By demonstrating how PSAT tilt is related to fish activity and developing methods for summarizing accelerometer tilt data for satellite transmission, our work has resulted in a new method for characterizing activity and assessing survival of Pacific halibut that is likely adaptable to a variety of benthic fish species. Our approach to assessing survival, which features comparing activity patterns between healthy fish, carcass tags, and weighted tags, is necessary for determining survival of Pacific halibut due to the sedentary nature of healthy fish and the flat terrain of the Bering Sea study area. Other PSAT methods for determining survival based on depth and temperature data alone (e.g., ) would not be effective under these conditions. Therefore, in addition to the ability to distinguish survival from mortality, this baseline study has also provided a valuable new method for obtaining information about Pacific halibut activity patterns that has a broad range of future applications.
Objective 1: Relating PSAT tilt to Pacific halibut activity
This study confirms that implementing accelerometer-based PSATs can provide direct measurements of Pacific halibut activity without the need to recapture tagged fish. PSAT tilt, actuated by swimming movement, was shown by direct observation in the laboratory and analysis of data from free-ranging fish to clearly delineate swimming activity. The majority of swimming bouts identified by tilt were accompanied by simultaneous changes in depth. However, even though our research to link PSAT tilt to Pacific halibut activity was conducted in an area with heterogeneous bathymetry, approximately 20% of the tilt-indicated movement events were not accompanied by depth changes. This is not surprising, considering that fish often swim at constant depth and may follow isobaths in high-relief habitat. For low-gradient terrain like the Bering Sea, the percentage of movement events that would only be detectable via acceleration would be expected to be much higher than observed in our initial study area in southeast Alaska.
PSAT tilt data provided a stronger signal than change in depth for detecting the hopping activity mode, which was the dominant activity mode for all three fish from Port Frederick. Most of the swimming bouts that were not accompanied by changes in depth occurred during the hopping activity pattern. Even when change in depth did accompany swimming bouts identified by PSAT tilt, depth changes were often close to the limit of tag measurement resolution and hourly changes were similar to tide-related depth changes. Therefore, the use of accelerometer PSATs provides the ability to identify an important behavior that could be missed with tags that measure only depth.
Objective 2: Characterize activity patterns of free-ranging fish
Our finding that free-ranging tagged Pacific halibut in Port Frederick, and the Bering Sea, displayed prominently diel activity patterns during the summer is similar to the results of a previous study on the behavior of Pacific halibut that employed depth-only archival tags. Scott et al.  found that individual Pacific halibut were active primarily during either day, night, or dusk/dawn during the summer foraging period. This strong tendency toward diel behavior produced clear patterns in acceleration data that greatly facilitated the identification of live, healthy fish with accelerometer PSATs.
Stationary behavior was a dominant activity mode for the fish tagged in Port Frederick. Pacific halibut are ambush predators and known to lie motionless on the seafloor, but the duration of completely stationary behavior has not been previously quantified. Scott et al.  identified a “tidal” mode in depth data that was prominent during summer months (along with diel behavior), where change in depth was related only to tidal cycles, and hypothesized that fish were inactive on the seafloor during this mode. In this scenario, the depth measured by the tag will fluctuate in direct relation to changes in water column height above the stationary fish resulting from tides. Based on the information from our study, activity identified as “tidal” by depth data alone could have resulted from completely stationary behavior. However, it could also have resulted from the hopping activity pattern, where changes in depth are infrequent and subtle. Thus, our study offers the first insights into the frequency and duration of stationary behavior that can be distinguished from movement that occurs at a constant depth.
The “hopping” and “sustained swimming” activity patterns identified in this study could result from different modes of foraging. Hopping behavior has been observed in juvenile Pacific halibut in a laboratory setting (C. Ryer, Alaska Fisheries Science Center, Newport, Oregon, personal communication) associated with foraging. Pacific halibut are visual foragers, and foraging activity is strongly related to light levels . However, they may also detect prey by olfaction , allowing them to forage in low-visibility settings, at low light levels, and at night. It is possible that different activity patterns correspond to foraging strategies in different visibility conditions, or vary according to prey targets.
The ability to characterize activity patterns with PSATs has many potential applications beyond assessing survival. For example, PSAT data could be used to estimate vulnerability to capture in the day versus night, in correlation with tidal flux, or link activity patterns to PSAT depth and temperature data. Information on activity patterns from PSATs could also be used to improve geolocation models through inclusion of directly measured behavioral states .
Objective 3: Develop PSAT summary metrics of fish activity
Well-designed summary metrics are critical for obtaining information on behavior without the need for physical recovery of tags. The KD metric detected activity and was robust to tidal currents whereas %tilt metric could be affected by tidal currents. Still, tidally influenced periods were easily identified because increased %tilt was accompanied by few or no knockdowns. When fish were active, the activity reported by the %tilt metric was much greater than the signal from tidal currents and varied at other temporal scales than tidal (e.g., diel, or semilunar). Finally, high values of %tilt is one characteristic of the sustained swimming movement pattern. Therefore, we consider the %tilt metric to be a valuable component for assessing activity patterns and survival even though it is occasionally vulnerable to detecting tilt that is caused by tidal currents.
In addition to possible effects of tidal currents on the tilt of PSATs, two other issues should be acknowledged. First, a tag on a fish that is swimming steeply downward is likely to retain a relatively vertical orientation thus might provide the same acceleration signal as a stationary fish. Some of the underdetections of both KD and %tilt metrics in the Port Frederick fish appear to have been due to steep downward movements. However, despite the chances for under-detection of individual movement bouts, overall activity patterns were still clearly evident in the KD and %tilt because extended periods of steep downward movements were relatively infrequent.
Additionally, tags on individual fish differed in the distribution of tilts measured during swimming bouts. Of the Port Frederick fish, Fish PF-1 and Fish PF-3 had tilt distributions centered at higher values than Fish PF-2. While some of these differences may relate to very slight variations among tags in sensor orientation relative to tag orientation, it is likely that fish vary in the distributions of their swimming speeds. Because of this variability among individuals in magnitude of tilt values when swimming, data sets should be compared to a range of known values or patterns in metrics rather than simply comparing among individuals. This can ultimately affect the choice of tilt threshold, as a chosen value must apply to all tags used in a given setting; in this study we chose a value that would intentionally allow some real movement to be missed while minimizing false indications of movement. Here, the choice was a matter of study context: the desire to develop protocols that would reduce the probability of inferring survival when fish have in fact died during the deployment period in the context of discard mortality rate estimation. For other subject populations and questions, different thresholds may be chosen to satisfy research objectives.
Our methods for summarizing accelerometer data based on simple tilt measurements have provided a simple, effective, low-cost PSAT that can be used to assess bycatch survival. Other methods for assessing survival of bycatch based on high-resolution accelerometer data have recently been developed . However, these methods require the physical recovery of tags after they release from the fish, and are therefore not feasible for remote locations such as the Bering Sea. Methods for summarizing high-resolution acceleration data for transmission to satellites have been developed to describe diving activity of a marine mammal . However, this approach requires more processing capability than our metrics do and requires the tag to be rigidly attached to the animal. Our approach is less computationally expensive and practical for application to fish as opposed to marine mammals.
Objective 4: Develop procedures for assessing survival of Pacific halibut bycatch
Based on the ability of PSATs to provide information on typical activity patterns of live Pacific halibut, procedures were developed for assessing survival of Pacific halibut bycatch. A substantial deployment of these tags on Pacific halibut released from Bering Sea trawlers using expedited release (i.e., deck-sorting) procedures has already been completed and a manuscript describing results has been submitted for publication (C. Rose, unpublished).
Ideally, guidelines chosen for assessing survival could be coded into an automated screening algorithm that would largely eliminate biases associated with relying upon individual interpretations, which are likely to vary according to the experience of the screener. However, while the evaluation steps detailed above are clear and objective, a large variation in activity patterns should be expected from large samples of at-large, potentially stressed fish. Distinguishing between mortality and premature tag release from a live fish may be challenging for short data sets, particularly given the period of low activity observed in healthy fish during the first few days following release. Our control data sets could not include observations of confirmed delayed mortality, so the current recommendations are based solely upon observations of acceleration profiles of healthy versus dead individuals. It is likely that the stress-induced death of a fish will produce data that take additional forms than have been detailed herein. Therefore, assessments should initially be made with these results as guidelines and then take into consideration the range of observations that emerge from the collection of additional data. Tag data should be examined in plots at a range of resolutions that allow assessment to be conducted across days and time-of-day (see example plots and additional details in Additional file 1).
Adapting methods for other applications (species, geographic regions)
The ability of the PSAT metrics to detect Pacific halibut activity patterns is important for assessing bycatch survival. The methods reported here are likely to be readily applicable to the closely related Atlantic halibut (Hippoglossus hippoglossus) as well as to other large flatfishes such as Greenland halibut (Reinhardtius hippoglossoides) and California halibut (Paralichthys californicus). Similar protocols might be developed for a host of other species that are sufficiently large to bear these tags. While these tags were successfully deployed on Pacific halibut as small as 55 cm in length, tag stress and setting appropriate thresholds to differentiate activity would likely be more difficult with smaller, weaker, and slower-swimming fish.
We found control data collected from tags on healthy fish, weighted tags, and carcasses to be critical for understanding and interpreting tag data and recommend similar procedures for other studies. Tags on fish that were known to be healthy when released were needed to characterize the normal range of activity patterns. Weighted tags provided the response of metrics to tides and wave action in the area of release. While our study was conducted in the summer with few storms, data from one weighted tag indicated that storm activity could produce significant KD values. Studies conducted in shallower waters than our study (range 53–366 m) during a storm season might be greatly affected. Likewise, %tilt values can certainly be affected by bottom currents, particularly if current speeds approach the normal swimming speeds of the subject fish. However, we found the %tilt metric to be valuable in detecting orientations of the PSAT that were not typical of live fish (e.g., extended periods of maximum tilt that could occur if a PSAT was lodged between the carcass and the substrate). Carcass tags were particularly informative, as the variety of patterns manifested by dead fish (e.g., scavenging action or the tag pinned underneath a carcass) is potentially much larger than for weighted tags and could be increased by wave or current action.
For more general application of methods developed here, we strongly recommend laboratory studies or retrieval of detailed data sets from free-ranging fish to understand the way that the PSAT moves when the fish swims and to set appropriate values for (1) the change in vertical acceleration needed to define a KD, and (2) the threshold value for %tilt used to define activity. These values would need to be adapted to the swimming characteristics and physical requirements of each subject species and study environment. For example, many shark species (Elasmobranchii) need to move constantly, so any period of time during which such a fish can be determined to be stationary should likely be interpreted as mortality. Other demersal species could have more extended periods of stationary behavior that would need to be accounted for in determination of mortality or slower swimming starts that could make a KD-like metric hard to establish. Different tag or tag attachment configurations would change tilt/speed relationships relative to those reported here and would therefore require unique threshold calibrations.
For our application for Pacific halibut, the vast majority of the acceleration measurements were static, allowing the data to be treated as tilt measurements. Dynamic accelerations, which could occur with species that move the tag more vigorously, or if the tag measurement resolution is increased above 1 Hz, could confound the use of tilt-based metrics by introducing excessive noise in the acceleration-tilt relationship.
Utility of PSATs for assessing survival of Pacific halibut
Utilization of PSATs for determining bycatch survival solves many issues encountered by other survival estimation methods. Mark-recapture studies, which infer mortality from the relative return rates of different classes of fish, require knowledge or assumptions about reporting rates, natural mortality, migration, and survival of the best-surviving class. They may also require intensive recovery efforts lasting years to obtain sufficient returns. Studies that retain the affected animals in enclosures (e.g., [19,20,21]), where their fates can be determined, can be affected by stressors that are added (e.g., limited movement, crowding, unfamiliar environmental conditions, insufficient food, and inability to avoid sand flea, Amphipoda spp., predation) or excluded (e.g., predators) by the enclosures or holding conditions. Holding studies also become increasingly difficult with larger and more mobile animals. By using PSATs, the tagged fish can be fully exposed to the same post-release environment they would experience if not tagged. Therefore, results more accurately reflect the untagged population compared to post-capture holding studies. Barring tag or transmission failure, data are received on all subject animals without the need for physical tag recovery, and are available for analysis soon after the tags release. This eliminates recovery rate and selectivity assumptions necessary to estimate survival with conventional tagging, as well as requiring lower initial tagged samples sizes to ensure a given level of recovery data and producing a much shorter and more-predictable timeline for obtaining those data than can be accomplished with conventional mark-recapture methods.
The development of accelerometer PSATs in this study provides several advantages for bycatch survival studies. Using only accelerometer sensors and relatively simple metric algorithms reduces tag costs, allowing for the use of larger sample sizes than would be employed using more expensive archival tags. This consideration is particularly important for bycatch survival experiments. In addition, accelerometer PSATs are valuable in areas with flat terrain, where changes in depth may not be an adequate signal for fish survival.
Knowledge of Pacific halibut bycatch survival is of particular concern considering the magnitude of bycatch and the cultural and economic importance of the directed fisheries. Bycatch mortality of Pacific halibut was estimated to be 3.2 M kg compared to the commercial harvest of 11.3 M kg in 2016 ; however, actual survival and mortality rates of released bycatch are currently poorly understood considering the number of confounding variables involved in previous studies [1,2,3]. In light of recent declines in estimated Pacific halibut stock biomass , improved understanding of bycatch survival will provide valuable information for setting future harvest limits for commercial and recreational halibut fisheries and Prohibited Species Catch limits for non-target fisheries.