Telemetry tag effects on juvenile lingcod - Wiley Online Library

Journal of Fish Biology (2013) 82, 1848–1857 doi:10.1111/jfb.12111, available online at wileyonlinelibrary.com

Telemetry tag effects on juvenile lingcod Ophiodon elongatus movement: a laboratory and field study J. S. F. Lee*, E. P. Tezak and B. A. Berejikian Manchester Research Station, Northwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, 7305 Beach Drive E, Port Orchard, WA 98366, U.S.A. (Received 6 November 2012, Accepted 19 February 2013) This study tested the behavioural effects of tagging subyearling and yearling lingcod Ophiodon elongatus with acoustic telemetry tags in laboratory tanks and in the natural environment (Puget Sound, WA). In the laboratory, tagged individuals showed less movement and feeding behaviour soon after tagging than untagged controls. The effect dissipated after c. 1 week, presumably as the tagged O. elongatus recovered from surgery or adjusted to the presence of the tags. This dissipation enabled a field study that compared early-tagged individuals with a long recovery period after tagging to recently-tagged individuals with a short recovery period after tagging. Consistent with findings from the laboratory experiment, recently tagged individuals showed less movement away from three release sites in Puget Sound than early-tagged individuals. Together, the laboratory and field results provide evidence of temporary tag effects on actual movement in the natural environment and provide a method for testing tag effects in the field. This study suggests that subyearling and yearling O. elongatus should be held for a recovery period before release. If holding after tagging is not an option, then movement data collected during the first week should be interpreted cautiously. Published 2013. This article is a U.S. Government work and is in the public domain in the USA.

Key words: acoustic telemetry; movement behaviour; site fidelity.

INTRODUCTION Acoustic telemetry tags emit acoustic signals that can be detected by hydrophones, and are powerful and popular tools for tracking animal movement (Heupel et al ., 2006). Use of acoustic telemetry technology has become widespread, partially due to the continued miniaturization of telemetry tags (Baras, 1991; Jepsen et al ., 2002; Heupel et al ., 2006). In contrast to other tagging technologies used in marine environments such as external tags, coded wire tags or passive integrated transponder (PIT) tags, telemetry tags do not require fish recapture to provide data and thus can provide much higher detection rates and repeated detections over time, with minimal post-tagging disturbance to the animal. All individuals must be disturbed during tag attachment. In all acoustic telemetry studies, the validity of the data rests on the important but rarely tested assumption that the telemetry tags do not affect fish movement (Thorsteinsson, 2002; Bridger *Author to whom correspondence should be addressed. Tel.: +1 360 871 8321; email: [email protected]

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& Booth, 2003; Oldenburg et al ., 2011). Laboratory studies of tag effects on behaviour and physiology suggest that tags may alter behaviour in the natural environment (Bridger & Booth, 2003). Laboratory studies typically compare the feeding behaviour, swimming speed, stamina, oxygen consumption, cortisol levels, growth or mortality of tagged and sham-tagged fishes (Jepsen et al ., 2001; Koed & Thorstad, 2001; Lacroix et al ., 2004; Zale et al ., 2005; Welch et al ., 2007; Chittenden et al ., 2009; Ammann et al ., 2012). Some laboratory studies have tested for tag effects on actual movement (as opposed to proxies for movement). Externally tagged lake whitefish Coregonus clupeaformis (Mitchill 1818) showed no significant changes in swimming activity (Anras et al ., 1998). In contrast, Thoreau & Baras (1997) found reduced blue tilapia Oreochromis aureus (Steindachner 1864) movement in tanks in the first few days after tagging and suggested a 3–4 day recovery period for field releases. As tag effects may diminish with a longer holding period before release (Oldenburg et al ., 2011), knowledge about the relationship between tag effects and the post-surgery holding period can help optimize release methods (Moore et al ., 1990). Simple laboratory environments enable controlled experiments to determine tag effects in well-defined settings. Proxies for movement or even actual movement in the laboratory, however, may or may not predict movement in the field. Inferring or predicting behaviour in the natural environment from laboratory behaviour studies is problematic for many reasons, including the vast differences in spatial scale (Thorsteinsson, 2002). Unknown telemetry tag effects on fish movement complicate interpretation of data from field experiments, and collecting the same type of movement data on non-tagged fishes (controls) is not possible (Rogers & White, 2007). For example, Mesing & Wicker (1986) observed erratic movements soon after the release of recently radio-tagged largemouth bass Micropterus salmoides floridanus (LeSueur 1822), but the lack of controls makes it difficult to know whether the erratic behaviour reflected capture stress, tagging stress, release stress or normal variation in behaviour. Similarly, blue marlin Makaira nigricans Lac´ep`ede 1802 and bluefin tuna Thunnus maccoyii (Castelnau 1872) exhibited greater depth distributions and fast swimming speeds for several hours to a few days after capture, telemetry tagging and release, although the lack of tagging controls makes it difficult to know whether altered behaviour is due to tagging stress or stress from capture (Holland et al ., 1990; Block et al ., 1992; Gunn & Block, 2001). Controls can be released with more traditional tags (e.g. external, PIT and coded wire tags) but movement data collected from these fishes provide different metrics from telemetry data. A combination of laboratory and field work may help determine whether telemetry tagging affects movement in the field (Cooke et al ., 2011). In this study, intraperitoneally tagged individuals were compared to untagged individuals in the laboratory to determine whether the acoustic telemetry tags would affect behaviour and whether the effect would dissipate with time. Positive answers to both questions allowed a test of whether a tag effect that dissipates over time could be replicated in a field study. In the field study, post-release movements of recently tagged individuals were compared to those of controls that had been tagged but allowed to recover long enough, according to the laboratory study, for the tag effect to dissipate. Published 2013. This article is a U.S. Government work and is in the public domain in the USA. Journal of Fish Biology 2013, 82, 1848–1857

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MATERIALS AND METHODS S T U DY S U B J E C T S Divers collected lingcod eggs Ophiodon elongatus Girard 1854 from rocky reefs in South Puget Sound between January and April in 2008 and 2009. Eggs were hatched in mesocosm bags and reared in increasingly larger land-based tanks as they grew (starting at 1·5 m but reaching 4·3 m diameter tanks by the time of the experiments). Ophiodon elongatus were initially fed newly hatched Artemia franciscana nauplii, weaned onto frozen and freeze-dried krill Euphausia pacifica and then moved onto commercial pellet feed. Rearing procedures generally followed the methods described by Rust et al . (2005). TA G G I N G F O R L A B O R AT O RY S T U D I E S On 1 June 2009, 12 O. elongatus yearlings from the 2008 egg collections were haphazardly selected, anaesthetized with MS-222 80 mg l−1 and measured for total length (LT ) and mass. Yearlings weighed 194·2 g (mean) at tagging (range: 184·7–210·9 g). For each individual, a Vemco V9P-1L acoustic telemetry tag (www.vemco.com; individually coded; 5·2 g in air; tag ranged from 2·5 to 2·8% of body mass) was inserted into the body cavity through a c. 1·5 cm ventral incision posterior to the pelvic girdle. The incision was then sutured with two independent monofilament surgeon’s knots. Each procedure lasted c. 2–4 min. Tags and surgical equipment were immersed in 100% ethanol between each tagging. A single experienced surgeon tagged all O. elongatus. Two colour-coded plastic beads (0·4 cm diameter × 0·2 cm width) were sutured anterior to the dorsal fin so that each O. elongatus could be individually identified. This same procedure was also used on 12 control yearlings (183·1 g; range: 170·9–211·3), except no incisions were made and no internal telemetry tag was implanted. A Wilcoxon test studied body mass differences between tagged and control groups. Immediately after each procedure, all tagged and control O. elongatus were placed together in a 4·3 m diameter flow-through tank with a 0·8 m water depth. A large canopy sheltered the tank from direct but not indirect sunlight. L A B O R AT O RY S W I M M I N G A N D F E E D I N G B E H AV I O U R Swimming and feeding data were collected for 3 weeks after tagging. From 2–5 (week 1), 8–12 (week 2) and 15–18 (week 3) June, daily spot checks were conducted by an observer at c. 0900 hours to record whether each individual was swimming or stationary in the tank. Ophiodon elongatus did not appear to alter their behaviour in response to the observer, who moved very slowly when near the tank. To minimize strain on the sutures, O. elongatus were not fed for 2 days after tagging. Ophiodon elongatus were fed 6 mm sinking pellets on 4 and 5 (week 1), 8–12 (week 2) and 15–18 (week 3) June. Each day, pellets were dropped into the tank one at a time. The identity of each O. elongatus that ate each pellet was recorded until all O. elongatus stopped eating. Ophiodon elongatus were fed to satiation to reduce the possibility that competition would influence results. No signs of aggression were apparent during feedings. Two response variables were calculated: (1) the number of times an individual was observed swimming within each week (swimming activity) and (2) the number of food items eaten within each week (feeding activity). Swimming activity and feeding activity were compared between tagged and control groups with Wilcoxon tests within each of the 3 weeks. Within-group Spearman rank correlations were calculated between body mass and swimming activity and between body mass and feeding activity for each of the 3 weeks. All reported P -values are after Bonferroni correction. L A B O R AT O RY E X P L O R AT O RY B E H AV I O U R Exploratory behaviour was tested 6 weeks after tagging (1–7 July). A 10 m × 1·5 m flume was divided in half, lengthwise with opaque dividers. Each O. elongatus was placed alone in one half of the flume for 3 h. As this environment was much larger than any environment the O. elongatus had previously experienced, this assay measured the tendency for O. elongatus Published 2013. This article is a U.S. Government work and is in the public domain in the USA. Journal of Fish Biology 2013, 82, 1848–1857


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to explore a new environment. Video cameras recorded movement throughout the flume. The flume was visually divided across its length into nine equal-sized sections for analysis. Every 5 min, the number of the section (1–9) in which the O. elongatus was found was recorded. Exploratory behaviour was summarized by counting the number of sections each O. elongatus visited in the 3 h test period. A Wilcoxon test was used to study differences between tagged and control O. elongatus.

F I E L D M O V E M E N T B E H AV I O U R In the laboratory observations, tagged O. elongatus initially showed less activity than controls, but the difference dissipated by c. 1 week after tagging. To test whether time after tagging would have an effect on O. elongatus movement under natural conditions, dispersal of subyearlings tagged 22 days before release was compared to dispersal of subyearlings tagged 2 days before release. The O. elongatus had been collected as eggs between January and March 2009. On 5 January 2010, Vemco V7-2L acoustic telemetry tags were implanted into 37 haphazardly selected O. elongatus (early-tagged) using the same procedure described above. Incisions on these 37 O. elongatus were closed with two separate sutures. Each tag weighed 1·6 g in air. The 37 O. elongatus weighed 119·7 g (mean) on 25 January 2010 (range: 68·4–182·9 g; tag ranged from 0·9 to 2·3% of body mass). On 25 January 2010, eight additional O. elongatus were tagged using the same methods (recently-tagged; 84·6 g (mean); range: 72·0–101·2 g; tag ranged from 1·6 to 2·2% of body mass). A Wilcoxon test compared body mass between the early-tagged and recently-tagged groups. On 27 January, all O. elongatus were stripped of their plastic beads, measured for LT and mass and released into three habitats in South Puget Sound (c. 15 km north-east of Olympia, WA). The plastic beads were used to keep track of which acoustic tags were released into which habitats. The habitats were characterized as (1) shallow (3 m deep; 13 early-tagged and two recently-tagged O. elongatus were released), (2) deeper rocky reef (15 m deep; 12 early-tagged and three recently tagged O. elongatus were released) and (3) deeper flat (15 m deep; 12 early-tagged and three recently tagged O. elongatus were released). The O. elongatus were dispersed among these three habitats to facilitate a larger study that was testing for effects of release habitat on subsequent movement behaviour of hatchery O. elongatus (Lee et al ., in press). A hydrophone array (Vemco VR28, mobile tracking) was towed behind a boat to survey the release sites on 28 January 2010, 2 February 2010, 23 February 2010, 18 May 2010, 5 October 2010 and 26 January 2011 (Lee et al ., in press). Boat speed was maintained between 4·5 and 6·0 km h−1 . At each release site, the mobile tracking routes were shaped like four concentric squares. The inside square was 70 m × 70 m, centred on the release site. Each of the subsequent three concentric squares was separated from the previous one by 35 m. While hydrophone read range can vary as a function of local acoustic conditions (Heupel et al ., 2006), range testing indicated that tags could be detected from up to 400 m away. In these range tests, a Vemco V7 tag was hung from a buoy 1 m below the water surface. The VR28 was towed at increasing distances from the buoy until the tag was no longer detected. In addition to the concentric squares, the hydrophones also listened for tags while stationary at each release site (in the centre of the concentric squares) for 15 min. The routes at the shallow release location were 14% shorter than the other release locations because water was not deep enough to safely tow the hydrophone array in all locations. Vemco VR28 units use four hydrophones to determine the direction of the signal origin. When an O. elongatus was detected, the operator recorded fish identification number, boat location and signal origin direction. If an O. elongatus was detected near more than one release site, signal origin direction was used to determine the site from which the tag signal came. Undetected O. elongatus were assumed to have moved away from the release site. Each day, detected O. elongatus were categorized as present and undetected O. elongatus were categorized as absent. A Wilcoxon test was used to determine whether early-tagged and recently tagged groups differed in the number of O. elongatus present and absent, only on days in which at least one O. elongatus was found. For early-tagged and recently-tagged O. elongatus, a Wilcoxon test was used to test whether body size predicted if O. elongatus were present or absent by the first survey (28 January). All reported P -values are after Bonferroni correction, if applicable. Published 2013. This article is a U.S. Government work and is in the public domain in the USA. Journal of Fish Biology 2013, 82, 1848–1857

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0·8

Swimming probability

NS 0·6

P < 0·001 NS

0·4

0·2

0·0

1 to 4

7 to 11

14 to 17

Number of days after implantation Fig. 1. Mean ± s.e. probability that a tagged Ophiodon elongatus ( , n = 12) or an untagged control ( , n = 12) was observed swimming (as opposed to stationary) after release into an observation tank (NS, not significant, P > 0·05).

RESULTS No O. elongatus died as a result of tagging. Tagged O. elongatus swam less than control O. elongatus in the first week but not in subsequent weeks (Fig. 1; week 1: Wilcoxon test, Z = −3·73, n = 24, P < 0·001; week 2: Wilcoxon test, Z = −0·06, n = 24, P > 0·05; week 3: Wilcoxon test, Z = −0·92, n = 24, P > 0·05). Tagged O. elongatus also ate fewer pellets than control O. elongatus in the first week but not in subsequent weeks (Fig. 2; week 1: Wilcoxon test, Z = −3·25, n = 24, P < 0·01; week 2: Wilcoxon test, Z =−2·17, n = 24, P > 0·05; week 3: Wilcoxon test, Z = −1·01, n = 24, P > 0·05). Differences in feeding between tagged and control O. elongatus in week 2 were significant before, but not after, the Bonferroni correction for the three weekly comparisons. Ophiodon elongatus from the tagged group were heavier than controls (Wilcoxon test, Z = 2·68, n = 24, P < 0·01). For both tagged and control groups, body mass did not correlate with feeding or swimming activity in any week (all P > 0·05; Table I). The number of sections explored at week 6 had a mean of 7·3 (range: 2–9) for both tagged and control O. elongatus (Wilcoxon test, Z = 0·00, n = 24, P > 0·05). Dispersal from release locations in Puget Sound was greater in early-tagged O. elongatus than recently tagged O. elongatus on the first day after release (28 January) but not significantly different between groups at 6 days after release (2 February), when only one O. elongatus remained at the release site (Fig. 3; day 1: Wilcoxon test, Z = 2·29, n = 45, P < 0·05; day 6: Wilcoxon test, Z = −0·41, n = 45, P > 0·05). All O. elongatus had dispersed by the next tracking day (23 February). Once an O. elongatus dispersed, it was never again detected within the four concentric mobile tracking routes surrounding its release site. The early-tagged group was heavier than the recently tagged group at the time of release (Wilcoxon test, Z = −3·58, n = 45, P < 0·001). On day 1 of the survey, body size did not affect dispersal of early-tagged O. elongatus (Wilcoxon test, Z = 0·42, n = 37, P > 0·05; sedentary O. elongatus: mean = 125·0 g, range=92·8–160·1 g; dispersing O. elongatus: mean = 118·9 g, range = 68·4–182·9 g) or of recently Published 2013. This article is a U.S. Government work and is in the public domain in the USA. Journal of Fish Biology 2013, 82, 1848–1857

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Number of pellets eaten per day

6

NS

5

P < 0·01

NS*

1 to 4

7 to 11

4 3 2 1 0

14 to 17

Number of days after implantation Fig. 2. Mean ± s.e. number of pellets eaten per tagged Ophiodon elongatus ( , n = 12) or per untagged control ( , n = 12) after release into an observation tank. Ophiodon elongatus were not fed for the first few days after tagging to minimize stress on the sutures. *, the effect 7–11 days after tagging was significant (P < 0·05) before, but not after, the Bonferroni correction for multiple comparisons (NS, not significant, P > 0·05).

tagged O. elongatus (Wilcoxon test, Z = −0·14, n = 8, P > 0·05; sedentary O. elongatus: mean=83·9 g, range = 72·5–97·4 g; dispersing O. elongatus: mean = 85·3 g, range = 72·0–101·2 g).

DISCUSSION Tagging with acoustic telemetry tags temporarily reduced the activity of hatcheryreared O. elongatus under laboratory conditions and detection of a tag effect Table I. Results from Spearman rank correlations (ρ) testing for an effect of Ophiodon elongatus size on feeding or swimming behaviour. Results are shown before (P ) and after (P b ) Bonferroni correction Behaviour, treatment Feeding, control

Feeding, implant

Swimming, control

Swimming, implant

Week 1 2 3 1 2 3 1 2 3 1 2 3

ρ −0·30 −0·15 −0·39 −0·05 −0·05 −0·04 0·39 −0·53 0·31 0·36 0·34 −0·07

n

P

Pb

12 12 12 12 12 12 12 12 12 12 12 12

>0·20 >0·50 >0·20 >0·50 >0·50 >0·50 >0·20 >0·05 >0·20 >0·20 >0·20 >0·50

>0·99 >0·99 >0·50 >0·99 >0·99 >0·99 >0·50 >0·20 >0·99 >0·50 >0·50 >0·99

n, sample size. Published 2013. This article is a U.S. Government work and is in the public domain in the USA. Journal of Fish Biology 2013, 82, 1848–1857

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NS

Percent gone from release site

100 P < 0·05 80 60 40 20 0

1

6

Number of days after release Fig. 3. Per cent of recently tagged Ophiodon elongatus ( , n = 8) and O. elongatus given 22 days to recover from tagging before release ( , n = 37) that were no longer detected near the release site 1 and 6 days after release into Puget Sound (NS, not significant, P > 0·05).

depended on the duration between surgical tagging and testing under natural conditions. In the laboratory, tags caused O. elongatus to reduce feeding and swimming activity during the first week after tagging but no effects on feeding, swimming activity or exploratory behaviour were found in subsequent weeks. Similarly in the field, recently tagged O. elongatus showed reduced movement compared to O. elongatus that had been held longer before release. The laboratory and field data indicate that O. elongatus and perhaps some other species should be held for at least 1 week after tagging. This might be most practical for hatchery-reared fishes that can be returned to their rearing vessels for an adequate period of time prior to release. For fishes captured from the natural environment that must be returned soon after tagging, natural movement may be initially impaired as a result of tagging and data from at least the first week should be interpreted cautiously. There are several potential stressors associated with acoustic telemetry (Jepsen et al ., 2002). Temporary effects on feeding and movement in tagged fishes may result from surgery stress (e.g. healing after incisions and sutures) or stress caused by the tag itself (e.g. buoyancy adjustment or adjustment to the presence of a new mass in the body). Effects due to surgery stress may potentially be overcome with alternate attachment methods (e.g. intragastric or external attachment), although these methods also introduce different potential complications and limitations (Bridger & Booth, 2003). The comparative nature of the field study allowed exclusion of the possibility that the reduced movement was due to release stress, as both early-tagged and recently tagged O. elongatus underwent the same release procedure. Release stress may very well have affected movement beyond the differences observed between recently tagged and early-tagged O. elongatus. A test for release stress would require a different experimental design to the one used in this study (Sulikowski et al ., 2006; Jepsen et al ., 2008). The differences between groups in both the laboratory and the natural environment were probably caused by treatment effects and not by differences in body size. Controls (laboratory study) and recently tagged individuals (field study) were smaller Published 2013. This article is a U.S. Government work and is in the public domain in the USA. Journal of Fish Biology 2013, 82, 1848–1857


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(mean) than, but still within the size range of, tagged individuals (laboratory study) and early-tagged individuals (field study). Also, body size did not correlate with laboratory swimming, laboratory feeding or field post-release movement behaviour, so there is no indication that body size differences caused the effects observed in this study. Furthermore, the laboratory and field work revealed temporary effects. If behavioural differences were due to body size differences, the behavioural differences should have persisted through time. Tag mass in this study never exceeded 3% of body mass. Body size effects may become important at greater relative tag masses (Brown et al ., 1999; Jepsen et al ., 2002; Chittenden et al ., 2009). The absence of an acoustic signal was interpreted as movement away from a release site. In certain environments, such as rocky reefs, structure can block signal transmission (e.g. when a fish enters a crevice between rocks; Heupel et al ., 2006; Simpfendorfer et al ., 2008). Several factors, however, indicate that interference from rocky reefs was not a significant problem in this study. First, wild and hatchery O. elongatus are not known to associate with structure until their second year of life or later (Cass et al ., 1990; Martell et al ., 2000; Lee et al ., 2011,). Second, in a related analysis of this study’s releases (Lee et al ., in press), O. elongatus detection did not differ among structured, barren and shallow habitats. If the rocky reefs interfered with signal transmission, there should have been lesser detections in structured habitats than in barren and shallow habitats. Third, only one of the three release sites contained significant structure. Fourth, despite mobile tracking at 1 day, 1 week, 4, 16, 36 and 52 weeks after release, none of the 45 released O. elongatus were ever redetected at the release sites after being classified as absent. If the O. elongatus were actually present but the signal was temporarily obstructed by structure, then they probably would have been detected on a subsequent mobile tracking day. Fifth, the circular mobile tracking routes allowed the hydrophone to experience a range of orientations to any O. elongatus present within the tracking routes, thus improving the likelihood that an O. elongatus present next to structure would be detected. Finally, dispersal by subyearling, wild and hatchery O. elongatus is a normal part of their life history (Cass et al ., 1990; Lee et al ., in press). This study combined laboratory and field studies to overcome some of the limitations of laboratory-only and field-only studies. The simple laboratory environment was used to compare tagged O. elongatus to untagged controls. The effect on movement in the laboratory was then confirmed in the comparative (early-tagged v . recently tagged individuals) field experiment, which was made possible by the transient nature of the laboratory tag effect. As transient tag effects have been demonstrated for other species in the laboratory, this experimental design may be possible in many other species. As far as is known, this is the first study to demonstrate a telemetry tag effect on movement in the field using a comparative method. While results may vary among response variables (Jepsen et al ., 2005), holding conditions (Oldenburg et al ., 2011), species (Jepsen et al ., 2005), source (wild v . hatchery; Peake et al ., 1997), tag attachment method (Berejikian et al ., 2007) and tag-to-bodymass ratio (Chittenden et al ., 2009), this study suggests that movement in laboratory studies can correlate with actual field movement and provides a comparative method for testing tag effects in the field. The authors thank T. Wright (Northwest Indian Fisheries Commission) and the dive teams led by O. Eveningsong (Washington Department of Fish and Wildlife) and M. Racine (Washington SCUBA Alliance) for egg collections. Ophiodon elongatus rearing and husbandry Published 2013. This article is a U.S. Government work and is in the public domain in the USA. Journal of Fish Biology 2013, 82, 1848–1857

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were conducted by M. Cook and J. Atkins. J. Atkins, K. Doctor, R. Endicott and M. Moore occasionally assisted with field surveys. Funding was provided by the Science Consortium for Ocean Replenishment (SCORE), the Washington Department of Fish and Wildlife’s Puget Sound Recreational Fisheries Enhancement Fund and NOAA Fisheries.

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Published 2013. This article is a U.S. Government work and is in the public domain in the USA. Journal of Fish Biology 2013, 82, 1848–1857