Survival of Atlantic halibut (Hippoglossus hippoglossus) following catch-and-release angling

Survival of Atlantic halibut (Hippoglossus hippoglossus) following catch-and-release angling

G Model ARTICLE IN PRESS FISH-4449; No. of Pages 8 Fisheries Research xxx (2016) xxx–xxx Contents lists available at ScienceDirect Fisheries Rese...

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ARTICLE IN PRESS

FISH-4449; No. of Pages 8

Fisheries Research xxx (2016) xxx–xxx

Contents lists available at ScienceDirect

Fisheries Research journal homepage: www.elsevier.com/locate/fishres

Survival of Atlantic halibut (Hippoglossus hippoglossus) following catch-and-release angling Keno Ferter a,∗ , Audun H. Rikardsen b , Tor H. Evensen c , Martin-A. Svenning d , Sean R. Tracey e a

Institute of Marine Research, PO Box 1870, N-5817 Bergen, Norway Department of Arctic and Marine Biology, UiT – The Arctic University of Norway, N-9037 Tromsø, Norway c Nofima AS, Muninbakken 9-13, Breivika, PO Box 6122, N-9291 Tromsø, Norway d Norwegian Institute for Nature Research, Arctic Ecology Department, Fram Center, PO Box 6606, Langnes, N-9296 Tromsø, Norway e Institute for Marine and Antarctic Studies, University of Tasmania, Private Bag 49, Hobart, TAS 7052, Australia b

a r t i c l e

i n f o

Article history: Received 29 January 2016 Received in revised form 18 May 2016 Accepted 25 May 2016 Handled by George A. Rose Available online xxx Keywords: Acoustic telemetry Behavior Pop-up satellite archival tags Post-release mortality Recreational fisheries Tagging

a b s t r a c t Catch-and-release (C&R) of Atlantic halibut (Hippoglossus hippoglossus) has been heavily debated as a management strategy to reduce fishing mortality of this species while maintaining angling opportunities in Norwegian recreational fisheries. However, little information exists on what proportion of the fish survive post release. To test if C&R affects short- and long-term survival of Atlantic halibut, halibut (>120 cm; N = 11) were caught on angling gear using commonly used fishing lures, and tagged with both pop-up satellite archival tags (PSATs) and acoustic transmitters. Survival was determined by the vertical migration patterns of individuals measured by the tags during individual monitoring periods ranging from 3 to 248 days (median 80 days) after the C&R event. No short-term mortality was observed post release. In terms of long-term survival, eight halibut were confirmed to have survived the monitoring periods while one halibut had insufficient data. For the other two individuals, the acoustic transmitters showed a cessation of vertical movement after 38 and 44 days, which could neither be verified nor disproven by the PSAT recordings (due to earlier detachment and tag malfunction of the PSATs). Since premature tag shedding was frequent in this study, it cannot be concluded if the cessation of vertical movement was because of tag shedding or delayed mortality. The results of this study indicate that Atlantic halibut is resilient to C&R angling, and that C&R of Atlantic halibut may be an effective management strategy to reduce fishinginduced mortality. However, the effects of severe hooking injuries, impacts on smaller individuals, and potential sublethal consequences of C&R were not covered in this study, and are still poorly understood. To minimize negative impacts of C&R and to promote fish welfare, fisheries managers are encouraged to implement best practice C&R angling guidelines for Atlantic halibut. © 2016 Elsevier B.V. All rights reserved.

1. Introduction Atlantic halibut (Hippoglossus hippoglossus) is widely distributed in the North Atlantic Ocean (Haug, 1990) and is highly valued by commercial and recreational fishing sectors. In Norwegian waters north of 62◦ N, the annual commercial landings of Atlantic halibut have increased significantly during the last decade, but are still less than those seen fifty to sixty years ago (Høines et al., 2009). While commercial fishermen in Norway are obliged to report all landings, little is known about the recreational catch, as anglers are

∗ Corresponding author: Keno Ferter, Institute of Marine Research, PO Box 1870, N-5817 Bergen, Norway. E-mail address: [email protected] (K. Ferter).

not required to report their catches (landings or releases). Except for landings sold by recreational fishermen to the commercial market (accounting for about 2.5% of the reported landings (Norwegian Directorate of Fisheries, 2012a)), the only data available on Atlantic halibut landings by marine recreational fisheries in Norway are for the marine angling tourism sector. Vølstad et al. (2011) estimated that 80 tons of Atlantic halibut were landed by one sector of the marine angling tourism industry during 2009, accounting for about 5% of the commercial landings that year. The authors pointed out however, that this estimate is uncertain, and that the study covered neither the entire tourist fishery nor the local recreational fishery. Considering the high participation rate in marine recreational fishing in Norway (ca. 33%; Vaage, 2015) and the increasing importance of marine angling tourism in Norway (Borch et al., 2011), the recre-

http://dx.doi.org/10.1016/j.fishres.2016.05.022 0165-7836/© 2016 Elsevier B.V. All rights reserved.

Please cite this article in press as: Ferter, K., et al., Survival of Atlantic halibut (Hippoglossus hippoglossus) following catch-and-release angling. Fish. Res. (2016), http://dx.doi.org/10.1016/j.fishres.2016.05.022

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ational catch of Atlantic halibut is expected to be substantial (e.g. Norwegian Directorate of Fisheries, 2012a). In 2012, the Norwegian Directorate of Fisheries evaluated if a closed season should be implemented for commercial and recreational fisheries during the summer months to ensure a sustainable fishery for Atlantic halibut in the future, mainly because recreational fishery effort is assumed to be high during this time of the year (Norwegian Directorate of Fisheries, 2012b). To date, this closed season has not been implemented, but the Directorate of Fisheries has asked for advice on potential alternative measures that could increase abundance of the Atlantic halibut stock north of 62◦ N, e.g. additional harvest measures for recreational fisheries including the introduction of a maximum landing size (Norwegian Directorate of Fisheries, 2012a). A study on catch-and-release (C&R) among marine angling tourists in Norway showed that the proportions of released fish of many target species are higher than 60% in northern Norway (Ferter et al., 2013). Even though the proportion of released Atlantic halibut was not estimated in that study, there are strong indications that the proportion released is also high for this species. In Norway, a minimum landing size of 80 cm is in place for halibut, with individuals smaller than this required to be released, i.e. regulatory C&R (Arlinghaus et al., 2007). Articles in the Norwegian media and on the internet suggest that voluntary C&R of Atlantic halibut of harvestable size is also becoming increasingly popular, both among marine angling tourists and local recreational anglers. In Iceland, since 2011, regulation requires all halibut that are caught and deemed to be in a good condition to be released (Solstrand, 2013). C&R is often seen as beneficial for fish stocks since it can potentially reduce fishing mortalities and at the same time maintain angling opportunities (Cooke et al., 2006), but it has also led to controversy and public debates in many countries (e.g. Aas et al., 2002; Cooke and Sneddon, 2007; Arlinghaus, 2008; Salmi and Ratamäki, 2011). One major issue with C&R is that the released fish may die due to hooking damage or other factors (Bartholomew and Bohnsack, 2005; Hühn and Arlinghaus, 2011). For example, Coggins et al. (2007) showed that even relatively low post-release mortality rates can render regulations such as minimum landing sizes ineffective. Moreover, released fish may experience sublethal impacts after the C&R event, e.g. increased levels of stress hormones (e.g. Meka and McCormick, 2005; Donaldson et al., 2011; Danylchuk et al., 2014) or changes in swimming behavior (e.g. Klefoth et al., 2008; Hoolihan et al., 2011; Ferter et al., 2015a). The possibility for such negative impacts of C&R has recently led to several public debates in the Norwegian media questioning the benefits to sustainable fisheries management and ethical tenability of C&R angling of halibut. For Atlantic halibut, the post-release survival is poorly studied because of practical limitations related to methods for testing the impacts in the field. Capture rates for this species are relatively low on angling gear. Thus, traditional tag-recapture studies are not appropriate, as they require a large number of tagged individuals to provide a sufficient number of tag returns to assess survival, making this method logistically prohibitive (Pollock and Pine, 2007). Furthermore, the species grows to sizes which make classical containment experiments difficult (Pollock and Pine, 2007). During the last two decades, however, acoustic and satellite tags have proven a useful tool to assess post-release survival by assessing the behavior of a fish once it is returned to the water (e.g. Stokesbury et al., 2011; Curtis et al., 2015; Ferter et al., 2015a). Both methods yield high resolution data on swimming depths, ambient water temperatures and other environmental parameters, and do not require recapture of the tagged fish. Acoustic transmitters are either implanted surgically or attached externally before the fish is released. Data are recorded and stored by acoustic receivers as

long as the fish is within detection range (Thorstad et al., 2013). Pop-up satellite archival tags (PSATs) are attached externally and detach from the fish at a pre-set date or when they remain at a constant depth for a defined period (e.g. at death). The tags then float to the surface and transmit the stored data via the Argos satellite system (Block et al., 1998). Seitz et al. (2014) tagged and released five Atlantic halibut caught by long line with PSATs. They showed that four individuals survived after tagging (159–296 days), while one tag failed to report. These individuals however, were caught with a different gear type to that commonly used for angling, and may therefore not be directly comparable. Considering the socio-economic importance of recreational fishing in Norway, an increase of C&R rates for Atlantic halibut, and the upcoming public debates on C&R practices for this species, the aim of this study was to quantify post-release mortality of Atlantic halibut from C&R angling. Post-release mortality of eleven halibut caught on typical angling gear was assessed based on vertical swimming movement registered by acoustic transmitters and PSATs after the release event. This information will contribute fact-based information to the ongoing public debate. 2. Materials and methods 2.1. Experimental angling The experimental angling was conducted in an area adjacent to Tromsø, northern Norway from June 2011 to August 2011 (Fig. 1). The area consists of several shallow banks and islands, sometimes separated by deeper trenches (100–200 m). Fishing occurred in depths of 10–30 m using rod and reel (80 lbs multifilament braid main line). As terminal tackle, 1.5 m long 1.00–1.20 mm monofilament leaders with artificial lures (385 g Storm Wildeye Giant Jigging Shad and 400 g Savage Gear Cutbait shad; both shads with the jig head hook only) or bait (dead bait fish on a 400 g Giant Jighead with one barbed size 4/0 treble hook on the dorsal side) were used. These lure and bait types are commonly used by professional anglers in Norway, and are assumed to minimize severe hooking injury. After being hooked, the angling duration was kept as short as possible (maximum of 15 min) which has been recommended for other species during C&R situations to minimize stress for the fish (e.g. Thorstad et al., 2003; Meka and McCormick, 2005). 2.2. Tagging procedure The fork length (FL) of the halibut was measured to the nearest cm. Fish >120 cm FL were tagged with a PSAT (in total, 10 X-tags (maximum depth error ±5.38 m), Microwave telemetry Inc., Columbia, MD and one MiniPAT (depth sensor accuracy ±1% of depth reading), Wildlife Computers, Redmond, WA, USA) and an acoustic transmitter (halibut 1–10: Vemco V9P-2L, 9 × 47 mm, with a built-in pressure sensor (depth sensor accuracy ±5 m) and halibut 11: Vemco V13, 13 × 36 mm, without a pressure sensor, Vemco Division, Amirix Systems Inc., Halifax, Canada) (Table 1). The first fish tagged (halibut 1) was brought onboard for processing. No irrigation was applied, but a wet towel was placed over the fish’s head and the fish was carefully held still during tagging. The total processing time was fifteen minutes. The remaining ten fish were tagged in the water while the fish were held alongside the boat. A barbed hook was used to pull through a 10 mm diameter line from the inside of the tip of the lower jaw, and a 10 mm soft multifilament nylon rope was wrapped around the tail to hold the fish stable to minimize damage to the fish during tagging. To attach the PSAT, a trocar was pushed through the dark-side skin (upper side) of the fish close to the fin ray supports of the dorsal fin approximately half-way on the anterior-posterior axis of the fish. A 1.2 mm

Please cite this article in press as: Ferter, K., et al., Survival of Atlantic halibut (Hippoglossus hippoglossus) following catch-and-release angling. Fish. Res. (2016), http://dx.doi.org/10.1016/j.fishres.2016.05.022

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Halibut ID

a b

2

3

4

5

6

7

8

9

10

11

107817 5399 28/06/11 146 01/08/11

107818 5401 29/06/11 167 15/11/11

107821 5397 29/06/11 160 15/01/12

107820 5400 30/06/11 137 15/01/12

107819 5402 01/07/11 123 15/12/11

10P0350 5394 08/07/11 192 17/08/11

107826 5395 11/08/11 132 15/04/12

107824 5396 11/08/11 163 15/02/12

107823 5398 11/08/11 136 15/02/12

107825 5403 12/08/11 154 15/03/12

107822 749a 13/08/11 153 15/01/12

28/07/11

09/08/11

15/01/12

06/10/11

15/12/11

17/08/11

15/04/12

29/11/11





15/01/12

91 28/07/11 30

6 25/07/11 26

9 13/01/12 198

3 18/09/11 80

60 15/12/11 167

81 17/08/11 40

100b 15/04/12 248

33 25/11/11 106

0 – –

0 – –

36 15/01/12 155

full memory

tag loss

programmed

tag loss

programmed

programmed

programmed

tag loss

tag failure

tag failure

programmed

05/08/11

14/07/11



08/08/11

20/07/11

22/07/11

15/09/11

16/09/11

24/09/11

15/08/11



38

15



39

19

14

35

36

44

3



no activity

tag failure

tag failure

no activity

no activity/outside range

outside range

outside range

outside range

no activity

poor data/outside range



This tag was an ID only transmitter and was not used to assess post-release survival. PSAT 107826 was found and data were directly downloaded from the tag.

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PSAT ID Acoustic tag ID Release date Fork length (cm) Programmed pop-off Actual pop-off (start of data transmission) Data received (%) Last PSAT activity Days of activity (PSAT) Termination reason (PSAT) Last acoustic tag activity Days of activity (acoustic) Termination reason (acoustic)

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K. Ferter et al. / Fisheries Research xxx (2016) xxx–xxx

Please cite this article in press as: Ferter, K., et al., Survival of Atlantic halibut (Hippoglossus hippoglossus) following catch-and-release angling. Fish. Res. (2016), http://dx.doi.org/10.1016/j.fishres.2016.05.022

Table 1 Overview of the angled and tagged Atlantic halibut in this study, pop-up satellite archival tag (PSAT) and acoustic transmitter characteristics, days of activity (i.e. vertical movement showing that the fish is alive) measured by each tag type, and the reasons for termination of measurements (i.e. end of monitoring period) for each tag type.

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Fig. 1. Overview of the study area north-west of Tromsø, Norway. Isobaths shown are the 5, 10, 20, 30, 40, 50, 100, 150, 200, and 250 m depth contours. The black dots indicate the positions of the nine acoustic Vemco VR2 W receivers, and the numbers in parentheses denote the number of tagged halibut caught and released at each location.

were fixed to the anchoring system by a rope, and orientated upside down approximately five meters below the surface. They detected signals from the acoustic transmitters when the tagged halibut was within a tested range of 300–1000m, depending on the current, wind conditions and the fish’s placement on the bottom. Acoustic data were downloaded from the receivers on October 23rd, 2011. 2.3. Assessment of post-release mortality

Fig. 2. Underwater picture of a tagged halibut immediately after the release. The pop-up satellite archival tag (left) and acoustic transmitter (right) are attached to two separate cords at the base of the dorsal fin on the dark-skin (upper) side of the fish.

monofilament tether which was sheathed with a thin individually numbered plastic tube with an attached 3 × 1 cm flat stainless steel arrowhead was pulled through the penetration hole of the trocar into the fish from the white-side skin (lower side) so that the arrowhead placed itself across the fin rays inside the fish. The PSAT was attached to the tether on the upper side of the fish using a cable ferrule. A second similar plastic-covered nylon cord was pulled into the fish as described above and used to attach the acoustic transmitter. The transmitter was attached to the cord using two cable ties which were tightened around the cord (Fig. 2). The entire process took from 15 to 30 min depending on weather conditions. The PSATs were programmed to detach from the fish after a period of 34–248 days (Table 1). The shorter deployments were programmed with a higher rate of measurements to obtain a higher resolution of depth recordings for some individuals. Five of the tags were programmed to release if the tag measured a constant pressure for 14 days (due to mortality or tag loss) before the preset release date. The remaining tags were not programmed with this function, as it was unknown how long a halibut may naturally reside at a constant depth in this study region. The acoustic transmitters were programmed to send a signal every 120 s until the on-board battery expired, predicted to be greater than 200 days according to the manufactures specifications. At least one acoustic receiver (VR2W, Vemco Division, Amirix Systems Inc., Halifax, Canada) was anchored at each release location (Fig. 1). The receivers

The monitoring period for each fish was determined by the maximum time for which at least one of the tag types reported data. A threshold for sufficient data quality was set to at least two depth recordings within a 24 h period from the same tag, but data gaps between two 24 h periods were permitted. Thus, the monitoring period was limited to the last day for which at least two depth recordings within a 24 h period were available. The maximum number of confirmed activity (i.e. vertical movement) days was used to determine the number of days a fish had survived after the release event. A cessation of vertical movement was defined as a depth change <10 m + tidal fluctuations recorded by a functional acoustic transmitter, <10.76 m + tidal fluctuations by a functional X-tag PSAT, and <2 × 1% of depth reading + tidal fluctuations by a functional MiniPAT PSAT for at least 14 days until the end of the monitoring period of that tag (i.e. with no vertical movement greater than the defined threshold recorded at a later stage during the monitoring period). These thresholds were chosen to account for depth sensor inaccuracy or signal transmission disturbance, and to account for registration of tidal changes (maximum 3 m in the study area) when a lost transmitter or tagged fish were lying on the sea floor. The 14 days threshold was chosen because halibut can spend extended periods of time resting on the sea floor (Seitz et al., 2014). For halibut 11, the acoustic transmitter (ID 749) did not have a pressure sensor, and since the PSAT monitoring period exceeded the acoustic monitoring period only the PSAT recordings were used to assess survival for this individual. The following rules were developed to assess short- (≤3 days) and long-term (>3 days) post-release mortality of the fish: (1) If both tag types indicated a cessation of movements of the tagged fish, this fish was deemed to be dead. (2) If one of the tags did not show any vertical movement but the other tag indicated vertical movement, it was assumed that one of the tags was shed prematurely or malfunctioning, and that the fish was alive. (3) If the PSAT reported a cessation of movement while still attached to the fish (i.e. not yet ascended to the surface) and no data were available from the acoustic transmitter, this fish was deemed to be dead. (4) If the acoustic transmitter reported a cessation of movement and

Please cite this article in press as: Ferter, K., et al., Survival of Atlantic halibut (Hippoglossus hippoglossus) following catch-and-release angling. Fish. Res. (2016), http://dx.doi.org/10.1016/j.fishres.2016.05.022

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no data were available from the PSAT, it remained unclear if the cessation of movement was because of tag shedding or mortality. 3. Results In total, eleven Atlantic halibut were caught and tagged, ranging in FL from 123 to 192 cm. None of these fish had severe hooking injuries or substantial bleedings, i.e. none of these fish was deepor foul-hooked. Nine out of the eleven individuals (i.e. halibut 2, 3, 4, 5, 6, 7, 8, 10, and 11) were confirmed to be alive for 3–248 days after the C&R event, as shown by their activity patterns from at least one of the tag types (Table 1, Fig. 3). Individuals for which complete data sets were reported from the PSATs showed extensive vertical migrations during the monitoring period. For the remaining two fish (halibut 1 and 9), the acoustic transmitters reported a cessation of movements during the monitoring period (i.e. after 38 and 44 days, Fig. 3). As the PSAT monitoring for halibut 1 was shorter than acoustic transmitter monitoring, and the PSAT for halibut 9 did not report any data, it remains unclear if the cessation of vertical movements reported by the acoustic tags was due to premature tag shedding or mortality. Tag loss was relatively prevalent in this study as at least three individuals (halibut 2, 4 and 8) lost their PSATs prior to the programmed pop-off date (i.e. the tags floated at the surface for several days before they started sending data). Additionally, two PSATs did not report any data (halibut 9 and 10), so these may have been shed prematurely and washed up on the shore which could have impeded successful data transmission. Halibut 4 lost the acoustic transmitter after 39 days (as indicated by a cessation of vertical movements), while the PSAT recorded vertical movement for an additional 41 days showing that the acoustic transmitter was shed from the fish (Fig. 3). 4. Discussion To the best of our knowledge, the present study is the first that investigated the post-release survival of angled Atlantic halibut, and shows that survival (at least in the short term) can be high if angling duration is kept short, and the fish are mouth-hooked and handled correctly during de-hooking. This holds true even though the halibut were handled longer than under normal angling conditions, and were additionally stressed by the tagging procedure and the burden of carrying the tag (Donaldson et al., 2008). Thus, the combined impacts of the C&R and tagging process in this study are likely to have led to a conservative estimate for post-release survival for mouth-hooked and correctly handled halibut. The high post-release survival is in line with studies on other marine species, which have shown that post-release mortality of angled fish can be very low for some species (e.g. Stokesbury et al., 2011; French et al., 2015). The results of the present study may however not be applicable to all angling situations, as some anglers still use lure and bait types causing more severe hooking injury (e.g. foul- and deep-hooking). Moreover, a certain level of experience is necessary to release halibut in this size range without harming the fish additionally, although this may have been outweighed by the tagging procedure in this study. The impacts of C&R vary not only between species but also between fisheries, and depend on several factors (Muoneke and Childress, 1994; Bartholomew and Bohnsack, 2005). In the present study, all halibut were hooked favorably which may partly explain the high survival. Deep-hooking may occur more frequently if the halibut are allowed to swallow the bait for an extended period of time, and foul hooking may be more frequently when additional treble hooks are used on the rubber shad, although no studies have been conducted to quantify this. Halibut with bleedings or

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more significant injuries could have suffered from higher mortality than found in the present study. For example, Neilson et al. (1989) observed that more than half of the Atlantic halibut caught by longline had open hooking wounds in the head region, and that 23% of the fish died within 48 h which is considerably higher than in our study. Similarly, Pacific halibut (Hippoglossus stenolepis) that were removed by automated de-hooking systems leading to substantial injury had significantly higher mortality than fish that were removed carefully from longline hooks (Kaimmer, 1994; Kaimmer and Trumble, 1998). Also, for other species, anatomical hooking location has been shown to be one of the most important mortality factors, as deep-hooking (i.e. hooking beyond the mouth cavity) and bleeding led to significantly higher mortality rates than mouth-hooking without bleeding (e.g. Bartholomew and Bohnsack, 2005; Alós et al., 2009; Weltersbach and Strehlow, 2013). One way to reduce deep-hooking when fishing with bait is the use of circle hooks which have been shown to reduce post-release mortality for many species but their efficiency seems to be speciesspecific (Cooke and Suski, 2004). Extended air exposure can lead to increased post-release mortality, which could have been problematic in the case of halibut 1 as this fish was handled for 15 min without irrigation (in contrast to the other individuals which were tagged in the water). It remains unclear if this fish died of if it lost its acoustic transmitter after 38 days. For Pacific halibut, however, Davis and Schreck (2005) observed significant mortality only after 40 min which, in most recreational angling situations, will not be reached. The size of the fish has also been described as an important predictor of mortality, with larger fish generally being more resilient than smaller ones (Davis, 2002), which was also the case in the study by Neilson et al. (1989). In the present study, only halibut >120 cm were included, which may have been more resilient to the C&R event than smaller individuals which have to be released by law. Thus, C&R impacts on smaller individuals should be studied to estimate post-release mortality and to develop best practice C&R guidelines for undersized halibut. For many species, capture depth and water column stratification has a significant impact on post-release survival due to the potential for barotrauma and thermal stress when brought to the surface from deeper water (e.g. Davis, 2002; St John and Syers, 2005; Jarvis and Lowe, 2008). Barotrauma is primarily caused by the expansion of air in the swimbladder due to rapid decompression leading to several internal and external barotrauma signs in several fish species (e.g. Hannah et al., 2008; Ferter et al., 2015b). Atlantic halibut do not have a swimbladder, and barotrauma is therefore not an issue. Capture depth may, however, play an indirect role if the water column is temperature-stratified and the fish are brought up from cool bottom water to warmer surface water. Exposing the fish to warmer surface water will increase thermal stress and the likelihood for post-release mortality (Davis, 2002). Yet, as halibut are mainly caught on shallower water depths by recreational anglers (as in the present study), temperature effects due to changes in water temperature are limited. Moreover, the present study was conducted during the summer months when surface water temperatures are highest, and the post-release survival was high even though the fish were handled for 15–30 min at the surface, which supports that this study resulted in a conservative estimate for post-release survival for mouth-hooked and correctly handled halibut. Even though the present study may not be applicable to all angling situations (due to favorable anatomical hooking locations and handling by experienced anglers in the present study), it shows that post-release mortality of Atlantic halibut can be very low under certain circumstances. Thus, C&R of Atlantic halibut is not likely to be a significant source of unaccounted mortality when anglers use similar terminal tackle, and angling and handling practices as those in this study. Several studies have shown that the poten-

Please cite this article in press as: Ferter, K., et al., Survival of Atlantic halibut (Hippoglossus hippoglossus) following catch-and-release angling. Fish. Res. (2016), http://dx.doi.org/10.1016/j.fishres.2016.05.022

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Fig. 3. Vertical movements of the eleven halibut after the C&R event. The colored dots are the depth and temperature recordings by the pop-up satellite archival tags (PSATs), while the grey dots are the depth measurements from the acoustic transmitters (as recorded by the acoustic receivers). Note: For halibut 2, minimum and maximum depth recordings were available from the PSAT for four days without time series depth recordings. These data were added as black dots because they prolonged the PSAT monitoring period for this individual.

tial negative impacts of C&R can be reduced significantly when anglers are educated on how to release the fish properly (Cooke and Suski, 2005; FAO, 2012). This highlights the need for the development and implementation of best practice guidelines that can be followed by anglers to minimize C&R impacts on Atlantic halibut. Such guidelines could not only increase the chances for post-release survival but also minimize sublethal impacts. Sublethal impacts such as increased levels of stress hormones and behavioral changes after the C&R event (Cooke et al., 2013) have negative implications for fish welfare (Cooke and Sneddon, 2007; Diggles et al., 2011) and should therefore be minimized. The present study did not include enough individuals or treatments to develop speciesspecific guidelines, which is why more general guidelines should be developed and implemented at this point. As general C&R guidelines, Cooke and Suski (2005) recommended the minimization of angling duration, use of artificial lures and barbless hooks, and minimization of air exposure and on-board handling, all of which would most likely also promote fish welfare in Atlantic halibut C&R fisheries. The thresholds chosen for the cessation of movement definition can be considered conservative, as they could have led to a false negative judgment of survivorship, i.e. individuals could have been deemed dead even though they actually were alive but only moving within the vertical range of these thresholds or if only acoustic transmitter signals from the threshold range were received. Moreover, the data quality threshold of at least two depths recordings

within a 24 h period led to a shorter monitoring period for halibut 10 (3 days) even though this individual was within receiver range briefly 19 days after release (on 31st Aug). In case of halibut 2 (acoustic transmitter ID 5401), the monitoring period for the acoustic transmitter was limited to the last day of meaningful data reporting (14th July). The fact that the acoustic transmitter of this individual reported a constant depth at approximately 25–30 m while the PSAT showed extensive vertical movement, then jumped to zero meters, then 20 m, and then jumped back to zero meters implies a malfunction of the depth sensor. It was difficult to obtain an appropriate control group (Pollock and Pine, 2007) due to logistical reasons, so if the tagging procedure had caused substantial mortality it would have been difficult to detect this, supporting that this study led to a conservative estimate for post-release survival under the given circumstances. It remains unclear if the two fish with reported cessation of vertical movements died or if they lost their acoustic tags prematurely. Tag shedding was relatively prevalent in this study, as premature shedding was confirmed for three PSATs (i.e. pop-up before the programmed release date; PSAT IDs 107818, 107820, and 107824) and at least one acoustic transmitter (i.e. the acoustic transmitter did not report any vertical movements while the PSAT did; acoustic transmitter ID 5400). In another ongoing study, several halibut which were externally tagged with data storage tags were recaptured. These tags were considerably worn down at recapture (A. Rikardsen, personal observation), indicating that the halibut may

Please cite this article in press as: Ferter, K., et al., Survival of Atlantic halibut (Hippoglossus hippoglossus) following catch-and-release angling. Fish. Res. (2016), http://dx.doi.org/10.1016/j.fishres.2016.05.022

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occasionally turn around and scratch themselves on the bottom which may lead to premature tag shedding. If the two halibut for which a cessation of vertical movements was observed actually died, it is unlikely that this mortality was linked to the capture and handling because the movements stopped 38 and 44 days after the C&R event. Several studies on other species have shown that most of the capture- and handling-related mortality occurs within 72 h post release (e.g. Wassenberg and Hill, 1993; Humborstad et al., 2009; Curtis et al., 2015; French et al., 2015). It is therefore not unlikely that these two fish survived and lost their acoustic transmitters, although this cannot be proven definitely. There are several aspects which should be addressed in future studies. As this study was limited to halibut >120 cm and did not cover a large range of different treatments (e.g. deep-hooking, foul-hooking and extended angling duration), future post-release mortality studies should also include smaller individuals and different treatments. The main challenge is, however, to find an appropriate experimental design given financial constraints, as a substantially larger sample size would be required for such studies. The use of PSATs to study the post-release mortality of Atlantic halibut has been shown to be an appropriate method here, but the cost of these tags still limits the number of individuals that can be tagged (see also Graves and Horodysky, 2015). Furthermore, future efforts should be directed towards sublethal impacts of the C&R event. Even though post-release mortality has been shown to be low in this study, sublethal impacts can still be significant (Davis and Schreck, 2005). While several of the halibut in this study showed extensive vertical migration behavior indicating recovery after the C&R event in the long run, small-scale behavioral changes in vertical movements post-release were not analyzed because it would have been difficult to separate tagging and handling effects from actual C&R effects (Donaldson et al., 2008; Ferter et al., 2015a). Reflex action mortality predictor (RAMP) scores have been shown to be a valuable method to assess capture and handling impacts on Pacific halibut (Davis and Ottmar, 2006) and other flatfish species (Barkley and Cadrin, 2012). Thus, RAMP can most likely also be used to predict capture-induced stress and post-release mortality in Atlantic halibut, which should be tested in future studies.

5. Conclusion In conclusion, this study shows that post-release mortality of Atlantic halibut can be very low if the fish are hooked in the mouth region, and handled and released properly. This opens up for the implementation of further harvest measures, e.g. a maximum landing size, which could reduce fishing mortality for larger individuals. To minimize negative impacts of C&R, managers are therefore encouraged to develop and implement best practice guidelines. As long as no data are available to develop species-specific guidelines, more general guidelines should be disseminated. This is of particular importance if further harvest measures will be implemented which would increase the practice of regulatory C&R. Sublethal impacts were not part of this study but need to be addressed in future studies, as their understanding is important to evaluate C&R of halibut from a fish welfare perspective.

Contributions Ferter processed the data, contributed to data analysis and wrote the manuscript. Rikardsen designed the study, conducted field work and contributed to manuscript preparation. Evensen and Svenning participated in planning and conduction of the fieldwork, and commented on the manuscript. Tracey contributed to data analysis and manuscript preparation.

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Acknowledgements Funding for this project was provided by UiT – The Arctic University of Tromsø and the Norwegian Institute for Nature Research in Tromsø. Further funding was provided by the tourist fishing project (“Kartlegging av turistfiske”) to KF through the Coastal Zone Ecosystem Program at the Institute of Marine Research. The authors are especially thankful to Per Jonasson and Tom Sivertsen for their great help during fishing and tagging, and Per Arne Horneland for assistance in graphical design. Moreover, the authors would like to thank three anonymous reviewers for the constructive feedback on an earlier version of this manuscript. All experimental procedures were conducted in accordance with the Norwegian regulation on animal experimentation and were approved by the Norwegian animal research authority (Forsøksdyrutvalget (www.fdu.no); FOTS IDs 3454 and 3641). References Aas, Ø., Thailing, C.E., Ditton, R.B., 2002. 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Please cite this article in press as: Ferter, K., et al., Survival of Atlantic halibut (Hippoglossus hippoglossus) following catch-and-release angling. Fish. Res. (2016), http://dx.doi.org/10.1016/j.fishres.2016.05.022