Time of death: behavioral responses of an oceanic whitetip shark, Carcharhinus longimanus, to capture by a longline fishing vessel

Bycatch mortality in longline fisheries is a major contributor to global declines in shark populations. The duration of time that an animal is hooked and the impacts of hooking on behavior affect the likelihood of mortality. However, limited information exists on the behavior of sharks to longline capture because of difficulties observing hooking events. Using a fortuitous recovery of an archival satellite tag, we describe the movement of an oceanic whitetip shark (Carcharhinus longimanus) and examine the behavior prior to its mortality in response to hooking on a longline. A 1.5 m (fork length) C.longimanus was tagged and released in good condition by a fisheries observer following initial capture on a US longline fishing vessel. After release, the shark resumed normal vertical behavior within 5 h. Over 198 days, the shark undertook wide-ranging movements throughout the Pacific between Samoa, Niue, and Tonga. The shark was hooked by a second longline vessel while conducting routine yo-yo diving between 0 and 120 m depth. For the first hour after being hooked the shark exhibited high swimming activity with rapid vertical movements between 20 and 40 m indicative of an initial struggle against the line. After this, the shark struggled at the surface for approximately 5 h, until it succumbed to exhaustion and died on the line. Fight time has a strong influence on the mortality rates of sharks captured in commercial longline fishing operations. Data obtained from this shark offers further understanding of capture behavior and time to mortality on a longline for C.longimanus which may assist managers as they work on options to reduce mortality rates for this threatened species.

and physiology while captured, and a limited understanding of the specific timepoints at which detrimental changes occur during the fishing process [4].
The oceanic whitetip shark (Carcharhinus longimanus, hereafter OCS) is an epipelagic, highly migratory species distributed throughout the world's tropical and subtropical waters.Once thought to be the most numerically abundant shark species in tropical waters [5,6], OCS populations have experienced significant declines throughout their range over the last several decades due to increased fishing pressure and high demand in the international shark fin trade [7][8][9].OCS are commonly caught in tropical tuna purse seine fisheries, hook and line fisheries, troll fisheries and pelagic and bottom trawls [10], yet the largest source of mortality of OCS is bycatch-related mortality in commercial longline fisheries [8,11].Following precipitous population declines, OCS was listed as 'Threatened' under the United States Endangered Species Act (ESA) [12] in 2018, as 'Critically Endangered' globally by the International Union for the Conservation of Nature (IUCN) also in 2018 [7], and under appendix II of the Conventions on the Conservation of Highly Migratory Species and on the International Trade of Endangered Species (CITES) in 2013.
Reducing fishing-related mortality to OCS continues to be a major goal of conservation and fisheries management organizations.Studies show increased survival of OCS with changes to operational and gear configurations and better fisher handling practices [2].For example, leaving sharks in the water and removing as much trailing gear as possible (i.e.< 2.5 m; [2]), removing shallower hooks in longline sets [14,15] and reducing soak time of hooks [16] has been shown to substantially increase the likelihood of survival for OCS and other species that are more sensitive to the lethal physiological changes of capture related stress [13].Observable capture behavior can be used to make inferences on the internal physiology of caught species and provide additional information on methods to reduce mortality for longline caught sharks [16,17].However, collection of such data for threatened species is difficult, as is directly observing the sequence of events that determines the likelihood of survival after capture.
Using a recapture of an OCS tagged with an accelerometer, we describe the movements, behavior and body activity prior to its mortality after hooking by a longline fishing vessel in the Pacific Ocean.Specifically, we investigate (i) the overall movements between tagging and recapture, (ii) the fine-scale behavior of an OCS posthooking, and (iii) the time taken for an OCS to fight against longline fishing gear prior to mortality.This data can be used to inform managers regarding options to reduce hooking mortality.

Methods
A 1.5 m (5ft, fork length) OCS was captured incidentally by a U.S.flagged, American Samoa (AS) permitted tuna longline vessel on 1 May 2018 (Fig. 1).AS permitted tuna vessels target albacore tuna (Thunnus alalunga) using deep-set longline fishing gear which includes; ~ 30 hooks per float; ~ 20 m long float lines; ~ 20 m long monofilament branchlines; and stainless steel circle hooks.A trained fisheries observer was onboard the vessel tagging sharks for a post release survival study.The shark was determined to be alive and in good condition, so the observer deployed a Pop-off Archival Tag (miniPAT, Wildlife Computers, Redmond, WA, USA) externally, anchoring the tether of the tag under the shark's dorsal musculature using a telescoping tagging pole.The mini-PAT collected and stored temperature, depth, irradiance and tri-axial acceleration (x-axis, y-axis, z-axis, ranging from −2 to 2 G at 0.05 G resolution) time series data at a sampling rate of 5 s (0.2 Hz).The shark was released after tagging by cutting the branchline and it swam away in 'good' condition (see Hutchinson et al. [2] for condition descriptions) with a circle hook and approximately 1 m of monofilament trailing gear.Tagging took approximately 3 min from the shark being brought alongside the vessel to release.
The same shark was recaptured south of Tonga by a Tongan commercial longliner, 198 days after initial tagging and release on 12 November 2018 (Fig. 1).The vessel was targeting bigeye tuna with a configuration including; 10 hooks set between floats; 20 m long float lines; 20 m long monofilament branchlines with lightsticks; and stainless steel circle hooks (Fig. 2).The mainline was set at 22:10 UTC for a targeted soak time of 12 h.The shark was reported to be dead on the line when the gear was retrieved and it was brought to the vessel where the tag was removed from the shark and stowed on board.

Data analysis
Location estimates were generated using the tag manufacturer's geolocation processing software WC-GPE3 (Wildlife Computers).GPE3 uses a gridded hidden Markov model with 0.25° by 0.25° grid spacing and the maximum likelihood location estimates are interpolated to a 0.025 by 0.025 grid spacing and smoothed with a cubic spline.The resultant maximum likelihood locations and probability surfaces were analyzed and visualized via the RchivalTag package in R [19].Additionally, depth time series data were used to identify and analyze characteristic dive patterns to assess; (i) time to recovery after the initial capture and tagging event, and (ii) the shark's vertical profile and hooking behavior.
The acceleration sampling interval (0.2 Hz) was too low to filter the static (tag orientation) and dynamic (tag movement) components from the raw acceleration.Therefore, standard acceleration metrics for body activity (overall dynamic body acceleration (ODBA) and tailbeat acceleration or cycle) could not be estimated.Rather, we conducted a qualitative examination of the tri-axial acceleration coupled with the depth recordings to estimate the hooking and mortality events.The z-axis measured acceleration along the vertical axis of the tag (from the antenna to the base pin attached to the tether) and was used as a general indicator of the shark's body orientation where recorded z-axis values of −1 G indicate the tag was static and in a vertical orientation with the antenna pointing towards the surface.All dates and times are reported in UTC for consistency because of the location of the tag deployment and recovery which crossed the international date line (Fig. 1).

Results
The OCS of unknown sex was tagged and released by an American Samoa permitted longline vessel due south of Samoa (Fig. 1) on May 1st, 2018 at 07:43 UTC.Immediately after tagging, the shark gradually swam down from the surface to 110 m over 41 min and began conducting narrow, irregular vertical movements between 110 and 140 m (Fig. 3).This erratic 'recovery' behavior lasted approximately 5 h (until 12:43 UTC), before the shark transitioned to normal "yo-yo" diving, moving from the top 20 m to 120 −140 m in an oscillatory manner (Fig. 3).Once normal swimming behavior resumed, the shark headed northeast towards Tongareva and remained within this region between June and July (Fig. 1).In August 2018, it began moving back in the direction it came and followed the bathymetry of underwater seamounts towards Niue (Fig. 1).In October 2018, the shark headed southwest towards Tonga where it was recaptured by a Tongan longline fishing vessel and died on 12 November 2018 south of Tonga (Figs. 1, 4).
The vertical profile and body acceleration of the shark was quantified across an 18-h period during capture on 12-13 November 2018 (Fig. 4).Just prior to capture, the shark was undertaking routine 'yo-yo' swimming behavior between 10 and 120 m (time A, Fig. 4) and had normal acceleration amplitude (lower panel, Fig. 4).At approximately 22:50 UTC on 12 November, the ascent phase of the last dive ended abruptly around 40 m where the shark presumably first experienced the tension from the line, (time C, Fig. 4).Based on the configuration of the longline gear (Fig. 2) and the depth records from the  4).The animal was able to make its way to the surface post-hooking (across 42 min) and at ~ 30 m, it performed a series of rapid vertical movements between 20 and 60 m (time C, Fig. 4) for an hour.This erratic behavior is also reflected in the wider acceleration amplitude values (lower panel, Fig. 4).The shark moved gradually shallower (times C-D, Fig. 4), and body activity remained high (compared to its normal swimming behavior) while the shark was holding near the surface at 00:12 suggesting that it was likely trying to stay near the surface while struggling against the line and with the weight of the fishing gear (time D, Fig. 4).The shark remained near the surface for approximately 4 h until 04:00 UTC, at which point the vertical profile showed the individual sank to 120 m (times E-F, Fig. 4).The associated low levels of acceleration amplitude between 04:05 and 04:19 (lower panel, Fig. 4) suggests the shark likely died at this point, weighing down the branch line and changing the orientation of the tag, as the shark's negatively buoyant body was hanging vertically from the line while the positively buoyant tag was attempting to orient with the antennae pointing towards the surface (z-axis (red), lower panel, Fig. 4).
At 04:38 (UTC) the shark was hauled towards the surface as the vessel began to retrieve the longline (time F, Fig. 4).At this point, tension from the mainline during the haul kept the shark's body near the surface for a period of 5 h (times G-H, Fig. 4).At 09:44 UTC, the shark was brought onboard where the tag was removed and stored on the vessel (time H, Fig. 4).From these observations, we can infer that the shark struggled against the gear for just under 5 h before dying on the line.

Discussion
Reducing fishing mortality for bycatch species that are subject to no retention measures, such as OCS requires improved knowledge of direct behavioral and physiological responses to capture.In this study, we use body acceleration and depth data to describe the response of an OCS to hooking in longline fishing gear.We show Fig. 2 Schematic representation (not to scale, adapted from [18]) of tropical tuna longline fishing gear configuration.The image shows; length of the floatline; length of the branchline; mainline; hook position; hooks between floats (HBF).Fishers use a set speed and specific distance between hooks that will allow hooks between floats with 20 m lines to fish at depths of ~ 200 m on average [18] that the individual struggled against the gear for approximately 5 h prior to dying on the line.Although from a single event, this dataset fills important knowledge gaps regarding the resilience of OCS to capture stress which can inform conservation management decisions for mortality mitigation of protected species.While many of the drivers of at-vessel mortality are difficult for fishers to control [16], knowledge of the effects of fishery characteristics (i.e., soak times and gear composition) can help inform the decision making process when accounting for trade-offs in catch versus mortality mitigation of endangered species [20,21].
OCS populations have undergone precipitous declines globally, and Western Central Pacific Ocean stock assessments have shown the stock is overfished with overfishing still occurring [8,22].Because fishing has been identified as the largest source of mortality for OCS, a series of conservation and management measures within all major tuna Regional Fisheries Management Organizations have been adopted.These include measures prohibiting retention of OCS in tropical tuna fisheries world-wide [23][24][25][26], and gear modifications such as banning shark lines [27,28] and a compulsory switch to monofilament (rather than wire) leader material to allow sharks to 'bite-through' the line [26,29].While these measures may be effective in reducing overall bycatch mortality [2,30,31], many caught individuals may be dead or dying by the time fishing gear is retrieved [15].At-vessel mortality rates for OCS in US fisheries are relatively high (21.5-32.7%,[2]).Thus, simple fishery modifications such as banning wire leaders to allow bite-offs [2,18,29,31], reducing time spent on a hook [16,20], and hook depth [14,15] may be tangible options for reducing fishing mortality rates for OCS and other important bycatch species [16,32].
Observing the sequence of behaviors before and during longline capture can provide key information on best practices to increase post-release survival rates for bycaught sharks [17].When it was first hooked on the line, the OCS observed here exhibited initial increases in overall body activity coupled with erratic narrow vertical movements.The capture behavior of this OCS was similar to that documented by [17] that showed hooking and capture initiates an immediate stress response and depending on condition, individuals may respond with high intensity burst swimming to escape and/or force oxygenated water over their gills to maintain ram ventilation [1,17].This prolonged exhaustive activity, over the course of 5 h, likely caused irreparable physiological damage leading to the death of the shark [1].Improved methodologies to reduce capture stress coupled with safe handling and release practices could provide important opportunities to increase post-release survivorship [2].Additionally, the depth of the hook on which the individual was caught may have influenced its susceptibility to capture.In this study, the OCS was caught on a hook between 40 and 100 m, confirming previous studies of increased catch rates of OCS on shallower hooks < 100 m [14,33] and on longline vessels targeting swordfish that operate to 100 m [34].We echo previous studies suggesting that the removal of shallow hooks on longline gear may be an effective mitigation option to reduce OCS bycatch [14,15,34].
The 5-hour time to mortality in this study suggests that shorter hook soak times may assist in reducing OCS mortality.However, further sampling is crucial to understand variability in time to mortality across individuals and species (see Additional file 2: Table S1 [4,35,36] for more information variability to capture stress across species).In general, OCS are thought to be relatively resilient to capture.OCS caught in pelagic longline gear have demonstrated post-release survival rates of up to 85% (provided they are in good condition at the vessel and trailing gear is minimized [2]), and 23.5% of hooked individuals can survive more than 8 h, with some surviving up to 14 h on the line (Additional file 2: Table S1, [20].The comparatively short time to mortality in this study may have been influenced by a relatively small body size of 150 cm FL [32,37], its condition at capture [2,36], and/ or its recent diving behavior [38,39].Although there was no evidence of external injuries, the individual had survived a previous hooking event on a longline 198 days earlier.Further, in the preceding 10 h before capture, the individual made deep-dives to 800 m (5 °C water temperature, Additional file 1:Figure S1) and was captured at 24.5 °C (the lower end of its preferred thermal range [15]).Quick movements into colder waters below the mixed layer are thought to be an important foraging strategy for OCS [32,40,41], yet can lead to high energy expenditure [42] and require rapid returns to shallow waters to prevent heat loss [43].Therefore, the relatively quick mortality in this case may have potentially been This dataset has identified the 'fight time' to mortality for an individual from a population that has been assessed as overfished with overfishing still occurring [8].Accurate and effective management to reduce fishing mortality to OCS will require a deeper understanding of the biotic and abiotic drivers of fishery interactions and animal behavior prior to and during capture.The combination of a reduction in hook soak times with the implementation of safe handling and release practices, such as minimizing trailing gear could improve the efficacy of current no-retention measures and thus, assist in the recovery of OCS populations [2,44].

Fig. 1 A
Fig. 1 A bathymetric map showing the maximum likelihood locations of the tagged OCS across the deployment period May-November 2018.Green circle indicates where the tag was deployed on 1 May 2018 and the red triangle indicates where the individual was re-captured and subsequently died on 12 November 2018

Fig. 3 A
Fig. 3 A The depth and recovery profile of the OCS after being tagged and released by a US commercial longline vessel on 1 May 2018.B shows the return to regular dive behavior across the first week (1-8 May) after the tagging and recovery event (designated by the red asterisk)

Fig. 4 A
Fig. 4 A visual depiction of depth use (upper panel) and tri-axial acceleration (lower panel; teal; x-axis, gold; y-axis, red; z-axis) for the OCS across an 18 h period between 12-Nov-2018 12:10 and 13-Nov-2018 01:30 UTC pre and post hooking.Each letter represents a change in shark behavior across the capture process.Points A-B show normal yo-yo diving behavior.Near point C the shark likely gets hooked or first experiences tension from the line if it was hooked during the ascent between points (B) and (C).Between points C and D, the shark fights actively against the gear and brings it towards the surface.Between points D and E, the shark struggles on the line at the surface, then gradually sinks (times E-F) while on the line.The negative value of the z-axis acceleration (red) indicates the tag was in an upright orientation, pointed towards the surface.The shark is brought to the surface between points (F) and (G) due to the tension from the haul of the longliner.Point H depicts the shark being handled near the vessel where it was recorded as dead on the line