ICES Journal of Marine Science: Journal du Conseil Advance Access originally published online on June 27, 2007
ICES Journal of Marine Science: Journal du Conseil 2007 64(8):1535-1542; doi:10.1093/icesjms/fsm087
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Simulated fishing experiments for predicting delayed mortality rates using reflex impairment in restrained fish
NOAA/NMFS/Alaska Fisheries Science Center, Hatfield Marine Science Center, 2030 SE Marine Science Drive, Newport, OR 97365, USA
Tel: +1 541 867 0256; fax: +1 541 867 0136; e-mail: michael.w.davis{at}noaa.gov
Davis, M. W. 2007. Simulated fishing experiments for predicting delayed mortality rates using reflex impairment in restrained fish. – ICES Journal of Marine Science, 64: 1535–1542.Development of efficient methods to predict discard and escapee mortality in fishing operations is essential to the conservation of sensitive fish stocks. For a few fisheries, mortality data are available from fishing experiments in the field; these require long-term holding or monitoring of fish in tanks, cages, or tag and recapture experiments to detect delayed mortality. A different approach to predicting discard and escapee mortality is to use reflex action mortality predictors (RAMP) consisting of relationships between mortality and reflex impairment for species of interest. Fish were towed in a net in the laboratory and then either restrained in foam-lined holders and rapidly tested for reflex impairment five minutes after towing, or held for up to 60 days to determine delayed mortality. Delayed mortality occurred up to 20 days after towing. RAMP was related to mortality with biphasic sigmoid functions. As fishing stressors increased in intensity, the first phase showed an increase in RAMP with no concomitant mortality. In the second phase, RAMP continued to increase, while mortality became apparent and increased. The measurement of RAMP in restrained fish on board fishing vessels during experiments to predict discard mortality and in caged free swimming fish to predict escapee mortality is feasible and advisable.
Keywords: delayed mortality, fish condition, reflex impairment, salmon, stress, survival
Received 8 August 2006; accepted 14 April 2007; advance access publication 27 June 2007.
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Introduction |
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 Top Introduction Material and methodsExperimental treatmentsTesting for reflex impairment...ResultsDiscussionReferences |
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The development of efficient methods for measuring bycatch discard and escapee mortality is a key problem for fisheries management. Mortality of fish bycatch has been a primary concern for fisheries managers for at least two decades (Alverson et al., 1994; Broadhurst, 2000; Kennelly and Broadhurst, 2002; Harrington et al., 2005). Total mortality of discards and escapees has generally been estimated using fishing experiments in which fish were exposed to fishing stressors. Fish that died immediately after fishing experiments were classified as immediate mortality, while fish that survived fishing experiments were placed in cages or tagged and recaptured to measure delayed mortality, methods that required long-term holding or monitoring of fish (ICES, 2000; Suuronen, 2005). Total mortality was then calculated as the sum of immediate mortality and delayed mortality. A different approach, which would significantly increase the scope and replication of fishing experiments, is to predict discard and escapee delayed mortality by observing fish condition immediately after fishing experiments. The results of these experiments could then be used to estimate immediate, delayed, and total mortality in fisheries.
Fish condition has been discussed as a general predictor for delayed mortality, but no guidance about how this would be accomplished over a range of fisheries has been given (Chopin and Arimoto, 1995). Condition indices for discard mortality have been developed for Pacific halibut, Hippoglossus stenolepis, based on wounding, and for sharks, based on revival time after discarding (Clark et al., 1992; Trumble et al., 2000; Hueter et al., 2006). To be a comprehensive predictor of bycatch mortality, fish condition must be correlated with discard and escapee mortality over a wide range of fishing conditions including but not limited to catch amount, wounding, environmental factors, and fish size. However, use of wounding, autopsies, plasma constituents, and complex behaviour as predictors for delayed and total mortality may be limited. These condition measures show inconsistent responses to different types of fishing conditions, including capture, environmental factors, fish size, and combinations of stressors (Olla et al., 1997; ICES, 2000; Davis, 2002, 2005; Parker et al., 2003; Davis and Schreck, 2005; Lupes et al., 2006). Types of fish wounds that occur during capture are highly variable and can be a major source of mortality in bycatch discards and escapees (ICES, 2000; Trumble et al., 2000; Suuronen, 2005). However, wounding may not predict bycatch mortality when other lethal stressors are present, which act without altering the extent of wounding (ICES, 2000; Davis, 2002; Suuronen, 2005). Measures currently used for fish condition all share the problem of responding to different fishing-related stressors in uncorrelated ways because temperature change, time in air, fish size, and combinations of stressors can confound relationships between fish condition and mortality (Neilson et al., 1989; Sangster et al., 1996; Davis, 2002). The diversity of fish stress response patterns makes comprehensive prediction of delayed and total mortality using existing condition measures unlikely.
Reflex impairment is a measure of fish condition that responds to a wide range of fishing conditions in a manner similar to stressor intensity, and has been used as a predictor for mortality in free swimming roundfish and flatfish (Davis and Parker, 2004; Davis, 2005; Davis and Ottmar, 2006). Extension of these results to restrained fish would allow the development of a reflex action mortality predictor (RAMP) of general use in fishing experiments. Escapee delayed and total mortality could be predicted using RAMP observed for free-swimming fish in cages that were recaptured after escaping from fishing gear. Delayed and total mortality for fish that were to be discarded could be predicted using RAMP in restrained fish observed on board fishing vessels prior to discarding.
The goal of this study was to test the hypothesis that reflex impairment in restrained fish could be used as a predictor for delayed and total mortality in fishing experiments with roundfish and flatfish that were towed in a net. The scope of the work was limited to demonstrating proof of concept using laboratory experiments to simulate fish capture in a net. An exhaustive analysis of the general applicability of reflex impairment to predict mortality in a wide range of species and fishing conditions in the field was not intended and remains a subject for future research.
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Material and methods |
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TopIntroductionMaterial and methodsExperimental treatmentsTesting for reflex impairment...ResultsDiscussionReferences |
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Fish capture and rearing
Three species of juvenile fish (2–4 cm total length TL) were collected in the field and transported to the laboratory. Walleye pollock, Theragra chalcogramma, were captured in spring at night with lights and a lift net in Point Townsend Bay, Washington (48°6'N 122°48'W), reared in 450-l tanks with flow-through seawater at 8–9°C, and fed daily to satiation on pelletized cod food. Northern rock sole, Lepidopsetta polyxystra, and Pacific halibut were captured during summer from Chiniak Bay, Kodiak Island, Alaska (57°43'N 152°18'W) with a beam trawl, reared in 450-l tanks with a thin layer of sand on the bottom and flow-through seawater at 8–9°C, and fed to satiation three times per week on krill, Euphausia superba, and pelletized salmon food. When the three species of fish grew to 7 cm TL, they were transferred to 3140-l tanks with sand on the bottom for flatfish and flow-through seawater at 8–9°C. Coho salmon, Oncorhynchus kisutch, smolts (14–15 cm TL) were obtained in spring from the Salmon River ODFW hatchery in Otis, Oregon, reared in 3140-l tanks with flow-through seawater at 8–9°C, and fed three times per week to satiation on pelletized salmon food.
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Experimental treatments |
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TopIntroductionMaterial and methodsExperimental treatmentsTesting for reflex impairment...ResultsDiscussionReferences |
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To test for correlations between reflex impairment and mortality, gradients of increasing fish mortality were created in the laboratory. Juvenile fish were towed in a net that simulated capture in the codend of a trawl to produce a range of mortalities based on results of previous studies in this laboratory (Olla et al., 1997; Davis et al., 2001; Davis, 2002). Tow duration differed among species as required by their different sensitivities to towing. Walleye pollock, coho salmon, and northern rock sole were towed and then transferred to tanks for recovery using methods described by Davis et al. (2001). Halibut were towed and then exposed to air (10°C) prior to transfer to recovery tanks. Halibut did not show significant mortality after 240 min tow duration and were exposed to air after 240 min tow duration to produce mortality. In brief, the towing apparatus had two nets that were cylindrical (1.2 m length, 0.7 m diameter) and constructed with 1.0 cm knotless nylon diamond mesh (Figure 1). Nets were attached to arms and were towed in a circle at 1.1 m s–1, a speed at which the fish did not swim and were pinned against the net. In each treatment (tow duration), paired replicate groups of fish were towed. Each replicate group had five fish towed together in a net. An equal number of groups were either tested for reflex impairment or were placed in recovery tanks (3140-l) to test for delayed mortality, and the proportion of fish in each group with reflex impairment or mortality was measured. The ideal way to conduct these experiments may have been to pair measurements of binomial data for reflex impairment and mortality in the same fish and treat each fish as a replicate. However, the possibility that reflex measurement and its associated handling could affect estimates of delayed mortality eliminated this option.
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Walleye pollock 13–18 cm TL were towed for 1, 10, and 15 min. Coho salmon 16–20 cm TL were towed for 5, 10, 15, and 30 min. Rock sole 15–25 cm TL were towed for 60, 120, and 240 min. Halibut 19–36 cm TL were towed for 240 min followed by exposure to air for 10, 20, 25, and 30 min. Replicate groups of baseline fish that were not towed were tested for reflex impairment or transferred to recovery tanks to test for delayed mortality. Numbers of replicate groups varied among treatments and are summarized in Table 1. In all, 210 walleye pollock, 140 coho salmon, 150 rock sole, and 180 halibut were tested in these experiments.
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Testing for reflex impairment and mortality |
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TopIntroductionMaterial and methodsExperimental treatmentsTesting for reflex impairment...ResultsDiscussionReferences |
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Reflex impairment was tested 5 min after towing for walleye pollock, coho salmon, and rock sole or after towing and exposure to air for halibut. Reflex impairment was defined as any decrease or complete inhibition of baseline reflex action. Individual fish were held in a restraining device for up to 60 s during reflex testing. The restraining device consisted of two pieces of white polyethylene (30 cm long x 7.5 cm wide x 1.1 cm thick) held together with a Velcro hinge at one end (Figure 2). Open cell foam (2.5 cm thick) was held to the inside surface of the restrainer by Velcro straps to cushion the fish and hold it securely without wounding. The fish was positioned mid-body in the restrainer with head and tail exposed, and the restrainer was held gently closed with a second Velcro strap connecting the open end. The shape and size of the restraining device can be modified in future studies to fit any shape and size of fish.
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Five reflex actions were observed in restrained fish. In the first (body flex), a fish was restrained and observed for movement of its whole body in response to restraint. In the second (operculum closure), an operculum on the restrained fish was lifted open with a nylon probe (3 mm diameter) and then released to test if the operculum actively returned to a closed position. In the third (mouth closure), the mouth of the restrained fish was opened with a probe and then released to test if the mouth actively returned to a closed position. In the fourth (gag response), a probe was inserted into the mouth and touched the throat of the restrained fish to test if the fish gagged. In the fifth (vestibular-ocular response), the restrained fish was rotated around the long body axis to test if the focus of an eye remained fixed on the investigator. Rock sole were not tested for vestibular-ocular response because baseline fish did not show this response. For individual fish, responses to each of the five reflex tests were scored as present (1) or absent (0), summed for individuals and for the five fish in a replicate experimental group, where the total possible score for a replicate group was 5 x 5 = 25. Then RAMP for each replicate group was calculated where RAMP = 1 – (total reflex response score for a replicate group / total score possible for a replicate group). RAMP ranged from 0.00 to 1.00, representing the proportion of reflex impairment where 0 = no impairment. Reflex actions used in this study were chosen based on preliminary studies (not reported), which identified actions that were presented consistently by baseline fish and were sensitive to stressors. In future studies with additional species, other reflex responses may be identified for testing and used in the same manner.
Immediate mortality was noted after fish were towed and placed in a recovery tank. Dead fish had no reflex actions, were removed from the tank, and were not included in calculating RAMP. Delayed mortality was scored by observing fish in tanks once per day for 21 d after towing. Dead fish were removed upon detection. Immediate, delayed, and total mortality were calculated as proportions in each replicate group of five fish. Fish were held for a total of 60 d after towing to observe any additional mortality.
Statistical analysis
Differences in reflex impairment associated with tow or tow and air duration and reflex type were tested for each species using mean values and Friedman's two-way analysis of variance (ANOVA). Increased RAMP, immediate mortality, delayed mortality, and total mortality associated with towing or towing and air duration were tested for each species using replicate group values and Kruskal–Wallis one-way ANOVA. Correlations between RAMP, immediate mortality, delayed mortality, and total mortality were tested for each species using replicate group values and Spearman rank correlation. Significant correlations between RAMP and total mortality were described with sigmoid curves (y = a/1 + e–(x – x0/b)) using replicate group values and tested for statistical significance using SigmaPlot 10.0 software. Statistical significance for all tests was set at p < 0.05.
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Results |
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TopIntroductionMaterial and methodsExperimental treatmentsTesting for reflex impairment...ResultsDiscussionReferences |
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Reflex impairment generally increased with tow duration in walleye pollock, coho salmon, and rock sole, or tow and air duration in halibut, and varied among reflex types (Tables 1 and 2). The gag response was impaired most in Coho salmon. Body flex and the gag response were impaired most in rock sole. Body flex, gag, and the vestibular-ocular response were impaired most in halibut. No differences in impairment were detected among reflexes in walleye pollock.
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RAMP increased significantly with tow duration in walleye pollock, coho salmon, rock sole, and with tow and air duration in halibut (Figure 3; Tables 3 and 4). Total mortality also increased significantly with stressor duration for all four species that were towed (Tables 3 and 4). Coho salmon, rock sole, and halibut showed increased immediate mortality after towing, while walleye pollock and rock sole showed increased delayed mortality after towing (Tables 3 and 4). Delayed mortality occurred up to 1 d after towing in halibut, 9 d in rock sole, and 20 d in walleye pollock and coho salmon. No further delayed mortality was noted in fish up to 60 d after towing.
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RAMP and total mortality were correlated in walleye pollock, coho salmon, rock sole, and halibut (Table 5) and showed significant sigmoid relationships (Figure 4). RAMP and delayed mortality were correlated in walleye pollock and rock sole, while RAMP and immediate mortality were correlated in coho salmon, rock sole, and halibut (Table 5). Sigmoid relationships were not plotted for RAMP and delayed mortality or immediate mortality. It is important to note that RAMP consistently predicted total mortality for the four species in this study, but was limited to subsets of species for prediction of immediate or delayed mortality (Table 5).
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Discussion |
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TopIntroductionMaterial and methodsExperimental treatmentsTesting for reflex impairment...ResultsDiscussionReferences |
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Patterns of immediate and delayed mortality varied widely among species and reflected their sensitivity to towing. The duration of towing needed initially to produce mortality varied from 5 to > 240 min, reflecting sensitivity to towing. The relative percentages of immediate and delayed mortality also varied with differences in sensitivity to towing among species. The most sensitive species, walleye pollock, showed little immediate mortality. Coho salmon and rock sole showed either equal amounts of immediate and delayed mortality or a predominance of immediate mortality. Halibut was the most resistant species and showed a predominance of immediate mortality and little delayed mortality. Based on the correlations observed, the most powerful use of RAMP would be to predict total mortality, which sums immediate and delayed mortality. Then, delayed mortality could be calculated by subtracting immediate mortality, which is easily observed immediately after capture and handling.
Other studies have shown that environmental stressors, handling, and other types of wounding from hooking produced varying patterns of immediate mortality and delayed mortality (Muoneke and Childress 1994; Edwards et al., 2004; Bartholomew and Bohnsack, 2005). Further study of delayed mortality in a wide range of bycatch species is needed to understand this process and how it varies with species and stressor types. Delayed mortality will not be significant when fish are exposed to stressors that produce a high percentage of immediate mortality. When a high percentage of immediate mortality is present in a fishing operation, it can be readily observed on board a fishing vessel. Studies in the field and the laboratory have shown that immediately lethal levels of stressors were evident for a wide variety of species within the normal range of fishing conditions, i.e. towing time, hooking location, increased temperature, and air time (ICES, 2000; Davis, 2002).
Fish condition as measured by reflex impairment was a significant predictor for mortality in walleye pollock, coho salmon, rock sole, and Pacific halibut under experimental conditions. Although few studies have measured fish condition using reflex impairment, this approach is an intuitively obvious use of information that is readily available from observations of fish exposed to fishing stressors (Davis and Parker, 2004; Davis, 2005; Davis and Ottmar, 2006). Researchers are encouraged to use reflex impairment as a sensitive tool for quantifying the effects of stressors (Olla et al., 1980; Schreck et al., 1997). RAMP is a new approach with general applicability to the problem of assessing fish health that has been impacted by human activity, including capture by fishing. RAMP directly measures in a non-invasive manner the sublethal effects of stressors as well as how close fish are to mortality. Furthermore, observations of concomitant changes in reflex impairment and physiology in fish exposed to stressors are likely to yield significant insights into linkages between physiology, behaviour, and mortality. Future research in laboratory and field settings may show that RAMP could also be useful in predicting mortality in invertebrates that are discarded or are captured and escape.
A sigmoid biphasic relationship between RAMP and total mortality was generally evident in restrained fish. A similar biphasic relationship was observed in free-swimming fish exposed to towing (Davis and Ottmar, 2006). RAMP initially increased in response to sublethal stressors. Then immediate or delayed mortality became evident and increased as RAMP continued to increase. The biphasic response of RAMP to sublethal and lethal levels of stressors is consistent with other related studies in which walleye pollock and sablefish showed impairment of feeding and startle responses to predators and increased mortality from predation or infection after prolonged swimming in a net and passage through, or impingement on, a net (Olla et al., 1997; Ryer, 2002; Davis and Parker, 2004; Ryer et al., 2004; Davis, 2005). Fish that have been discarded or escaped from fishing gear will likely show reflex impairment, which may contribute to increased mortality from predation after encountering fishing gear.
The time after stress induction at which reflex actions were tested was chosen based on a previous study of reflex impairment in free-swimming fish (Davis and Ottmar, 2006). Preliminary experiments (not reported) with free-swimming and restrained fish showed that reflexes tested at 5 min and 60 min after towing did not show changes in reflex impairment associated with increasing recovery time. The beginning of recovery from reflex impairment probably occurred between 3 h and 24 h after exposure to stressors (Davis, 2005). In future field fishing experiments using reflex impairment, it would seem prudent to test fish as soon as possible after final exposure to stressors. This test timing would eliminate possible effects of reflex recovery and would optimize the detection of reflex impairment. For future use of RAMP in field experiments, a time course study of reflex impairment after exposure to standard stressors for the species of interest would confirm that reflex actions would not change during the testing period.
Interspecific differences in the relationship between RAMP and mortality were apparent. The transition from 0% to 100% mortality occurred over a narrow range of RAMP scores for sensitive species such as walleye pollock and coho salmon. Less sensitive species such as rock sole and Pacific halibut showed a wider ranger of RAMP scores over which mortality increased. Using RAMP to predict mortality in sensitive species may be difficult because of high variability associated with the rapid increase in mortality rates over a narrow range of RAMP. Prediction of mortality in sensitive species may be improved by finding and using other reflex responses that are more resistant to the effects of stressors and result in a wider range of RAMP values. Previous laboratory and field fishing experiments have shown that prediction of mortality rates in sensitive species is generally difficult and variable because mortality increased rapidly with small increases in stressor intensity (ICES, 2000; Davis, 2002).
Differences in sensitivity to stressors may exist between fish in the laboratory and wild fish, resulting in relationships between reflex impairment and mortality that would not be valid for field use. Fish used in the present study were generally smaller than fish that are discarded. Also, fish were held in the laboratory for extended periods of time. While the predictions of mortality using RAMP derived from laboratory fish are not expected to be valid for wild fish, the concept of predicting mortality based on reflex impairment should be valid in field conditions. Basic fish biology, physiology, and behaviour does not vary between laboratory and field; only the degree of expression of specific behaviour and stress responses. Expansion of the results of this study to wild fish and field fishing conditions would require identifying sets of reflexes that are consistently present in baseline wild fish and that are impaired by all relevant fishing stressors.
The process of developing RAMP for predicting bycatch species mortality in field fishing experiments includes identifying appropriate reflex responses for baseline fish and generating RAMP curves for mortality prediction (Figure 5). In the first step, appropriate reflex actions are identified using baseline fish captured and held with a minimum of stress. The principal requirement is to identify three to six reflex responses that are consistently presented by baseline fish after stimulation and that occur in a manner that can clearly be scored as present or absent. The second step is to generate the RAMP curve using field fishing experiments that simulate actual fishing conditions of concern and include relevant factors that result in a wide range of mortality. Potential factors include, but are not limited to, gear design and deployment, catch size, wounding, temperature change, time in air, light intensity, fish size, and combinations of factors (ICES, 2000; Davis, 2002; Suuronen, 2005). Consistent responses of RAMP to stressors and the ability to sample numerous fish quickly on board ship or in cages without long-term monitoring makes RAMP a potentially powerful and efficient method for predicting discard and escapee mortality. New fishing experiments that include a broad range of conditions and extensive replication, possibly with RAMP, could be conducted to model bycatch mortality and to evaluate the efficacy of changes in fishing practices and bycatch reduction devices.
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Acknowledgements |
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This research was made possible through the sustained efforts of members of the NOAA Alaska Fisheries Science Center Fisheries Behavioral Ecology Program by providing assistance in obtaining permits, collecting and rearing fish, and conducting experiments. Team members include Michele Ottmar, Paul Iseri, Scott Haines, Mara Spencer, Rich Titgen, Tom Hurst, Cliff Ryer, Al Stoner, and Cindy Sweitzer. Animal care and use was according to protocols prescribed by the American Fisheries Society (http://www.fisheries.org/html/Public_Affairs/Sound_Science/Guidelines2004.shtml).
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