© 2004 by ICES/CIEM International Council for the Exploration of the Sea/Conseil International pour l'Exploration de la Mer
Laboratory evidence for behavioural impairment of fish escaping trawls: a review
Fisheries Behavioral Ecology Program, Alaska Fisheries Science Center, National Marine Fisheries Service, Hatfield Marine Science Center 2030 Marine Science Drive, Newport, OR 97365, USA
*Tel: +1 541 867 0267; fax: +1 541 867 0136. e-mail: cliff.ryer{at}noaa.gov.
It is now widely accepted that for some species a proportion of the undersized fish escaping trawl codends die as a direct result of stress, with 10% to 30% mortality commonly cited. It has also been suggested that there may be indirect or behaviourally mediated mortality; fish that encounter and escape the trawl, only to experience stress-induced behavioural deficits and succumb to predators in the hours or days afterwards. The goal of this review was to evaluate the plausibility of this behaviourally mediated, yet unobserved mortality. Three laboratory studies utilizing cod (Gadus morhua), walleye pollock (Theragra chalcogramma), and sablefish (Anoplopoma fimbria) have assayed for behavioural impairment in fish following application of stressors designed to simulate entrainment and escape from trawls. Where impairments in anti-predator capabilities occurred, it was determined that trawl-stressed fish exhibited reduced swimming speed, reduced shoal cohesion, and reduced predator vigilance compared to control fish. Although stressed fish appeared to rapidly recover their ability to avoid being eaten by predators, measurements of more subtle aspects of escapee behaviour suggest that impairments may persist for days after stressor application. Although these studies demonstrate that more investigation is required, when combined with a more extensive literature demonstrating that a variety of stressors can impair fish anti-predator behaviour, it is reasonable to conclude that many fish species escaping trawl codends will likely suffer behavioural deficits that subject them to elevated predation risk. As such, there is probably mortality associated with trawl fisheries that is generally unrecognized, unmeasured, and unaccounted for in current stock assessment models. Further, these studies demonstrate that behavioural competency needs to be considered in the design and implementation of by-catch reduction devises and strategies.
Keywords: by-catch, predation, stress, trawl
Received 12 March 2003; accepted 21 April 2004.
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Introduction |
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Discarded by-catch has been estimated at approximately one-quarter of the worldwide fisheries catch (Alverson et al., 1994). As fish stocks have come under increasing harvest pressure, there has also been increasing societal and regulatory pressure upon fishers to decrease the discard of undersized fish and non-target species. One of the most common methods for reducing by-catch in trawl fisheries involves increasing the mesh size or changing mesh geometry in the codend, thereby allowing undersized fishes to escape at depth, before they reach the vessel's deck. Although it is commonly assumed that these escapees survive, field studies indicate that mortality, as a direct consequence of injuries and stress incurred during trawl passage, can be extensive (Suuronen et al., 1995; Sangster et al., 1996; Suuronen et al., 1996a; Erickson et al., 1999). This category of fishery-induced mortality is commonly referred to as unobserved by-catch (Crowder and Murawski, 1998). In this paper, another possible indirect source of mortality among trawl escapees is explored; predation upon fish that become behaviourally impaired by their interaction with trawl gear. The existence of predation-mediated mortality of trawl escapees has been suggested (Chopin and Arimoto, 1995; Crowder and Murawski, 1998), yet only three published studies, all of them laboratory-based, have examined this topic (Løkkeborg and Soldal, 1995; Ryer, 2002; Ryer et al., 2004a). Necessarily, this review focuses on these three studies, but also integrates relevant literature that addresses stressors experienced by fish during their entrainment and subsequent escape from trawls, as well as more generic studies of stress-induced behavioural impairment in fish.
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Stressors experienced by escapees |
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TopIntroductionStressors experienced by...Escapee vulnerability to...Behavioural basis of impairmentDuration of impairmentConclusionsReferences |
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The stressors experienced by undersized fish in trawls prior to and during escape vary and are influenced by a myriad of factors, including trawl configuration, tow speed, catch size, and environmental parameters such as temperature and light, as well as species-specific characteristics such as body size, body form, sustained and burst swim speeds, and gear avoidance behaviour. In this paper I concentrate on the stressors experienced by roundfish which possess sustained swimming capabilities. While species that lack sustained swimming capabilities, e.g. many flatfish species, will often rapidly pass from the trawl mouth to the codend (personal observation), many roundfish will swim either ahead of, or in the trawl, for prolonged periods prior to their passing to the codend (Wardle, 1983; Suuronen et al., 1997). It is not until the codend, where the path of least resistance terminates, that fish typically seek to penetrate the trawl meshes and escape (i.e. black tunnel effect; Glass et al., 1995), most typically immediately forward of the accumulating catch (Main and Sangster, 1990; Suuronen et al., 1996a; O'Neill et al., 2003). Since water velocity decreases with increasing distance down-net from the trawl mouth (Broadhurst et al., 1999; O'Neill et al., 2003), where fish swim in the net will be determined by their maximum sustained swimming speed. How long they swim will be determined by their endurance. Swimming to exhaustion can result in osmotic imbalance (Turunen et al., 1996) and decreased glycogen levels in liver and muscle tissues (Suuronen et al., 1996a). In addition, while swimming in the trawl, fish may physically contact the net meshes, other fish, and debris, causing skin damage and scale loss (Sangster et al., 1996). Suuronen et al., (1997) noted that herring Clupea harengus swimming in a midwater trawl "were often seen to strike against the netting and their scales were seen coming through the meshes". Fish may also be temporarily pressed against other fish in the catch ball, or pinned against net meshes prior to escape. Finally, during the act of mesh penetration, i.e. escape, fish may sustain further damage to skin and scales, the extent of which will be determined by the fish's size relative to the mesh openings and the magnitude of current shear resulting from differences in relative water velocity inside vs. outside the codend. The stressors experienced by fish during their trawl passage will also be influenced by environmental variables. For example, low ambient illumination or high turbidity may render fish unable to orient relative to the gear (Glass and Wardle, 1989; Olla et al., 2000), thereby increasing gear contact (Ryer and Olla, 2000) and the likelihood of physical injury. Similarly, temperature may influence escape behaviour (Özbilgin and Wardle, 2002) and/or magnify the effects of other stressors (Davis, 2002). Ultimately, these physiological and physical insults may either directly or indirectly, through an induced cascade of additional physiological changes, degrade behavioural responses to external stimuli, potentially rendering escapees more vulnerable to predation (Schreck et al., 1997).
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Escapee vulnerability to predation |
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TopIntroductionStressors experienced by...Escapee vulnerability to...Behavioural basis of impairmentDuration of impairmentConclusionsReferences |
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Is it reasonable to expect that stress incurred during escape from trawl codends may render fish more vulnerable to predation? The first laboratory experiments addressing this question were conducted with juvenile age 1+ year cod (mean total length = 18.2 cm) (Gadus morhua), forced to swim at 0.19–0.31 m s–1 in a 2.1-m-long miniature trawl (70-mm mesh; Løkkeborg and Soldal, 1995). At the end of 30 min, the tow speed was increased for 5 min to encourage fish to drop back in the net and penetrate the mesh; fish passing through the net meshes were retained in a 16-mm knotless mesh cover. Four of these fish were then transferred to a bucket, which already contained four control fish, suspended in a tank (1.0 m x 2.5 m, 1.0 m deep) containing five larger adult cod. Trawl-stressed fish were identifiable by a small clip on the caudal fish, which presumably did not influence their performance. Trawl-stressed and control juvenile cod were subsequently released into the predator (large cod) tank, where they remained for 30 min or until 50% of the fish were consumed. Over the course of eight replicate trials, approximately equal numbers of trawl-stressed (x = 1.88, s.e. = 0.23) and control juvenile cod (x = 1.75, s.e. = 0.31) were eaten (paired t[14] = –0.32, p = 0.376), suggesting no appreciable effect of trawl-stress on the ability of juvenile cod to avoid predation by larger conspecifics. Field studies of trawl escapees suggest that cod are resistant to direct mortality (Main and Sangster, 1990; Suuronen et al., 1996b), so perhaps it is not unexpected that they are also resistant to stress-induced behavioural impairment. However, the authors pointed out several potential problems which may have biased this experiment. First, the trawl-stressed fish did not swim to exhaustion or experience extended physical contact with the net meshes or other fish, as may commonly occur under actual fishing conditions. Second, the predation tank was relatively small and the predators could easily capture both control and stressed fish, potentially masking any difference between groups. Lastly, stress associated with their transfer between their holding tank and the predation tank may have compromised the anti-predator behaviour of control fish.
This basic experimental design, developed by Løkkeborg and Soldal (1995), was subsequently utilized in more extensive experiments using juvenile 1+ year walleye pollock (Theragra chalcogramma) (17–22 cm total length) and 1+ year sablefish (Anoplopoma fimbria) (22–31 cm), incorporating a wider range of trawl stressors, a larger predation tank, and control fish that were not subjected to transfer stress immediately prior to predation trials (Ryer, 2002; Ryer et al., 2004a). Both walleye pollock and sablefish are commercially important in the North Pacific, with juveniles potentially encountering and escaping from trawl gear in a variety of fisheries (Fritz, 1996; Sampson et al., 1997). Comparison of these two species is also of interest owing to the fact that walleye pollock are a rather "fragile" species with regard to their ability to survive physical stress; whereas, sablefish are more "durable" in this respect. Olla et al. (1997) demonstrated this difference in susceptibility to physical stress by towing both species in a net where they were pinned against the meshes at a speed of 0.95 m s–1 for 15 min; walleye pollock experienced 100% mortality during the 14 d afterwards, compared to 0% mortality for sablefish. To assay sublethal effects upon behaviour, fish were sequentially exposed to stressors simulating those experienced by trawl escapees, then, along with an equal number of control fish, were subjected to predation by a lingcod (Ophiodon elongates) (for details, see Ryer, 2002). Briefly, the simulated trawl scenario for walleye pollock entailed forced swimming of groups of five fish in a net for 90 min at 0.33 m s–1, followed by a 3-min period of crowding in a chamber containing water-filled balloons, simulating an accumulating catch. Next, fish were transferred to one-half of a bisected 3-m diameter arena where they volitionally swam ("escaped") through a 4.3-cm square mesh codend to join five control fish. Immediately afterwards the partition bisecting the arena was raised, exposing both treatment and control fish to the predator. After 30 min, the walleye pollock were removed and enumerated. Treatment and control fish were distinguishable by means of small fin clips on either the dorsal or ventral margin of the caudal fin. Fin-clipping did not appear to impair fish performance, but in any case both control and treatment fish were fin-clipped in each trial, with the assignment of clips (dorsal or ventral) alternated during successive trials. For sablefish, three trawl scenarios were examined: (i) swimming for 90 min followed by escape (seven replicate trials), (ii) swimming for 90 min followed by 3 min of crowding prior to escape (six replicate trials), and (iii) swimming for 60 min, then towing at the same speed for 30 min with fish pinned against the net mesh, followed by 3 min crowding before escape (six replicate trials, Ryer et al., 2004a). To pin fish against the net meshes, fish were confined to a small area in the rear of the net where they were unable to swim. As can be seen from Figure 1, both walleye pollock and sablefish exposed to a range of simulated trawl passage scenarios were consumed in significantly greater numbers than were control fish (paired t-test, p < 0.05 for each), indicating increased vulnerability to predation. Although sustained swimming was sufficiently stressful to make fish more vulnerable to predation, the more marked effect observed in sablefish which were towed while pressed (pinned) against the meshes for 30 min suggests that increased physical contact with gear will likely magnify this effect. Juvenile sablefish thus pinned also experienced greater physical damage, i.e. torn fins and abrasions (Ryer, unpublished data). This is consistent with the findings of field studies, where it was concluded that physical contact with gear increased physical damage to fish and direct mortality (e.g. Suuronen et al., 1996a).
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Were the stressors utilized in these experiments realistic? These stressors were likely mild compared to what fish experience in actual trawls. In separate experiments, both walleye pollock and sablefish exposed to the same laboratory stressors experienced no mortality for five weeks afterwards. This is in marked contrast to the previously cited field studies, where mortality was often substantial in the first week following trawl passage. Therefore, if anything, the behavioural impairments experienced by fish escaping actual trawls are probably greater than those which increased vulnerability to predation in these laboratory experiments. Further, both juvenile walleye pollock and sablefish, which possess differing dispositions with regard to surviving potentially lethal stressors, suffered similar increases in vulnerability when subjected to relatively mild non-lethal stressors simulating escape from trawls. The lack of behavioural impairment in cod may reflect the more "durable" nature of this species, although differences in experimental protocols may have played a role. Thus, while the available experimental evidence suggests that behavioural impairment may be common among a variety of fish species, it would be advisable that future studies examine a greater variety of species, adopting uniform approaches for administering sublethal stressors and assessing behavioural impairment.
Although the studies which have directly examined the effects of stress upon the survival of fish escaping trawls are relatively few, other stressors have also been demonstrated to produce behavioural impairments in fish (reviewed by Mesa et al., 1994). Both Chinook salmon smolts (Oncorhynchus tshawytscha) and coho salmon smolts (O. kitsuch) are rendered more vulnerable to predation by handling stress (Olla and Davis, 1989, 1992; Olla et al., 1995). Chinook smolts stressed by agitation, simulating dam passage, are more vulnerable to predation by pike-minnows (Ptchocheilus oregonensis) (Mesa et al., 1994). Similarly, stressors such as temperature shock (Coutant, 1973; Webb and Zhang, 1994), disease (Mesa et al., 1998), toxicants (Brown et al., 1985; Little et al., 1990), and starvation (Herting and Witt, 1967) increase fish vulnerability to predation. Thus, it appears likely that the stressors associated with entrainment and subsequent escape from trawls, rather than being unique, are simply further additions to a growing suite of stressors known to impair fish behaviour and render fish more vulnerable to predation.
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Behavioural basis of impairment |
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TopIntroductionStressors experienced by...Escapee vulnerability to...Behavioural basis of impairmentDuration of impairmentConclusionsReferences |
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What aspects of escapee behaviour are impaired such that they become more vulnerable to predation? This question was addressed in another set of laboratory experiments in which fish were again subjected to stressors simulating trawl passage, then allowed to escape into a 3-m arena where their behaviour could be monitored during each of four 20-min predator challenges over 3 d (Ryer, 2002; Ryer et al., 2004a). In this case, the predator was an adult sablefish (48–53 cm) which had been temperature shocked such that it swam continuously about the arena eliciting fright reactions from juvenile walleye pollock and sablefish, but did not actually attempt to capture them. Control groups were not subjected to any stressors, while the swim escape groups were subjected to the identical stressors as in the prior experiment. For the higher trawl-stress scenarios, procedures for walleye pollock and sablefish differed; walleye pollock were exposed to sustained swimming, followed by crowding prior to escape, while sablefish were exposed to the additional stress of being pinned against the net mesh while being towed for 30 min. For both species, six groups (six fish each) were subjected to each treatment. As can be seen in Figure 2, in the minutes immediately after escape, several aspects of escapee behaviour were impaired relative to control fish. First, trawl-stressed fish swam slower than controls (pollock: F[2,15] = 16.45, p < 0.001; sablefish: F[2,15] = 4.60, p = 0.028) (Figure 2a). This was particularly evident in the pollock subjected to the swim/crowd/escape scenario. Many of these fish appeared disoriented and swam at angles to the horizontal or in tight circles at the water surface. Second, stressed fish were less adept at maintaining cohesive shoals, as evidenced by their greater nearest-neighbour distances (pollock: F[2,15] = 7.47, p = 0.006; sablefish: F[2,15] = 7.17, p = 0.007) (Figure 2b). Maintaining a cohesive shoal aids in predator detection (Magurran et al., 1985) and coordination of escape responses (Pitcher and Parrish, 1993), which can result in predator confusion (Neill and Cullen, 1974; Landeau and Terborgh, 1986), thereby decreasing prey vulnerability to predation. Finally, stressed fish allowed predators to make closer approaches before taking evasive action or in some cases failed to respond to approaching predators (pollock: F[2,15] = 11.38, p = 0.001; sablefish: F[2,15] = 5.90, p = 0.013) (Figure 2c). These impairments could have profound implications for survival, as even a brief hiatus in predator detection or avoidance behaviour could not only make fish more vulnerable to predator attacks, but could actually attract the attention of predators, which often survey prey for signs of vulnerability (oddity effect: Hobson, 1968; Landeau and Terborgh, 1986; Theodorakis, 1989). It is possible that pain, resulting from physical damage or physiological imbalance, may reduce fish vigilance towards potentially threatening stimuli. Sneddon et al. (2003) reported that rainbow trout (Oncorynchus mykiss) subjected to pain demonstrate reduced avoidance of novel and potentially threatening objects compared to control fish. The importance of a fish's vigilance in maintaining a safe distance between itself and a potential predator was also demonstrated in the previously described vulnerability experiment utilizing walleye pollock and lingcod (Ryer, 2002). The closer an approaching lingcod got to a walleye pollock, the more likely it was to lunge, and the smaller the distance at initiation of a lunge, the greater the likelihood of the pollock being captured. Therefore, along with behaviour which renders stressed fish more conspicuous to predators, i.e. reducing swim speed and shoaling, an inability to counter predator approaches with appropriately timed avoidance behaviour will likely be a major contributor to the increased vulnerability of trawl-stressed escapees.
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Where, and under what conditions, a fish escapes will also impact its behaviour and survival. Escape from trawls into suboptimal habitats or social contexts may further reduce the effectiveness of innate behavioural responses to predators. For example, some demersal fish species are found in close association with particular emergent structures in low relief soft bottom habitats, such as isolated rock outcrops, shell, sand waves, sponges, and other biogenic structures, which are often patchily distributed (Thrush et al., 2002; Ryer et al., 2004b). Fish displaced from these habitats by entrainment and subsequent escape from trawls may find themselves in inappropriate habitats where their innate behavioural repertoires are ineffective at countering predation (e.g. refuging). Similarly, fish that rely upon shoaling to counter predation risk may find themselves alone upon escape from the trawl and at increased risk of predation until they can locate and rejoin a shoal (Pitcher and Parrish, 1993). Thus far, these issues have not been addressed through either field or laboratory studies.
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Duration of impairment |
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TopIntroductionStressors experienced by...Escapee vulnerability to...Behavioural basis of impairmentDuration of impairmentConclusionsReferences |
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In evaluating the potential for indirect mortality mediated by behavioural impairment, the question arises; what is the likely duration of behavioural impairment? Thus far, available laboratory studies offer incomplete and conflicting results. In a repeat of the sablefish predation vulnerability experiments described previously, it was again demonstrated that immediately after being subjected to the swim/pin/crowd/escape trawl scenario, the trawl-stressed sablefish were more vulnerable to predation by lingcod than were control fish (n = 6 trials, paired t[5] = 3.87, p = 0.005) (Ryer et al., 2004a). However, when trawl-stressed sablefish were allowed 2 h of recovery prior to lingcod exposure, performance had improved and they were consumed in numbers comparable to those of control fish (n = 9 trials, paired t[8] = 0.00, p = 0.500) (Figure 3). This would suggest that behavioural impairment is brief, a matter of minutes, to an hour or so; not days. However, direct measurement of escapee avoidance behaviour suggests that complete recovery may take longer (Ryer et al., 2004a). When subjected to the swim/pin/crowd/escape treatment and then monitored during predator challenges (adult sablefish) at 0, 2, 24, and 72 h, juvenile sablefish did not fully recover to nominal behaviour during 72 h (n = 6 trials each of trawl-stressed and controls, F[1,30] = 7.99, p = 0.018), as measured by approach distances between predator and prey (Figure 4). Additional experiments will need to be done to determine which, if either, of these approaches provides the best methodology for measuring recovery.
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Intertwined with the duration of behavioural impairment is the nature of the predatory threat to which escapees are subject. If predator encounters are infrequent and the duration of impairment short, then the likelihood of significant stress-related predation mortality is small. If however, encounters with predators are frequent, then even brief periods of disorientation and behavioural impairment may significantly increase the likelihood of mortality. For many shoaling species, predators are often in nearly constant contact (Pitcher, 1980; Parrish, 1992), following the shoal and concentrating attacks on conspicuous individuals (Hobson, 1968; Landeau and Terborgh, 1986; Theodorakis, 1989). Similarly, long-range attraction of predators by olfactory cues (Løkkeborg et al., 1995) may aggregate predators in areas of intensive fishing effort. In some extreme instances, predators even follow trawls, capturing prey as they exit the codend meshes and by-catch reduction devices (Broadhurst, 1998).
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Conclusions |
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TopIntroductionStressors experienced by...Escapee vulnerability to...Behavioural basis of impairmentDuration of impairmentConclusionsReferences |
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Success of by-catch reduction strategies which reduce the number of undersized and non-target fish arriving on the deck is no certain guarantee that fish are escaping the trawl in a behaviourally competent condition. Although there have been no adequately designed field studies to determine whether trawl escapees indeed suffer behaviour impairments sufficient to render them vulnerable to indirect mortality through predation, the laboratory studies reviewed here clearly demonstrate this is a likely outcome for many species. Furthermore, where field studies demonstrate substantial direct mortality in the first several days after trawl passage, it is highly likely that at least some of the surviving fish suffer adverse behavioural effects in the following hours and/or days. A variety of other stressors have been demonstrated to render fish more vulnerable to predation, including handling, agitation simulating dam passage, temperature, toxicants, and disease. This would suggest that, rather than being unique, trawl passage has fairly generic influences upon fish behaviour that are shared by other natural and anthropogenic classes of stressors. As pointed out by Chopin and Arimoto (1995), rather than reducing the chances of undersized fish coming into contact with trawl gear, management regulations have more often focused on providing opportunities for undersized and non-target species to escape from gear after they have become entrained (e.g. minimum mesh sizes) and after they have been exposed to a wide spectrum of stressors. As in the case of direct mortality resulting from trawl passage, the laboratory studies reviewed here suggest that behavioural impairment will be greatest when fish suffer prolonged physical contact with the trawl gear and/or other fish and debris. Therefore, by-catch reduction methodologies that facilitate the rapid volitional escape of undersized and non-target fish from trawls would appear superior to methodologies that rely upon more mechanical separation in the codend after prolonged swimming and exhaustion. These conclusions may also have relevance for understanding the effect of multiple stressors upon the behavioural competence and ultimate fate of fish which are retained by nets only to be discarded (Davis, 2002).
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Acknowledgements |
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I thank Erick Sturm and Michele Ottmar for their contributions to this work, and Allan Stoner, Michael Davis, Chuck Hollingworth, and two anonymous reviewers for their comments on an early version of the manuscript. Cindy Sweitzer facilitated manuscript preparation.
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References |
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