Juvenile and adult hardhead Mylopharodonconocephalus oxygen consumption rates: effectsof temperature and swimming velocity

Nann A. Fangue & Dennis E. Cocherell & Felipe La Luz &

Joseph J. Cech Jr. & Lisa C. Thompson

Received: 30 October 2013 /Accepted: 18 June 2014# Springer Science+Business Media Dordrecht 2014

Abstract California’s populations of hardheadMylopharodon conocephalus, a species of special con-cern, have declined, possibly due to dam constructionwith consequent temperature and water-velocity chang-es, and the introduction of non-native species.Environmental temperature effects on this large (to60 cm SL) cyprinid, and its swimming abilities, arenot well known. To address these deficiencies and toassist conservation efforts, we measured resting andswimming metabolic rates of adult and juvenile hard-head acclimated to four temperatures (11, 16, 21, or25 °C). Resting metabolic rates (RMR, mg O2

kg−0.79 h−1) generally increased with acclimation tem-perature, in adults and juveniles, with low to moderatethermal sensitivity (Q10 range: 1.33–2.04). Swimmingmetabolic rates, in Brett-style respirometers, of adultsranged from 209 to 1342 mg O2 kg

−1 h−1 at velocitiesfrom 30 to 90 cm s−1, and juveniles ranged from 393 to769 mg O2 kg

−1 h−1 from 10 to 50 cm s−1. Adults werelethargic at 11 °C and juveniles frequently refused toswim at 11 and 16 °C, but all fish swam well at 21 and25 °C. These results suggest that hardhead are well-

suited for sustained aerobic activity over a range of flowvelocities, at moderate temperatures (ca. 16 to 21 °C).However, juveniles, emerging in spring, may not be ableto perform in cold water and/or high flow velocities,providing a caution to dam managers and regulators toavoid spring and summer operations whereby juvenilesexperience conditions outside of those occurring in un-regulated rivers.

Keywords Hardheadminnow. Pulsed flows .

Mylopharodon conocephalus . Temperature . Sustainedand restingmetabolic rates

Introduction

Hardhead, Mylopharodon conocephalus, are large (to60 cm SL) cyprinids that inhabit medium to largeCalifornia streams to ca. 1,500 m elevation (Moyle2002). These fish prefer clear runs and deep (>80 cm)pools, where maximum temperatures reach 20–28 °C(Knight 1985; Baltz et al. 1987). Hydroelectric damsand the timing and magnitude of water releases from theresulting reservoirs, especially for electrical power gen-eration and recreation-related flows, have modifiedmany of the natural, seasonal, thermal and hydrologicalregimes of hardhead habitat (Young et al. 2011). Thesealterations in combination with the introduction of non-native species (centrarchid basses in particular) haveresulted in fragmented distributions, population declinesand some local extirpations of native hardhead (Moyleet al. 1995; Moyle 2002). The hardhead is currently

Environ Biol FishDOI 10.1007/s10641-014-0292-1

N. A. Fangue (*) :D. E. Cocherell : F. La Luz :J. J. Cech Jr. : L. C. ThompsonDepartment of Wildlife, Fish, and Conservation Biology,University of California Davis,One Shields Avenue, Davis, CA 95616, USAe-mail: nafangue@ucdavis.edu

L. C. ThompsonCenter for Aquatic Biology and Aquaculture, University ofCalifornia Davis,One Shields Avenue, Davis, CA 95616, USA

listed as a species of special concern by the CaliforniaDepartment of Fish and Wildlife and the US ForestService.

Typical hydroelectric dam operations involve once ortwice daily peak water flows that coincide with peakelectricity demand periods (Cushman 1985; Houck et al.1995). Dam operations may result in sediment scouring,reduced primary productivity, changes in turbidity andoxygen levels, as well as changes in water temperatureand velocity that likely affect the bioenergetics andswimming performances of the resident fishes, includ-ing hardhead (Cech et al. 1990; Facey and Grossman1990). Whereas extreme temperatures probably drivefish away from affected areas (Myrick and Cech2005), more subtle temperature increases may increasemetabolic demands and foraging requirements of affect-ed fishes (Cech et al. 1990). Similarly, whereas extreme-ly high water velocities or velocity pulses may displacesome fishes downstream (Erman et al. 1988; Jeffrieset al. 2006; Chun et al. 2011), less extreme velocityincreases can either increase metabolic demands(Davison 1997) or force behavioral changes if hydrauliccover is available. For example, Cocherell et al. (2011)showed that adult rainbow trout (Oncorhynchusmykiss), equipped with tail-beat-frequency transmitters,apparently sought such cover (e.g., behind boulders) in aCalifornia stream during a flow pulse. Such responsesmay decrease swimming-associated metabolic costs(Rosenfeld and Boss 2001), although foraging time,which is of prime importance for stream fishes (Hilland Grossman 1993), may also decrease. Because thegrowth rates of juvenile fishes and the reproductive ratesof adults are driven, positively, by adequate nutrition(Wurtsbaugh and Davis 1977; Cech et al. 1992), tem-perature and velocity increases may decrease a streamfish’s survival rate.

Ectothermic fishes’ metabolic demands are highlyinfluenced by temperature and exercise (Fry 1947;Brett 1964; Ultsch et al. 1978; Schurmann andSteffensen 1997; Claireaux and Lagardère 1999).Oxygen consumption (MO2) rates measure the oxida-tive metabolic demands of fishes (see reviews by Fry1971; Brett 1971), and resting (maintenance) metabolicrates (RMR) typically increase ca. two to three-fold witha 10 °C temperature increase (Schmidt-Nielsen 1990).Increases in swimming activity also usually increasemetabolic rates (swimming metabolic rate, SwMR, de-fined as the oxygen requirements associated with exer-cise), due to the increased aerobic energy demands of

exercising red muscle, especially as hydrodynamic dragand associated muscular power output requirementsincrease at higher swimming velocities (Rome et al.1993; Webb 1994). Therefore, increases in stream tem-peratures and velocities could dramatically increaseRMR and SwMR and thus the foraging requirementsof the affected fishes (Cech et al. 1994). Insights fromthese metabolic measures should assist environmentalresource managers towards setting water temperaturesand velocities (e.g., via water releases from reservoirs)to assist efforts to conserve hardhead populations inCalifornia streams.

To increase hardhead-related biological informationand to assist hardhead and stream-ecosystem conserva-tion efforts, particularly those related to temperature andwater velocity modification through hydroelectric dammanagement, we measured resting and swimming met-abolic rates of juvenile and adult hardhead acclimated tofour environmentally relevant temperatures (11, 16, 21,or 25 °C). Based on previous studies on hardhead swim-ming (Myrick and Cech 2000), metabolic responses tohypoxia and acute temperature changes (Cech et al.1990), blood-oxygen equilibria (Kaufman et al. 2013),and temperature preferences (Cocherell et al. 2013), weexpected that hardhead would perform best at 16–21 °C.

Methods

Fish collections and transport

We captured adult fish, via angling, using earthwormsnear the bottom, from the South Fork American Riverand North Fork Feather River in March throughNovember 2010 (water temperature range: 8.0 to19.5 °C). The South Fork American River has two pop-ulations of hardhead in the Chili Bar and Slab Creekreservoirs. The North Fork Feather River has a series ofreservoirs associated with hydro-power plants aboveOroville Dam which support relatively large populationsof hardhead. We sampled Cresta Reservoir at the dam,upstream in Poe Reservoir, and Rock Creek Reservoirupstream of Rock Creek Dam and at Chipps Creek.

After capture, fish were held in transport ice-chests(140-l) of river water with up to six fish per ice-chest.Temperature and dissolved oxygen levels were moni-tored and maintained at river levels throughout thefishing day by adding fresh river water, including justprior to the ca. 2 to 4-h vehicle transport to the Center for

Environ Biol Fish

Aquatic Biology and Aquaculture (CABA) at theUniversity of California, Davis. Novaqua Plus™ wasadded as a prophylactic treatment to reduce transportstress and protect the fish’s slime coat from netting andhandling, and ice chests were aerated during transport.Upon arrival at CABA, fish were transferred to aerated555-l tanks held within ±1.5 °C of the capture location,with continuous flows of air-equilibrated well water,until experimental acclimations.

Juvenile fish were caught using cylindrical minnowtraps, with two 2.5 to 3-cm diameter openings, placednear shore in riparian debris (fallen trees and submergedvegetation), less than a meter deep, on the lower FeatherRiver (December 2010, Gridley, CA; water temperature:11.5 °C). Captured juveniles were loaded into 3-mm-thick polyethylene bags (ca. 50 fish per bag) containingca. 9 l river water and ca. 2 ml NovAqua Plus™. Theremaining head space in the bag was filled with oxygenand sealed for the ca. 2-3-h trip to CABA. At CABA,fish were placed into 140-l circular tanks, at maximumdensities of 80 fish/tank, supplied with chilled flow-through well water at 11.2 °C.

Fish maintenance and laboratory acclimation

Adult fish were fed a mix of different sized SilverCup®fish pellets at 4.8 g feed per fish per day, supplementedwith rinsed and halved live earthworms. In general, ittook adults several weeks to transition to commercialfeed. Earthworms were re-offered in tanks where fishwere not eating the pellet diet, and this was repeated asnecessary through the acclimations and experimentaltreatments.

Juvenile fish were fed Rangen, Inc. trout starter diet(<0.6 mm) mixed with >0.6 mm Silvercup™ feed. Thiswas supplemented with frozen larval and adult brineshrimp (San Francisco Bay Brand® Sally‘s FrozenBaby Brine Shrimp™) throughout the study. Juvenileswere fed an excess ration where a minimal amount ofuneaten food was present each morning from the previ-ous day’s feeding. Commercial diets were loaded into anautomatic feeder for the daytime feedings.

Adults were kept at CABA in aerated, 555-l tanksand juveniles were kept in 140-l circular tanks held atone of four acclimation temperatures (11, 16, 21, or25 °C±0.5 °C), with continuous flows of well water(conductivity 670–700 μS cm−1, dissolved oxygen>95 % saturation, and pH 8.1), at densities up to 25fish/tank, prior to experiments. Both Feather (n=52) and

American River (n=29) adult fish were mixed togetherin a single tank for each acclimation group, throughrandom draw when separating fish into acclimationtanks. Tank temperatures were adjusted at 1 °C d−1,and fish were kept a minimum of 30 days at theiracclimation temperature before an experiment. In orderto minimize the number of hardhead removed fromwildpopulations, individual hardhead of each life stage par-ticipated in both RMR and SwMR measurements, withat least 30 days between experiment types.

Resting metabolism

To ensure adult fish were in a post-absorptive state, theywere placed into cylindrical, acrylic chambers (13.03 lvolume, 64 cm long x 15 cm diameter; Cech et al. 1979)the night before experimentation. Fish struggled only afew seconds when initially entering the chamber beforebecoming very quiescent, exhibiting very shallow ven-tilatory beats during the acclimation and experimentalperiods. Respirometers were placed into an insulated,fiberglass 300-l tank and connected to the water-supplymanifold via a submersible pump (Danner Model No. 2)with the bath water set to the fish’s acclimation temper-ature. The water bath was heavily aerated, via air stones,and for the warmer water treatments a 17-l trickle col-umn (wet-dry filter) was added to maintain dissolvedoxygen at>95 % saturation. The fiberglass tank wasthen mostly covered with heavy black plastic sheetingto minimize disturbances to the fish.

Juvenile experiments were conducted with the samemethods as for adults; except for the chamber size andtype (glass) and video equipment. For juveniles wechose either a 225-ml or 470-ml glass respirometer,based on fish size (Cech 1990). Because preliminaryexperiments showed that juvenile hardhead were lessquiescent than the adults, an underwater video camera(Speco Model No.627) equipped with IR (850 nm)lights was used to observe the hardhead remotely.Many juveniles showed active pectoral fin movementsthroughout the experiments, and some were observed tomake repeated circles in the chambers. Measurementsduring those intervals where active circular movementswere noted were removed from the data set.

We used intermittent respirometry for hardheadRMR, where flushing periods of well-oxygenated wateralternated with measurement periods during which therespirometer was sealed and the oxygen declined due tofish respiration. Water was sampled (3 ml) at the time at

Environ Biol Fish

which the chamber was sealed and again just before itwas unsealed and flushed to determine the oxygen par-tial pressure. This procedure was repeated, remotelythrough the valve manifold to avoid disturbing the fish,until three measurement periods were completed, and amean oxygen difference was determined, for each fish.Oxygen partial pressures (PO2, mm Hg) were measuredusing a polarographic electrode (Model E101, AnalyticSensors, Inc.), which was thermostatted to the measure-ment temperature of the fish, connected to a calibrated,polarographic amplifier (AM Systems). These data wereconverted to O2 concentrations (mg O2 l−1) using thenomogram of Green and Caritt (1967). Post-experimentfish were measured for mass and lengths, and placedinto a post-test holding tank. Resting metabolic rate datawere reported as mass-independent metabolic rate ad-justed using a scaling exponent of 0.79 (Clarke andJohnston 1999). RMRs were calculated by using theinitial vs. final O2 concentration difference, elapsed timein the respirometer, fish mass, and respirometer volume,following Cech (1990):

RMR ¼ O2 Að Þ –O2 Bð Þð Þ�V½ �=M−0:79=T

where RMR was O2 consumption rate (mg O2

kg-0.79 h−1), O2 (A) was the concentration (mg O2 l−1)

at the start of the interval in water, O2 (B) was theconcentration (mg O2 l

−1) at the end of the interval inwater, V was the chamber’s volume (13.03-l less thefish’s volume, assuming 1 kg=1 l) (Virani and Rees2000),Mwas the fish’s mass (kg), and Twas the elapsedtime during the measurement (h). All respirometerswere thoroughly flushed between experiments, bleachedand rinsed weekly, and biweekly assessments of back-ground (“blank”) oxygen consumption without a fishpresent revealed no changes in water oxygen concentra-tion during a 30-min measurement period at alltemperatures.

To evaluate the influence of temperature on RMR,we calculated temperature coefficients (Q10) betweentemperature acclimation groups. The Q10 is defined asa rate of change in a biological system over a 10 °Cchange in temperature (Cech et al. 1994):

Q10 ¼ yMO2=xMO2ð Þ10= Ty − Txð Þ

where yMO2 was the rate at the higher temperature,xMO2 was the rate at the lower temperature, Ty wasthe higher temperature (°C), and Tx was the lowertemperature (°C).

Swimming metabolism

For the adult (wet mass >500 g) SwMR experiments weused a velocity-calibrated (electromagnetic flow meter,Marsh-McBirney Model No. 201D) Brett-style (Brett1964) swimming respirometer (volume: 660 l,Cocherell et al. 2011). Fish were placed inside therespirometer, which was set to a 5 cm s−1 water velocityand a flushing flow of 12 l min−1, the night before theexperiment to allow for handling stress to subside and toensure post-absorptive status. Thermostatted chillersand heaters maintained water bath and respirometertemperatures within ±0.5 °C of the fish’s acclimationtemperature.

In the morning following acclimation, the cham-ber’s water velocity was increased to 30 cm s−1, therespirometer was sealed, and an initial PO2 watersample (3 ml) was taken. After ca. 1 h, anothersample, which was ≥10 mm Hg less than that ofthe initial sample, was taken, and the flushingpumps were then restarted to flush the respirometerwith air-equilibrated water from the bath for ca.30 min. Then, the water velocity was increased by15 cm s−1 and allowed to stabilize (ca. 5 min), therespirometer was sealed, and another initial PO2

sample was taken. This procedure was repeated atincreasing velocity steps until the fish became fa-tigued twice (i.e., could not swim off the rearscreen in the respirometer) at its highest swimmingvelocity, typically after 10–12 h. The number ofvelocity steps completed by an individual fish var-ied, resulting in differential n values among veloc-ity steps. Oxygen levels never fell below 80 %saturation during any swimming period, and allrespirometers were assessed for background oxygenconsumption and bleached and rinsed as previouslydescribed. Fish were allowed to recover for 30 minbefore they were weighed, measured, and placed ina post-test holding tank. Swimming metabolic ratedata were calculated as:

SwMR ¼ O2 Að Þ –O2 Bð Þð Þ�V½ �=M=T

where SwMR was O2 consumption rate (mg O2

kg−1 h−1), O2 (A) was the concentration (mg O2 l−1)

at the start of the interval in water, O2 (B) was theconcentration (mg O2 l

−1) at the end of the interval inwater, V was the chamber’s volume (13.03-l less thefish’s volume, assuming 1 kg=1 l) (Virani and Rees

Environ Biol Fish

2000), M was the fish’s mass (kg), and T was theelapsed time during the measurement (h) (Brett andGlass 1973).

Juvenile hardhead SwMR experiments were con-ducted in a modified 4.94-l swimming respirometer(Loligo® Systems Model No. SW10050). This wascoupled to a single-channel respirometry system withgalvanic electrode (Loligo® Systems Model No.DAQ-PAC-G1) and Loligo’s AutoResp™ software.In preliminary swimming experiments (n=3) wefound that hardhead acclimated to 11 °C were un-willing to swim after an overnight acclimation.Decreasing their chamber acclimation time to30 min resulted in more successful swimming re-sponses. Insertion of a clear, acrylic tube (27.5 cmlong x 7 cm diameter) in the swimming chamber ofthe respirometer prevented these small hardhead fromutilizing boundary layers near the vertical rectangularwalls. Thick landscape fabric, allowing filtered lightentry only through the top of the respirometer, ob-scured the fish’s view of the researchers. Hardheadwere monitored remotely via video cameraequipment.

After the 30-min acclimation, water velocity wasincreased to 10 cm s−1 for the first velocity step. Thechamber’s flush pump was shut off and an electronicvalve sealed the chamber. The respirometer PO2 wasrecorded every 10 min, until a 5-mm Hg decrease wasachieved. The chamber was then flushed for 10 min andthe water velocity was increased by another 10 cm s−1.Stepwise velocity increases, sealing and flushing of thechamber, and associated PO2 measurements were con-tinued until the fish fatigued twice within a velocityinterval. Because of their small size, it was very difficultto detect whether juvenile hardhead were “tail prop-ping” (e.g., from fatigue) against the rear screen.Therefore, we used one of two visible signs of fatiguebefore terminating each experiment: S-bending by thefish against the rear screen or when fish had greater than50 % of its body in contact with the rear screen. Thenumber of velocity steps completed by an individualfish varied, resulting in differential n values amongvelocity steps.

Mean tailbeat frequency (TBF, beats/min) in adultfish was calculated as the mean for each fish per velocitystep, and reported as the grand mean for all fish per step.A single fish could have had as few as one TBF deter-mination or as many as eight, depending on the numberof velocity steps completed, and fish that failed a

velocity step for SwMR could still provide TBF data.Swimming speeds, in body lengths per second, wereestimated across water velocities using the mean fishfork length for each acclimation group for convenienceto readers accustomed to working with relative swim-ming speeds.

Statistical analyses

Fish mass, TBF, RMR, and SwMR were analyzed viaANOVA with lifestage, water velocity, and/or accli-mation temperature as factors. All data met the as-sumption of homogeneity of variance and data werelog transformed where necessary to meet the assump-tion of normality. Post-hoc comparisons were per-formed among groups with the Holm-Sidak proce-dure. Simple linear regression analysis was used tomodel the relationship between water velocity andTBF. No statistical tests were performed on SwMRdata from 11 to 16 °C acclimated juvenile hardheaddue to the few successful experiments completed atthese cooler temperatures. All statistical analyseswere conducted using SigmaPlot TM (Release 12.0),SPSS Inc. statistical software. Statistical decisionswere based on an alpha level of 0.05.

Results

Fish size

The mean masses of adult hardhead used in RMRexperiments ranged from 680 to 743 g and did not differamong temperature acclimation groups (F3,75=0.266,P=0.849, Table 1). The effect of acclimation temper-ature on juvenile hardhead mass (range 2.8–6.2 g)was significant (F3,70=21.250, P=0.001, Table 1).Juvenile fish masses increased significantly with ac-climation temperature in most groups (P ≤0.023)although the mean masses of the 21 and 25 °C accli-mation groups were indistinguishable (P =0.095).The mean masses of adult hardhead in SwMR exper-iments ranged from 749 to 808 g and did not differsignificantly among temperature acclimation groups(F3,76=1.841, P=0.147, Table 1). The effect of accli-mation temperature on juvenile hardhead mass (range3.34 - 10.2 g) was significant (F3,68 = 45.219,P <0.001, Table 1) and increased with acclimationtemperature in all groups (P≤0.005, Table 1).

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Resting metabolism

A two-factor ANOVA revealed a significant effect oflifestage (F1,145=29.179, P <0.001) on RMR (mg O2

kg-0.79 h−1) of hardhead, with adult hardhead RMRsexceeding those of juvenile fish (Fig. 1). The effect ofacclimation temperature was also significant (F3,145=47.350, P <0.001) with RMRs of adult and juvenilehardhead increasing significantly at each acclimationtemperature (P <0.001 for all comparisons). There wasno significant interaction between lifestage and acclima-tion temperature (F3,145=0.524, P=0.666). Across theentire thermal acclimation range, Q10 values for RMR inadult and juvenile hardhead were 1.53 and 1.56,

respectively (Table 1) suggesting low to medium ther-mal sensitivities. The Q10 was slightly lower at 11–16 °C and 16–21 °C in adults and juveniles (Q10=1.33-1.61), remained low in juveniles (Q10=1.59 at21–25 °C), but increased to 2.04 in adult hardhead atwarmer temperatures.

Adult hardhead swimming metabolism and tailbeatfrequecies

Adult hardhead from all temperature acclimationgroups consistently achieved swimming velocitiesof 90 cm s−1. Two-way ANOVA revealed a signifi-cant effect of both acclimation temperature (F3,247=

Table 1 Average (±SE) wet mass and fork length for adult andjuvenile hardhead acclimated to 11, 16, 21, and 25 °C and tested inRMR or SwMR experiments. Temperature quotients (Q10) werecalculated between acclimation groups and across the thermal

acclimation range (11–25 °C) from RMR values. Superscriptletters denote significant differences in mass between acclimationgroups within hardhead lifestage

Lifestage Acclimation group (°C) RMR Mass (kg) RMR FL (cm) Temperaturerange (°C)

Q10 SwMR Mass (kg) SwMR FL (cm)

Juvenile 11 0.0028a (0.00018) 5.66 (0.15) 11–16 1.61 0.00334a (0.0001) 6.2 (0.20)

Juvenile 16 0.0043b (0.00021) 6.62 (0.15) 16–21 1.48 0.00506b (0.00051) 7.2 (0.20)

Juvenile 21 0.0055c (0.00036) 7.73 (0.20) 21–25 1.59 0.00661c (0.00036) 8.1 (0.24)

Juvenile 25 0.0062c (0.00045) 7.93 (0.25) 11–25 1.56 0.0102d (0.00072) 9.8 (0.28)

Adult 11 0.705A (0.05) 37.0 (0.99) 11–16 1.33 0.807A (0.042) 39.3 (0.69)

Adult 16 0.743A (0.07) 36.8 (1.06) 16–21 1.39 0.808A (0.067) 38.9 (0.92)

Adult 21 0.736A (0.49) 38.8 (0.82) 21–25 2.04 0.751A (0.047) 39.2 (0.74)

Adult 25 0.680A (0.48) 38.8 (0.91) 11–25 1.53 0.749A (0.048) 39.4 (0.71)

Acclimation Temperature (oC)

0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30

MO

2 (

mg

O2 k

g-0

.79

h-1

)

0

5

10

15

20

25

30

35

40

45

50

55

60

65

70

n = 19,16, 22,17

n = 21,19, 20,19

a

b

c

d

(A)

(B)

Fig. 1 Mean (±SE) restingmetabolic rate (RMR) of adult(white circle) and juvenile (blackcircle) hardhead at acclimationtemperatures of 11, 16, 21, and25 °C. Both acclimationtemperature and lifestage werestatistically significant maineffects. Lower case letters denotestatistically significant differencesbetween thermal acclimationgroups, and capital letters denotea significant difference betweenlifestages in RMR. Sample size(n) for each acclimation group isgiven in order of increasingacclimation temperature

Environ Biol Fish

9.916, P <0.001) and swimming velocity (F4,247=34.274, P <0.001) on SwMR of adult hardhead, withno significant interaction (F12,247=0.808, P=0.642).Overall, 25 °C acclimated fish had SwMRs that weresignificantly lower than the other acclimation groups(P <0.001 for all comparisons, Fig. 2). SwMRs in-creased significantly with increasing swimming ve-locities except between 75 and 90 cm s−1 whereSwMR values did not differ (P =0.502, Fig. 2).

Two-way ANOVA revealed a significant effect ofacclimation temperature (F3,1792=60.636, P <0.001)and swimming velocity (F4,1792 =1178.076, P<0.001) on TBF of adult hardhead, with a signifi-cant interaction (F12,1792=2.191, P =0.010). As ex-pected, post hoc tests revealed that in all thermalacclimation groups, the mean TBF of adult hardhead

was significantly higher at each successive increasedvelocity step tested (P ≤0.004 for all comparisons;Fig. 2). At 30 cm s−1, mean TBFs of 16 and 25 °Cacclimated fish did not differ (P =0.947), but weresignificantly higher than those of 11 °C acclimatedfish and lower than 21 °C acclimated fish (P≤0.013for all comparisons). At 45 cm s−1, 21 °C acclimatedfish had significantly higher TBFs than all otheracclimation groups which did not differ significantlyfrom one another (P values≤0.028 for all compari-sons). At both 60 and 75 cm s−1 swimming veloci-ties, TBFs of 16, 21, and 25 °C acclimated fish didnot differ (P values ≥0.126), but were significantlyhigher than those of 11 °C acclimated fish (P values≤0.001). At 90 cm s−1, 21 °C acclimated fish hadsignificantly higher TBFs compared to those of 11

Water Velocity (cm s -1)

0 10 20 30 40 50 60 70 80 90 100 110 120

Swim

min

g M

etab

olic

Rat

e (m

g O

2 Kg-1

h-1)

0

100

200

300

400

500

600

700

800

900

1000

1100

Tailb

eat F

requ

ency

(bea

ts m

in-1

)

0

20

40

60

80

100

120

140

160

180

200

220

240n = 12,15,15,15,7n = 15,18,15,15,13r² = 0.989 p = 0.0005TBF = 42.92 + 1.43 * cm s-1

11oC Adult HHA

C D

D

B

a

b

c

d

e

A

1 BL/sI

2 BL/sI

3 BL/sI

(*)

Water Velocity (cm s-1)

0 10 20 30 40 50 60 70 80 90 100 110 120

Sw

imm

ing

Met

abol

ic R

ate

(mg

O2

Kg-1

h-1)

0

100

200

300

400

500

600

700

800

900

1000

1100

Tailb

eatF

requ

ency

(bea

ts m

in-1

)

0

20

40

60

80

100

120

140

160

180

200

220

240n = 8,12,15,14,6n = 11,17,17,16,14r² = 0.982 p =0.0010TBF = 48.69 + 1.55* cm s-1

16oC Adult HHA

B

C

D

D

a

b

c

d

e

B

1 BL/sI

2 BL/sI

3 BL/sI

(*)

Water Velocity (cm s-1)

0 10 20 30 40 50 60 70 80 90 100 110 120

Sw

imm

ing

Met

abol

ic R

ate

(mg

O2

Kg-1

h-1)

0

100

200

300

400

500

600

700

800

900

1000

1100

Tailb

eat

Freq

uenc

y (b

eats

min

-1)

0

20

40

60

80

100

120

140

160

180

200

220

240n = 13,17,17,14,9n = 17,18,18,16,14r2 = 0.996 p < 0.0001TBF = 50.18 + 1.64* cm s-1

21oC Adult HHA

B

C

DDa

b

c

d

eC

1 BL/sI

2 BL/sI

3 BL/sI

(*)

Water Velocity (cm s-1)

0 10 20 30 40 50 60 70 80 90 100 110 120

Sw

imm

ing

Met

abol

ic R

ate

(mg

O2

Kg-1

h-1)

0

100

200

300

400

500

600

700

800

900

1000

1100

Tailb

eat

Freq

uenc

y (b

eats

min

-1)

0

20

40

60

80

100

120

140

160

180

200

220

240n = 17,19,18,18,7n = 19,20,18,18,17r2 = 0.998 p = <0.0001TBF = 46.91 + 1.58 * cm s-1

25oC Adult HHA BC

D D

a

b

c

d

e

D

1 BL/s 2 BL/s 3 BL/s

( )

Fig. 2 Mean (±SE) swimming metabolic rate, SwMR (blackcircle) and tailbeat frequency, TBF (white circle) of adult hardheadacclimated to 11 (A), 16 (B), 21 (C), and 25 °C (D). The105 cm s−1 TBF was excluded from statistical analysis due tolow sample sizes (n<3). Capital letters denote a significant differ-ence in SwMR between velocity steps across all panels, anddifferent symbols in parentheses indicate significant differencesin SwMRamong acclimation temperature groups across all panels.For TBF data, lower case letters denote statistically significant

differences in TBF between velocity steps within each temperatureacclimation group. Significant differences in TBF between thermalacclimation groups within each velocity step are given in the text.Sample size (n) for each acclimation group is given in order ofincreasing acclimation temperature. Fish swimming speeds (inbody lengths s−1, BL s−1) and regression models for the relation-ship between TBF and water velocity are shown for each thermalacclimation group

Environ Biol Fish

and 16 °C acclimated fish (P values≤0.040) but nothigher than 25 °C acclimated fish (P =0.297). TheTBF of the 16 °C acclimated fish was significantlyhigher than that of the 11 °C fish (P=0.025).

Juvenile hardhead swimming metabolism

Many juvenile hardhead, especially those acclimated to11 and 16 °C, were reluctant to swim in the respirome-ter, precluding meaningful analyses of their SwMRs.The 21 and 25 °C acclimation groups had seven andsix fish, respectively, that completed the 50 cm s−1 ve-locity step with 12–16 fish completing all other lowerswimming velocity steps (Fig. 3). Also, the 21 and25 °C acclimated fish swam with fewer impingementsand “tail-propping” events than were observed amongfish acclimated at lower temperatures. Two-wayANOVA revealed a non-significant effect of acclimationtemperature (F1,130=0.146, P=0.703) and a significanteffect of swimming velocity (F4,130=21.180, P<0.001)on SwMR of juvenile hardhead, with a significant inter-action (F4,130=3.303, P =0.013). In both acclimationgroups, SwMRs at the 50 cm s−1 swimming velocitywere highly variable. Interestingly, the 21 °C acclimatedfish had a significantly higher SwMR, compared to the

25 °C acclimated fish, when swimming at 50 cm s−1

(P=0.003).

Discussion

Temperature effects on hardhead metabolic rates

We measured resting metabolic rates at several environ-mentally relevant temperatures because these rates are abasic property in fish indicative of bioenergetics costs,and are used to make direct comparisons to other spe-cies, under similar conditions. We did not test hardheadat extreme temperatures (high or low, e.g., that wouldhave caused metabolic depression or death). For exam-ple, we did not test fish at 30 °C, due to their generalavoidance of the 28 °C zone in a 3-m-diametertemperature-preference apparatus (Cocherell et al.2013), or below 11 °C, because we rarely caught hard-head when river water temperatures were below 10 °C.Hardhead generally increase their RMRs with tempera-ture increases (Fig. 1), but the increases were low tomoderate (Q10s≤2), compared with other ectothermicvertebrates (Schmidt-Nielsen 1990), including fishes(Winberg 1956; Brett 1964). These results correspondto the ca. 1.5 Q10 shown by hardhead acclimated to 10

Water Velocity (cm s -1

)

0 5 10 15 20 25 30 35 40 45 50 55 60 65

Sw

imm

ing

Me

tab

olic R

ate

(m

g O

2 K

g-1

h-1

)

0

100

200

300

400

500

600

700

800

900

1000

1100

21oC; n = 19,19,17,16,7

25oC; n = 16,15,13,12,6

A A

A

B

C

a a

ab

b b

(*)

1 BL/s

I

2 BL/s

I

3 BL/s

I

4 BL/s

I

5 BL/s

I

6 BL/s

I

7 BL/s

I

Fig. 3 Mean (±SE) swimming metabolic rate, SwMR, of juvenilehardhead acclimated to either 21 °C (white circle) or 25 °C (blackcircle). Note that the 60 cm s−1 data are not included in thestatistical tests due to the low sample sizes (n=1 for both points).Capital (21 °C) and lower case (25 °C) letters denote statisticallysignificant differences in SwMR between velocity steps within

temperature acclimation groups. An asterisk (*) indicates a signif-icant difference in SwMRs at a specific swimming velocity. Sam-ple sizes (n) for each thermal acclimation group are given in orderof increasing water velocity. Fish swimming speeds (in bodylengths s-1, BL s-1) are also shown

Environ Biol Fish

and 20 °C range (Cech et al. 1990). Recently, Kaufmanet al. (2013) showed that the temperature sensitivity ofhardhead blood-oxygen affinity was very low below19 °C, somewhat higher between 19 and 25 °C, andmuch higher between 25 and 30 °C. The hardhead’smoderate responses to temperatures <25 °C (i.e., in Q10

and in blood oxygen affinity) should allow it to movebetween stream reaches, characterized by various tem-peratures, with minimal increases in energetic demandsand without compromising its oxygen delivery systemto metabolizing tissues, including exercising red muscle(Cech et al. 1990; Kaufman et al. 2013). Furthermore,field and laboratory studies show that hardhead pre-ferred temperatures in the 19–20 °C range (Knight1985; Cocherell et al. 2013). In his review of optimaltemperatures for fishes, Jobling (1981) concluded thatthere was a close correlation between preferred temper-atures and those where maximal growth rates areexhibited.

Relative to other stream fishes, our Q10 data basedon mass adjusted RMRs (range 1.33-2.04) suggestthat hardhead have a relatively low to moderate ther-mal sensitivity. Clarke and Johnston’s (1999) reviewfound a within-species, median Q10=2.40, suggestingthat hardhead show a degree of evolutionary adjust-men t to Ca l i fo rn ia s t r eams . Reds ide dace(Clinostomus elongates, Cyprinidae) inhabit headwa-ter streams in the Great Lakes and upper MississippiRiver watersheds (USA and Canada, Bailey andSmith 1981). Novinger and Coon (2000) found thatthese dace increased their metabolic rates at increasedacclimation temperatures over 6–20 °C at a moretypical Q10=2.3. The dace’s comparatively higherthermal sensitivity may afford more metabolic scopefor activity during colder season conditions (Clarkeand Johnston 1999). In contrast, the hardhead’s rela-tively lower thermal sensitivity may allow extra en-ergy allocations towards growth or reproduction inthe comparatively warmer seasonal temperatureranges in California’s rivers and streams (Brett1964; Warren and Davis 1967). Similarly, Cechet al. (1994) found that northern pikeminnow(Cyprinidae), which inhabit Columbia River basinhabitats north of California, had a relatively lowQ10 (1.80) over 18–21 °C, but a much higher Q10

(3.23) than did hardhead over the colder 9–15 °Crange. Both juvenile and adult hardhead showed sim-ilar trends between acclimation groups with smallchanges over 11–25 °C.

Adult hardhead swim performance, swimmingmetabolic rates, and tailbeat frequencies

Overall, adult hardhead performed well in our Brett-styleswimming respirometers. Fish were easily capable ofreaching 75 cm s−1, with many reaching 90 cm s−1 watervelocities. A few exceptional fish swam continuously at105 cm s−1 for 30–40 min, double the swimming speedsthat Myrick and Cech (2000) observed for sub-adulthardhead (Ucrit range 47–57 cm s−1), but their fishweighed considerably less (ca. 15 - 20 %) than oursdid. Kaufman et al. (2013) predicted sustained aerobicperformances from hardhead from the rather high Bohreffects (i.e., blood-oxygen affinity losses with decreasingpH) and blood oxygen capacities. At lower velocitiesand temperatures adult hardhead spent much of theirtime refusing to swim and apparently trying to avoidactivity (e.g., clinging to the bottom, trying to escape,“tail propping” on the rear screen). This was especiallytrue at the lower water velocities where intermittentswimming was used until moderate velocities wereachieved. In contrast, fish tended to swim well at lowervelocities at the higher temperatures and spent less timeavoiding directed swimming into the current. Within aspecies’ limits, muscles are usually more efficient atwarmer temperatures. Also, the viscosity of water de-creases somewhat as water warms, facilitating swim-ming. Rome et al. (1984) observed that the water veloc-ity threshold for recruitment of fast motor muscle units ina cyprinid correlated with decreased water temperature.Thus, non-adapted fish would need to use more white(anaerobic) musculature at lower swimming speeds, po-tentially decreasing maximum sustained swimming ve-locity. Interestingly, Cocherell et al. (2011) swam rain-bow trout in the same chamber as was used in this studyand found mean adult trout Ucrits at only 74 cm s−1

(mean mass 874 and SL 34.6). Comparing these troutwith our hardhead suggests that adult hardhead have anequal or greater capacity for aerobic swimming at warm-er temperatures (19 °C).

In our tests of adult hardhead active swimming wefound a strong positive correlation between tailbeatfrequency and metabolic rate with increasing watervelocity. Steinhausen et al. (2005) also found high cor-relations between tailbeat frequencies, swimmingvelocities, and SwMRs in two marine fishes. Ourhardhead data are comparable to cyprinid data fromZhang et al. (2012), who observed SwMRs starting atca. 200 mg O2 kg−1 h−1 and exceeding 900 mg O2

Environ Biol Fish

kg−1 h−1 at higher velocities. Mean MO2 rates rangedfrom 209 to 1342mgO2 kg

−1 h−1 for our adult hardheadat velocities from 30 up to 90 cm s−1, which estimatesthe maximal continuous rate of oxygen consumption(aerobic activity) in hardhead. A plateau was observedat 90 cm s−1 in adults, possibly due to fish nearingfatigue (Fry 1971). Fry (1971) noted that locomotoractivity changes associated with temperature are respon-sible for plateau effects when looking at non-linearrelationships of metabolic rate and temperature. In theswimming respirometers, the adult hardheads’ higherSwMRs at the lower temperatures at several of theswimming velocities were unexpected. However, theseresults were probably attributable to the unsettled natureof these wild fish at the lower temperatures (especially at11 and 16 °C) as they sought hydraulic cover or escapefrom the apparatus.

Juvenile hardhead swim performance and swimmingmetabolic rates

The 50 cm s−1 velocity may approach the juvenile’smaximum sustained swimming velocity, because lessthan 50 % of fish that successfully completed the40 cm s−1 velocity step subsequently completed the50 cm s−1 velocity step. Unsteady swimming(including burst and glide swimming as white musclefibers are recruited to maintain position in a strongcurrent, Jayne and Lauder 1994) is often observed neara fish’s maximum speed, presumably causing signifi-cant deviations in aerobic SwMRs. Myrick and Cech(2000) found rainbow trout’s Ucrit to range over acomparable 46–55 cm s−1 at 10 to 19 °C, despite thetrout’s somewhat larger size (mass range: 11–18 g).Interestingly, this cyprinid swimming performance isnot limited to hardhead. Sutphin et al. (2007) observedthat Sacramento splittail (Pogonichthys macrolepidotus,Cyprinidae) of standard length 7.9 cm, similar to that ofour hardhead, reached a Ucrit of 63 cm s−1.

The juvenile fish in our study did not perform aswell as the adults did in a similar type of swimmingrespirometer, especially at lower temperatures. Mostof the juveniles refused to swim at 11 °C and 16 °Cwith only a total of seven of 36 individuals actuallyswimming in any velocity step to provide metabolicdata. From the 11 °C group only one fish progressedto 30 cm s−1 and in the 16 °C group, only one fishprogressed to 40 cm s−1. The 21 °C and 25 °Cjuvenile hardhead groups fared much better with

several fish progressing to the 50 cm s−1 velocitystep, comparable to Myrick and Cech (2000) resultsfor hardhead weighing 102–194 g. We did not testjuvenile hardhead at night, although some evidencesuggests that cyprinids can shift to being nocturnal atlowered water temperatures, which could improvetheir chances of swimming in an artificial swimmingchamber (Greenwood and Metcalfe 1998), nor did weemploy a potentially stressful electric (typically 3v)grid as our downstream screen to induce swimmingand discourage “tail propping.”

Implications for hardhead stream management

Temperature levels in streams and rivers may limit theability of hardhead to maintain their populations underchanging conditions (e.g., modifications of hydrologicand thermal regimes, introduced species, and globalclimate change). The results of this study suggest thathardhead are well-suited for sustained aerobic activityover a range of instream flow regimes and moderatetemperature (ca. 16 to 21 °C). To protect both adult andjuvenile hardhead, avoid temperatures in excess of 25 °C,particularly if environmental hypoxia may be present(Kaufman et al. 2013). To protect adult hardhead, avoidunseasonal high velocities, such as those associated withpulsed flows (Young et al. 2011), when water tempera-tures are near or less than 11 °C. If this is not possible,ensure that the habitat contains structure that adult hard-head could use as shelter to avoid higher velocities, andensure that high velocities are of short enough durationthat hardhead will have adequate opportunities to feed.Upstream of Slab Creek Reservoir hardhead have accessto several miles of river reaches and tributaries, althoughcold water flowing from higher elevations may limittheir winter and spring movements. On the other hand,colder water may offer a refuge from introduced warmwater predators and competitors. Smallmouth bass(Micropterus dolomieu, Centrarchidae) were caught inthe lower two reservoirs, but only when temperatureswere above 17.3 °C, and it has been suggested that thepresence of smallmouth bass may limit hardhead distri-butions at warmer temperatures (Baltz et al. 1987).Juvenile hardhead in wild, naturally flowing systemsin California would emerge in late spring and wouldexperience only warm water and low flow velocitiesduring the summer while growing toward adult sizeand metabolic characteristics. It may be that juvenilehardhead are not well-suited for cold water and/or high

Environ Biol Fish

flow velocities. If so, our results provide a caution to dammanagers and regulators regarding the flow and temper-ature changes incurred during spring and summer damoperations that may cause juvenile hardhead to experi-ence higher flow velocities and colder temperatures thanwould normally occur in unregulated rivers. To protectjuvenile hardhead, avoid high velocities such as thoseassociated with pulsed flows at times of the year whenjuvenile hardhead lifestages are present, and water tem-peratures are 16 °C or less, especially if the habitat lacksstructure where young fish could shelter to avoid highervelocities. If juvenile hardhead are unwilling or unable toswim actively under cold, fast water conditions they maybe more vulnerable to predation, and/or unable to feedand grow at adequate rates. Our study did not considerbiotic variables including competition, predation, para-sitism, or fish behavior (Cech et al. 1990) that mayinteract with physical variables such as temperature,dissolved oxygen or water velocity to determine hard-head performance under field conditions. Given theseuncertainties, we encourage managers to exercisecaution in the determination and implementation oftemperature and flow standards for hardhead. Theresults of this study provide guidance to managersto allow them to make more knowledgeable trade-offs between water flows to support native Californiafishes and other water uses.

Acknowledgements We thank P. Young for her assistance inidentifying the need for this study; The California Department ofFish and Wildlife for assistance with our Scientific CollectionPermit; K. Thomas, C. Garman, J. Rowan, and R. Vincik ofCDFW, J. Williams of the US Forest Service - Eldorado NationalForest, R. Aramayo of Garcia and Associates, M. Obedzinski ofCalifornia SeaGrant Extension Program; B. Center of CampLotusfor access to the Nugget property and B. Williams and E. Sheltonof Pacific Gas and Electric for access upstream of the Chili BarDam facility; H. Nelson, R. Coalter, S. Cocherell, J. Reardon, B.Williamson, O. Patton, B. DeCourten, J. Poletto, N. Ho, D.Jauregui, N. Nordman, T. Baghdassarian, C. Baier, A. Pietrzyk,M. Richmond, E. Kelly, N. Brinton, E. Bush, A. Avila-Hanson, S.Brandl, D. Cheng, M. Figueroa, J. DeYoung, D. Hu, A. Fratzke,M. Gilliam, M. Saberi, K. Long, M. Zhang, J. Dexter, T. Nguyen,and J. Yu with help in fish capture, husbandry, and experimentalassistance; the Upper American River Foundation, Granite BayFlycasters, and the Sac-Sierra Chapter of Trout Unlimited forassistance with hardhead capture; and E. P. Scott Weber III, P.Lutes, and E. Hallen for their advice on fish husbandry. Thisresearch was funded by California Energy Commission PublicInterest Energy Research grant PIR-08-029 and the University ofCalifornia Agricultural Experiment Station (grant no. 2098-H toNAF). We thank our project manager J. O’Hagan for guidancethroughout the project as well as two anonymous reviewers forconstructive comments to improve this manuscript. All study

animals were treated in accordance with UC Davis’ InstitutionalAnimal Care and Use Committee guidelines (protocol # 15774).

References

Bailey RM, Smith GR (1981) Origin and geography of the fishfauna of the Laurentian Great Lakes Basin. Can J Fish AquatSci 38:1539–1561

Baltz DM, Vondracek B, Brown LR, Moyle PB (1987) Influenceof temperature on microhabitat choice by fishes in aCalifornia stream. Trans Am Fish Soc 116(1):12–20

Brett JR (1964) The respiratory metabolism and swimming per-formance of young sockeye salmon. J Fish Res Bd Can 21:1183–1226

Brett JR (1971) Energetic responses of salmon to temperature. Astudy of some thermal relations in the physiology and fresh-water ecology of sockeye salmon (Oncorhynchus nerka). AmZool 11:99–113

Brett JR, Glass NR (1973) Metabolic rates and critical swimmingspeeds of sockeye salmon (Oncorhynchus nerka) in relationto size and temperature. J Fish Res Bd Can 30:379–387

Cech JJ (1990) Respirometry. In: Schreck CB, Moyle PB (eds)Methods of Fish Biology. American Fisheries Society,Bethesda, Maryland, pp 335–362

Cech JJ, Campagna CG,Mitchell SJ (1979) Respiratory responsesof largemouth bass (Micropterus salmoides) to environmen-tal changes in temperature and dissolved oxygen. Trans AmFish Soc 108:166–171

Cech JJ, Mitchell SJ, Castleberry DT, McEnroe M (1990)Distribution of California stream fishes: influence of environ-mental temperature and hypoxia. Environ Biol Fish 29:95–105

Cech JJ, Schwab RJ, Coles WC, Bridges BB (1992) Mosquitofishreproduction: effects of photoperiod and nutrition.Aquaculture 101:361–369

Cech JJ, Castleberry DT, Hopkins TE, Petersen JH (1994)Northern squawfish, Ptychocheilus oregonensis, O2 con-sumption rate and respiration model: effects of temperatureand body size. Can J Fish Aquat Sci 51:8–12

Chun SN, Cocherell SA, Cocherell DE, Miranda JB, Jones GJ,Graham J, Klimley AP, Thompson LC, Cech JJ (2011)Displacement, velocity preference, and substrate use of threenative California stream fishes in simulated pulsed flows.Environ Biol Fish 90(1):43–52

Claireaux G, Lagardère J-P (1999) Influence of temperature, oxy-gen and salinity on the metabolism of the European sea bass.J Sea Res 42:157–168

Clarke A, Johnston NM (1999) Scaling of metabolic rate withbody mass and temperature in fish. J Animal Ecol 68:893–905

Cocherell SA, Cocherell DE, Jones GJ, Miranda JB, ThompsonLC, Cech JJ, Klimley AP (2011) Rainbow troutOncorhynchus mykiss energetic responses to pulsed flowsin the American River, California, assessed by electro-myogram telemetry. Environ Biol Fish 90:29–41

Cocherell DE, Fangue NA, Klimley PA, Cech JJ Jr (2013)Temperature preferences of hardhead Mylopharodonconocephalus and rainbow trout Oncorhynchus mykiss inan annular chamber. Environ Biol Fish. doi:10.1007/s10641-013-0185-8

Environ Biol Fish

Cushman RM (1985) Review of ecological effects of rapidlyvarying flows downstream from hydroelectric facilities. NAm J Fish Manage 5:330–339

Davison W (1997) The effects of exercise training on teleost fish, areview of recent literature. CompBiochemPhysiol 117A:67–75

Erman DC, Andrews ED, Yoder-Williams M (1988) Effects ofwinter floods on fishes in the Sierra Nevada. Can J FishAquat Sci 45:2195–2200

Facey DE, Grossman GD (1990) The metabolic cost of maintain-ing position for four North American stream fishes: effects ofseason and velocity. Physiol Zool 63:757–776

Fry FEJ (1947) Effects of the environment on animal activity. Univ.Toronto Stud. Biol. Ser. 55, Ontario Fish Res Lab Publ 68

Fry FEJ (1971) The effect of environmental factors on the phys-iology of fish. In: Hoar WS, Randall DJ (eds) FishPhysiology. 6 Academic Press, New York, pp 1–98

Green EJ, Caritt DE (1967) New tables for oxygen saturation ofseawater. J Mar Res 25:140–147

Greenwood MFD, Metcalfe NB (1998) Minnows become noctur-nal at low temperatures. J Fish Bio 53:25–32

Hill J, Grossman GD (1993) An energetic model of microhabitatuse for rainbow trout and rosyside dace. Ecology 74:685–698

Houck A, Kaufman B, Petersen J (1995) Smallmouth bass in theHorseshoe Bend Reach of the San Joaquin River: Limitingfactors and bioenergetic modeling. Report prepared forSouthern California Edison Company. Rosemead, CA

Jayne BC, Lauder JV (1994) How swimming fish use fast andslow muscle fibers: implications for models of vertebratemuscle recruitment. J Comp Physiol A175:123–131

Jeffries CA, Klimley AP, Merz JE, Cech JJ (2006) Movement ofSacramento sucker, Catostomus occidentalis, and hitch,Lavinia exilicauda, during a spring release of water fromCamanche Dam in the Mokelumne River, California.Environ Biol Fish 75:365–373

Jobling M (1981) Temperature tolerance and the finalpreferendum: rapid methods for the assessment of optimumgrowth temperatures. J Fish Bio 19:439–455

Kaufman RC, Coalter R, Nordman NL, Cocherell DE, Cech JJ,Thompson LC, Fangue NA (2013) Effects of temperature onhardhead minnow (Mylopharodon conocephalus) blood-oxygen equilibria. Environ Biol Fish 96:1389–1397

Knight NJ (1985) Microhabitats and temperature requirements ofhardhead (Mylopharodon conocephalus) and SacramentoSquawfish (Ptychocheilus grandis), with notes for someother native California stream fishes. Doctoral dissertationUniversity of California, Davis

Moyle PB (2002) Inland fishes of California (ed). Press,University of California

Moyle PB, Yoshiyama RM, Wikramanayake ED, Williams JE(1995) Fish species of special concern, 2nd edn. Report tothe California Department of Fish and Game, Sacramento

Myrick CA, Cech JJ (2000) Swimming performances of fourCalifornia stream fishes: temperature effects. Environ BiolFish 58:289–295

Myrick CA, Cech JJ (2005) Effects of temperature on the growth,food consumption, and thermal tolerance of age-0 Nimbus-strain steelhead. N Am J Aquacult 67:324–330

Novinger DC, Coon TG (2000) Behavior and physiology of theredside dace, Clinostomus elongates, a threatened species inMichigan. Environ Biol Fish 57:315–326

Rome LC, Loughna PT, Goldspink G (1984) Muscle fiber recruit-ment as a function of swim speed and muscle temperature incarp. Am J Physiol 247:272–279

Rome LC, Swank D, Corda D (1993) How fish power swimming.Science 261:340–43

Rosenfeld JS, Boss S (2001) Fitness consequences of habitat usefor juvenile cutthroat trout: energetic costs and benefits inpools and riffles. Can J Fish Aquat Sci 58:585–593

Schmidt-Nielsen K (1990) Animal physiology: adaptation andenvironment. University of Cambridge Press, Cambridge,602 pp

Schurmann H, Steffensen JF (1997) Effects of temperature, hyp-oxia and activity on the metabolism of Atlantic cod, Gadusmorhua. J Fish Biol 50:1166–1180

Steinhausen MF, Steffensen JF, Andersen NG (2005) Tail beatfrequency as a predictor of swimming speed and oxygenconsumption of saithe Pollachias virens and whitingMerlagius merlangus during forced swimming. Mar Bio148:197–204

Sutphin ZA, Myrick CA, Brandt MM (2007) Swimmingperformance of Sacramento splittail injected with sub-cutaneous marking agents. N Am J Fish Manage 27:1378–1382

Ultsch G, Boschung H, Ross M (1978) Metabolism, critical oxy-gen tension and habitat selection in darters (Etheostoma).Ecology 59:99–107

Virani NA, Rees BB (2000) Oxygen consumption, blood lactateand inter-individual variation in the gulf killifish, Fundulusgrandis, during hypoxia and recovery. Comp BiochemPhysiol 126:397–405

Warren CE, Davis GE (1967) Laboratory studies on the feedingbioenergetics and growth of fishes. In: Gerking SD (ed) TheBiological Basis of Freshwater Fish Production. Blackwell,Oxford, pp 175–214

Webb PW (1994) The biology of fish swimming. In: Maddock L,Bone Q, Rayner JMV (eds) Mechanics and physiology ofanimal swimming. Cambridge University Press, Cambridge,UK, pp 45–62

Winberg GG (1956) Rate of metabolism and food requirements offishes. Nauchn. Tr. B. SSR. Gos. Unrv. V.I. Lenina, Minsk.,253 p. (Transl. fromRussian by Fish. Res. Board Can. Transl.Ser. No. 194. 1960)

WurtsbaughW,Davis GE (1977) Effects of fish size and ration levelon the growth and food conversion efficiency of rainbow trout,Salmo gairdneri Richardson. J Fish Bio 11:89–104

Young PS, Cech JJ, Thompson LC (2011) Hydropower-relatedpulsed-flow impacts on stream fishes: a brief review, concep-tual model, knowledge gaps, and research needs. Rev FishBiol Fish 21(4):713–731

Zhang W, Cao ZD, Fu SJ (2012) The effects of dissolvedoxygen levels on the metabolic interaction between di-gestion and locomotion in Cyprinid fishes with differentlocomotive and digestive performances. J Comp PhysiolB 182(5):641–650

Environ Biol Fish