 1C for juvenile chinook, Brett,1952). 2. Study system Our experiment sites were located in the Torpy River watershed in northern interior British Columbia (Fig. 1), a region characterized by flat or gently rolling surfaces with poorly organized drainage patterns (Rosberg and Aitken, 1981). The soils are primarily glacial lacustrine silts and clays (Mac Donald et al., 1996). Tree composition is primarily hybrid white spruce (Picea glauca x engelmannii) in upslope areas with a mixture of engelmann spruce (Picea engelmannii), subalpine fir (Abies lasiocarpa) and interior western hemlock (Tsuga heterophylla) in lowlands and riparian. Chinook salmon adults enter the lower Torpy system in late July and spawn in late August (Rosberg and Aitken, 1981). These are of the ‘stream-type’ race and juveniles rear in the system for one to two years (Healey, 1991). The average annual escapement of adults to the Torpy River watershed is approximately 2100 with a historical maximum escapement of 4000 (1981–1992; Mac Donald et al., 1996). Juvenile chinook are the numerically dominant anadromous fish in this system. Other species present include rainbow trout (O. mykiss), bull trout (Salvelinus confluentus), prickly sculpin (Cottus Asper), northern squawfish (Ptychocheilus oregonensis), burbot (Lota lota), white sucker (Catostomus commersoni), and rocky mountain whitefish (Prosopium williamsoni), though no data are available on their absolute or relative abundances. Since 1956, the Torpy River watershed has been extensively logged, with operations peaking during the 1970s (Rosberg et al., 1981). As of 1996, approximately 15% of the watershed, and 50% of the lower Torpy had been logged (Mac Donald et al., 1996). Forest harvesting in the lower Torpy River has concentrated almost exclusively in low gradient floodplain and riparian areas, which typically contains the most valuable juvenile fish habitat. Logging roads and stream crossing networks are extensive. 3. Methods 3.1. Experimental sites and procedures We used three un-named tributaries and one sidechannel of the Torpy River as experimental sites. Their riparian had never been logged. The tributary experiment consisted of five trials conducted in 1997 and 1998. The side-channel experiment consisted of two trials conducted in 1998. Tributaries had similar habitat characteristics: average bankfull widths of 1–2.5 m, all flowed southerly, all low gradient (1–2%), substrate composition of 70% fines and 30% gravels, and all had abundant physical cover in the form of undercut banks, over-hanging vegetation, deep pools and ample in-stream woody debris. The side-channel resembled the tributaries though it was larger and

ARTICLE IN PRESS J.T. Quigley, S.G. Hinch / Journal of Thermal Biology 31 (2006) 429–441

431

Fig. 1. Location of the Torpy River Watershed in British Columbia, Canada.

connected to the mainstem at its upstream and downstream ends. It had low velocity glides and deep pools entirely composed of fine sediments with an average channel width of approximately 3.5 m. Tributaries were largely groundwater fed; side-channels were surface water fed from the adjoining Torpy River. Tributaries and side-channels had very different thermal patterns with tributaries generally being much cooler in the summer. Physical cover was limited to overhanging vegetation, deep pools and some large wood. Habitat and water quality assessment methods are detailed in RIC (1997). Sections within the tributaries and side-channels, approximately 100 m in length, were selected for experiments—each containing a minimum of two sets of pools, riffles, and glides (sensu RIC, 1997). Enclosure nets (1 mm mesh) were installed at the downstream, centre and upstream end of each section thereby creating two, 50 m sections. This effectively isolated groups of fish within upstream sections (the ‘control’) and downstream sections (the ‘treatment’). At the ends of each section, two-way weirs were installed across the wetted channel at a 301 angle towards the downstream end, enabling an assessment of upstream and downstream movement direction. Movement data were only collected in 1998. The duration of each experiment was approximately 3.5 h divided into pre-heating (1 h), heating (1.5 h) and post-heating phases (1 h). Each experiment began at 11:00 am. Streams were heated by pumping water from the stream to a series of heaters, using a variable speed Honda portable pump (50 gpm) (Model WB15) connected to a

non-collapsible hose. Water was pumped at a rate of 16 L/ min through four propane powered instantaneous hot water heaters (Bosch Booster Pressure Wash Model W400K5, 117 000 btu), and reintroduced into the stream 25 1C above ambient stream temperature through a diffuser system to ensure mixing. Each diffuser unit was constructed from five household showerheads. Water intake was located downstream of the diffuser unit to ensure maximum heating. Heated water was added to the middle of treatment sections. The water heaters were only ignited during the heating phase of the experiment, yet the pump was operated during all phases to ensure that responses exhibited by juvenile chinook were a result of the elevated temperature. Twelve temperature data loggers (Onset instruments) were deployed at 10 m intervals within each experiment site. Two loggers were placed immediately upstream from the heating apparatus and the rest were placed downstream. Loggers recorded temperature every 5 min during experiments and for several days before and after experiments. Upstream loggers were used to collect reference data. Dissolved oxygen was measured once daily using a hand-held YSI model 550 probe. Discharge was measured once daily by flow metre and measuring tape according to standard methodology (RIC, 1997; Schuett-Hames et al., 1994) prior to each trial. Four video cameras (Citizen model JSS 1012C) housed in dark green, waterproof, aluminium housings (approx. dimensions: 50 mm  105 mm) with Lexan lids for optical clarity were used to observe fish behaviour. In both

ARTICLE IN PRESS 432

J.T. Quigley, S.G. Hinch / Journal of Thermal Biology 31 (2006) 429–441

treatment and control sections one camera was positioned at mid-channel and aimed downstream and another was positioned at the stream margin aimed towards midchannel, perpendicular to flow. Sections of 1 cm diameter PVC pipe, marked at 5 cm intervals, were installed upright in the substrate in the field of view of the underwater cameras. The pipes functioned as reference points to ensure that the field of view was the same area (generally 1 m  1 m), in both side-view and frontal view cameras, as well as between treatment and control sections. Two, 25.4 cm, black and white monitors (Citizen model JSS 1012M) contained in rainproof Lexan housings, tinted to eliminate sun glare, were used to display images which were recorded by two VHS video recorders (Sanyo model VHRH607), also in Lexan housings. The underwater video cameras and recording system were powered by a Honda variable speed generator.

was then disrupted by ultrasonication for 1 min (B. Braun Biotech, Braun-Sonic L, Allentown, PA, 18103). Five millilitres of diethyl ether was added to samples which were mixed then centrifuged at 1000g for 5 min. The water component was frozen in liquid nitrogen and the ether decanted. Samples were then re-extracted and the ether fractions combined. Ether was evaporated under a stream of nitrogen gas. Following complete evaporation of ether, 2 ml of phosphate buffered saline (1.5 mM KH2PO4, 2.7 mM Na2HPO4, 150 mM NaCl, pH 7.4) containing 2% bSA (bovine serum albumin) was added to samples which were kept at 4 1C and vortexed frequently for 2 h. Cortisol concentrations were determined by radioimmunoassay using 125I (Diasorin, Stillwater Minnesota, 550820285). Efficiency of extraction was determined from spiking paired samples with cortisol and was found to be 92–95%.

3.2. Stress measures

3.3. Behavioural measures

Cortisol is a hormone responsible for regulating hydromineral processes, growth, and the immune system in teleost fish. These functions are important for an individual fish’s health and fitness. Cortisol increases rapidly in the body (e.g., 3–30 min) in the presence of a variety of stressors and is commonly used as an indicator of acute stress in fish (Donaldson et al., 1984). Continued production of cortisol can inhibit growth and reduce disease resistance (Anderson, 1990). During the heating phase, juvenile chinook (n ¼ 6–10/section) were sampled using electroshocking in both control and treatment sections for analysis of whole body cortisol. To determine if containment within netted sections affected acute stress levels, juveniles (n ¼ 6–10 from each site) were also collected for cortisol assessment by electroshocking during the pre-heating phase in the control and upstream of the control in the absence of any nets (unnetted). Sampled fish were snap frozen on dry ice (o 60 s) for transport to the laboratory. Such rapid processing of samples ensures that electroshocking will not cause an endocrine response (Sumpter et al., 1986). Due to a shortage of dry ice during one side-channel trial, the snap frozen approach could not be used so blood plasma was extracted and centrifuged in the field as an alternative means of assessing cortisol levels. Because we used different techniques for examining cortisol, results could not be statistically compared between the two side-channel trials. However, relative comparisons are still valid between whole body and plasma cortisol levels as they have been shown to demonstrate similar trends in studies of physiological stress in brown and rainbow trout (Pottinger and Mosuwe, 1994). Whole body cortisol content was determined with a method modified from Feist et al. (1990). Briefly, frozen fish were ground into powder using a mortar and pestle in a slurry with liquid nitrogen which was then evaporated off. Distilled water, 300 mL, was added to each sample which

During all phases of experiments, every 15 min, we assessed numbers of juvenile chinook captured at weirs to provide an index of movement. We made underwater video recordings of fish behaviours (described in detail below) in both treatment and control sections throughout all phases of the experiments. Each phase of every trial was divided into 10 equal time intervals with 30 intervals per trial. A systematic random approach was used to extract behavioural data from the underwater video recordings. Approximately a 1.5 min period within each interval (total time approximately 15 min/phase) was randomly chosen for data extraction. Fish behaviours were only recorded that were completely contained within the sample period. Behaviours that began prior to or ended after a particular sample period were not included. Information on the following behaviours was transcribed from the video tapes: feeding attempts, aggression, yawning, fleeing, fish numbers, and fish minutes. These behaviours, which are described in detail below, were selected because they were quantifiable, repeated across treatments, were readily identifiable, and were biologically relevant for temperature manipulation studies. In all cases, frequencies of behavioural activities were recorded. We did not extract duration, intensity or pattern of behavioural activities. Feeding attempts were defined as the number of foraging attempts per minute. The high resolution of the cameras enabled the observation of individual prey items. Feeding attempts consisted of a rapid opening and closing of the mouth for a potential prey item and often coincided with a change in orientation in the water column, or small movement to capture a prey item. Foraging success was not quantified. Aggression was defined as any agonistic behaviour directed toward another fish, which included chasing, nipping, and charging (Hartman, 1965; Chapman, 1962). Yawning was defined as the protracted and excessive gaping of the mouth, and was easily distinguishable from feeding due to an absence of a potential prey item, a lack of

ARTICLE IN PRESS J.T. Quigley, S.G. Hinch / Journal of Thermal Biology 31 (2006) 429–441

any change in position or orientation in the water column, and a very protracted and excessive gaping of the mouth. Fleeing was defined as evasive behaviour, most often displayed in response to another aggressive individual. Fleeing fish were displaced from their territory or previously occupied position either temporarily or permanently. The number of fish observed per sampling period was recorded from the video tapes. However, we had no means of identifying individual fish so we did not use this information to assess abundance, but used it to provide a general index of activity levels. The frequencies of extracted behaviours were divided by the time observed to provide a frequency of behaviour per minute that could be compared between different sections and phases of experiments. The total time that each fish was in the field of view in each section (treatment, control) was summed for each phase of the experiment (pre-heating, heating, post-heating) to provide an accumulated time. This was divided by the sample period time to provide an estimate of equivalent number of fish viewed per minute, termed ‘‘fishmin’’. 3.4. Data analysis All data were visually inspected for normality and homogeneous variances. Cortisol and behavioural data were log transformed to minimize the effects of heterogenous variances. Trials were treated as replicates thus data were consolidated and averaged accordingly to provide single response variables. Univariate ANOVAs were used to analyse cortisol data and two-way, repeated measures ANOVAs for movement data. The factors in the models included the effect of time (pre-heat, heat, post-heat), location (control, treatment), a statistical block for the effect of individual streams, and the effect of the day on the response variable. The effect of the day of the experiment is used to control for many different effects that vary over different experiment dates and cannot be considered constant over all dates, such as ambient water temperature, ambient air temperature, UV radiation, etc. Behavioural data were analysed using a Poisson process to compare response variables among trials because these data were not normally distributed due to the large number of zeros in the variables. Bonferroni multiple range tests were used to determine which response variable means differed (i.e. pre-heat, heat, post-heat). Least square means (LS Means) were used to calculate means for a posteriori tests. To determine the directionality of movement (upstream or downstream), Chi-square tests were used to test the independence of the upstream and downstream variables in the control and treatment sections. All tests were considered to be significant to a P p 0.05. Descriptive statistics (mean, 7 1 SE) were used to describe the temperature data and the side-channel cortisol results. Temperature data from the two upstream reference data loggers (control) and the downstream data loggers (treatment) were pooled for the pre-heating phase, and

433

categorized into upstream (t1 pre-heating) and downstream (t2 pre-heating). Temperature means calculated from the preheating phase from the upstream reference means were subtracted from the downstream sites. This served as a correction factor to ensure that any variation in temperature recorded during the heating phase was a function of the heating apparatus, and not due to differences in calibration. The mean temperature from the upstream loggers during the heating phase (t1 heating) was subtracted from the mean temperature from the downstream loggers during the heating phase (t2 heating). The correction factor calculated from the pre-heating data was subtracted from this value to determine the mean temperature increase during the heating phase: DH ¼ ðt2 heating  t1 heating Þ  ðt2 preheating  t1 preheating Þ. 4. Results 4.1. Environment Discharge was relatively low and invariant during trials in tributaries (mean, SE, n; 0.06 m3/s, 0.017, 5) and sidechannels (mean, SE, n; 0.0077 m3/s, 0.0007, 2). Dissolved oxygen concentrations were measured at the start of a trial and at the conclusion of the heating phase. Within each trial, start and end values did not differ so only start values are subsequently reported. Dissolved oxygen concentrations, averaged among days, did not vary much among all trials (n ¼ 7; 8.3–10.4 mg/L). These oxygen concentrations represent fully saturated values and are high enough so as not to cause impairment of feeding, growth or swimming performance of juvenile salmonids (Bjornn and Reiser, 1991). Experimental increases in temperatures during individual trials ranged from 0.4 to 3.8 1C and ambient temperatures ranged from 7.4 to 23.6 1C (see Table 1 for details on individual trials). In 1997, mean stream temperature increase (DH) in tributary trials was 0.4 1C (n ¼ 2 trials; SE ¼ 0) and mean ambient stream temperature was 7.7 1C (n ¼ 2; SE ¼ 0.3). In 1998, mean DH in tributary trials was 1.6 1C (n ¼ 3 trials; SE ¼ 0.3) and mean ambient temperature was 12.8 1C (n ¼ 3 trials; SE ¼ 1.7). For the pooled 1997 and 1998 tributary trials, the mean DH was 1.1 1C (SE ¼ 0.3) and mean ambient temperature was 10.7 1C (SE ¼ 1.6). In 1998, mean DH in side-channel trials was 3.1 1C (n ¼ 2 trials; SE ¼ 0.7) and mean ambient water temperature was 21.4 1C (n ¼ 2 trials; SE ¼ 2.2). 4.2. Cortisol For tributary trials, elevations in mean cortisol concentrations ranged from 116% to 253% in treatment sections compared to control sections (Table 1). Pooling the 1997 and 1998 tributary data, we found that cortisol concentrations were significantly higher (ANOVA, Po0.01) in treatment sections (mean7SE; 4.0770.59 ng/g) compared to controls (mean7SE; 2.2970.33 ng/g). We found no

ARTICLE IN PRESS J.T. Quigley, S.G. Hinch / Journal of Thermal Biology 31 (2006) 429–441

434

Table 1 Trial date, habitat type (tributary—T; side-channel—S), mean ambient water temperature (AT), experimental temperature increase (DT), and final temperature (FT) for each trial Trial date

Habitat

AT

DT

FT

Nnet

Net

Control

Treatment

97/09/19

T

7.4

0.4

7.8

16.7

1.08 (0.13,3) 3.06 (1.16,6) 2.28 (0.45,10) 54.07 (8.78,10) 3.48 (0.21,8) 2.45 (0.13,8)

21.6

n/a

5.14 (1.21,8) 4.10 (1.17,8) 2.36 (0.29,8) 314.34 (54.27,7) 3.50 (0.37,8) 2.86 (0.28,9) 10.0 (1.66,9)

4.25 (0.88,8) 2.39 (0.49,7) 2.37 (0.32,9) 175.19 (55.07,7) 2.89 (0.32,10) 2.14 (0.31,8) 18.33 (2.09,8)

6.94 (1.66,7) 5.77 (1.27,8) 3.48 (0.53,12) 167.79 (46.53,6) 3.36 (44,8) 5.42 (1.42,8) 12.43 (1.83,8)

97/09/29

T

8

0.4

8.4

98/07/21

T

9.6

1.9

11.5

98/08/01

S

23.6

3.8

27.4

98/08/03

T

13.1

1.9

15

98/08/13

T

15.6

1.1

98/08/15

S

19.2

2.4

16

(A)

0

4.3. Behaviour

8

a

a

b

b

a

b

4

16 12

a

a

8 4 0

(B)

4.3.1. Movement In tributary trials total number moving in treatment sections was not different than control sections between the different experimental phases (P ¼ 0:484) (Fig. 2a, Table 2). However, in side-channel trials, the total number moving increased over 64 times in the treatment sections during the heating phases compared to the pre-heating phases (Bonferroni, P ¼ 0:017) (Fig. 2b) (Table 2). There was no difference in total number moving in the control sections (Bonferroni, P ¼ 0:700). In the treatment sections, direction of fish movements during the heating phases of side-channel trials was primarily upstream, compared to a tendency for downstream movement in the control sections. Approximately 68% of the juvenile chinook in the treatment sections (n ¼ 140) moved upstream and 32% moved downstream as a result of the temperature manipulations, compared to 28% in the

12

20 Total number moving

statistical differences in cortisol concentrations (P ¼ 0:06) between fish in un-netted (1.7770.26 ng/g) or netted sections (3.0870.45 ng/g) though there was a trend to higher values (74% higher) in netted fish. In side-channel fish, cortisol was assessed from plasma for trial 1 but whole bodies for trial 2 therefore absolute levels are not comparable between trials so statistical analyses were not possible; however, the similarity in trends between the two trials are very compelling. Specifically, treatment levels of cortisol in both were lower than control levels (Table 1). Interestingly, this is the opposite of the results we found in the tributary experiments. The control levels of cortisol in trial 2 of the side-channel experiment, which uses comparable methods to the tributary experiments, were
6 times higher than tributary controls (Table 1) indicating that fish were significantly more stressed in the side-channel prior to initiating the heating experiment.

Total number moving

Temperatures are expressed in 1C. Mean cortisol (71 SE, n) is reported for control and treatment phases and for non-netted (nnet) and netted (net) samples. Cortisol is expressed as whole body concentrations (ng/g) except for 98/08/01 which is expressed as plasma cortisol (ng/ml).

Control

Treatment Pre - heat

Heat

Fig. 2. Mean total movement of juvenile chinook during tributary (A) and side-channel (B) heating trials. Error bars represent 71 SE. Bars with similar letters did not differ. Means are based on three and two trials, respectively.

control sections (n ¼ 64) moving upstream and 71.9% moving downstream (w2 ¼ 28:061, df ¼ 1, P ¼ 0:001). 4.3.2. Feeding In tributary trials, mean feeding in treatment sections did not differ between pre-heating and heating phases (w2 ¼ 0:16, df ¼ 1, P ¼ 0:690), but increased two times from heating to post-heating phases (w2 ¼ 14:93, df ¼ 1, Po0.001), and also increased between pre-heating and

ARTICLE IN PRESS J.T. Quigley, S.G. Hinch / Journal of Thermal Biology 31 (2006) 429–441

435

Table 2 F statistics, degrees of freedom (df), and associated probability levels (* indicates significance) for ANOVAs on behavioural variables in tributary and sidechannel experiments F statistic

P-value

Variable

Factor

Tributary total number moving

Time Location* Location  time

1.46 8.65 0.56

1,6 1,6 1,6

0.273 0.026 0.484

Side-channel total number moving

Time Location Location  time*

6.16 1.67 9.41

1,4 1,4 1,4

0.068 0.266 0.037

Tributary feeding attempts

Time* Location* Location  time*

9.95 15.45 26.25

2 1 2

0.007 o0.001 o0.001

Side-channel feeding attempts

Time* Location Location  time*

9.51 0.28 13.36

2 1 2

0.009 0.599 0.001

Tributary yawning per minute

Time Location* Location  time

0.61 8.55 0.26

2 1 2

0.737 0.004 0.876

Tributary aggression per minute

Time Location* Location  time*

1.73 12.05 11.78

2 1 2

0.421 o0.001 0.003

Tributary fleeing per minute

Time Location* Location  time*

2.2 12.98 9.82

2 1 2

0.334 o0.001 0.007

Tributary fishmin

Time Location Location  time

0.23 0.24 0.13

2,10 1,10 2,10

0.798 0.634 0.882

Tributary total fish

Time Location Location  time

0.71 3.22 0.04

2,10 1,10 1,10

0.516 0.103 0.959

Side-channel fishmin

Time* Location* Location  time* Time Location Location  time

12.64 16.58 11.08 4.15 0.17 4.59

2,5 1,5 2,5 2,5 1,5 2,5

0.011 0.010 0.0145 0.087 0.696 0.074

Side-channel total fish

df

Factors include time (pre-heating, heating, post-heating) and location (control, treatment).

post-heating phases (w2 ¼ 13:84, df ¼ 1, Po0.001) (Fig. 3a) (Table 2). In control sections, feeding decreased significantly from pre-heating to heating phases (w2 ¼ 12:05, df ¼ 1, Po0.001), but did not differ between heating and post-heating phases (w2 ¼ 1:06, df ¼ 1, P ¼ 0:302), or pre-heating and post-heating phases (w2 ¼ 3:09, df ¼ 1, P ¼ 0:079). In side-channel trials, feeding in treatment sections did not differ between pre-heating and heating phases (w2 ¼ 0:02, df ¼ 1, P ¼ 0:894), but increased 56 times from the heating to post-heating phases (w2 ¼ 10:34, df ¼ 1, P ¼ 0:001). Feeding also increased between pre-heating and post-heating phases (w2 ¼ 26:17, df ¼ 1, Po0.001) (Fig. 3b) (Table 2). In control sections, similar to the

tributary experiment, feeding decreased significantly from pre-heating to heating phases (w2 ¼ 5:25, df ¼ 1, P ¼ 0:022), and from pre-heating to post-heating phases (w2 ¼ 4:56, df ¼ 1, P ¼ 0:033). Feeding did not differ between heating and post-heating phases in control sections (w2 ¼ 0:06, df ¼ 1, P ¼ 0:812). In all trials, the increase in the frequency of feeding did not occur simultaneously with increased temperature, but rather lagged behind temperature manipulations, occurring instead during the post-heating phase. 4.3.3. Yawning In tributary trials mean yawning per minute was greater in control sections (0.061/min 70.023) than treatment

ARTICLE IN PRESS J.T. Quigley, S.G. Hinch / Journal of Thermal Biology 31 (2006) 429–441

436

0.5

(A)

3

0.4

2.5 2 1.5 1

a

b

b

ab

abc

c

Fleeing per minute

Feeding attempts per minute

3.5

0.3 0.2

a

b

b

b

a

b

a

a

a

ab

a

b

0.1

0.5 0

(D)

0

6

Fishmin (equivalent # fish/mnute)

Feeding attempts per minute

7

5 4 3 2 1

a

a

b

ab

b

c

0 (B)

(E)

Aggression per minute

0.5

(C)

6 5 4 3 2 1 0 Pre-Heating

Heating

Post-Heating

0.4 0.3 0.2

a

b

b

b

a

b

0.1

Pre-Heating

Heating

Post-Heating

Fig. 3. Mean feeding attempts per minute during tributary trials (A), side-channel trials (B), mean aggression per minute during tributary trials (C), mean fleeing per minute during tributary trials (D), and mean fishmin during side-channel trials (E). Error bars represent 7 1 SE. Bars with similar letters did not differ. Means are based on number of trials (sidechannels: n ¼ 2; tributaries: n ¼ 5). Shaded bars represent treatments, controls indicated by hatched bars. Specific behavioural results are only represented in figures if the overall ANOVA models (Table 1) indicated significant results.

sections (0.014/min 7 0.008) (w2 ¼ 6:52, df ¼ 1, P ¼ 0:011). There was no interaction between location and time (Table 2). 4.3.4. Aggression and fleeing In tributary trials, aggression in control sections decreased from pre-heating to heating phases (w2 ¼ 8:33, df ¼ 1, P ¼ 0:004), and increased from heating to postheating phases (w2 ¼ 11:61, df ¼ 1, Po0.001), but did not differ between pre-heating and post-heating phases (w2 ¼ 0:62, df ¼ 1, P ¼ 0:432) (Table 2) (Fig. 3c). In treatment sections, aggression did not differ between preheating and heating phases (w2 ¼ 0:54, df ¼ 1, P ¼ 0:464),

heating and post-heating phases (w2 ¼ 2:30, df ¼ 1, P ¼ 0:129), or pre-heating and post-heating phases (w2 ¼ 0:85, df ¼ 1, P ¼ 0:356). Aggression was greater in control sections during pre-heating phases (w2 ¼ 8:28, df ¼ 1, P ¼ 0:004), as well as during post-heating phases compared to treatment sections (w2 ¼ 12:34, df ¼ 1, Po0.001). Aggression did not differ between control and treatment sections during heating phases (w2 ¼ 0:48, df ¼ 1, P ¼ 0:487) (Fig. 3c). Mean fleeing per minute followed the same pattern as the aggression results (Table 2) (Fig. 3d). Statistical analyses were not possible in side-channel trials because the models did not converge (one factor in

ARTICLE IN PRESS J.T. Quigley, S.G. Hinch / Journal of Thermal Biology 31 (2006) 429–441

the model had a variance of zero). In the treatment sections, mean aggression and fleeing per minute declined to zero during the heating and post-heating phases. In contrast, mean aggression and fleeing per minute increased during heating and post-heating phases in control sections. 4.3.5. Fishmin and total fish In tributary trials we found no differences in mean fishmin or total fish observed (Table 2). In side-channel trials, fishmin did not differ among any of the phases (Bonferroni, P ¼ 1:00, for all contrasts) in control sections. In treatment sections, fishmin did not differ between preheating and heating phases (Bonferroni, P ¼ 0:052), or heating and post-heating phases (Bonferroni, P ¼ 1:00). Fishmin was greater during pre-heating compared to postheating phases (Bonferroni, P ¼ 0:021) (Fig. 3e) (Table 2). There were no differences in total fish observed in sidechannel trials (Table 2). 5. Discussion The most relevant contrasts within our experiments are those between the pre-heating and post-heating phases. The rationale for this are twofold. First, it is well established that the cortisol stress response can take up to 30 min or longer to be expressed (Donaldson et al., 1984) and it can take even longer still for behaviours to respond to changing cortisol levels, so fish may be at different levels of response during portions of the 1.5 h heating phase. It is reasonable to assume that by the start of the post-heating phase, cortisol and related behavioural changes will be fully expressed. Second, there is a possibility that the act of heating could have caused many small organisms to perish thereby altering the nature of dissolved organic matter. Thus, some behavioural and stress responses during the heating phases could have been due to olfactory detection of the altered water chemistry. Interestingly, we did observe some changes in control responses during the heating phase of experiments (i.e. feeding, aggression, fleeing in the tributaries). However, these changes were short-term in nature as they disappeared after the heaters were shut-off—controls did not differ between pre-heating and post-heating phases with any variable. Our replicated experiment is the first study to manipulate temperatures of natural streams to assess acute physiological and behavioural effects on juvenile salmonids. We found that juvenile chinook rearing in groundwater fed tributaries were generally unaffected behaviourally by the rapid temperature increases of
1–2 1C that we imposed; however, feeding attempts almost doubled. Metabolic demand and ability for activities (such as feeding) increase nearly exponentially with increasing temperature (Brett, 1995). Juvenile chinook may have facultatively adjusted foraging rates in an attempt to meet heightened metabolic demands from elevated temperatures (i.e. Nislow et al., 1998). It is also possible that benthic prey may have become more active in response to warmer water making

437

them more visible to fish predators. Other measures of activity such as aggression or fleeing did not change suggesting that the temperature increase did not immediately affect competitive or predatory interactions. Surprisingly, we found that temperature increase caused fish in the tributary trials to be physiologically stressed. The enclosure nets also appeared to elicit a stress response, however, cortisol levels declined over time in the nets indicating that physiological recovery was occurring, in contrast to our observations in the treatment sections where it did not occur. The reasons for the stress response are not clear. The fact that the magnitude of increase was small (o2 1C) and final temperatures spanned the preferred thermal range of this species (
12–14 1C) had led us to expect that fish would have readily acclimated. It is possible that the preferred thermal range for this northern population is cooler than that reported in the literature which is largely based on more southernly populations (i.e. in Brett, 1952). Though not examined with juvenile fish, laboratory swim performance assessments of adult salmonids have revealed population-specific thermal optimal ranges (i.e. temperatures where metabolic costs are minimized) which are closely linked to the adults natal water temperatures (Lee et al., 2003). Within-species, optimal temperatures varied among adult populations by at least 3 1C (Lee et al., 2003). Thus, our modest temperature increase may have significantly eclipsed the actual preferred thermal range accounting for the stress response that we found. Juvenile chinook rearing in the side-channel were more behaviourally affected by the rapid temperature increase than were fish in tributaries. This was probably due to the fact that the temperature increase was greater (
2–4 1C) than that imposed on tributary fish, but most importantly, initial ambient temperatures were much higher (
19–24 1C). We found that feeding rate increased over 56 times, and as with tributary fish, this may have been a response to increased metabolic demands. Fish also displayed behaviours indicative of stress and avoidance. Movements were very rapid in the treatment sections as evidenced by the short amount of time (e.g. fishmin) that fish spent in the view of our video cameras—erratic swimming is a behaviour commonly observed in laboratory studies examining upper lethal thermal limits in freshwater fish (Beitinger et al., 2000). Fish appeared to be searching for cooler water. Movement was initially downstream and then upstream, many fish eventually locating a small area in our upstream treatment enclosure where temperatures were about 3 1C cooler. In control sections, the tendency was for fish to move just in the downstream direction during a trial. Although not quantified, in the treatment sections of side-channel trials many fish oriented towards the surface at an angle of about 301 and moved in large aggregations (10–20 fish). Laboratory experiments have shown that thermally shocked salmonids will exhibit such abnormal posture (Coutant, 1973). Field observations of juvenile Atlantic salmon have revealed that at temperatures

ARTICLE IN PRESS 438

J.T. Quigley, S.G. Hinch / Journal of Thermal Biology 31 (2006) 429–441

above 22 1C, they abandon territories and form aggregations (Gibson and Cunjak, 1986). Aggregative behaviour is a mechanism that may facilitate survival (Brett, 1970). Energy not used for defending territories can be used to pay for higher metabolic costs of activity and used to help with predator defence. Clearly predator defence is a concern because during the heating phase of side-channel trials, aggregations were always in association with some form of structure such as large wood. In control sections, neither aggregations nor association with large wood were evident. The cessation of territorial behaviour in sidechannel trials suggests that increased movements is an avoidance response, and does not reflect the displacement of fish arising from unsuccessful social interactions (Chapman, 1962). If the increase in movement during sidechannel heating trials was a result of increased social interactions and subsequent displacement through competitive exclusion, the rate of aggression would be expected to increase, which it did not. Side-channels are a very stressful environment for juvenile chinook to rear in during summer. Fish captured upstream from the enclosure nets prior to the start of experimental heating had cortisol levels five times greater than typical basal levels reported for juvenile salmonids (Sumpter et al., 1986; Fagerlund et al., 1995) and over four times the level in the control sections of tributary trials. This was probably a result of the relatively high ambient temperatures. The netted fish exhibited even higher plasma cortisol levels, elevated approximately six times that of the un-netted phase, undoubtedly due to the combined stress of high ambient temperatures and net-enclosure. Cortisol levels did not increase as a result of rapid heating, but rather showed a trend to levels below control values. Such a lack of response to a known acute stressor can indicate chronic stress (Hontela et al., 1992). A chronically stressed fish that is unable to further raise its cortisol levels when subjected to an additional acute stressor exhibits an ‘impaired stress response’. Cortisol production may decline to or below baseline levels under conditions of chronic stress resulting from impairment of the hypothalamic– pituitary–interrenal (HIP) axis (Hontela et al., 1997). This has been observed for chronic (e.g. 3–4 week) exposure to water pollutants (e.g. Nolan et al., 2003). Thus, our treatment cortisol responses suggest that side-channel fish were already experiencing significantly high levels of physiological stress before the treatment and that the treatment was additionally stressful. Indeed, some mortality, in the form of floating fish carcasses, was evident in the treatment section of the first side-channel trial during heating when the ambient temperature (
24 1C) was elevated approximately 4 1C. We estimate that at least 10% of the population in the treatment perished (Quigley, 2003) as temperatures approached the upper thermal limit for the species (Beitinger et al., 2000). No mortality was evident in the control section or in the other trial. Rapid, modest water temperature increases like we simulated are known to be caused by different anthro-

pogenic activities (e.g. thermal discharges from industrial cooling water, reservoir outlets, river level fluctuations from operations at hydroelectric dams, streamside logging). Often these activities result in persistently higher water temperatures, or they may cause temperatures to rapidly fluctuate higher and lower than ambient. Though our experiments were only designed to test acute effects of warming, our results suggest that chronically elevated temperatures of the magnitude in our study would be extremely detrimental for the side-channel fish, even if the temperatures were not acutely lethal (e.g. temperature increases were o27 1C). There are several lines of evidence to support this. First, under current ambient temperatures, side-channel fish are suffering from relatively high levels of physiological stress and have relatively lower foraging rates (in comparison to tributary fish). This habitat type is clearly sub-optimal and these baseline observations may help to explain why side-channel fish are generally smaller, and occur in lower abundance than tributary rearing fish (Quigley, 2003). Larger juvenile salmonids have a greater likelihood of surviving the winter (Tschaplinski et al., 2004). Though our temperature increases led to increased foraging rates, side-channel juveniles would likely lose weight when temperature is further elevated because of decreased food conversion efficiency (Reid et al., 1995) and because physiological stress is energetically costly. For instance, acute stress which resulted in a doubling of cortisol levels in juvenile steelhead, comparable to the magnitude of effect in our study, reduced their energy reserves by approximately 25% (Barton and Schreck, 1987). Reductions in growth, appetite, condition, and food conversion efficiency have been reported in rainbow trout after cortisol levels were chronically elevated by 200% (Gregory and Wood, 1999), a level commensurate with that exhibited by chinook in our study subjected to a mean temperature increase of about 1 1C in our side-channels. Second, chronic elevations of cortisol are known to reduce disease resistance, fecundity and tolerance to additional non-thermal stressors (Thomas, 1990; Fagerlund et al., 1995; Feist and Schreck, 2002). Chronic elevation in cortisol to levels similar to our acute levels have been found to reduce white blood cell numbers and impair osmoregulatory function and swimming performance in juvenile chinook (Maule et al., 1988), and cause a decline in condition factor in brown trout (Pickering and Duston, 1983). A malfunctioning HIP axis can itself impair osmoregulation, decrease disease resistance and limit growth. Third, high stress levels can impair the ability of juvenile salmonids to avoid predators (Sylvester, 1972; Olla et al., 1992; Olla and Davis, 1989) and it is well established that predators capture substandard prey disproportionately from prey populations (Mesa et al., 1994; Temple, 1987). For instance, increases in cortisol levels of approximately 300–500% elevated vulnerability to predation in juvenile coho salmon (Olla et al., 1992, 1995). Whitefish fry exposed to heat shock had reduced levels of predator avoidance behaviours (Yocom and Edsall, 1974).

ARTICLE IN PRESS J.T. Quigley, S.G. Hinch / Journal of Thermal Biology 31 (2006) 429–441

It is not clear what the chronic effects would be of our rapid, modest temperature changes to tributary rearing juveniles. We did not anticipate that fish would be acutely stressed by our temperature increases, however, if stress levels were to continually be elevated, then this may contribute to lower growth and survival, as we discussed above for chronic effects to side-channel fish. However, we found no behavioural evidence that fish were stressed and noted that foraging rates were elevated. Field research on juvenile coho salmon has shown that when cool temperatures (e.g. below preferred ranges) were elevated for several weeks into their preferred range, summer growth rates increased (presumably due to higher foraging rates) leading to larger fish and higher rates of over-winter survival (Tschaplinski et al., 2004). The fact that fish were physiologically stressed, yet showed no evidence of dispersal supports previous suggestions that groundwater fed tributaries are preferred rearing habitats for the streamtype race of chinook salmon (Quigley, 2003; Bradford et al., 2001; Scrivener et al., 1994). Juvenile salmonids will endure sub-lethally stressful environments for short periods if habitat quality is otherwise very good (Birtwell et al., 1999). Aspects of our experimental design created some limitations to interpretation which need consideration. First, the temperature increases in tributaries were smaller (1–2 1C) than those in side-channels (2–4 1C) because of constraints with our heating equipment and capability to warm cold tributaries. Had we been able to warm the tributaries to higher levels, we could have better assessed how juveniles were affected by temperatures that clearly were warmer than their laboratory-assessed preferred range. Second, needed are longer-term observations (i.e. beyond 1 h after heating) on stress levels, or alternative chronic measures of stress (i.e. interrenal nuclear diameters), in order to better evaluate the duration of stress responses. Third, to assess the generality of our findings, experiments such as ours need to be conducted on other populations of juvenile chinook because thermal preferences and upper limits may differ with population. Juvenile chinook have been described as the most tolerant of the Pacific salmon species to elevated temperatures (Brett, 1952), so our results may reflect conservative responses in terms of what we may find with other salmonid species.

Acknowledgements An earlier version of this manuscript was greatly improved by comments from Drs. Max Blouw, Michael Healey, and Steve Macdonald. Field assistance was provided by Vesna Kontic, Paul Welch, and Laura Genn. Jason Bourgeois and Dr. Mark Shrimpton provided technical support. Lana Klassen assisted with data extraction of underwater video recordings. Thanks to the staff at CANFOR (Prince George) for their support of this research. Financial support was provided from Forest

439

Renewal British Columbia and the Natural Sciences and Engineering Research Council of Canada. References Adams, S.M., 1990. Biological indicators of stress in fish. Am. Fish. Soc. Symp. 8. Anderson, D.P., 1990. Immunological indicators: effects of environmental stress on immune protection and disease outbreaks. Am. Fish. Soc. Symp. 8, 38–50. Barton, B.A., Schreck, C.B., 1987. Metabolic cost of acute physical stress in juvenile steelhead. Trans. Am. Fish. Soc. 116, 257–263. Beitinger, T., Bennet, W., McCauley, R., 2000. Temperature tolerances of North American freshwater fishes exposed to dynamic changes in temperature. Environ. Biol. Fish. 58, 237–275. Birtwell, I.K., Korstrom, J.S., Fink, R.P., Tanaka, J.A., Tiessen, D.I., Fink, B.J., 1999. The effects of thermal change on juvenile chum salmon behavior, distribution and feeding: laboratory and field studies. In: Hawkins, S., Kondzela, C., Wilmot, R., Guthrie, C., Pohl, J., Nguyen, H. (Eds.), Proceeding of the 19th Northeast Pacific Pink and Chum Salmon Workshop, March 3–5, 1999. Juneau, Alaska, pp. 87–92. Bisson, P.A., Davis, G.E., 1976. Production of juvenile chinook salmon, (Oncorhynchus tshawytscha), in a heated stream. NOAA Fish. Bull. 74, 763–774. Bjornn, T.C., Reiser, W.D., 1991. Habitat requirements of salmonids in streams. In: Meehan, W.R. (Ed.), Influences of Forest and Rangeland Management on Salmonid Fishes and their Habitat. American Fisheries Society Publication 19, Bethesda, Maryland, pp. 83–138. Bradford, M.J., Grout, J.A., Moodie, S., 2001. Ecology of juvenile chinook salmon in a small non-natal stream of the Yukon River drainage and the role of ice conditions on their distribution and survival. Can. J. Zool. 79, 2043–2054. Brett, J.R., 1952. Temperature tolerance in young Pacific salmon, genus Oncorhynchus. J. Fish. Res. Board Can. 9, 265–323. Brett, J.R., 1970. Temperature—fishes, In: Kinne, O. (Ed.), Marine Ecology, vol. 1. Environmental Factors, Part 1. Wiley-Interscience, London, pp. 513–560. Brett, J.R., 1971. Energetic responses of salmon to temperature. A study of some thermal relations in the physiology and freshwater ecology of sockeye salmon (Oncorhynchus nerka). Am. Zool. 11, 99–113. Brett, J.R., 1995. Energetics. In: Groot, C., Margolis, L., Clarke, W.C. (Eds.), Physiological Ecology of Pacific Salmon. UBC Press, Vancouver, pp. 1–68. Chapman, D.W., 1962. Aggressive behaviour in juvenile coho salmon as a cause of emigration. J. Fish. Res. Board Can. 19, 1047–1080. Coutant, C.C., 1973. Effect of thermal shock on vulnerability of juvenile salmonids to predation. J. Fish. Res. Board Can. 30, 965–973. Donaldson, E.M., Fagerlund, U.M., McBride, J.R., 1984. Aspects of the endocrine stress response to pollutants in salmonids. In: Cairns, V.W., Hodson, P.V., Nriagu, J.O. (Eds.), Contaminant Effects on Fisheries. Wiley, New York, NY, pp. 213–221. Fagerlund, U.H.M., McBride, J.R., Williams, I.V., 1995. Stress and tolerance. In: Groot, C., Margolis, L., Clarke, W.C. (Eds.), Physiological Ecology of Pacific Salmon. UBC Press, Vancouver, pp. 461–503. Feist, G., Schreck, C.B., 2002. Ontogeny of the stress response in chinook salmon, Oncorhynchus tshawytscha. Fish Physiol. Biochem. 25, 31–40. Feist, G., Schreck, C.B., Fitzpatrick, M.S., Redding, J.M., 1990. Sex steroid profiles of coho salmon (Oncorhynchus kisutch) during early development and sexual differentiation. Gen. Comp. Endocrinol. 80, 299–313. Gibson, J.R., Cunjak, R.A., 1986. An investigation of competitive interactions between brown trout (Salmo trutta L.) and juvenile Atlantic salmon (Salmo salar L.) in rivers of the Avalon Peninsula, Newfoundland. Canadian Technical Report of Fisheries and Aquatic Sciences No. 1462, p. 82.

ARTICLE IN PRESS 440

J.T. Quigley, S.G. Hinch / Journal of Thermal Biology 31 (2006) 429–441

Glova, G.J., Mason, J.C., 1977. Interactions for food and space between sympatric populations of juvenile coho salmon and coastal cutthroat trout in a stream simulator during winter and spring. Fisheries and Marine Service Manuscript Report No. 1429, 31pp. Gray, R.H., 1990. Fish behaviour and environmental assessment. Environ. Toxicol. Chem. 9, 53–67. Gregory, T.R., Wood, C.M., 1999. The effects of chronic plasma cortisol elevation on the feeding behaviour, growth, competitive ability and swimming performance of juvenile rainbow trout. Physiol. Biochem. Zool. 72, 286–295. Hartman, G.F., 1965. The role of behaviour in the ecology and interaction of underyearling coho salmon (Oncorhynchus kisutch) and steelhead trout (Salmo gairdneri). J. Fish. Res. Board Can. 22, 1035–1081. Healey, M.C., 1991. Life history of chinook salmon. In: Groot, C., Margolis, L. (Eds.), Pacific Salmon Life Histories. UBC Press, Vancouver, pp. 311–393. Hontela, A., Rasmussen, J.B., Audet, C., Chevalier, G., 1992. Impaired cortisol stress response in fish from environments polluted by PAHs, PCBs, and mercury. Arch. Environ. Contam. Toxicol. 22, 278–283. Hontela, A., Daniel, C., Rasmussen, J.B., 1997. Structural and functional impairment of the hypothalamo–pituitary–interrenal axis in fish exposed to bleached kraft mill effluent in the St. Maurice River. Quebec. Ecotoxicol. 6, 1–12. Iger, Y., Balm, P.H., Jenner, H.A., Wendelaar Bonga, S.E., 1995. Cortisol induces stress-related changes in the skin of rainbow trout (Oncorhynchus mykiss). Gen. Comp. Endocrinol. 97 (2), 188–198. Lee, C.G., Farrell, A.P., Lotto, A.G., MacNutt, M.J., Hinch, S.G., Healey, M.C., 2003. Effects of temperature on swimming performance and oxygen consumption in adult sockeye (Oncorhynchus nerka) and coho (O. kisutch) salmon stocks. J. Exp. Biol. 206, 3239–3251. Levy, D.A., 1992. Potential impacts of global warming on salmon production in the Fraser watershed. Canadian Technical Report of Fisheries and Aquatic Sciences No. 1889, 96pp. Linton, T.K., Reid, S.D., Wood, C.M., 1999. Effects of restricted ration on the growth and energetics of juvenile rainbow trout exposed to a summer of simulated warming and sublethal ammonia. Trans. Am. Fish. Soc. 128, 758–763. Mac Donald, L.B., Leone, F.N., Rowland, D.E., 1996. Salmon Watershed Planning Profiles for the Fraser River Basin within the Prince George Land and Resource Management Plan. Prepared for Department of Fisheries and Oceans Fraser River Action Plan, p. 153. Maule, A.G., Schreck, C.B., Bradford, C.S., Barton, B.B., 1988. Physiological effects of collecting and transporting emigrating juvenile chinook salmon past dams on the Columbia River. Trans. Am. Fish. Soc. 117, 245–261. Mesa, M.G., Poe, T.P., Gadomski, D.M., Petersen, J.H., 1994. Are all prey created equal? A review and synthesis of differential predation on prey in substandard condition. J. Fish Biol. 45 (Suppl. A), 81–96. Mesa, M.G., Weiland, L.K., Wagner, P., 2002. Effects of acute thermal stress on the survival, predator avoidance, and physiology of juvenile fall chinook salmon. Northwest Sci. 76 (2), 118–128. Nislow, K.H., Folt, C., Seandel, M., 1998. Food and foraging behavior in relation to microhabitat use and survival of age-0 Atlantic salmon. Can. J. Fish. Aquat. Sci. 55, 116–127. Nolan, D.T., Spanings, F.A.T., Ruane, N.M., Hadderingh, R.H., Jenner, H.A., Wendelaar Bonga, S.E., 2003. Exposure to water from the lower Rhine induces a stress response in the rainbow trout Oncorhynchus mykiss. Arch. Environ. Contam. Toxicol. 45, 247–257. Olla, B.L., Davis, M.W., 1989. The role of learning and stress in predator avoidance of hatchery-reared coho salmon (Oncorhynchus kisutch) juveniles. Aquaculture 76, 209–214. Olla, B.L., Davis, M.W., Schreck, C.B., 1992. Comparison of predator avoidance capabilities with corticosteroid levels induced by stress in juvenile coho salmon. Trans. Am. Fish. Soc. 121, 544–547. Olla, B.L., Davis, M.W., Schreck, C.B., 1995. Stress-induced impairment of predator evasion and non-predator mortality in Pacific salmon. Aquaculture Res. 26, 393–398.

Pickering, A.D., Duston, J., 1983. Administration of cortisol to brown trout, Salmo trutta L., and its effects on the susceptibility to Saproleginia infection and furunculosis. J. Fish. Biol. 23, 163–175. Pottinger, T.G., Mosuwe, E., 1994. The corticosteroidogenic response of brown and rainbout trout alevins and fry to environmental stress during a ‘‘Critical Period’’. Gen. Comp. Endocrinol. 95, 350–362. Quigley, J.T., 2003. Experimental field manipulations to stream temperatures and suspended sediment concentrations to quantify the behavioural and physiological effects on juvenile chinook salmon. M.Sc. Thesis, UBC, p. 147. Reid, S.D., Dockray, J.J., Linton, T.K., McDonald, D.G., Wood, C.M., 1995. Effects of a summer temperature regime representative of a global warming scenario on growth and protein synthesis in hardwater and softwater-acclimated juvenile rainbow trout (Oncorhynchus mykiss). J. Therm. Biol. 20, 231–244. Resources Inventory Committee (RIC), 1997. Freshwater Biological Sampling Manual. Government of BC. /http://www.for.gov.bc. ca/ric/Pubs/Aquatic/freshwaterbio/index.htmS. Rosberg, G.E., Aitken, D., 1981. Adult chinook salmon studies in four tributaries to the upper Fraser River. DSS Contract no: 05SB.FP5010-SP124, p. 140. Rosberg, G.E., Aitken, D., Oguss, E., 1981. Juvenile chinook salmon studies in four tributaries to the upper Fraser River, 1981. Prepared by Beak Consultants Ltd. for Department of Fisheries and Oceans, 401 Burrard Street, Vancouver, BC. DSS Contract no: 05SB.FP501-0SP124, p. 158. Schuett-Hames, D., Pleus, A., Bullchild, L., Hall, S., 1994. Ambient Monitoring Program Manual Timber-Fish-Wildlife. TFW-AM9-94001. Northwest Indian Fisheries Commission. Olympia, Washington, USA, 128pp. Scrivener, J.C., Brown, T.G., Andersen, B.C., 1994. Juvenile chinook salmon (Oncorhynchus tshawytscha) utilisation of Hawks Creek, a small and non-natal tributary of the upper Fraser River. Can. J. Fish. Aquat. Sci. 51, 1139–1146. Sumpter, J.P., Dye, H.M., Benfey, T.J., 1986. The effects of stress on plasma ACTH, -MSH, and cortisol levels in salmonid fishes. Gen. Comp. Endocrinol. 62, 377–385. Sylvester, J.R., 1972. Effect of thermal stress on predator avoidance in sockeye salmon. J. Fish. Res. Board Can. 29, 601–603. Temple, S.A., 1987. Do predators always capture substandard individuals disproportionately from prey populations? Ecology 68 (3), 669–674. Thomas, P., 1990. Molecular and biochemical responses of fish to stressors and their potential use in environmental monitoring. Am. Fish. Soc. Symp. 8, 9–28. Thomas, R.E., Gharrett, J.A., Carls, M.G., Rice, S.D., Moles, A., Korn, S., 1986. Effects of fluctuating temperature on mortality, stress, and energy reserves of juvenile coho salmon. Trans. Am. Fish. Soc. 115, 52–59. Tschaplinski, P.J., Hogen, D.L., Hartman, G.F., 2004. Fish-forestry interaction research in coastal British Columbia—the Carnation Creek and Queen Charlotte Islands studies. In: Northcote, T.G., Hartman, G.F. (Eds.), Fishes and Forestry: Worldwide Watershed Interactions and Management. Blackwell Publishing, pp. 389–412. Waldichuk, M., 1993. Fish habitat and the impact of human activity with particular reference to Pacific salmon. In: Parsons, L.S., Lear, W.H. (Eds.), Perspectives on Canadian Marine Fisheries Management. Canadian Bulletin Fisheries and Aquatic Science, vol. 226, pp. 295–337. Wedemeyer, G., 1973. Some physiological aspects of sublethal heat stress in the juvenile steelhead trout (Salmo gairdneri) and coho salmon (Oncorynchus kisutch). J. Fish. Res. Board Can. 30, 831–834. Yocom, T.G., Edsall, T.A., 1974. Effect of acclimation temperature and heat shock on vulnerability of fry of lake whitefish (Coregonus clupeaformis) to predation. J. Fish. Res. Board Can. 31, 1503–1506.

ARTICLE IN PRESS J.T. Quigley, S.G. Hinch / Journal of Thermal Biology 31 (2006) 429–441

Further reading Brown, R.S., 1999. Fall and early winter movements of cutthroat trout, Oncorhynchus clarki, in relation to water temperature and ice conditions in Dutch Creek, Alberta. Environ. Biol. Fish. 55, 359–368. Brown, R.S., MacKay, W.C., 1995. Fall and winter movements of and habitat use by cutthroat trout in the Ram River, Alberta. Trans. Am. Fish. Soc. 124, 873–885. Brown, T.G., McMahon, T., 1988. Winter ecology of juvenile coho salmon in Carnation Creek: summary of findings and management implications, pp. 108–117. In: Chamberlin, T.W. (Ed.), Proceedings of the Workshop: Applying 15 years of Carnation Creek Results. Pacific Biological Station, Nanaimo, British Columbia, 239pp. Hartman, G.F., Scrivener, J.C., 1990. Impacts of forestry practices on a coastal stream ecosystem Carnation Creek, British Columbia. Can. Bull. Fish. Aquat. Sci. 223, 148pp. Hearn, W.E., 1987. Interspecific competition and habitat segregation among stream-dwelling trout and salmon: a review. Fisheries 12 (5), 24–31. Huntingford, F.A., 1976. The relationship between inter- and intraspecific aggression. Anim. Behav. 24, 485–497.

441

Kaeding, L.R., 1996. Summer use of coolwater tributaries of a geothermally heated stream by rainbow and brown trout, Oncorhynchus mykiss and Salmo trutta. Am. Midland Natl. 135, 283–292. Keenleyside, M.H.A., Hoar, W.S., 1954. Effects of temperature on the response of young salmon to water currents. Behavior 7, 77–87. Lee, R.M., Rinne, J.N., 1980. Critical thermal maxima of five trout species in the southwestern United States. Trans. Am. Fish. Soc. 109, 632–635. Meehan, W.R. (Ed.), 1991. Influences of Forest and Rangeland Management on Salmonid Fishes and Their Habitats. American Fisheries Society Special Publication 19. Reiser, D.W., Bjornn, T.C., 1979. Habitat requirements of anadromous salmonids. In: Meehan, W.R. (Ed.), Influence of Forest and Rangeland Management on Anadromous Fish Habitat in the Western United States and Canada. U.S. Forest Service, General Technical Report PNW-96. Portland, Oregon, pp. 1–54. Rood, K.M., Hamilton, R.E., 1995. Hydrology and water use for salmon streams in the Upper Fraser Habitat Management Area, British Columbia, Canadian Manuscript Report Fisheries Aquatic Sciences No. 2294, 170pp. Welsh Jr., H.H., Hodgson, G.R., Harvey, B., Roche, M.F., 2001. Distribution of juvenile coho salmon in relation to water temperatures in tributaries of the Mattole River, California. North Am. J. Fish. Manage. 21, 464–470.