Characterization of Depth Distributions, Temperature Associations, and Seasonal Migrations of Atlantic Halibut in the Gulf of St. Lawrence using Pop-Up Satellite Archival Tags

Abstract

The fishery for Atlantic Halibut Hippoglossus hippoglossus in the Gulf of St. Lawrence (Gulf) is currently experiencing its highest landings since the 1950s. However, the absence of information on adult habitat use has limited the development of new survey methodologies. The aim of this study was to use pop-up satellite archival tags on large (≥108-cm) halibut in the Gulf to provide data on seasonal temperature associations, depth distributions, and migrations. Twenty Atlantic Halibut were tagged in 2013 and 15 were tagged in 2015 at two different locations in the northern Gulf. Atlantic Halibut overwintered in the central and northern Gulf based on six tag pop-offs. In the winter in both studies, halibut were distributed at 160–440 m depth with a narrow temperature association of 5.5–6.5°C, which corresponded with the bathymetry and hydrography of the Gulf rather than the deeper and colder waters of the continental shelf where the southern stock occurs. Spawning rises were identified from the depth data for two halibut in 2013 and six halibut in 2015. In the summer, halibut had a wide range of depth (20–200 m) and temperature (−1.5°C to +15.0°C) associations, and tag pop-offs in August indicated feeding grounds off the northwestern coast of Newfoundland. There was a broad geographic distribution of final pop-offs in 2013, but in 2015 all tags popped off close (<55 km) to the original tagging site. These seasonal depth distributions and temperature associations will be used to inform Atlantic Halibut stock assessments and management decisions.

Received June 29, 2016; accepted May 3, 2017

There are limited biological data on stock structure and movement of Atlantic Halibut Hippoglossus hippoglossus in the Gulf of St. Lawrence (Northwest Atlantic Fisheries Organization [NAFO] divisions 4RST; hereafter, Gulf), particularly involving mature halibut that are not well sampled by research vessel trawl surveys (Bourdages et al. 2015). The Gulf stock is currently assessed using indices of juvenile abundance and size structure derived from research vessel surveys and fishery catch rates, and the dearth of information on large Gulf halibut has hampered the estimation of spawning stock biomass (SSB). Moreover, limited knowledge on the spatiotemporal dynamics of adults has delayed the development of new survey methodologies that could improve management.

Atlantic Halibut on the east coast of Canada are managed as two separate stocks, the Gulf stock and the Scotian Shelf and southern Grand Banks stock (NAFO divisions 3NOPs4VWX5Zc; hereafter, the southern stock). In contrast to the Gulf stock, the southern stock has been the focus of an extensive multiyear conventional tagging program and a widespread longline survey since 1998, which has allowed Fisheries and Oceans Canada (DFO) to estimate exploitation rates, describe the movements and spatial distribution of halibut, and estimate population size (den Heyer et al. 2013; DFO 2015a; Trzcinski and Bowen 2016). The southern stock has greatly benefited from proactive management strategies after the last population crash in 1993, including reductions in total allowable catch, introduction of minimum size limits, and gear changes (Trzcinski and Bowen 2016). Furthermore, the development of biological reference points for the southern stock, using data obtained from tagging programs and longline surveys, contributed to the fishery obtaining a Marine Stewardship Council (MSC) certification in 2013, which can increase market access and landed value to harvesters.

Also in contrast to the Gulf stock of Atlantic Halibut, the closely related Pacific Halibut H. stenolepis has been managed by the International Pacific Halibut Commission (IPHC) since 1923, making it one of the longest-studied groundfish stocks (Clark et al. 1999). Pacific Halibut have been the focus of an extensive research program since 1925 (Kaimmer 2000), which has included hundreds of tagging studies (using conventional, acoustic, and archival tags) and, since 1998, annual standardized longline surveys. In combination, those efforts have informed scientists and managers on stock structure, migration patterns, and population biology (e.g., Skud 1977; Trumble et al. 1990; Loher and Seitz 2006, 2008). Changes in the fishery, such as local depletions, minimizing commercial fisheries during spawning, and changes in growth and recruitment patterns, were identified by these sampling programs and contributed to the management of Pacific Halibut (Clark et al. 1999; Seitz et al. 2003; Loher 2011). Pacific Halibut is currently managed by the IPHC as one stock from northern California to the USA–Russian border (Stewart and Martell 2015), although recent analyses have demonstrated significant genetic substructure within the managed range (Drinan et al. 2016). Pacific Halibut fisheries have been MSC certified as sustainable in both the USA and Canada since 2006 and 2009, respectively.

The aim of this study was to use pop-up satellite archival tags (PSATs) to provide biological data on movement patterns and habitat use of large Gulf halibut for the development of new halibut stock assessment inputs. The PSATs transmit depth, temperature, and light data at high temporal resolution (10–60 min) recorded during a preprogrammed time period. Importantly, data acquisition and tag pop-off locations are fishery-independent because each tag is scheduled to detach from the fish on a specific date, then float to the surface and transmit its data to the Argos satellites for the duration of its battery life (approximately 2 weeks). Because of these features, PSATs have provided important biological information for Pacific Halibut and for the southern stock of Atlantic Halibut, such as locations of winter spawning and summer feeding grounds, spawning behavior, and migration patterns (e.g. Loher and Seitz 2006; Seitz et al. 2007; Armsworthy et al. 2014).

We hypothesized that the Gulf stock of Atlantic Halibut would demonstrate seasonal movements to deep waters for winter spawning and to shallow waters for summer feeding, similar to the seasonal cycle described for the adjacent stock (Armsworthy et al. 2014). Based on previous conventional tagging studies (McCracken 1958; D. Archambault, DFO, Institut Maurice-Lamontagne, unpublished data), we predicted that large Gulf halibut would remain closely associated with the Gulf year-round and not move south to spawn on the continental shelf with the southern stock. The depth distribution and seasonal migration data can inform the design of a longline survey directed at Gulf halibut, which is proposed to occur in September after most of the commercial fishery (May–September), but has not yet been established (DFO 2015b). A standardized longline survey and associated conventional tagging program would increase the scientific basis for Gulf halibut stock assessment and fisheries management allowing for the development of an abundance index.

METHODS

Tagging operations

The first tagging study was conducted October 1–2, 2013; 20 PSATs (X-Tag, Microwave Telemetry, Columbia, Maryland) were deployed on large (≥108 cm FL) Atlantic Halibut offshore from Port au Choix on the northwestern coast of Newfoundland (50.6°N, 57.6°W) (Figure 1A; Table 1). The 20 PSATs were programmed to pop-off after periods of 3 (n = 3), 6 (n = 3), or 12 months (n = 14). While the main objective was to characterize halibut habitat use and movements over 12 months, six tags were programmed to provide pop-up locations near the onset (early January) and near the ending (early April) of the winter spawning season (Gascon 1995).

TABLE 1. Pop-up satellite archival tag deployment locations and data transmission details for Atlantic Halibut tagged near Port au Choix, northern Gulf of St. Lawrence, on October 1–2, 2013. The data column represents the percentage of the transmitted data set that could be retrieved from the tag. Minimum distance traveled corresponds to the distance between deployment and pop-off locations. Satellite tag used was X-Tag. All deployment dates are in 2013; all pop-off dates are in 2014 except the first two, which are in 2013.

Tag identification	Deployment date	FL (cm)	Programmed deployment duration (months)	Latitude at release (°N)	Longitude at release (°W)	Pop-off date	Data resolution (%)	Latitude at pop-off (°N)	Longitude at pop-off (°W)	Sampling period (d)	Minimum distance traveled (km)
131915	Oct 1	130	3	50.596	57.559	Dec 10	1 (60 min)	50.711	57.424	73	16
131933	Oct 2	145	12	50.596	57.559	Dec 20	7 (30–60 min)	50.706	57.613	80	13
131916	Oct 1	129	3	50.596	57.559	Jan 2	1 (60 min)	50.383	57.759	94	28
131914	Oct 1	116	3	50.596	57.559	Jan 4	0	Data failed quality tests
131918	Oct 2	122	6	50.596	57.559	Apr 2	13 (60 min)	48.846	60.019	183	263
131917	Oct 2	113	6	50.596	57.559	Apr 3	1 (60 min)	48.632	61.086	184	335
131919	Oct 2	113	6	50.596	57.559	Apr 7	5 (60 min)	50.356	58.048	188	44
131932^a	Oct 1	140	12	50.596	57.559	Jul 24	100 (2 min)	51.139	56.981	297	73
131931^b	Oct 1	108	12	50.596	57.559	Oct 1	100 (2 min)	50.693	57.768	365	18
131924^b	Oct 1	125	12	50.596	57.559	Oct 1	100 (2 min)	50.648	57.776	365	16
131920^b	Oct 1	126	12	50.596	57.559	Oct 1	100 (2 min)	50.785	57.385	365	24
131923	Oct 1	121	12	50.596	57.559	Oct 2	41 (30–60 min)	49.82	62.122	366	336
131921	Oct 2	121	12	50.596	57.559	Oct 2	35 (30–60 min)	47.657	57.321	365	571
131926^b	Oct 2	139	12	50.596	57.559	Oct 2	100 (2 min)	50.753	57.458	365	19
131925	Oct 2	122	12	50.596	57.559	Oct 2	40 (30–60 min)	50.013	65.85	365	612
131927^b	Oct 1	125	12	50.596	57.559	Oct 6	100 (2 min)	51.658	55.897	370	171
131930	Oct 1	115	12	50.596	57.559	^c
131929	Oct 2	165	12	50.596	57.559	^c
131928	Oct 2	146	12	50.596	57.559	^c
131922	Oct 2	108	12	50.596	57.559	^c

^a PSAT recovered by harvester during commercial fishery.

^b PSAT recovered upon pop-off using goniometer.

^c Did not respond.

FIGURE 1. Approximate pop-up locations of 27 pop-up satellite archival tags (PSATs) and one additional tag retrieved from the commercial Atlantic Halibut fishery in the Gulf of St. Lawrence (points are offset to illustrate all symbols). (A) Original PSAT tagging location off Port au Choix, Newfoundland, in October 2013 (blue circle). Three tags popped off after 3 months (orange circle 3), three tags popped off after 6 months (orange circle 6), three tags popped off after 12 months (yellow star), five tags were physically retrieved after 12 months (pink star), and one tag was physically retrieved from the commercial fishery in July (green star). (B) Original PSAT tagging location off Trout River, Newfoundland, in October 2015 (blue circle). Four tags popped off after 10 months (orange circle 10), four tags were physically retrieved after 10 months (green star), one tag popped off after 12 months (orange circle 12), and four tags were physically retrieved after 12 months (pink star).

The second tagging study was conducted October 4–6, 2015, and 20 PSATs (n = 7, X-tag; n = 13, MiniPAT, Wildlife Computers, Redmond, Washington) were deployed on 15 large (≥110 cm FL) Atlantic Halibut offshore from Trout River, Newfoundland (49.5°N, 58.1°W) (Figure 1B; Table 2). This tagging study was focused on characterizing habitat use and seasonal movements of sexed, mature fish. A veterinary ultrasound was used to determine the sex of the halibut (Loher and Stephens 2011). We double-tagged five female fish with one of each PSAT (X-Tag and MiniPAT); the purpose of this double-tagging experiment was to compare data acquisition and performance of the two tag types over 365 d at liberty. The 20 PSATs were programmed to pop-off after 10 (n = 8) or 12 months (n = 12). The release date after 10 months (mid-August) was programmed to provide pop-up locations during the summer feeding period.

TABLE 2. Pop-up satellite archival tag deployment locations and data transmission details for Atlantic Halibut tagged near Trout River, northern Gulf of St. Lawrence, on October 4–6, 2015. The data column represents the percentage of the transmitted data set that could be retrieved from the tag. Minimum distance traveled corresponds to the distance between deployment and pop-off locations. Satellite tag type used was MiniPat (MP) or X-Tag (XT). Tag identifications accompanied by superscripts 1, 2, 3, 4, or 5 represent double-tagged fish; that with superscript 5* was not included in data analysis. All deployment dates are in 2015; all pop-off dates are in 2016.

Tag identification	Tag type	Deployment date	FL (cm)	Sex	Programmed deployment duration (months)	Latitude at release (°N)	Longitude at release (°W)	Pop-off date	Data resolution (%)	Latitude at pop-off (°N)	Longitude at pop-off (°W)	Sampling period (d)	Minimum distance traveled (km)
152848^a	MP	Oct 5	141	F	10	49.378	59.114	Aug 15	100 (15 s)	49.533	58.888	315	24
150616	MP	Oct 5	144	F	10	49.490	59.005	Aug 18	72 (10 min)	49.500	59.107	318	7
150619	MP	Oct 5	141	F	10	49.490	59.005	Aug 15	64 (10 min)	49.974	59.073	315	54
152850	MP	Oct 5	152	F	10	49.490	59.005	Aug 15	45 (10 min)	49.523	59.048	315	5
150617^a	MP	Oct 5	154	F	10	49.490	59.005	Aug 16	100 (15 s)	49.539	59.012	316	5
152851	MP	Oct 5	142	F	10	49.490	59.005	Aug 15	72 (10 min)	49.491	59.062	315	4
150618^a	MP	Oct 6	110	M	10	50.029	58.467	Aug 15	100 (15 s)	49.910	57.870	314	45
150615^a	MP	Oct 6	110	M	10	50.029	58.467	Aug 16	100 (15 s)	49.814	58.196	315	31
151406^1	XT	Oct 4	162	F	12	49.874	59.182	^b
152846^1,a	MP	Oct 4	162	F	12	49.874	59.182	Oct 5	100 (15 s)	49.906	59.006	367	13
151405^2	XT	Oct 5	147	F	12	49.378	59.114	^b
152852^2	MP	Oct 5	147	F	12	49.378	59.114	^b
151408^3	XT	Oct 5	161	F	12	49.378	59.114	^b
150620^3,a	MP	Oct 5	161	F	12	49.378	59.114	Oct 5	100 (15 s)	49.402	59.145	367	3
151402^4	XT	Oct 5	155	F	12	49.378	59.114	^b
152849^4	MP	Oct 5	155	F	12	49.378	59.114	Oct 5	6 (10 min)	49.250	59.064	367	15
151404	XT	Oct 5	148	F	12	49.490	59.005	Oct 5	0	Data failed quality tests
151403	XT	Oct 5	148	F	12	49.490	59.005	^b
151407^5*,a	XT	Oct 5	174	F	12	49.490	59.005	Oct 5	100 (2 min)	49.430	59.084	366	9
152847^5,a	MP	Oct 5	174	F	12	49.490	59.005	Oct 5	100 (15 s)	49.438	59.186	366	14

^a PSAT recovered upon pop-off using goniometer.

^b Did not respond.

For both studies, halibut were caught using longline gear equipped with #16 circle hooks and baited with cut Atlantic Herring Clupea harengus. Longlines were soaked for approximately 10 h at depths between 100 and 220 m. The PSATs were attached to halibut using sterilized titanium darts linked to the tags using 180-kg-test monofilament tethers covered with black polyolefin shrink wrap tubing (Seitz et al. 2003). The dart was inserted under the pterygiophores on the dorsal, eyed-side of the fish.

Pop-up satellite archival tags

The X-Tag PSATs recorded depth (±0.34–5.38 m resolution from 0 to 1,296 m), temperature (±0.16–0.23°C resolution), and light intensity level (±4 × 10⁻⁵ lx resolution at 555 nm) data every 2 min (2013, 2015), and MiniPAT PSATs recorded depth (±0.5 m), temperature (±0.1°C), and light intensity (5 × 10⁻¹² to 5 × 10⁻² W/cm²) every 15 s (2015) throughout the deployment period (hereafter, archived data). Data transmitted through the Argos low-orbiting satellite system is limited such that data sampling intervals of 10 min (MiniPAT) and 15, 30, or 60 min (X-Tag) were expected (hereafter, received data) (Tables 1, 2). When we physically retrieved tags, we were able to access the archived data, which provided either 2-min (X-Tag) or 15-s (MiniPAT) continuous recording resolution (Tables 1, 2).

We were unsure whether we would obtain geolocation light data from the PSATs due to the threshold depth (~200 m for X-tag, >300 m for MiniPAT) at which light levels in Gulf waters may decrease to below the sensors’ detection capabilities, so PSATs were preprogrammed to pop-off at different temporal scales to provide data on fish locations at 3, 6, 10, or 12 months. Halibut locations at time of pop-off were determined onboard the receiving satellites, which measured the Doppler effect on the tags’ transmission frequency. Locations were determined with an accuracy of 250–1,500 m, and these data were provided by the Argos satellite system. The PSATs were preprogrammed to release at specific time intervals and not to release from the fish if a constant depth was maintained for an extended period of time, as halibut may spend long periods on the ocean bottom.

Physical recovery of PSATs that had popped off and were adrift or awash was attempted in October 2014, August 2016, and October 2016 in the Port au Choix and Trout River regions using an Argos goniometer (CLS America, Lanham, Maryland). This device was composed of a CLS RGX-134 digital receiver with RG-58 direction finding antenna that allows detection and tracking of actively transmitting (401.650 MHz Argos signal) PSATs in the field.

Data analyses

To allow a closer examination of halibut behavior over 12 months, monthly mean depth and temperature associations by tagging study were calculated. The number of tags used in each monthly mean calculation varied due to tag pop-offs at 3 and 6 months in the 2013 tagging study and at 10 months in the 2015 tagging study. Resolutions varied between received and archived data sets, so we calculated a monthly mean for each individual and then averaged the means across individuals in each tagging study.

Relative frequency distribution histograms of depth (10-m bins) and temperature (0.5°C bins) data were also used to portray the annual patterns of depth and temperature associations of halibut in each tagging study. Due to the range in data resolution expected from the two tagging studies, we standardized the data by calculating a relative frequency histogram per individual and then aggregated these histograms across individuals in each tagging study. Histograms for 3, 6, and 12 months are shown separately for each tagging study. In the 2015 tagging study, the archived data resolution (15 s–2 min) was standardized to 2 min. A log scale representing the number of observations was used to better highlight depths and temperatures occupied at the extremes of the distributions.

In previous studies on Pacific Halibut, spawning rises were identified from archived data from physically retrieved PSATs. Pacific Halibut demonstrated putative spawning behavior that consisted of a conspicuous routine of 6–10 vertical ascents lasting approximately 10 min, approximately 65 h apart, and then ascending to a shallower depth after the final spawning rise (Seitz et al. 2005). Using these same criteria, we visually examined the archived depth data from all physically retrieved PSATs from January 1 to April 1 to identify potential spawning rises.

RESULTS

Tagging Operations

In the 2013 tagging study, tagged Atlantic Halibut ranged in size from 108 to 165 cm FL (mean ± SD, 126.5 ± 14.4 cm FL; Table 1), and halibut were not sexed. In the 2015 tagging study, the 13 tagged females ranged in size from 141 to 174 cm FL (mean ± SD, 151.5 ± 9.7 cm FL), and the two tagged males were both 110 cm FL. Given the dimorphic median size at maturity (L50) (92 cm FL for males at 8–9 years and 130 cm FL for females at 12–13 years) for Gulf halibut (DFO 2013), many of the larger fish in the 2013 tagging study were likely to be females, and all of the tagged fish in the 2015 tagging study were likely to be mature.

Pop-Up Locations

In the 2013 tagging study, 14 PSATs successfully released from their host fish and reported a pop-off location (Figure 1A; Table 1). These tags popped off after recording for periods of approximately 3 (n = 3), 6 (n = 3), and 12 months (n = 8). One additional tag was physically recovered in July 2014 through the halibut commercial fishery in the Strait of Belle Isle, so we had access to data from a total of 15 PSATs (Table 1). Five of the 12-month PSATs were physically recovered during the week of scheduled release (October 2–3, 2014) off Port au Choix using a CLS America goniometer. Four PSATs did not report and one PSAT popped-off after 3 months, but the received data failed the quality test by the tag manufacturer (Table 1). One tag that was preprogrammed to pop-off after 12 months popped off after about 3 months, and these data were used in the analysis of the 3-month pop-offs.

In the 2013 tagging study, three PSATs popped off from early December 2013 to early January 2014 and were located, on average, 19 km from the tagging site (Figure 1A; Table 1). Three additional PSATs popped off in early April 2014. One of these three PSATs popped off 44 km from the tagging site (Figure 1A; Table 1), and the other two PSATs popped off in the central Gulf near the junction of the Esquiman and Laurentian channels, at a mean distance of 299 km from the tagging site (Figure 1A; Table 1). In October 2014, a full year after tagging, five out of the eight reporting PSATs popped off in the Port au Choix area within 75 km from the tagging site (Figure 1A; Table 1). The remaining four tags either popped off in the northwestern Gulf (n = 2), off the southern coast of Newfoundland (n = 1), or were retrieved by the halibut fishery in July 2014 at the northern tip of Newfoundland’s northern peninsula (n = 1); these tags were an average distance of 423 km from the tagging site (Figure 1A; Table 1).

In the 2015 tagging study, 13 PSATs successfully released from their host fish and reported a pop-off location (Figure 1B; Table 2). Of these 13 PSATs, 10 were from females (two tags popped off one female fish) and two were from males (Table 2). The13 PSATs popped off after recording for periods of 10 (n = 8) and 12 (n = 5) months. Eight of the 13 PSATs were physically recovered using the CLS America goniometer (Table 2). The tag pop-off locations in August and October 2016 were all close (<55 km) to the original tagging site in the northern Gulf (Figure 1B). There was a markedly different rate of pop-off success between the PSATs from the two manufacturers. Two of the seven X-Tag tags popped off, while 12 of the 13 MiniPAT tags popped off (Table 2). Six tags did not report (n = 5, X-Tag; n = 1, MiniPAT), and one X-Tag failed data quality tests by the manufacturer (Table 2). The lack of pop-off success of the X-Tag tags was reflected in the double-tagging experiment, where only one of the five X-Tag tags popped off compared with four of the five MiniPAT tags, and both tags popped off from only one of the five halibut. For this individual, we have included both tag pop-off locations in our analysis (Figure 1B; Table 2), but we have not included the data from the X-Tag (tag 150407) in the analysis as the use of these data would artificially inflate our sample size. Therefore, for the 2015 tagging study, only data from the MiniPAT PSATs were used. Due to the low success rate of the double-tagging experiment, the results were not presented here.

In the 2013 tagging study, light-based geolocation estimates provided by the manufacturer proved to be unreliable with many position estimates on land and unfeasible daily movement extent, which may have been due to the depth of the fish. The light-based geolocation data from the 2015 tagging study is currently being tested for accuracy. Therefore, only the initial tagging and pop-off locations from both studies were used in this analysis.

Depth Distributions and Temperature Associations

In the 2013 tagging study, received data rates were variable and low (1–13%) for the six PSATs that popped off between December and April (Table 1; Figure 2), likely due to the anomalously thick sea ice that characterized the winter of 2014 (Galbraith et al. 2015). Received data sets increased to 35–41% of the transmitted data for the three PSATs that popped off in waters free of ice in October 2014 (Table 1; Figure 3). For the six PSATs that were physically recovered, the entire 2-min resolution data set was accessed (Figure 4).

FIGURE 2. Received depth and temperature profiles from three PSATs deployed on Atlantic Halibut in the Gulf of St. Lawrence for a period of 3 months (upper three panels) and three PSATs deployed for a period of 6 months (lower three panels) in the 2013 tagging study. Data transmission rates to the Argos satellites were low likely due to unexpected heavy ice cover at the time of pop-off.

FIGURE 3. Received depth and temperature profiles through the Argos satellites from eight PSATs (2013 tagging study: n = 3 [tags 131921, 131923, 131925]; 2015 tagging study: n = 5 [tags 152851, 150616, 152849, 150619, 152850]) deployed on Atlantic Halibut in the Gulf of St. Lawrence for 10 or 12 months.

FIGURE 4. Archived depth and temperature profiles from 13 PSATs deployed on Atlantic Halibut in the Gulf of St. Lawrence and preprogrammed for 10 months in the 2015 tagging study (n = 4; tags 152848, 150617, 150618, 150615) and for 12 months in the 2013 (n = 5; tags 131927, 131931, 131926, 131924, 131920) and 2015 (n = 3; tags 150620, 152847, 152846) tagging studies. One tag was physically retrieved after 10 months in the 2013 tagging study (tag 131932).

In the 2015 tagging study, five of the MiniPAT tags transmitted data (6–72%, 10-min resolution; Figure 3), and seven MiniPAT tags were physically retrieved and the entire 15-s resolution data set was accessed (Figure 4). One X-Tag was physically retrieved after 12 months and the entire 2-min resolution data set was accessed but not included in this analysis as it was part of the double-tagging experiment.

In both studies, the majority of fish moved into progressively deeper waters from October to March, reaching mean depths of 250 m in February 2014 and 400 m in February 2016 (Figure 5, upper panel). Two female halibut from the 2015 tagging study did not demonstrate this pattern (tags 150616, 150619) and remained at a constant depth (200–250 m) year-round (Figure 4). The fish tagged in the two studies encountered a similarly narrow range of mean temperatures (5.5–6.5°C) as the months progressed from October to February (Figure 5, lower panel). In the 2013 tagging study, it appeared that the halibut moved through the cold intermediate layer (~75–100-m thick layer of water, <1°C in summer, in the Esquiman Channel; see Galbraith et al. 2015) in late June and migrated into warmer, shallower waters from July to September (4–15°C, 20–200 m) (Figures 4, 5b). In the 2015 tagging study, 5 of the 13 fish did not appear to have moved through a cold intermediate layer, with associated temperatures remaining steady at 5–6°C annually for these fish (Figures 3, 4). Halibut in the 2015 tagging study remained in deeper and cooler waters from July to September (3–10°C, 100–200 m) compared with halibut in the 2013 tagging study (Figure 5).

FIGURE 5. Monthly mean depths and temperatures recorded by 15 PSATs deployed on Atlantic Halibut in the Gulf of St. Lawrence from October 2013 to September 2014 (upper panel) and 12 PSATs from October 2015 to September 2016 (lower panel). Error bars represent SDs.

In the 2013 tagging study, from October to December, halibut that had been tagged for 3 or 6 months had a similar spread of depth distributions as the halibut tagged for 12 months, and the former were distributed at depths of 160–250 m (Figure 6a). From January to April, the data sets from the fish with 6-month tags had a wider spread of depth distributions than those with 12-month tags, including records as deep as 400 m, although in both data sets halibut were frequently distributed at 180–250 m (Figure 6b). The annual (October to September) data sets had a wide spread of depth distributions (10–350 m) for halibut, with the most frequented depths occurring at 20–70 m and 160–250 m (Figure 6c). From October to March, the 3- and 6-month data sets had a similarly narrow range of temperature associations as the annual data sets (2.5–7.0°C), and halibut frequently were distributed at 5.5–6.0°C (Figure 6 d, e). Annually, halibut experienced a wide range of temperatures (from −1.5°C to +15.0°C) but were still highly associated with 5.5–6.0°C (Figure 6f).

FIGURE 6. Relative frequency distribution of (a, b, c) depth (10-m bins) and (d, e, f) temperature (0.5°C bins) recorded by nine PSATs deployed on Atlantic Halibut in the Gulf of St. Lawrence that yielded high received and transmitted data sets (35–100%) for the periods (a, d) October–December 2013, (b, e) October 2013–March 2014, and (c, f) October 2013–September 2014. Line plots correspond to frequency distributions of depth and temperature recorded by (a, d) six PSATs and (b, e) three PSATs deployed for shorter time periods and yielded lower received data (1–13%). A log scale is used to represent the number of observations to better highlight depths and temperatures occupied at the extremes of the distributions.

In the 2015 tagging study, halibut were distributed deeper at 3 and 6 months (140–450 m; Figure 7a, b) than in the 2013 tagging study, but halibut experienced a similar range of temperatures during this same time period (2.5–7.0°C) and were frequently distributed at 5.5–6.5°C (Figure 7d, e). Annually, halibut were frequently distributed deeper than the halibut tagged in the 2013 tagging study. The annual data sets had a wide spread of depth distributions (30–460 m), with the most frequented depths for halibut occurring at 180–250 m and 400–460 m (Figure 7c). Halibut experienced a restricted range of temperatures (−0.5°C to +10°C) in 2015 than in the 2013 tagging study; however, halibut in the 2015 tagging study were still highly associated with 5.5–6.5°C (Figure 7f).

FIGURE 7. Relative frequency distribution histograms of (a, b, c) depth (10-m bins) and (d, e, f) temperature (0.5°C bins) recorded by 11 PSATs deployed on Atlantic Halibut in the Gulf of St. Lawrence in the 2015 tagging study. Tags used in this analysis had varying sensor recording resolutions (from 2 to 10 min) and data transmission rates (45–100%), as well as preprogrammed recording times (10 or 12 months). A log scale is used to represent the number of observations to better highlight depths and temperatures occupied at the extremes of the distributions.

Visual inspection of the archived data from the physically retrieved tags indicated that two halibut (131931, 131932) in the 2013 tagging study and two males (150615, 150618) and four females (150617, 150620, 152846, 152847) in the 2015 tagging study were undergoing putative spawning rises (Figure 8; Table 3). These fish were rapidly vertically ascending and descending 25–150 m in January and February from a starting depth of 300–400 m before ascending to a final depth of approximately 200–300 m after the last spawning rise (Figure 8; Table 3). The halibut from the 2015 tagging study were located deeper in the water column (~400 m) than were halibut from the 2013 tagging study (~300 m) (Table 3). The spawning behavior appears different between known male and female halibut, with clear vertical ascents (4–6) over a shorter period of time (10–17 d) in female fish (Figure 8a, b; Table 3) and a more sporadic (7–8 rises) and protracted (21– 24 d) vertical ascent pattern in males (Figure 8c, d; Table 3). Based on these two behavior types, in the 2013 tagging study one halibut (131931) was likely male, with putative spawning rises almost every day for 23 d (Figure 8d; Table 3), and one halibut (131932) was likely female with five vertical ascents over 17 d (Table 3).

TABLE 3. Atlantic Halibut putative spawning rises visually identified from archived data from physically retrieved PSATs from two tagging studies (2015 and 2013). The number of rises and length of spawning rise duration varied between known sexes (available for the 2015 tagging study only). The number of spawning rises and duration of behavior was different between the two halibut from the 2013 tagging study.

Tag identification	Year of experiment	Sex	FL (cm)	Date of first rise	Start depth (m)	Final depth (m)	Number of rises	Number of days
150617	2015	F	154	Feb 18, 2016	420	250	4	10
150620	2015	F	161	Feb 15, 2016	400	250	6	17
152846	2015	F	162	Jan 28, 2016	390	300	5	14
152847	2015	F	174	Jan 30, 2016	450	250	5	14
150615	2015	M	110	Jan 31, 2016	440	200	7	24
150618	2015	M	110	Jan 28, 2016	350	250	8	21
130931	2013	Unknown	108	Jan 18, 2014	330	250	25	23
130932	2013	Unknown	140	Feb 9, 2014	300	250	5	17

FIGURE 8. Based on visual inspection, the putative spawning rises of (a, b) two known female Atlantic Halibut from the 2015 Gulf of St. Lawrence tagging study, (c) a known male from the 2015 tagging study, and (d) a potential male from the 2013 tagging study. Arrows identify spawning rises.

DISCUSSION

We found evidence of seasonal migrations, winter spawning, and year-round residency of Atlantic Halibut in the Gulf, which supports the management of two separate Atlantic Halibut stocks in eastern Canada. Seasonal changes in temperature and depth associations identified in our study constitute important information to support the development of a longline survey within suitable adult habitat. In both tagging studies, the majority of Gulf halibut demonstrated markedly different depth and temperature associations in winter than in summer. In the winter, Gulf halibut were distributed at 160–440 m with a narrow temperature association of 5.5–6.5°C. In the summer, Gulf halibut moved into shallower waters (20–200 m) and experienced a wide range of temperatures (−1.5°C to +15.0°C). However, there were differences between studies, which may have been due to spawning behavior, interannual differences in oceanographic conditions in the Gulf, and use of different feeding grounds.

Limitations of PSATs include premature pop-offs and tags that do not report (30% in this study), the amount of data the tag can record vastly exceeding what it can transmit (e.g., 1–70% of data at 10–60-min resolution received through satellites in this study), and high expense per unit, which limits sample size (reviewed in Patterson and Hartmann 2011). The sample size used in this study (28 reporting of the 40 deployed PSATs) represents an average sample size compared with other satellite tagging studies (mean, 20 tags reporting of 27 tags deployed in 34 studies; range, 1–234 tags deployed) (reviewed in Musyl et al. 2011).

Based on visual inspections of the depth data from the physically retrieved tags, a total of six (two males and four females) out of seven individuals in the 2015 tagging study exhibited spawning behavior in January and February, while two out of six halibut in the 2013 tagging study exhibited spawning behavior. The spawning halibut tagged in the 2015 tagging study were located deeper in the water column (400 m) than were the halibut tagged in the 2013 tagging study (250 m). This interannual difference in depth associations could be due to occupation of different spawning grounds. However, none of these individuals occurred at depths typical of spawning in the southern stock (800–1,000 m) (Armsworthy et al. 2014). In the 2015 tagging study only, two females did not undergo seasonal migrations and remained at a constant depth (200–300 m) and temperature (5–6°C) year-round. These two females may have been undergoing skip-spawning as they were likely to have been mature based on their size (141 and 144 cm FL relative to an L50 for females of 130 cm). Previous research indicates that mature Pacific Halibut and Atlantic Halibut may not always spawn annually (Loher and Seitz 2008; Seitz et al. 2016).

In the 2013 tagging study, tag pop-off locations in the northern and central Gulf in December and April suggest overwintering in the Gulf, and all annual tags but one popped off in the northern Gulf. In the 2015 tagging study, all tags popped off in the northern Gulf. Tag pop-offs in August 2016 on shallow shelf areas along the western coast of Newfoundland suggest that this is a feeding ground for halibut. This area is known to be important summer feeding grounds and nursery areas for Atlantic Cod Gadus morhua, Atlantic Herring, and Capelin Mallotus villosus (reviewed in Dufour and Ouellet 2007). Halibut in the 2013 tagging study experienced a wider range of summer temperatures (−1.5°C to +15.0°C) than did halibut in the 2015 tagging study (0–10.0°C), which may indicate the use of different feeding grounds between the two tagging studies.

Our results are supported by two Gulf halibut conventional tagging studies that found the majority of recaptures to be within the Gulf close to their original tagging sites (McCracken 1958; D. Archambault, unpublished data). While tag pop-off locations suggest that the majority of tagged Atlantic Halibut resided in the northern Gulf year-round, due to having no usable at-liberty geolocation data from the PSATs in the 2013 tagging study, we cannot state unequivocally that no halibut tagged in this study moved into the southern management region during their time at liberty. Therefore, further research will focus on using temperature and depth data, in association with the bathymetry and hydrography of the ecosystem and tag pop-off locations, to model the seasonal migration patterns of halibut using a geolocation model (e.g., Le Bris et al. 2013).

Atlantic Halibut have demonstrated seasonal migratory behavior in the southern management area as well, based on PSAT data. In the winter, halibut have been observed distributed at depths of 500–1,000 m (maximum depth, 1,640 m) and a mean temperature association of 4.7°C with PSAT pop-offs having occurred within the tagging area on the edge of the continental shelf (Armsworthy et al. 2014). There was minimal variation in the temperatures that were experienced among the summer months (4.2–5.2°C), and halibut migrated progressively deeper from May to September with depth distributions of 400–800 m (Armsworthy et al. 2014). The marked differences in summer depth and temperature associations that were revealed for Atlantic Halibut tagged in the Gulf relative to those reported within the southern stock (Armsworthy et al. 2014) indicate that the two stocks migrate to different summer feeding grounds.

Seasonal migration behavior has also been identified in Pacific Halibut and Norwegian Atlantic Halibut. Pacific Halibut had deeper depth distributions (300–700 m) in winter than in summer (0–400 m); however, seasonal temperature associations were not evident for Pacific Halibut in the eastern Gulf of Alaska, where halibut were associated with 5–7°C year round, unlike in the western Gulf of Alaska where halibut experienced a broad range of temperatures (5.0–11.6°C) (Loher and Seitz 2006). Norwegian Atlantic Halibut tagged in a fjord were associated with depths of 1,000 m and temperatures of 5.8–7.4°C in winter and experienced shallower depths (<500 m) and warmer temperatures (7.5–11.4°C) in summer; furthermore, halibut were hypothesized to have remained year-round within the fjord, potentially forming an isolated spawning population, based on depth and temperature associations and the fjord’s bathymetry (Seitz et al. 2014). Seasonal differences in depth and temperature associations are common among Pacific and Atlantic halibut stocks, and this variability is presumably a reflection of the ecosystems that they inhabit.

The Atlantic Halibut fishery in the Gulf is currently experiencing its highest landings since the 1950s (DFO 2015b). However, the absence of information on adult habitat use has hampered the development of new survey methodologies. This study revealed higher variability in habitat distribution in the winter and summer. Therefore, longline surveys aiming to obtain an index of abundance of adult Gulf halibut should be conducted in the spring or fall in order to maintain relatively low coefficients of variation. This would allow the survey to index changes in habitat usage over seasonal time scales, thus providing high probability of accurately surveying the abundance and distribution of mature Atlantic Halibut while reducing overall survey costs. Our study provides novel data applicable to an underresearched but increasingly valuable fishery resource.

ACKNOWLEDGMENTS

This research was funded by the Newfoundland and Labrador Department of Fisheries and Aquaculture and the by the Research and Development Corporation of Newfoundland and Labrador Ignite Grants to J. A. D. F and D. R. We thank J. Spingle, E. Carruthers, D. Kamada, K. Krumsick, and the Fish, Food and Allied Workers for their important contributions to field work logistics. We also express our gratitude to halibut harvesters L. Gaslard, R. Gaslard, P. Gaslard, R. Dobbin, F. Dobbin, C. Dobbin, E. Dobbin, D. Lavers, J. Anderson, and A. Crocker who contributed to halibut tagging operations and tag recoveries. Two anonymous reviewers and the subject editor, Ana Parma, provided valuable feedback on earlier drafts of this article.