© 2005 International Council for the Exploration of the Sea
Recuperation and behaviour of Pacific cod after barotrauma
a National Marine Fisheries Service, Alaska Fisheries Science Center, Resource Assessment and Conservation Engineering Division 7600 Sand Point Way NE, Seattle, WA 98115-0070, USA
b National Marine Fisheries Center, NOAA Fisheries 301 Research Court, Kodiak, AK 91615, USA
*Correspondence to D. G. Nichol: tel: +1 206 526 4538; fax: +1 206 526 6723. e-mail: dan.nichol{at}noaa.gov.
A total of 624 Pacific cod was captured, tagged with data-storage tags, and released in the Gulf of Alaska and eastern Bering Sea from 2001 to 2003. Cod were captured with pot or jig gear at depths ranging from 32 to 127 m. As of January 2004, 272 tags (44%) were recovered, with fish at liberty from 2 days to 1.5 years. The tags, which collected time, depth, and temperature information, revealed behaviour patterns common to nearly all recaptured fish. Analysis of swimbladder function suggests that these patterns resulted from swimbladder ruptures and deflation. In most cases, fish immediately dived to the bottom and then, within hours, returned to shallower depths. Fish that subsequently descended back to the depth at which they were captured, did so at rates ranging from 4.9 to 23.2 m day–1. Observations of bubbles being released from cod as they neared the surface during capture, indicated that cod swimbladders can rupture. A series of X-rays taken of live cod immediately after capture and subsequently at 24 h, revealed that ruptured swimbladders were sealed within 24 h. The loss of gas from the swimbladder, and the subsequent loss in buoyancy, inhibited most cod from remaining near the bottom. Their quick return to shallow water after an initial escape response indicates either a need or preference to reside at a depth at which they are more neutrally buoyant. Although rates of descent were highly variable among individuals, smaller individuals tended to descend faster than larger ones. Rates of descent were most likely limited by the secretion rate of gas into the swimbladder. Future tagging work for species such as Pacific cod need to recognize the recuperation period that is necessary before natural vertical or horizontal migrations can be evaluated.
Keywords: barotrauma, behaviour, buoyancy, cod, data-storage tags, migration, swimbladder
Received 30 December 2004; accepted 4 May 2005.
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Introduction |
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 Top Introduction Material and methodsResultsDiscussionReferences |
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Tagging studies on Pacific cod (Gadus macrocephalus) in Alaska have been conducted as a means of understanding their seasonal movements (Shimada and Kimura, 1994). Such knowledge is essential background to assessments of the impact that commercial fisheries have on the cod resource and on the species that forage on cod. Pacific cod have been one of the most commercially important fish in Alaska with annual catches over the last 10 years averaging 64 093 t in the Gulf of Alaska (Thompson et al., 2003) and 180 188 t in the eastern Bering Sea and Aleutian Islands' region (Thompson and Dorn, 2003). In the last few years, the cod resource has come under increased fishery regulation in the form of area closures, owing to fisheries interactions with the endangered Steller sea lion (Fritz et al., 1995). The placement and efficacy of these closures require an understanding of how migration patterns of Pacific cod affect time and space interactions of Steller sea lions, Pacific cod, and commercial fisheries.
Tagging studies which capture fish from great depth risk inflicting injuries that can affect the natural behaviour of the fish. "Barotrauma", defined here as the physical trauma resulting from a rapid reduction in pressure, is common among fish captured from depth, particularly among those with physoclistous swimbladders such as Pacific cod. While abrasion-induced injuries can be minimized with certain capture methods (e.g. pot or hook and line), injuries derived from barotrauma are difficult to avoid. Such injuries can include bloated eyes, everted stomachs, and ruptured swimbladders. Before seasonal-migration patterns or more specific vertical-migration patterns can be fully examined, we must first assess whether or not the tagging process introduces abnormal behaviour.
Studies have shown how the extent and rates of vertical migration in Atlantic cod (Gadus morhua) are limited by physical laws that relate to buoyancy and the physiological process of secretion and resorption of gas into and from the swimbladder (Tytler and Blaxter, 1973; Blaxter and Tytler, 1978; Harden Jones and Scholes, 1985; Arnold and Greer-Walker, 1992). Given that Atlantic cod are closely related to Pacific cod (Cohen et al., 1990; Westrheim, 1996), behavioural similarities in their response to tagging and the effects of barotrauma might be expected. Here, the patterns of vertical movement immediately after tagging, the time and rate at which cod return to their depth of capture, and the effects of capture on the swimbladder are examined. The discussion relates cod behaviour to the function of the swimbladder, with particular reference to research previously conducted on Atlantic cod.
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Material and methods |
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Tagging procedure
A total of 624 Pacific cod was tagged with electronic data-storage tags (see specifications below) off Kodiak Island in the Gulf of Alaska, and off Unimak Island in the eastern Bering Sea from 2001 to 2003 (Figure 1; Table 1). There were two release sites off Kodiak Island, viz. inside Kupreanof Strait and near Ugak Bay, and three off Unimak Island, viz. off Cape Sarichef, off Amak Island, and off Akun Island.
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Cod were initially captured with pots and hook and line gear at bottom depths ranging from 32 to 127 m near Unimak Island (Table 1). The pots were steel-framed with dimensions of 2.1 x 2.1 x 0.9 m or 2.3 x 2.3 x 1.2 m, and 4 x 4-cm to 6 x 6-cm stretched nylon mesh. They were "soaked" during both daylight and night-time hours from 5.2 to 22 h off Kodiak Island and from 3.8 to 102 h off Unimak Island. Both the pots and the hook-and-line gear were retrieved at a minimum rate of 20 m min–1. The captured cod were transferred to a tank supplied with running seawater and were retained in the tank only long enough to determine if they could maintain buoyancy near the bottom of the tank without apparent difficulty and if they lacked serious external damage.
Data-storage tags were attached externally, beneath the anterior dorsal fin, using 0.5 mm stainless-steel wire as described in Nichol and Somerton (2002). The cod were measured to the nearest centimetre total length (TL). Sizes of tagged cod ranged from 49 to 85 cm TL. The fish were released at the site of initial capture immediately after tagging.
Tag specifications
The data-storage tags were of the Lotek Wireless LTD-11001 type and recorded pressure (depth) and temperature. The tags had a maximum recording depth of 600 m, with accuracy of ±1.5 m if fish remained in less than 150 m, ±3 m if fish depth exceeded 150 m, and ±6 m if fish depth exceeded 300 m. Water temperature was recorded with an accuracy of ±0.3°C. The frequency of data recordings decreased with time at liberty, starting at 14-s intervals and decreasing to 30-min intervals after 341 days. The average recording interval for tags in this study was 13 min.
Tag recovery
Tagged fish were captured in commercial trawl, pot, longline and jig fisheries. A cash reward was paid as an incentive for returning the tags. Capture information included latitude, longitude, depth, and date of capture. Specimen information included fish length, sex, and fish weight.
Definition of recuperation
To define recuperation parameters used in subsequent analysis, a description of the general behaviour patterns exhibited by Pacific cod after release is provided here. Cod typically display a short-term, post-tagging behaviour involving a rapid descent to the bottom and return to shallow water, followed by a more gradual descent (Figure 2). Descents after fish release were categorized into three types: ‘A’ if the cod gradually descended to at least the sampling depth; ‘B’ if a gradual descent ended at a depth less than the sampling depth; and ‘C’ if the descent was not gradual and cod spent most of the time near the bottom soon after release. Date, time, depth, and temperature were recorded at common behaviour junctures such as the end of "escape dives" after release, the shallow-water point prior to gradual descents, and the point at which a cod's descent stopped (Figure 2).
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The recuperation-end date was defined as the date and time at which a cod no longer exhibited a consistent descent, or when a cod's descent reached the sampling depth. The recuperation period (RP) was defined as the period between fish release and the recuperation-end date. The depth at recuperation was calculated as the average tag depth for the 24 h following the recuperation-end date. The period prior to gradual descents (PP) was also examined (Figure 2).
Analysis of descent rate and recuperation period
Curves used to describe gradual descents (Descent types A and B) were fitted to the 12 most shallow depth/times within each 24-h day, excluding extreme surface-directed movements (Figure 2). Only data where descents were continuous were included. If descents were stepped, only the first step was included. Linear and quadratic equations were fitted to the depth and elapsed-time data as follows:
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is the error term. The significance (p < 0.05) of the quadratic term, ß2(days)2, was used to determine if descents were curvilinear in nature. Linear descent rates were described by ß, the slope of the fitted linear equation. Curvilinear descent-rate values were estimated by the average of the instantaneous slopes along the descent curve.
Multiple linear regression (S-PLUS, 2000) was used to relate the recuperation period (RP), the period prior to descent (PP), and the descent rate (DR) to other factors as follows:
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i is the normally distributed error, and 
, 
, 
, 
, 
, 
, and 
are coefficients. The factor site refers to one of the five release sites and temperature is the mean temperature during the period examined for each tag. Descent curvature denotes whether descents were linear or curvilinear in nature. Interaction effects were also tested. Least significant (p > 0.05) variables and interactions were removed from the model in a backward stepwise manner. Residuals were examined to test the assumption that errors were normally distributed.
Swimbladder examination
Live, adult Pacific cod were captured off Kodiak Island using pot and trawl gear at depths greater than 90 m and held in the laboratory at the Kodiak Fisheries Research Center during October and November 2002. Radiographic images (soft X-rays), which highlight gas-filled swimbladders in fish (Gosline, 1948; Horne and Clay, 1998), were taken of 15 individual cod every other day over a period of seven days. Each cod was anaesthetized using clove oil, and radiographic images of the live cod were taken from the lateral orientation using a mobile veterinarian X-ray unit (XTEC Laseray 90P portable veterinary unit). Initial X-rays were taken 24 h after capture for 11 of the cod, and 30 min after capture for the remaining four fish.
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Results |
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As of January 2004, 272 of the 624 tags deployed on Pacific cod had been recovered. A total of 247 tags functioned long enough to examine Pacific cod "recuperation" behaviour after tagging and release (Table 1).
Common behaviour patterns
Most cod began an "escape dive" immediately after release (Figure 2; Table 2). In all, 51% of these dives were to within 10 m of the initial-capture depth (or bottom) and lasted an average of 1.3 h in duration.
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A total of 85% of the cod underwent a gradual descent (Descent types A and B; Figure 3) after the initial escape dive and return to the surface (Table 2). The remaining fish (15%) underwent an acute descent and spent most of the "recuperation period" near the bottom (Descent type C; Figure 3). Among cod that underwent gradual descents, most (77%) did so in a curvilinear route (Table 2). Significant negative quadratic terms ß2(days)2 in the quadratic-descent equation indicated a slowing of the descent in 65% of these cod, and significant positive terms indicated an increase in descent rate for 12% of these cod (Table 2).
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Vertical excursions (e.g. >5 m) away from the gradual descents (or fitted curves) were almost exclusively towards deeper water (Figure 2). Although rare, some cod did undergo short-term, surface-directed excursions away from the gradual-descent line, but only after gradual descents were deeper than 50–60 m.
Descent-type differences among release sites
Percentages of the three descent types differed between the five release sites. Most noticeably, the westernmost release site (near Akun Island; Figure 1) had a much higher prevalence (61%) of cod that did not undergo a gradual descent (Descent type C) than the others (Table 2). Most of the cod released near Akun Island dived to the bottom immediately after release, but unlike most released at the other sites, they managed to stay near the bottom (Figure 3c). The 39% of cod released off Akun that did return to shallow water prior to a gradual descent, took longer to do so (1.1 days on average) than cod released off Sarichef (0.75 days), Amak (0.73 days), Kupreanof (0.61 days), or Ugak (0.51 days).
Descent type related to fish length
Cod that gradually descended to at least the sampling depth (Descent type A), were on average larger than cod whose gradual descent either fell short of the sampling depth (Descent type B), or those that stayed on or near the bottom immediately after release (Descent type C) (Figure 4). A two-way ANOVA relating fish length to the descent types observed within each release site confirmed that cod that stayed near the bottom soon after release (Descent type C) were generally smaller than those that underwent gradual descents (Figure 4).
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Descent rate and recuperation period
Descent rates (DR) ranged from 4.9 to 23.2 m day–1 for cod that underwent gradual descents to at least the depth at which they were originally sampled (Figure 5). Smaller cod tended to descend faster than larger cod (Table 3). Cod captured and released near Akun Island tended to descend faster than the other four release sites. Males descended slightly slower than females. Neither water temperature nor sampling depth appeared to have an effect on descent rate. Descent rates and recuperation periods were highly variable among individuals (Tables 3 and 4; Figures 5 and 6).
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The recuperation period (RP) ranged from 1.6 days (sampling depth = 30 m) to 16.7 days (sampling depth = 100 m) for cod that gradually descended to the sampling depth (Descent type A, n = 112). For cod that gradually descended (Descent types A or B), the recuperation period was significantly dependent upon the depth of recuperation and fish length (Table 4). Smaller cod tended to recuperate faster than larger cod. No differences were found among the five release sites or among sexes, and water temperature had no apparent effect on the recuperation period (Table 4).
The period prior to gradual descent (PP), ranged from 1 h to 5.2 days and averaged 15.4 h among cod with Descent types A or B (Figure 6). None of the factors or interactions tested had a significant (p > 0.05) influence on PP.
Multiple recaptures
Three cod, two from the Kupreanof releases and one from off Unimak Island (Akun) were captured and released twice before their final capture (Figure 7). This allowed a comparison of behaviours between first and second releases for the same fish. Data from tag 210 indicated that this cod essentially did not undergo a gradual descent after the second release, remaining instead in relatively shallow water (<50 m) (Figure 7). Cod 145 descended slower after its second release (6.2 m day–1) than after its first release (9.6 m day–1), as did Cod 1344, which descended at 4.3 m day–1 after its second release and 13.4 m day–1 after its first.
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Laboratory results of swimbladder examination
Radiographic images of cod 24 h after capture showed inflated swimbladders. Therefore, if swimbladders had sustained any damage, they had been repaired within the first 24 h. Among the four cod for which radiographic images were taken 30 min after capture, only one (cod 9, 72 cm TL) showed evidence of a deflated swimbladder. After 48 h, the deflated swimbladder in this cod had increased in size. After 90 h, the swimbladder had been restored to an expanded shape (Figure 8). This cod survived in the live tank for another 4 days (168h after capture) with a fully inflated swimbladder. The cause of mortality is unknown but a post-mortem dissection of this fish showed a fully intact and inflated swimbladder.
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Discussion |
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Knowledge of the effect of the tagging process and the time required to recuperate from it is an important prerequisite to understanding natural migration patterns. Pacific cod display behaviour patterns that can be attributed to barotrauma suffered during the tagging process. These often include an initial escape dive to the bottom, followed by a quick return to shallow water, and a gradual descent back to the bottom (Figure 2). Recuperation can take from 2 to 17 days depending on the depth to which the fish are returning. Much of this time is spent in midwater, as opposed to the cod's natural habitat near the bottom. Because the same post-release behaviour has been observed for Atlantic cod (Arnold and Greer-Walker, 1992; Thorsteinsson, 1995; Godø and Michalsen, 2000; Heffernan et al., 2004), common physiological reasons for this behaviour are suspected. This behaviour is mostly attributable to the loss of gas from the swimbladder, the resulting change in buoyancy, and the subsequent refilling of the swimbladder.
Swimbladder rupture
Given the depths of capture and the rate of the capture ascents, most if not all of the cod in this study ruptured their swimbladder during the ascent phase. Three lines of evidence support this statement. First, bubbles were observed rising from cod as the capture gear (pots and hook and line) approached the surface. Second, swimbladders do not have the elastic properties (Sand and Hawkins, 1974) to resist rupture given the rate and depth from which these cod were retrieved. Natural ascent rates are limited by the rate at which cod can resorb gas from the swimbladder (Harden Jones and Scholes, 1985). A pressure change from 8 to 1 ATA, equivalent to a cod brought to the surface after being neutrally buoyant at 77.5 m, would require at least 10 h of decompression time in order to avoid rupturing the swimbladder (Tytler and Blaxter, 1973). Considering that reductions of pressure greater than 50% can result in swimbladder ruptures for Atlantic cod (Tytler and Blaxter, 1973), ruptures would be expected for cod captured (and acclimated) at depths greater than 30 m. Finally, the behaviour of cod after release is consistent with fish that have lost gas from the swimbladder. If the cod had not ruptured their swimbladders, the expectations are that they would return to and stay at the depth near bottom where they were captured and near neutrally buoyant. Instead, most cod returned to shallow water. The loss of gas rendered cod less buoyant, so neutral buoyancy occurred closer to the surface instead of near the capture depth.
Swimbladders in Pacific cod do not entirely deflate after rupture. Radiographic images of Pacific cod taken 24 h after capture (n = 11) and 30 min (n = 4) after capture revealed inflated swimbladders in all but one fish. These cod were captured from depths >90 m and retrieved at a rate (>20 m min–1) that certainly would have ruptured their swimbladders. The secretion process via the gas gland is a slow process [e.g. Atlantic cod are known to take 10 h to inflate their swimbladder in shallow water after deflation (Scholander et al., 1956; Wittenberg et al., 1964)]. Therefore, it is highly unlikely that inflation via secretion accounted for the inflated swimbladders, particularly after only 30 min. The one Pacific cod in this study whose swimbladder did deflate (Figure 8) took >48 h to re-inflate its swimbladder while in a 2-m deep tank. If ruptures were relatively small, a rapid repair might be expected. Shasteen and Sheehan (1997) reported that largemouth bass (Micropterus salmoides) are capable of healing their swimbladders within 17 h of a 0.5-cm hole being made in the swimbladder. Those bass whose swimbladders were punctured with a needle were neutrally buoyant immediately after gas release. Ruptures in Pacific cod swimbladders must have been sufficiently small that they did not entirely deflate.
Factors that affect descent rate and recuperation
The rate of the gradual descent of a cod after release is consistent with the rate of gas-gland secretion necessary to maintain neutral buoyancy. Harden Jones and Scholes (1985) indirectly calculated the rate of gas secretion in small Atlantic cod (25–50 cm), which corresponded to a descent rate of 0.066T + 0.25 mA h–1 (Arnold and Greer-Walker, 1992) where T = temperature. Given the temperatures observed during descents in this study (2.0–6.7°C), the calculated rates of descent based on the secretion rate for Atlantic cod range from 9.2 to 16.6 m day–1. These rates correspond to both natural (Arnold and Greer-Walker, 1992) and post-release (Thorsteinsson, 1995; Heffernan et al., 2004) descents. Gas-gland secretion rates, shown to be dependent on fish size (Harden Jones and Scholes, 1985), may account for the observed relationship between descent rate and cod length (Tables 3 and 4; Arnold and Greer-Walker, 1992). Although secretion rates for Pacific cod may differ from those of Atlantic cod, it is possible that the observed descent rates in this study (4.9–23.2 m day–1) are mostly a function of the rate of gas secretion. In this scenario, the swimbladders were functional as soon as the cod began their gradual descent.
The descent rates, in part, reflect the variability of secretion rates, but the site-specific factors and perhaps the severity of injury also contribute to this variability. Cod released off Akun Island descended significantly faster than cod from other areas (Table 3). Akun-released fish also had a greater tendency to acutely descend and stay near the bottom (Table 2 and Figure 3C), rather than undergo a gradual descent. It is suspected, in these cases, that cod migrate to the bottom and cope with being negatively buoyant for some time until gas secretion into the swimbladder has compensated for the pressure change. It is unclear why Akun cod were more likely to stay at the bottom. The fact that a greater percentage of smaller fish appeared to forego a gradual descent than larger fish (Figure 4) may indicate that smaller fish were more capable of coping with being negatively buoyant. Given that cod captured more than once descended more slowly after the second capture, the severity of injury – assuming that a second rupture of the swimbladder compounds the injury from the first – may also affect the rate of descent.
Both water temperature and the depth of capture were expected to influence either the descent rate or the time of recuperation, but they did not do so. Experiments have shown a direct relationship between water temperature and the rate of gas secretion into the swimbladder (McNab and Mecham, 1971; Harden Jones and Scholes, 1985). It was therefore expected that descent rates would increase with increasing temperature. However, the lack of a significant temperature effect in this study (Tables 3 and 4), may reflect the narrow range of temperatures observed here (2.0–6.7°C) compared with the experimental ranges (0–17°C) tested for Atlantic cod. The temperature ranges that individual cod encountered during descents were quite small, varying by less than 0.7°C per descent. Recuperation periods were expected to increase with increasing depths of capture, but no relationship was found (Table 4). Therefore, while a rupture of the swimbladder and subsequent post-release behaviour should be expected for cod captured at depths exceeding 30 m, the severity of injury does not necessarily increase with increasing depths of capture.
Why are gradual descents curvilinear?
The decrease in gradual-descent rates, observed for most of the cod in this study, is attributed to the process of diffusion or leakage of gases from the swimbladder (Denton et al., 1972; Lapennas and Schmidt-Nielson, 1977; Ross, 1979; Strand et al., 2005). Because this leakage increases with increasing depth, and secretion rates are independent of depth, the net rate of gas accumulation in the swimbladder decreases with increasing depth (Strand et al., 2005). Consequently, if cod choose to descend at the maximum rate while maintaining constant (e.g. neutral) buoyancy, descent rates should decrease with increasing depth. For the minority of cod whose gradual-descent rate increased with increasing depth, we offer two possibilities. Some, we suggest, chose initially to descend at less than the maximum rate, while maintaining constant buoyancy, then increased their rate as depth increased. Others descended at a rate that exceeded the capacity for them to maintain a constant buoyancy and compensated for a changing buoyancy in other ways (e.g. hydrostatic lift).
Explanation of short-term excursions
Short-term excursions away from the "gradual-descent curve" were most often towards the bottom, and rarely towards the surface (Figure 2). Assuming the gradual-descent curves represent the depth at which cod are neutrally buoyant, the absence of surface-directed movements can be explained by the concept of "free vertical range" as defined by Arnold and Greer-Walker (1992). Cod that undergo vertical movements that occur faster than they can compensate for, via either gas secretion (gas gland) or gas resorption (oval) into or from the swimbladder, are subject to changes in buoyancy. Changes in buoyancy are more severe per unit change in depth in shallow water than in deeper water. A quick vertical excursion away from a depth at which a cod is neutrally buoyant will be more difficult or more energetically costly in shallow water than in deeper water. With rapid movements towards the surface, cod risk another rapid expansion and rupture of the swimbladder, and they risk the chance of an uncontrolled ascent. With quick vertical movements towards the bottom, cod must cope with negative buoyancy, but there is no risk of further injury to the swimbladder. Furthermore, the bottom can be viewed as the "destination" where cod were originally captured. Quick excursions towards the bottom may indicate attempts to return to this destination. Given that Pacific cod commonly feed on demersal prey (Jewett, 1978), downward excursions may be necessary to satisfy feeding requirements.
When are cod recuperated?
Recuperation in Pacific cod can be considered complete only after they have returned permanently to a near-bottom habitat, and appear to have completely adapted their buoyancy to that depth. Even those cod that did not undergo a gradual descent and spent most of the time near the bottom soon after release usually exhibited the need to periodically migrate up to a depth that was, in all probability, close to neutral buoyancy (e.g. Figure 3c). Neither periodic excursions of this nature nor consistent gradual descents were evident after cod were at liberty longer than a month. Gradual descents illustrate a situation where cod are returning to a preferred depth after a loss of gas from the swimbladder and reduced buoyancy. Even though swimbladders are sealed and functional, cod are not considered fully recuperated at this point because most appeared unable to return successfully to their natural habitat.
Implications for future research
Future tagging studies of Pacific cod, and other species such as walleye pollock (Theragra chalcogramma) that also possess physoclistic swimbladders, are imminent. In the Bering Sea, where management of Pacific cod and walleye pollock has become a critical issue owing to possible fisheries interaction with endangered Steller sea lions (Fritz and Brown, 2005), knowledge of short-term fish movements between commercial-fishing locations and trawl-exclusion areas would be valuable (P. Munro, pers. comm.). This study documents the behaviour of Pacific cod after their capture from the depths they commonly inhabit, and demonstrates that although swimbladders commonly rupture, the event is not catastrophic and that they are quickly repaired. Furthermore, cod obviously survive the tagging process, and they appear to resume natural behaviour after a period lasting no longer than 23 days. Considering the depths at which Pacific cod commonly occur and the physical and physiological factors involved during capture ascents, it does not seem feasible to employ capture techniques designed to avoid swimbladder rupture. Consequently, the knowledge that a specific recuperation event will occur should help researchers evaluate future tag data, whether spaghetti or electronic tags are being deployed.
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Acknowledgements |
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We thank Dan Urban, Carrie Worton, Ron Kutchick, and Dave Kubiak for their efforts during the tagging charters off Kodiak, and Peter Munro, Sandi Neidetcher, Erica Fruh, Elaina Jorgenson, and Barney Baker for their help during the charter off Unimak Island. Dave Somerton made many helpful comments during analysis. We are indebted to John Horne and Jason Sweet for their training on and use of their radiographic equipment. Dusty Parsons, Jennifer Watson, and Russ Seither were invaluable during the tag-recovery process. We thank all the fishers and processing-plant personnel who helped retrieve the tags, and the personnel from the RV "Resolution" and FV "Fierce Allegiance" who were responsible for capturing cod prior to tagging. Dave Somerton, John Horne, Cliff Ryer, Gary Walters, and one anonymous reviewer provided constructive reviews of this manuscript.
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Footnotes |
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1 Reference to trade names does not imply endorsement by the National Marine Fisheries Service, NOAA.
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References |
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Arnold G.P. and Greer-Walker M. (1992) Vertical movements of cod (Gadus morhua L.) in the open sea and the hydrostatic function of the swimbladder. ICES Journal of Marine Science 49:357–372.
Blaxter J.H.S. and Tytler P. (1978) Physiology and function of the swimbladder. Advances in Comparative Physiology and Biochemistry 7:311–367.[Medline]
Cohen D. M., Inada T., Iwamoto T., Scialabba N. (1990) Gadiform fishes of the world (Order Gadiformes). An annotated and illustrated catalogue of cods, hakes, grenadiers and other gadiform fishes known to date. FAO Fisheries Synopsis, no. 125, vol. 10. 442 pp.
Denton E.J., Liddicoat J.D., Taylor D.W. (1972) The permeability to gases of the swimbladder of the conger eel (Conger conger). Journal of the Marine Biological Association of the United Kingdom 52:727–746.[Web of Science]
Fritz L.W. and Brown E.S. (2005) Survey- and fishery-derived estimates of Pacific cod (Gadus macrocephalus) biomass: implications for strategies to reduce interactions between groundfish fisheries and Stellar sea lions (Eumetopias jubatus). Fishery Bulletin US 103:501–515.
Fritz L.W., Ferrero R.C., Berg R.J. (1995) The threatened status of Steller sea lions, Eumetopias jubatus, under the Endangered Species Act: effects on Alaska groundfish fisheries management. Marine Fisheries Review 57:214–27.
Godø O.R. and Michalsen K. (2000) Migratory behaviour of northeast Arctic cod, studies by use of data-storage tags. Fisheries Research 48:127–140.[CrossRef][Web of Science]
Gosline W.A. (1948) Some possible uses of X-rays in ichthyology and fishery research. Copeia 1:58–61.
Harden Jones F.R. and Scholes P. (1985) Gas secretion and resorption in the swimbladder of the cod Gadus morhua. Journal of Comparative Physiology B 155:319–331.[CrossRef]
Heffernan O., Righton D., Michalsen K. (2004) Use of data-storage tags to quantify movements of cod: effects on acoustic measures. ICES Journal of Marine Science 61:1062–1070.
Horne J.K. and Clay C.S. (1998) Sonar systems and aquatic organisms: matching equipment and model parameters. Canadian Journal of Fisheries and Aquatic Sciences 55:1296–1306.
Jewett S.C. (1978) Summer food of the Pacific cod, Gadus macrocephalus, near Kodiak Island, Alaska. Fishery Bulletin US 76:700–706.
Lapennas G.N. and Schmidt-Nielson K. (1977) Swimbladder permeability to oxygen. Journal of Experimental Biology 67:175–196.
McNab R.A. and Mecham J.A. (1971) The effects of different acclimation temperatures on gas secretion in the swimbladder in the bluegill sunfish, Lepomis macrochirus. Comparative Biochemistry and Physiology 40A:609–616.[Medline]
Nichol D.G. and Somerton D.A. (2002) Diurnal vertical migration of the Atka mackerel Pleurogrammus monoterygius as shown by archival tags. Marine Ecology Progress Series 239:193–207.[Web of Science]
Ross L.G. (1979) The permeability to oxygen and the guanine content of the swimbladder of a physoclist fish, Pollachius virens. Journal of the Marine Biological Association of the United Kingdom 59:437–441.[Web of Science]
Sand O. and Hawkins A.D. (1974) Measurements of swimbladder volume and pressure in the cod. Norwegian Journal of Zoology 22:31–34.
Scholander P.F., Van Dam L., Ennes T. (1956) The source of oxygen secreted into the swimbladder of cod. Journal of Cellular and Comparative Physiology 48:517–522.[CrossRef][Web of Science]
Shasteen S.P. and Sheehan R.J. (1997) Laboratory evaluation of artificial swim bladder deflation in largemouth bass: potential benefits for catch-and-release fisheries. North American Journal of Fisheries Management 17:32–37.[CrossRef]
Shimada A.M. and Kimura D.K. (1994) Seasonal movements of Pacific cod, Gadus macrocephalus, in the eastern Bering Sea and adjacent waters based on tag-recapture data. Fishery Bulletin US 92:800–816.
S-PLUS. (2000) S-PLUS 2000 User's Guide. (Data-analysis products division, MathSoft, Seattle, WA).
Strand E., Jorgensen C., Huse G. (2005) Modelling buoyancy regulation in fishes with swimbladders: bioenergetics and behaviour. Ecological Modelling 185:309–327.[CrossRef][Web of Science]
Thompson G.G. and Dorn M.W. (2003) Assessment of the Pacific cod stock in the eastern Bering Sea and Aleutian Islands area. Section 2 in Stock-assessment and fishery-evaluation report for the groundfish resources of the Bering Sea/Aleutian Islands region. Available from North Pacific Fishery Management Council, 605 West 4th Ave., Suite 306, Anchorage, AK 99501.
Thompson G.G., Zenger H.H., Dorn M.W. (2003) Assessment of the Pacific cod stock in the Gulf of Alaska. Section 2 in Stock-assessment and fishery-evaluation report for the groundfish resources of the Gulf of Alaska. Available from North Pacific Fishery Management Council, 605 West 4th Ave., Suite 306, Anchorage, AK 99501.
Thorsteinsson V. (1995) Tagging experiments using conventional tags and electronic data – storage tags for the observations of migration, homing and habitat choice in the Icelandic spawning stock of cod. ICES Document CM 1995/B: 19. 16 pp.
Tytler P. and Blaxter J.H.S. (1973) Adaption by cod and saithe to pressure changes. Journal of Sea Research 7:31–45.
Westrheim S.J. (1996) On the Pacific cod (Gadus macrocephalus) in British Columbia waters, and a comparison with Pacific cod elsewhere, and Atlantic cod (G. morhua). Canadian Technical Report of Fisheries and Aquatic Sciences 2092: 390 pp.
Wittenberg J.B., Schwend M.J., Wittenberg R.A. (1964) The secretion of oxygen into the swimbladder of fish. Journal of General Physiology 48:337–355.
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