Behavioral impairment after escape from trawl codends may not be limited to fragile fish species

Fisheries Research 66 (2004) 261–269

Behavioral impairment after escape from trawl codends may not be limited to fragile fish species Clifford H. Ryer a,∗ , Michele L. Ottmar a , Erick A. Sturm b a

b

Fisheries Behavioral Ecology Program, Alaska Fisheries Science Center, NMFS, NOAA, Hatfield Marine Science Center, Newport, OR 97365, USA Southwest Fisheries Science Center, NMFS, NOAA, 110 Schaffer Road, Santa Cruz, CA 95060, USA Received 4 February 2003; received in revised form 11 June 2003; accepted 9 July 2003

Abstract Field studies indicate great variability between fish species in their susceptibility to direct mortality resulting from stress incurred during entrainment and escape through trawl codends. Moreover, stressors that do not directly kill fish may still cause indirect mortality, such as behavioral impairment leading to predation. However, it is unknown whether resistance to direct mortality also imparts resistance to behavioral impairment. Juvenile sablefish Anoplopoma fimbria are more resistant to direct mortality resulting from physical damage and stress than are walleye pollock Theragra chalcogramma. We measured juvenile sablefish resistance to behavioral impairment resulting from simulated trawl passage and compared results to those for walleye pollock, a species already studied. Juvenile sablefish (18–27 cm) were subjected to three levels of simulated trawl/escape stressors in the laboratory: (1) control: no stressors; (2) swim: forced swimming for 90 min at 0.33 m s−1 in a towed net, followed by escape through 8 cm square mesh; and (3) swim/pin: forced swimming for 60 min, then pinning against net meshes for 30 min, followed by 3 min crowding prior to escape. Subsequently, we examined sablefish behavior in the presence of a threatening but non-lethal predator (38–49 cm sablefish). In a second experiment, equal numbers of trawl-stressed and control fish were mixed and exposed to predation by a lingcod Ophiodon elongatus (62–87 cm). The first experiment demonstrated that sablefish suffered the same behavioral impairments as walleye pollock: stressed fish swam slower, shoaled less cohesively and allowed the predator to approach closer than did controls. In the second experiment all three levels of trawl stress caused fish to be consumed in greater numbers (by lingcod) than control fish, again, like walleye pollock. Therefore, although differing in susceptibility to potentially lethal stressors, both species exhibited similar impairments in response to sub-lethal stressors. This suggests that for numerous fish species, behaviorally impaired individuals escaping codends may be consumed by predators, contributing to unobserved mortality. Published by Elsevier B.V. Keywords: Unobserved fishing mortality; Bycatch; Stress; Predator–prey; Trawl escapees; Anoplopoma fimbria

1. Introduction It is becoming increasingly apparent that there may be unobserved mortality associated with many ∗ Corresponding author. Tel.: +1-541-867-0267; fax: +1-541-867-0136. E-mail address: [email protected] (C.H. Ryer).

0165-7836/$ – see front matter. Published by Elsevier B.V. doi:10.1016/S0165-7836(03)00197-8

commercial fisheries (Chopin and Arimoto, 1995; Alverson and Hughes, 1996; Crowder and Murawski, 1998). For many trawl fisheries, the expanded use of larger mesh sizes and square meshes, as well as other bycatch reduction devices (BRDs) means that many more undersized and non-target species are sorted from the catch at depth, never appearing on the deck of a boat. Field studies demonstrate that

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many undersized fish escaping trawls die from physical injuries and physiological impairment in the hours and days that follow (Suuronen et al., 1995, 1996ab; Sangster et al., 1996). Importantly, differences between species and fish sizes appear to be substantial. For example, Baltic cod Gadus morhua experienced 1% mortality (Suuronen et al., 1996a), haddock Melanogrammus aeglifinus and whiting Merlangius merlangius experienced 11–52% and 14–48% mortality, respectively (Sangster et al., 1996), while herring Clupea harengus experienced 30% mortality for large fish (12–17 cm) and 72% mortality for small fish (<12 cm) (Suuronen et al., 1996b). These studies demonstrate what is common knowledge among both fishers and researchers; that fish species have greatly differing abilities to withstand physical and physiological stress, and generalizations about escapee survival must be made with caution. While field studies have proven effective at estimating direct mortality resulting from an escapee’s passage through the trawl, there is scant information regarding another potentially important indirect source of mortality, that is, fish which become behaviorally impaired by their passage through the codend and subsequently succumb to predation. Although no field experiments have been conducted to examine this possible source of mortality, in laboratory experiments juvenile walleye pollock exposed to stressors simulating trawl passage were shown to be more vulnerable to predation by lingcod Ophiodon elongatus (Ryer, 2002). Thus, it is possible that current estimates of unobserved mortality may be low because they do not account for indirect predation related mortality. Since fish species differ in their susceptibility to mortality resulting from potentially lethal stressors, we hypothesized that they also differ in their susceptibility to behavioral impairment resulting from non-lethal stressors. For example, juvenile sablefish Anoplopoma fimbria are more “durable” than walleye pollock, in terms of their ability to survive rough physical treatment; juvenile sablefish, 15–19 cm total length (TL), can be towed for 15 min in a net at 0.95 m s−1 (pinned against the meshes) with no mortality 14 days later, whereas, comparably sized walleye pollock experience 100% mortality (Olla et al., 1997). Being less susceptible to physical trauma, we hypothesized that sablefish would also be less susceptible to stress-induced behavioral impairment than

walleye pollock. To address this hypothesis we present the results of two experiments examining the possible effects of trawl passage upon juvenile sablefish. In the first we exposed juvenile sablefish to stressors designed to simulate passage through a trawl and then monitored their behavior in the presence of a threatening, but non-lethal predator. We then compare these data to those previously acquired for walleye pollock, to determine whether the stressors had comparable effects upon the behavior of the two species. In the second experiment, we sought to determine whether stressors simulating trawl-passage made sablefish more vulnerable to predation and the approximate time until recovery. This was accomplished by combining trawl-stressed fish with unstressed fish and then exposing them to a lethal predator, allowing direct comparison of relative mortality. In addition to being a useful “model” species for studying the effects of stress upon fish survival and behavior (Davis, 2002), sablefish support a valuable fishery, with 26,000 MT landed in US and Canada during 1999 (FAO, 2002), at an ex-vessel value of approximately 100 million US dollars. Juvenile/undersized sablefish occur in modest numbers in the bycatch of a variety of bottom (personal observation) and midwater trawl fisheries (Sampson et al., 1997) with the potential for larger numbers of sub-yearling fish passing through codends unnoticed. 2. Material and methods 2.1. Non-lethal predation experiment Juvenile sablefish (18.3–26.6 cm TL) were subjected to a non-lethal but threatening larger sablefish predator (38–49 cm TL) after sequential exposure to stressors simulating those associated with entrainment and escape from a trawl. Anti-predator behavior was then monitored over a 72 h period. 18 h prior to exposure to experimental stressors, groups of 6 juvenile sablefish were transferred into 6 replicate 6400 L circular arenas (3 m diameter, 0.9 m depth), monitored by overhead video cameras. Arenas received a continuous flow of 9–11 ◦ C seawater and were illuminated by fluorescent lighting (4 ␮mol photons m−2 s−1 at water surface). The following morning, groups were subjected to one of three trawl-stress treatments: swim/pin, swim, and control.

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The swim/pin trials simulated sustained swimming followed by pinning against the meshes of the net, then crowding to simulate accumulating catch prior to escape through codend meshes. Sablefish were dip-netted from their arenas and transferred in a bucket to the net-towing apparatus (see Olla et al., 1997 for a complete description of the tow-tank design and Ryer, 2002 for details on the tow-net apparatus design). The net was towed at a speed of 0.33 m s−1 for 60 min. Because of the small size of this net, compared to a real trawl, relative (to the net) water velocity was 0.33 m s−1 throughout the net. In contrast, relative water velocity in a trawl decreases from the mouth to the codend. Assuming relative water velocity in the codend is 30% of that at the trawl mouth (Thiele et al., 1997), the 0.33 m s−1 at which fish were forced to swim in our apparatus would correspond to a trawl tow speed of approximately 1.0 m s−1 (2 knots). Given that tow speeds for commercial trawls generally range from 2 to 5 knots, this swim speed likely represents the low-end of what fish commonly experience in trawls, but was chosen in this, and the prior study of walleye pollock, as it assured that all fish would be able to swim in the confines of the net without becoming pinned against the meshes. The light level in the tow-tank was 1 ␮mol photons m−2 s−1 at water surface. During the tow, fish typically maintained position swimming in the center of the cylinder and/or in the front of the mesh sleeve. After 60 min, the tow was interrupted and the fish were gathered to the rear of the net sleeve. The net was cinched so that the fish were restricted to a smaller bag in which they were unable to swim, and were thus pinned against the meshes of the net when towed. The fish were then towed in this configuration at the same speed for an additional 30 min. Typical bottom trawl durations in north Pacific fisheries can range from 1 to 6 h, depending on depth and fish abundance. It is unknown how long individual fish swim in trawls, so this tow duration represents a best guess based upon data on sablefish swimming endurance (Olla et al., 1997), as well as published and personal observation of fish swimming behavior from video cameras mounted in trawl codends (Suuronen et al., 1996a,b). After towing, the cover of the tow net was removed and fish were gently poured into the crowding apparatus where they were subjected to a 3 min period of ‘crowding’, while they were transferred back to their arena. Briefly, the

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crowding apparatus consisted of a seawater chamber in which fish were confined to the spaces between water-filled balloons (see Ryer, 2002 for more detail). After 3 min, fish were transferred to the codend escape-cone, where they escaped through knotless square mesh (9 mm diameter poly-twine, mesh openings 4.3 cm on sides, 6.0 cm diagonal) into the observation arena (see Ryer, 2002 for more detail). All fish ‘escaped’ through the codend mesh in less than 30 s. The swim trials simulated sustained swimming followed by immediate escape through a codend. The sablefish were towed for 90 min followed by transfer to the codend escape-cone, without the “pin” and “crowding” sequence. For control trials the juvenile sablefish remained in the arena. Six replicate trials of each treatment were conducted. All trials were videotaped for later analysis of prey and predator behavior. For each trial, juvenile sablefish (prey) faced four predator challenges, the first immediately after they “escaped” into the observation arena, the second 2 h later, then 1 and 3 days later. For each challenge a single 2+ years sablefish (predator) was dip-netted into the arena and left for 20 min, after which it was removed from the arena. Predators experienced a +4 ◦ C temperature change, which inhibited any overt attempt by the predator to consume the prey, but insured continuous swimming around the perimeter of the arena. There were two instances in which a predator remained motionless on the bottom of the arena for 1 min before it commenced swimming and two other instances where the predator was removed 2–3 min early, because it began to attack prey. 1, 2, 3, and 6 days post-treatment, each group of prey was fed pelletized food over a 3 min period and the number of fish within each group that consumed at least one pellet was recorded. On day 6, several hours after feeding, the prey were dip-netted from their arenas, measured and transferred to holding tanks and monitored daily for mortality over a 4-week period. Juvenile sablefish ranged from 18.3 to 26.6 cm TL with no differences in mean lengths between treatments (mean length (S.E.)—control: 21.7 (0.4); swim: 22.1 (0.4); swim/pin: 21.8 (0.3); analysis of variance, ANOVA (Sokal and Rohlf, 1969): F2,15 = 0.34, P = 0.714). From videotapes of predator challenges, we digitized the swim path of each prey, as well as the predator during a 2 min period, beginning 8 min

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after predator introduction. From this time series of two-dimensional coordinates, we calculated swim speeds and the distances between fish. From intra-fish distances we determined nearest-neighbor distance (Clark and Evans, 1954) for each prey and distance between each prey and the predator at 0.5 s intervals. From the distance-to-predator data we determined closest-approach distance, i.e. the smallest distance, between each prey and predator during the 2 min period. Nearest-neighbor and distance-to-predator data were averaged over the 2 min period for each fish and then averaged by trial. Swim speed and closest-approach distance were averaged for each trial. Data were homoscedastic (Barlett’s test; Sokal and Rohlf, 1969) and were analyzed by repeated measures ANOVA (Hicks, 1982). Where a statistical effect was significant (P < 0.05), a Tukey’s test was conducted (Sokal and Rohlf, 1969). Data for sablefish control and swim treatments were compared to a data set for comparably sized (17.1–21.6 cm TL) walleye pollock (Ryer, 2002). The data were analyzed by three-way repeated measures ANOVA (Hicks, 1982), examining treatment, time after stress, and species. 2.2. Lethal predation experiment Equal numbers of control and stressed juvenile sablefish were combined and exposed to a lingcod predator to compare their relative vulnerability to predation. The stressed sablefish were subjected to one of three treatments: swim/pin, swim/crowd, or swim. These treatments were identical to those described for the non-lethal experiments, except for the additional treatment, swim/crowd, which simulated sustained swimming, followed by crowding (without pinning), prior to escape through a codend. Four arenas, the same utilized for the non-lethal experiments, were fitted with opaque plastic vertical partitions that had numerous 1.2 cm holes, allowing for water movement from one side to the other. Water entered the arena through an inflow pipe on the predator side and exited via an overflow fitting on the prey side. A lingcod (62–87 cm TL) that had not been fed for 10–14 days was placed on the opposite side of the partition. The partition could be raised completely out of the arena using ropes connected to the partitions and running through pulleys attached to the ceiling.

18 h prior to the experiments, 4 groups of 5 sablefish were measured for total length and then received a lower or upper caudal fin clip to allow for identification of control versus stressed groups (fin clips were alternated for each trial). The caudal clipping removed a minute portion of the fin, which was not thought to comprise fish health or performance. Each group was transferred to an arena with the partition separating prey from predator. The next morning, the stress group was dip-netted from their arena, subjected to a treatment, and exited the escape-cone into the arena with their corresponding control group. Next, the lights were turned off for approximately 30 s and the partition was raised, then the lights were switched back on. When the lights were turned off, videotape recording began and continued for 30 min after the lights were turned back on. At the end of the 30 min trial partitions were lowered, sablefish (prey) were removed and enumerated by fin clip to determine the number of control, and stressed fish consumed. Six replicate trials each for the swim/pin and swim/crowd treatments, and seven replicate trials for the swim treatment were conducted. Additionally, we conducted six trials in which sablefish exposed to the swim/pin treatment were allowed 2 h to recover before the partition was raised exposing them to predation (for comparison, we also conducted nine more 0 h recovery trials). Total lengths of prey ranged from 22.0 to 30.7 cm. Mortality data were analyzed using one-tailed paired t tests (Sokal and Rohlf, 1969). 3. Results 3.1. Non-lethal predation experiments Sablefish exposed to simulated trawl-passage exhibited no gross behavioral impairments; however, their behavior was affected in subtle ways when compared to control fish. First, immediately after escape, the swim/pin fish swam significantly slower than controls, with the swim fish exhibiting intermediate speeds (Fig. 1a, Table 1). This lethargy did not appear to be influenced by proximity to the predator. Although swimming speeds increased in the following hour/days, this general pattern of differences between treatments persisted. Second, simulated trawl-passage compromised the ability of juvenile sablefish to shoal

Closest-approach distance (cm)

Nearest-neighbor distance (cm)

-1

Swimming speed (cm•s )

C.H. Ryer et al. / Fisheries Research 66 (2004) 261–269

30

(a)

20 control swim swim/pin

10 0

0

2

24

72

2

24

72

(b)

80 70 60 50 40 30 20

0

125

(c)

100 75 50 25 0

0

2

24

72

265

more wary of the predator over time, this pattern of differences between treatments persisted throughout the 72-h recovery period (Table 1). Differences in the behavior of trawl-stress and control sablefish were not attributable to differences in predator behavior over the recovery time periods. There were no significant differences in the swimming speed of the predators between treatment (F2,15 = 3.24, P = 0.068) or over time (F3,45 = 0.24, P = 0.868). We compared the swim and control trials conducted with sablefish in this experiment to identical trials conducted with walleye pollock from a previous experiment (Ryer, 2002). In all measured tests: swim speed, nearest-neighbor distance, and closest predator approach distance, both sablefish and walleye pollock responded similarly, that is, there were no significant ANOVA interactions involving both species and treatment. Trawl-stressed fish swam slower (F1,20 = 5.87, P = 0.025), shoaled less cohesively (F1,20 = 4.56, P = 0.045), and allowed a predator to approach closer than did control fish (F1,20 = 4.57, P = 0.045). 3.2. Lethal predation experiment

Hours since simulated trawl-stress

Fig. 1. Behavior of juvenile sablefish exposed to a predator at times ranging from 0 to 72 h after simulated trawl-passage: (a) mean swimming speed (±1 S.E.); (b) mean nearest-neighbor distances (±1 S.E.); (c) mean closest-approach distance (±1 S.E.).

cohesively. Immediately after escape, both swim and swim/pin fish shoaled less cohesively than control fish, as indicated by greater nearest-neighbor distances (Fig. 1b). Trawl-stressed fish often swam solitarily or in smaller groups, rather than as a large cohesive shoal, which was more typical of control fish. Both swim/pin and swim fish appeared to gradually recover their ability to shoal over 24 h, but statistically there were no differences in nearest-neighbor distances between treatments from 2 h onwards (Table 1). Lastly, simulated trawl-passage impaired the ability of sablefish to maintain distance between themselves and a predator (Fig. 1c). Swim/pin fish allowed the predator to approach significantly closer than did the controls, with swim fish intermediate between these. Often, trawl-stressed fish exhibited either no response to the approach of the predator or delayed avoidance (i.e. darting away) until the predator was very close. Although fish from all treatments appeared to become

Fish stressed by simulated trawl-passage were more vulnerable to predation than control fish (Fig. 2). In all three trawl-stress treatments (swim, swim/crowd, swim/pin) stressed fish were consumed in significantly greater numbers than control fish (swim: t6 = 2.26, P = 0.032, swim/crowd: t5 = 0.387, P = 0.006, swim/pin: t5 = 3.99, P = 0.005). Sablefish appeared to recover rapidly from trawl-stress (Fig. 3). In the recovery experiment, swim/pin fish were consumed in greater numbers than controls immediately after escape (t5 = 3.87, P = 0.005), but after 2 h, comparable numbers of swim/pin and control fish were consumed (t8 = 0.00, P = 0.500). 4. Discussion Fish species can differ dramatically in their ability to survive both physical and physiological stress (Davis, 2002; Sangster et al., 1996). Because sablefish are more “durable” in this respect, compared to walleye pollock (Olla et al., 1997), we expected that they would also be less susceptible to behavioral impairment resulting from sub-lethal stressors. How-

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Table 1 Swim speed, nearest-neighbor distance and closest-approach distance analysis at 0, 2, 24 and 72 h after simulated-trawl passagea

Swim speed ANOVA Treatment Treatment × replicate Time Treatment × time Treatment × time × replicate

d.f.

SS

MS

F

2 15 3 6 45

32554.7 46661.1 78545.8 3348.2 31826.4

16277.4 3110.7 26181.9 558.0 707.3

2 15 3 6 45

136970 517035 342309 154435 268383

68485 34469 114103 25739 5964

9.54726 18.1249 18.4982 3.15766 11.0195

4.77363 1.20833 6.16606 0.52628 0.24488

P

5.23

0.019

37.02 0.79

0.001 0.583

1.99

0.172

19.13 4.32

0.001 0.002

3.95

0.042

25.18 2.15

0.001 0.066

Treatment: S/P S C Time: 0 h 2 h 24 h 72 h Nearest-neighbor ANOVA Treatment Treatment × replicate Time Treatment × time Treatment × time × replicate

0 h: C S S/P 2 h: C S S/P 24 h: C S S/P 72 h: C S S/P Closest-approach ANOVA Treatment Treatment × replicate Time Treatment × time Treatment × time × replicate

2 15 3 6 45

Treatment: S/P S C Time: 0 h 2 h 25 h 72 h a

Treatment: C, controls; S, swim; S/P, swim/pin. Homogeneous subgroups of means are underlined.

suppression of feeding may be of little consequence, even a brief hiatus in predator avoidance capabilities can have profound implications for survival. As a consequence, sablefish subjected to simulated trawl passage were consumed in greater numbers than were control fish, as were walleye pollock. This occurred regardless of whether the stressors were mild (swim treatment) or more severe (swim/pin treat-

3 Sablefish consumed

Sablefish consumed

ever, this was not the case; sablefish exhibited the same subtle behavioral changes seen in walleye pollock. Considering only control and swim treatments from non-lethal experiments for both species, which were conducted using identical protocols, the same effect of trawl-stress was evident in both sablefish and walleye pollock: decreased swim speed, decreased shoaling and lowered vigilance. While stress-induced

2

1

0

c

s

c

s/c

c

s/p

Simulated trawl-stress treatments Fig. 2. Mean number (±1 S.E.) of control and trawl-stressed sablefish consumed during 30 min encounters with a lingcod predator. Treatments: C, control; S, swim; S/C, swim/crowd; S/P, swim/pin.

2

0h

2h

1

0

c s/p Treatment

c s/p Treatment

Fig. 3. Mean number (±1 S.E.) of control (C) and swim/pin (S/P) sablefish consumed during 30 min encounters with a lingcod predator after 0 and 2 h of recovery.

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ment). Therefore, despite considerable differences in their susceptibility to direct stress-induced mortality, both juvenile sablefish and walleye pollock appear equally susceptible to subtle behavioral impairments resulting from sub-lethal stressors, which confer increased vulnerability to predation. If, as suggested by our results, behavior impairment is a common consequence of interaction with trawl gear, then predation upon behaviorally impaired fish may contribute to unobserved mortality in many fisheries. That stress may impair behavior is not a new observation (Schreck et al., 1997). A wide variety of sub-lethal stressors have been documented to impair fish behavior, rendering them more vulnerable to predation (reviewed by Mesa et al. (1994), Olla et al. (1997)). The stressors utilized in this study likely simulated the minimum level of what juvenile sablefish and walleye pollock experience in commercial gear: (1) the swim speed was at the low end of the 0.3–0.8 m s−1 experienced by fish in commercial trawls and fish did not swim to exhaustion; (2) they were spared the more extreme physical damage that can accompany crowding and collisions with debris, invertebrates and other fish; (3) even when pinned against codend meshes, fish were not subjected to the compressive forces likely experienced as a catch ball accumulates; and (4) during escape fish were not subjected to the shear forces resulting from differential water velocity inside versus outside the net. The relatively mild nature of these laboratory stressors is verified by the absence of any mortality in fish monitored for up to 5 weeks. It follows that these laboratory studies represent a conservative test of the hypothesis that trawl passage impairs fish behavior. Sablefish that were pinned against the meshes during simulated trawling exhibited more pronounced behavioral deficits than fish which merely “swam” prior to escape. Walleye pollock that were “crowded” were also more affected than those that merely swam (Ryer, 2002). Similarly, in our lethal predation experiments, there was a pattern of greater proportional mortality for stressed fish, relative to controls, when the trawl stressors included pinning. This suggests that physical contact with trawl gear, as well as other fish and debris, is likely a principle factor controlling sub-lethal and lethal stress for fish escaping trawl codends. How a fish performs in a trawl, that is, how well it avoids physical contact and injury during its passage, will be influ-

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enced by a myriad of factors, including: gear-specific characteristics such as mesh size, tow speed, tow duration and catch size. Additionally, ambient illumination at fishing depth will influence the behavior of fish relative to trawl gear (Glass and Wardle, 1989). In a laboratory experiment, Ryer and Olla (2000) observed that juvenile walleye pollock struck an approaching net more frequently in the dark (<1.0 × 10−8 ␮mol photons m−2 s−1 ) than in the light (1.7 × 10−3 ␮mol photons m−2 s−1 ). If failure to detect and orient relative to moving trawl gear results in more physical contact with the gear and resultant injury, it will likely magnify both direct mortality and behavioral impairment. In support of this hypothesis, Suuronen et al. (1995) documented lower direct mortality of vendace Coregonus albula escaping a trawl codend in late afternoon and early evening (30–40%) than in the late evening and at night (60–80%). Our results may also be relevant to the fate of fish that are captured and subsequently discarded. It is estimated that nearly one-quarter of the world-wide fisheries catch is discarded (Alverson et al., 1994). For fish that have a swim bladder or other organs that expand as they are brought up from depth, survival is highly unlikely. However, for other discarded fish which do not have a swim bladder, have a bladder or other organs that do not inflate when brought to the surface, or fish brought up from shallow depths, survival is possible. The stressors affecting these fish include exhaustion, physical damage, temperature shocks and air exposure/anoxia, to name but a few, and fish of differing sizes and species vary considerably in their resistance (Davis, 2002). In most cases these stressors will be more severe than those simulated in this study and it is reasonable to assume that in addition to direct mortality, some fish will become behaviorally impaired by the capture/discard process and be consumed by predators or scavengers in the minutes, hours or days afterwards. For behavioral impairment to be of consequence, there must be predators nearby to capitalize upon the deficits in a fish’s defenses. Large predatory fish often accompany their prey during their daily movements and migrations (Hobson, 1968; Pitcher, 1980; Parrish, 1992), and as such, will often be pre-positioned to concentrate attacks upon impaired escapees, which behave “oddly” relative to non-trawl-impacted fish in the school (oddity effect: Hobson, 1968; Landeau

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and Terborgh, 1986; Theodorakis, 1989). Trawling may also aggregate predators/scavengers, creating localized areas of intensive predation pressure (Caddy, 1973; Kaiser and Spencer, 1994, 1996; Ramsay et al., 1996, 1998; Prena et al., 1999). It is not unreasonable to expect that piscivorous fish, which respond to longline baits from great distance (Løkkeborg et al., 1995), would also be attracted to the dead, dying and impaired fishes left in a trawl’s wake. Lastly, birds, fish and marine mammals are known to follow trawlers, consuming discards as well as fish escaping from the gear (Broadhurst, 1998). While knowledge of how fishing operations may aggregate or otherwise influence the spatial distribution of predators clearly needs to be expanded through focused research, these studies suggest that in many instances predators will have ample opportunity to exploit fish which become impaired during escape from trawls or from capture and subsequent discard. In conclusion, although sablefish have a greater capacity to survive severe stress, like walleye pollock they are none-the-less susceptible to the same behavioral impairments arising from exposure to sub-lethal stressors. These behavioral impairments render both sablefish and walleye pollock more vulnerable to predation. This suggests that resistance to mortality does not necessarily impart resistance to behavioral impairment. If this is a general phenomenon, affecting a wide variety of species and fisheries, it suggests that increasing meshes size to achieve mechanical separation in the codend, may be a less effective means of bycatch reduction than counting fish on the deck would suggest. Further, it may represent yet another source of uncertainty in modeling fisheries, particularly in heavily exploited stocks. Ideally, bycatch reduction should be achieved by avoiding fishing where non-target fish are prevalent. In lieu of this, BRDs should be developed and employed that guide fish out of the net as rapidly as possible, before they are exhausted and physically damaged through contact with other fish, debris and/or net meshes.

Acknowledgements We thank Richard Titgen and Mara Spencer for assistance with conducting these experiments. Michael Davis and Allan Stoner provided constructive criti-

cism of this manuscript and Cindy Sweitzer assisted in its preparation.

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