Basin-scale reproductive segregation of Pacific halibut ( Hippoglossus stenolepis )

Abstract

Pacific halibut Hippoglossus stenolepis (Schmidt) is presently considered to consist of a single spawning population extending from California through the Bering Sea. However, this satellite tagging investigation suggests that geographic landforms and discontinuities in the continental shelf appear to limit the interchange of mature Pacific halibut among large marine ecosystems and delineate the boundaries of potential spawning components in the Gulf of Alaska and Bering Sea, with smaller components along the Aleutian Islands. The geographic segregation of these spawning components may be reinforced by regional behavioural adaptations and different temperature regimes in each area. These results suggest that the Pacific halibut population may be segregated into somewhat discrete spawning units among which less mixing is likely than that which occurs within them. As such, future stock assessment metrics may be most effective in preserving population function if spawning ecology is treated as a basin-scale process.

Full text

Fish Manag Ecol. 2017;24:339–346. wileyonlinelibrary.com/journal/fme 
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© 2017 John Wiley & Sons Ltd
DOI: 10.1111/fme.12233
ORIGINAL ARTICLE
Basin- scale reproductive segregation of Pacific halibut
(Hippoglossus stenolepis)
A. C. Seitz1 | T. J. Farrugia1 | B. L. Norcross1 | T. Loher2 | J. L. Nielsen3
1College of Fisheries and Ocean
Sciences, University of Alaska Fairbanks,
Fairbanks, AK, USA
2International Pacific Halibut Commission,
Seattle, WA, USA
3South Sound Research Institute, Longbranch,
WA, USA
Correspondence
Andrew C. Seitz, College of Fisheries and
Ocean Sciences, University of Alaska
Fairbanks, Fairbanks, AK, USA.
Email: acseitz@alaska.edu
Funding information
Aleutian Pribilof Island Community
Development Association; Central Bering
Sea Fishermen’s Association; Exxon Valdez
Oil Spill Trustee Council; International Pacific
Halibut Commission; North Pacific Research
Board; U.S. Geological Survey–Alaska Science
Center; University of Alaska Fairbanks College
of Fisheries and Ocean Sciences
Abstract
Pacific halibut Hippoglossus stenolepis (Schmidt) is presently considered to consist of a
single spawning population extending from California through the Bering Sea.
However, this satellite tagging investigation suggests that geographic landforms and
discontinuities in the continental shelf appear to limit the interchange of mature Pacific
halibut among large marine ecosystems and delineate the boundaries of potential
spawning components in the Gulf of Alaska and Bering Sea, with smaller components
along the Aleutian Islands. The geographic segregation of these spawning components
may be reinforced by regional behavioural adaptations and different temperature re-
gimes in each area. These results suggest that the Pacific halibut population may be
segregated into somewhat discrete spawning units among which less mixing is likely
than that which occurs within them. As such, future stock assessment metrics may be
most effective in preserving population function if spawning ecology is treated as a
basin- scale process.
KEYWORDS
dispersal, electronic tag, migration, population structure, PSAT
1 | INTRODUCTION
Pacific halibut Hippoglossus stenolepis (Schmidt) inhabits continental
shelf areas of the eastern Pacific Ocean from California to the Bering
Sea and has experienced sustained commercial exploitation for the
last century (International Pacific Halibut Commission, 1998). Long-
term mean yield in the fisheries of Alaska and Canada over the last
century has been >27,000 t (International Pacific Halibut Commission,
unpublished). However, a 16- year time- series of declining age- 8 bio-
mass (Stewart, Leaman, Martell & Webster, 2013), declining mean
size- at- age and a 5- year trend of declining age- 8 recruitment (Stewart
et al., 2013), ultimately led to 10 consecutive years of harvest reduc-
tions with total fishery removals in 2014 nearing the lowest levels in
over 100 years (Stewart & Martell, 2015). During this period, total
removals declined from a historical high of approximately 45,000 t
to less than 19,000 t. This was accompanied by declines in spawn-
ing stock biomass, which is currently estimated to be near the lowest
levels observed since at least the early 1980s and potentially since
before the initiation of commercial harvests in the late 1800s (Stewart,
2017). These declines in the Pacific halibut stock drew attention to
the need to understand regional population structure more fully and
led to formal recommendations that the International Pacific Halibut
Commission (IPHC) develop spatially explicit approaches to assess-
ment and harvest strategy (Francis, 2008; Medley, 2008).
In particular, the abundance decline did not occur simultaneously
across management areas, but was first noted in the eastern Bering
Sea (BS; Hare, 2006; Hare & Clark, 2006) and the Aleutian Islands re-
gion (AI; Hare, 2006), followed by the western Gulf of Alaska (GOA;
Hare, 2010) and finally the eastern GOA (Hare, 2011). Currently, age
structure within the harvested catch also varies regionally: substantial
abundance of relatively old Pacific halibut (age- 25+) still exists around
the AI, while fish >age- 20 are nearly absent in the eastern GOA, and
intermediate age structure is exhibited in landings from the west-
central GOA and eastern BS (Stewart, 2017). In addition to potentially
resulting from spatially variable exploitation patterns, such obser-
vations are consistent with the hypothesis that recruitment and mi-
gratory dynamics are spatially variable (sensu Webster, 2010). These
observations led to the IPHC to use “areas- as- fleets” (AAF) models

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(Stewart, Monnahan & Martell, 2016) that allow for regional- scale in-
puts that account for spatial variance in some demographics, produc-
tivity and fleet dynamics.
Despite the spatial dynamics that are accounted for using AAF
approaches, management of eastern Pacific halibut continues under
the assumption that the stock is represented by a single spawning
population from California through the eastern BS, which drives many
fundamental modelling processes and management decisions (Clark &
Hare, 2006; Stewart & Martell, 2015). This paradigm of spawning pop-
ulation structure rests largely upon tagging studies (Hilborn, Skalski,
Anganuzzi & Hoffman, 1995; see review in Kaimmer, 2000; Webster,
Clark, Leaman & Forsberg, 2013) and analyses of larval distribution
(Bailey & Picquelle, 2002; Skud, 1977; St- Pierre, 1989; Van Cleve &
Seymour, 1953) that have indicated dispersal over broad geographic
expanses corroborated by historical genetic analyses (Bentzen, Britt
& Kwon, 1999; Grant, Teel, Kobayashi & Schmitt, 1984) that failed to
demonstrate significant genetic population structure within the east-
ern Pacific Ocean. However, both genetic results and conventional
tagging data are subject to limitations and equating summertime stock
distribution to area- specific spawning contribution fails to account for
seasonal migratory dynamics in adults.
Neither of the genetic studies upon which the single- stock para-
digm currently rests (Bentzen et al., 1999; Grant et al., 1984) reflected
the full geographic extent of known spawning in the eastern Pacific
Ocean and relied upon samples collected on feeding grounds that lead
to ambiguity regarding the relevance of those results to spawning pop-
ulation structure. By contrast, analyses using modern genetic tech-
niques (Drinan, Galindo, Loher & Hauser, 2016; Hauser, Spies & Loher,
2006; Nielsen, Graziano & Seitz, 2010) and samples that were col-
lected at spawning grounds representing most of the managed range
(Drinan et al., 2016) have indicated that at least weak genetic popula-
tion structure exists. Specifically, although even the most- recent anal-
yses have failed to produce evidence of genetic population structure
along a north–south axis extending from the U.S. Pacific Northwest
(PNW) through the south- eastern BS, reproductive isolation is appar-
ent, moving from east to west along the Aleutian Ridge (Drinan et al.,
2016; Nielsen et al., 2010).
Conventional tagging results are subject to biases introduced from
tag shedding, mortality and differential reporting over time and area.
But perhaps their greatest limitation in the current context is that a
relatively small proportion of the available conventional tag data pro-
vides insights regarding spawning dynamics, per se. Specifically, the
vast majority of tag recoveries have occurred via the directed com-
mercial fishery that only occurs during spring through autumn. By
contrast, it is has been generally established that adult Pacific halibut
migrate from their shallow summer feeding grounds to spawn during
the winter from early November to late March (Loher, 2011; Loher &
Seitz, 2008; St- Pierre, 1984) on grounds concentrated along the con-
tinental slope and in depressions on the continental shelf (St- Pierre,
1984). In early spring, these adults migrate back to continental shelf
feeding grounds (IPHC, 1998; Loher, 2011). Because the vast major-
ity of conventional tag recoveries for Pacific halibut have been from
summer grounds, it is possible that conclusions about movement have
been derived from fish from multiple spawning groups that may be
mixed on common summer feeding grounds.
Recent pop- up satellite archival tag (PSAT) studies have generated
a body of winter location data absent of potential recapture or report-
ing biases, but these data have been analysed and reported exclu-
sively within oceanographic basins (Loher, 2008, 2011; Loher & Blood,
2009; Loher & Seitz, 2006, 2008; Seitz, Loher, Norcross & Nielsen,
2011). These studies indicate most Pacific halibut remain in the basin
in which they were tagged, but intra- and inter- regional movement,
depth and temperature patterns have not been quantitatively exam-
ined. Therefore, the goal of this article was to integrate the new in-
sights gained from these satellite tagging investigations to describe
mechanisms of potential population structure for Pacific halibut and to
relate the observed scales of mixing to recent genetic results and the
spatial scales over which it might be appropriate to estimate biological
reference points for stock management. To accomplish this, regional
variation in the environment and behaviour of Pacific halibut is exam-
ined and then interpreted in the context of potential subpopulation
structure with respect to spawning ecology.
2 | MATERIALS AND METHODS
2.1 | Study area
Regional spawning characteristics and ecology of Pacific halibut, in-
cluding locations, timing, depth and temperature, were examined
using PSATs. To accomplish this, the geographic range of Pacific hali-
but in the north- eastern Pacific Ocean, which represents the core of
this species’ range, was divided into four regions based upon approxi-
mate boundaries of large marine ecosystems (Figure 1). The PNW
was the northern portion of the California Current Ecosystem, which
approximately corresponds to the area south of the entrance of the
Strait of Juan De Fuca (King et al., 2011). The GOA was the area be-
tween the entrance of the Strait of Juan De Fuca and the south side
of Amukta Pass in the AI (Ladd, Hunt, Mordy, Salo & Stabeno, 2005;
Seitz et al., 2011; Stabeno et al., 2004). The BS was the area between
the north side of Amukta Pass to the US–Russian international border
(Seitz et al., 2011; Stabeno, Schumacher & Ohtani, 1999). The AI were
the area west of Amukta Pass (Ladd et al., 2005; Seitz et al., 2011). In
the context of this study, an important feature is seafloor topography,
which is relatively continuous in the PNW, GOA and BS. By contrast,
the AI have several deep passes, some of which are >800 m, which are
characterised by vigorous tidal mixing (Hunt & Stabeno, 2005).
2.2 | Tagging
From 2001 to 2008, PSATs (Wildlife Computers Mk10) were exter-
nally attached (Seitz, Wilson, Norcross & Nielsen, 2003) to Pacific hali-
but (n = 202) during the summer offshore of the PNW (n = 18 in 2006;
Loher & Blood, 2009), in the GOA (n = 86 in 2001–2002 and 2006;
Seitz et al., 2003; Loher & Seitz, 2006; Loher & Blood, 2009), in the
BS (n = 69 in 2002, 2006 and 2008; Seitz et al., 2011) and near the AI
(n = 29 in 2004 and 2008; Seitz et al., 2011). While attached to fish,

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SEITZ ET al.
PSATs measured ambient water temperature, depth of the tag and
ambient light intensity. On pre- programmed dates, the tags released
from the fish, floated to the ocean surface and transmitted archived
data, including summarised daily maximum and minimum tempera-
tures and depths, to the Argos satellite system. The tags’ endpoint
positions were determined from the Doppler shift of the transmitted
radio frequency in successive uplinks received during one satellite
pass (Keating, 1995).
To increase the likelihood of the tags collecting information about
spawning characteristics and ecology, two criteria were followed.
First, to ensure a high probability of tagging mature fish that were
likely to spawn, Pacific halibut that were at least 105 cm fork length
(FL) were selected for tagging (Clark, Hare, Parma, Sullivan & Trumble,
1999). To quantify the extent to which this was successful, the total
number of fish tagged, by region and overall, that were likely to have
been immature (Imcum) at time of tagging (sensu Loher & Blood, 2009)
was calculated, using size- specific maturity data collected during IPHC
setline surveys, as follows:
where FLl = fork length of the nth fish and Pil = proportion of the sur-
veyed population at the given length that was determined to have
been immature via macroscopic gonad examination. For each fish in
the sample, its probability of being immature was assigned the rate
of immaturity observed over all Pacific halibut of the same length
sampled during the setline survey conducted during the summer in
which that fish was tagged. Second, most of the tags (n = 162) were
pre- programmed to pop- up and transmit data during the peak of the
winter spawning season, which lasts from late December to mid-
March (Loher, 2011; Loher & Seitz, 2008). As such, pre- programmed
pop- up dates ranged from 15 January to 1 March for these tags. The
remaining tags, all deployed in 2008 in the BS (n = 36) and AI (n = 4),
were programmed to detach 365 days after deployment, during sum-
mer. However, eight tags that prematurely detached during the mid-
winter spawning season were also considered in this study (BS n = 7;
AI n = 1).
2.3 | Data analyses
Of the tags that reported to satellites during the winter spawning
season, putatively spawning fish were identified as those that were
located in water >200 m deep on the pop- up date of the tag, deter-
mined by the maximum depth on the last day of the tag deployment.
This specification for putatively spawning fish was derived from pre-
vious studies based on winter surveys in which it was concluded that
Pacific halibut spawning is concentrated along the edge of the con-
tinental shelf at depths generally >180 m, but could be more wide-
spread and occur along the entire coast (St- Pierre, 1984). Further
evidence from electronic tagging indicates that spawning occurs in
depths >274 m (Loher & Seitz, 2008). Therefore, spawning depths
were specified as those >200 m as this depth typically represents
the edge of the continental shelf and is a compromise between in-
formation from traditional winter surveys and recent electronic tag-
ging. Therefore, in subsequent analyses, an a priori assumption was
made that the data came from PSATs attached to spawning Pacific
halibut.
Regional spawning characteristics and ecology of Pacific halibut
were analysed using length of tagged fish, winter pop- up locations,
daily maximum depths, and daily maximum and minimum temperatures
of putatively spawning fish tagged in the PNW (n = 10), GOA (n = 48),
BS (n = 24) and AI (n = 12). To examine size of the fish that were tagged
in this study, the mean length of tagged fish in each region was cal-
culated and compared using a Kruskal–Wallis test because of unequal
variance in size among regions. To examine horizontal movement asso-
ciated with spawning, the mean horizontal displacement of all putative
Im
cum =
n
∑
i=l
Pil(FLl
),
FIGURE1 Release and pop- up locations of Pacific halibut tagged with pop- up satellite archival tags in the north- east Pacific Ocean. Dashed
lines delineate the boundaries of the four regions used for analyses in this study

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SEITZ ET al.
spawners in a region was the mean great circle distance between the
summer release and final winter locations, calculated in ArcGIS v.10.
Regional mean horizontal displacements were compared using a
Kruskal–Wallis test because of unequal variance among regions.
To examine vertical movement associated with spawning, three
analyses on maximum depths experienced by Pacific halibut were
conducted. In these maximum- depth analyses, it was assumed that
Pacific halibut spend the majority of their time on or near the sea floor,
and therefore, maximum daily depths measured by a tag represent
the depth of the seafloor in the area occupied by the fish that day
(Seitz et al., 2003). To conduct the analyses, daily maximum depths
were categorised as occurring during the non- spawning (before 27
December) or spawning (between 27 December and 8 March) sea-
son (Loher, 2011; Loher & Seitz, 2008). Within the non- spawning and
spawning seasons, daily maximum depths were averaged by month to
produce monthly mean maximum depths, which avoided pseudo repli-
cation and autocorrelation associated with using daily depth informa-
tion. Because portions of December were included in both spawning
and non- spawning seasons, two mean depths were calculated for this
month, one for the non- spawning portion (1–26 December) of the
month and one for the spawning portion (27–31 December). In the
first depth analysis, to determine whether depths occupied by Pacific
halibut differed between non- spawning and spawning seasons in
each region, monthly mean maximum depths of all fish during spawn-
ing and non- spawning seasons were pooled by region and compared
using a Welch’s two sample t test which assumed unequal variances.
In the second analysis, to determine whether spawning- season depths
differed among regions, monthly mean maximum depths during the
spawning season of all fish pooled by region were compared using
a four- level one- way ANOVA with unequal variances. In the third
analysis, to determine whether the difference in non- spawning- and
spawning- season depths varied among regions, monthly mean max-
imum depths of all fish pooled by region during non- spawning and
spawning seasons were compared using a two- way ANOVA and a
mixed- effects model was used to describe the variance in depth ex-
plained by season and region. Statistical analyses were performed
using R version 2.13.2 (Institute for Statistics and Mathematics, Vienna
University of Economics and Business, Austria). Statistical significance
was assessed at α = .05.
Regional temperatures experienced by Pacific halibut were qual-
itatively compared by calculating the monthly mean minimum and
maximum temperatures experienced by all fish in each region. In con-
trast to depth comparisons, in which maxima experienced by fish were
quantitatively analysed under the assumption that the fish spent most
of their time near the maxima, temperature minima and maxima were
qualitatively examined because water temperature frequently fluctu-
ates at a constant depth. Therefore, it is not reasonable to assume that
the fish spent most of their time near the minima or maxima, nor is the
proportion of time spent at specific temperatures between the minima
and maxima known, making it impossible to estimate a representative
water temperature for each day.
3 | RESULTS
A total of 94 PSATs provided data about spawning characteristics and
ecology of Pacific halibut throughout their range in the north- east
Pacific Ocean (Table 1). Significant differences in size of tagged fish
existed among regions (Kruskal–Wallis χ2 = 14.483, df = 3, P = .002)
and a post hoc Kruskal–Wallis multiple comparison test showed that
the Pacific halibut tagged in the PNW were significantly smaller than
those in both the AI and GOA. Fish tagged in all regions had a high prob-
ability of being mature; individual maturity probabilities ranged from
78% to 100% while regional means ranged from 89.4 ± 1.5% (PNW) to
94.3 ± 1.7% (AI). Significant differences in mean maturity probabilities
existed among regions (Kruskal–Wallis χ2 = 10.772, df = 3, P = .013), but
due to the conservative nature of the post hoc Kruskal–Wallis multiple
comparison test, no significant differences among regions were identi-
fied in pairwise comparisons. In no region did the cumulative probability
of having tagged immature fish (Imcum) exceed ~10% of the total availa-
ble sample size. Resulting Imcum values were PNW = 1.06 (of n = 10 fish);
GOA = 3.50 (of n = 48), BS = 2.51 (of n = 24) and AI = 0.68 (of n = 12).
During winter, the majority (95.7%) of Pacific halibut tagged
during the summer remained in the region in which they were tagged
TABLE1 Summary of sample sizes and mean (±SE) fish lengths, maturity probabilities, horizontal displacements and maximum non-
spawning and spawning depths of Pacific halibut tagged in four regions
Region # PAT tags
Mean total
length (cm)
Mean maturity
probability (%)
Mean horizontal
displacement (km)
Mean non- spawning
depth (m)
Mean spawning
depth (m)
AI 12 129.0 ± 4.3* 94.3 ± 1.7 62.2 ± 13.7 250.0 ± 18.7 494.2 ± 15.4*
BS 24 114.7 ± 1.7*,† 89.5 ± 1.0 100.8 ± 37.4 312.3 ± 14.6 475.5 ± 23.1*
GOA 48 124.1 ± 1.8* 92.7 ± 0.8 213.6 ± 38.2 237.8 ± 6.4 353.8 ± 8.9†
PNW 10 113.4 ± 3.0†89.4 ± 1.5 415.6 ± 140.5 236.5 ± 11.1 324.4 ± 21.7†
AI, Aleutian Islands; BS, Bering Sea; GOA, Gulf of Alaska; PNW, Pacific Northwest.
Asterisks (*) and daggers (†) indicate statistically similar groups determined by post hoc multiple comparison tests (α = .05) when significant differences
were found among mean regional values using ANOVA (mean depth during the spawning season) and Kruskal–Wallis (fish length) tests. A Kruskal–Wallis
test showed significant differences in probability of maturity among regions (P = .013), but multiple comparison tests did not reveal any significant pairwise
differences. A Kruskal–Wallis test showed so significant differences among mean regional horizontal displacements, while mean regional non- spawning-
season depths were not compared. In all regions, mean non- spawning- season depths were significantly shallower than mean spawning- season depths
(Welch’s t test, P < .001).

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SEITZ ET al.
(Figure 1). The only four fish that emigrated from their tagging region
were all from the PNW; thus, 40% of the fish tagged in this area dis-
persed from it during the winter. Mean horizontal displacement varied
considerably among regions (Table 1), but regional differences were
insignificant (Kruskal–Wallis χ2 = 6.859, df = 3, P = .077). In general,
the PNW fish displayed the greatest mean difference and variability in
distance between non- spawning and spawning locations, while the AI
fish displayed the smallest difference and variability.
A total of 798 monthly mean maximum depths (AI = 95, BS = 191,
GOA = 425, PNW = 87) provided information about seasonal depths
in each region (Table 1, Figure 2). In all four regions, the mean non-
spawning- season depths were significantly shallower than the depths
during the spawning season (P < .001, Table 1, Figure 2). Within the
spawning season, significant differences in monthly mean depths
among regions existed (F3,224 = 27.95, P < .001; Table 1). In general,
the spawning- season depths of Pacific halibut in the AI and BS regions
were deeper than those exhibited by fish in the GOA and PNW regions.
Specifically, a post hoc Tukey HSD test showed that the spawning-
season depths of AI and BS (P = .896), and GOA and PNW (P = .632)
halibut were not significantly different, but spawning- season depths
between AI and GOA, AI and PNW, BS and GOA, and BS and PNW
(P < .001) were significantly different. A significant interaction term in
the two- way ANOVA (F3,790 = 7.11, P < .001) indicated that significant
differences in depths between the non- spawning and spawning sea-
sons existed among the four regions. In general, Pacific halibut in the
AI region showed the greatest difference in depths between spawn-
ing and non- spawning seasons, whereas fish tagged in the PNW re-
gion showed the least difference in depths between the two seasons
(Table 1, Figure 2). Additionally, Pacific halibut in the AI and BS regions
had similar spawning- season depths, but not non- spawning depths,
while fish from the GOA and PNW regions spent the non- spawning
and spawning seasons at similar depths (Table 1, Figure 2). The mixed-
effects model showed that the variability in depth between non-
spawning and spawning seasons (seasonal variance = 9,789.9) had a
greater contribution to the overall depth variance than the variability
among regions (region variance = 2,038.7).
The mean temperature range experienced by Pacific halibut varied
among regions (Figure 3). The PNW and GOA fish experienced rela-
tively constant, warm temperatures throughout the year while BS fish
experienced relatively constant, cool temperatures. By contrast, the AI
fish experienced relatively warm temperatures during the summer and
cool temperatures during the winter. In general, the water tempera-
tures ranged between 6.0 and 7.5°C for PNW and GOA fish during the
winter spawning season. During this same time, water temperatures
occupied by AI and BS fish were much cooler and ranged from approx-
imately 3.5 to 4.0°C.
4 | DISCUSSION
The low rate of spawning dispersal among regions by Pacific halibut
and the different depths occupied during the spawning season sug-
gest that reproductive segregation of this species occurs among dif-
ferent regions throughout its range. This is consistent with genetic
analyses (Drinan et al., 2016; Nielsen et al., 2010) that have identified
significant genetic structure in the Aleutian Islands region relative to
the remainder of the eastern stock. Differences in probability of ma-
turity among regions were marginal, all tagged fish had a relatively
high probability of being mature, and there was no clear relationship
between fish size and dispersal characteristics. Thus, it is likely the
reproductive segregation observed in this study was not related to
regional differences in fish size and probability of maturity; rather, the
low rate of spawning- season dispersal among regions appears to be
FIGURE2 Monthly mean (±SE) maximum depths of putatively
spawning Pacific halibut in four regions in the north- eastern Pacific
Ocean, measured by pop- up satellite archival tags. Spawning depth
(>200 m) and peak spawning season (shaded area) were delineated
based on previous winter fishing surveys (St- Pierre, 1984) and
electronic tagging (Loher & Seitz, 2008) studies
FIGURE3 Monthly mean minimum and maximum temperatures
experienced by putatively spawning Pacific halibut in four regions
in the north- eastern Pacific Ocean, measured by pop- up satellite
archival tags

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associated with bathymetric and hydrographic properties in the con-
nections among regions. The horizontal segregation of spawning com-
ponents may be reinforced by vertical segregation as mean spawning
depths differed between northern and southern regions.
Discontinuities in the continental shelf and hydrographic proper-
ties in connections among regions appear to limit the seasonal inter-
change of Pacific halibut among some areas. Specifically, none of the
fish tagged in the AI, BS and GOA dispersed among these tagging areas
between summer feeding and winter spawning seasons, whereas sea-
sonal migration between the GOA and PNW was relatively common.
The AI, BS and GOA are separated from each other by passes, some of
which are deep (>800 m), and all are characterised by swift currents
and strong turbulence (Hunt & Stabeno, 2005). In this study, none of
the tagged fish traversed these passes separating regions. It is not likely
that these passes are complete barriers to dispersal as Pacific halibut
are powerful swimmers that are able to disperse >1,000 km season-
ally (Loher & Seitz, 2006), and previous conventional tagging studies
(Skud, 1977) and PIT tagging studies (Webster, Clark & Forsberg, 2008)
have documented both juvenile and adult Pacific halibut moving across
passes. Rather, these passes appear to reduce the dispersal of adult
halibut among these three regions, relative to the rates that would be
observed in the absence of such features (Seitz et al., 2011). In con-
trast to the AI, BS and GOA, which are all separated by passes, the
continental shelf and slope as well as the hydrography of PNW are con-
tiguous with those of GOA and approximately 40% of the fish tagged
in PNW dispersed to GOA for the winter spawning season. As such,
without strong turbulence and deep passes, Pacific halibut from GOA
and PNW may intermingle more often. Consequently, ocean passes
with strong turbulence may delineate three spawning components of
Pacific halibut in the GOA/PNW, BS and AI.
Although differences in mean regional horizontal displacement of
Pacific halibut were insignificant, intraregional seasonal dispersal dis-
tance appears to be influenced by the distance between major discon-
tinuities in the continental shelf in each region, rather than fish size.
Specifically, the PNW and GOA regions have the longest continuous
continental shelf and slope that are not intersected by passes with
strong turbulence and, as such, the Pacific halibut in these regions had
largest mean and maximum seasonal dispersal distances. By contrast,
the fish along the Aleutian chain, a region characterised by several rel-
atively deep passes formed by discontinuities in the continental shelf,
undertook the smallest mean seasonal dispersals to winter spawning
grounds. Insignificant differences in mean seasonal displacement be-
tween even PNW and AI, the regions with the largest and smallest
mean seasonal displacements, were likely obfuscated by large variance
caused by some fish in PNW that undertook relatively small dispersals
between summer feeding and winter spawning locations. This vari-
ance may be a function of a small number of immature fish that may
have occurred within each sample population, adult skip- spawning
(sensu Loher & Seitz, 2008), or the existence of undocumented local
spawning groups populated by year- round PNW residents (Loher &
Blood, 2009). It is unlikely that these observations of regional mean
horizontal displacement are a result of regional mean fish size, as there
is no obvious relationship between them.
In addition to a lack of intermingling of Pacific halibut from dif-
ferent parts of its range on common spawning grounds, regional dif-
ferences in mean spawning- season depths exist. The winter spawning
locations of AI and BS fish were significantly deeper than those from
PNW and GOA, and there was no clear relationship between regional
mean spawning- season depth and fish size. Rather, regional spawning-
season depths appeared to track geographic trends in ambient water
temperatures, which were relatively cold in AI and BS and relatively
warm in PNW and GOA. It is likely that these regional differences
in spawning depths evolved as local adaptations for maximising the
survival of their progeny, given ambient water temperatures in each
region. If regional differences in spawning depths are heritable, these
may further reinforce the horizontal separation of spawning compo-
nents of Pacific halibut by causing additional vertical spawning segre-
gation among individuals from regions within this species range.
Genetic analyses partially support the findings that basin- scale
reproductive segregation among individual adult Pacific halibut may
occur. Using nuclear microsatellite loci, Nielsen et al. (2010) detected
significant (P < .05) heterogeneity between Pacific halibut from AI
and those from BS and GOA (FST range: .007–.008). Similarly, in a
population- wide analysis that used samples collected in winter and a
substantially larger suite of both anonymous and expressed sequence
tag (EST) linked microsatellites, Drinan et al.’s (2016) pairwise compar-
isons between western Aleutian sampling locations and those in the
BS and GOA were consistently significant (P value range: .001–.011)
at FST values (range: .001–.0103) that were similar to those derived
by Nielsen et al. (2010). These findings of genetic divergence of Pacific
halibut from AI not only imply that adults are reproductively segre-
gated, but that barriers to gene flow also exist for larval and juvenile
stages. These gene flow barriers may result from local retention mech-
anisms (Sponaugle et al., 2002), such as clockwise island circulation
around the Aleutian Islands (Ladd et al., 2005; Stabeno et al., 1999),
that may entrain the Pacific halibut larvae as they drift in the pelagia
for up to 6 months (Thompson & Van Cleve, 1936). Another possible
barrier to Pacific halibut gene flow among regions is contra- natant mi-
gration of juveniles to their natal region after advection among regions
during their 6- month larval drifting phase (Cushing, 1975, 1981).
In contrast to the findings of genetic divergence in adult Pacific
halibut from AI, no evidence has yet been found of genetic divergence
of Pacific halibut in BS and GOA (Drinan et al., 2016; Nielsen et al.,
2010). This may be because of the resolution of reproductive segrega-
tion provided by genetics and tagging studies. Specifically, the sample
size of this study is likely too small to detect infrequent interchange
of spawning adult Pacific halibut between BS and GOA that erases
significant genetic divergence between the two regions. Additionally,
genetic divergence between the two areas may be erased by advec-
tion of larvae between regions during their 6- month pelagic phase
(Thompson & Van Cleve, 1936) without accompaniment by contra-
natant migration by vagrants to their natal region.
To reconcile the contrasting results from this tagging study and
genetic analyses, additional information about Pacific halibut move-
ment is needed. First, because less than a year of data were obtained
from a fish species that may live up to 50 years, longer- term electronic

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SEITZ ET al.
tag deployments are necessary to capture observations necessary for
maintaining population structure, such as regional fidelity to spawning
areas and interannual dispersal. Second, because tagging large animals
likely results in observations being biased in favour of sexually mature
females (Clark et al., 1999), electronic tag deployments on other de-
mographic components including all males and immature females are
necessary to understand fully dispersal among regions. Unfortunately,
it was not possible to observe the movements of these demographic
components because of the relatively large size of the tags and con-
cern for the health of the fish. However, current efforts using relatively
small electronic tags are underway to understand the movement pat-
terns and behaviour of males and immature females.
Nevertheless, the current analysis provides insight about basin-
scale reproductive segregation of Pacific halibut throughout its range
in the north- east Pacific Ocean. When modelling fished populations,
it is important to consider temporal scales relevant to the prosecu-
tion of their fisheries which are typically subgenerational for long- lived
fishes such as Pacific halibut, as opposed to multigenerational times-
cales at which population- genetic signals evolve. Specifically, Drinan
et al. (2016) demonstrated that even very low levels of migratory
exchange would be sufficient to homogenise allele frequencies and
that reproductive segregation would need to be maintained for >500
generations to reach migration- drift equilibrium. By contrast, the cur-
rent analysis suggests that, even if components of the eastern Pacific
halibut population appear to be mixed fully at genetic timescales, in-
terbasin dispersal among spawning groups may occur at low enough
rates to impede the recovery of spawning stock biomass if spawning
groups are differentially depleted among regions. For example, if the
abundance of spawners in the eastern Bering Sea was depleted to a
low level, there is little evidence that it would increase markedly soon
thereafter as a result of seasonal exchange with the Gulf of Alaska
spawning population. This is corroborated by PIT tag studies that sug-
gested that migration of Gulf of Alaska spawning stock is unlikely to
influence the abundance of Bering Sea spawning stock to any appre-
ciable degree on interannual timescales (Webster et al., 2013).
It is recommended that IPHC further investigate the assump-
tion that the eastern Pacific halibut stock is represented by a single
spawning population from California through the eastern BS. Should
additional evidence be discovered supporting the concept of regional
subpopulations, population function may be best preserved by modi-
fying fundamental modelling approaches and management decisions.
For example, regionally explicit harvest policy metrics could be estab-
lished, including regionally variable target exploitation rates (sensu
Martell, Stewart & Leaman, 2013) that apply spawning stock biomass
of females thresholds as regional components that reflect functional
spawning ecology. Understanding regional productivity, spawning dy-
namics and spawning biomass distribution during the active spawning
season are critical to any such endeavours.
ACKNOWLEDGMENTS
This project was made possible by the captains and crews of the fish-
ing vessels Angela Lynn, Blackhawk, Bold Pursuit, Free to Wander,
Heritage, Kema Sue, Norska, Pacific Sun, Pender Isle, Proud Venture,
Rocinante, Star Wars II, Waterfall and Wind Dancer; International
Pacific Halibut Commission (IPHC) Sea Samplers R. Ames, K. Attridge,
K. Bareza, D. Barrett, B. Biffard, A. Delisle, E. Ekroth, H. Emberton, A.
Knot, E. Lardizabal, J. Lucke, L. Mattes, M. Monk, D. Rafla, T. Saltau,
J. Spencer, A. Vatter and A. Williams; IPHC Port Sampler L. O’Neil;
IPHC Annual Setline Survey Managers K. Ames, E. Anderson- Chau,
C. Dykstra, T. Geernaert and E. Soderlund for logistical assistance; D.
Wilson of United States Geological Survey- Alaska Science Center; and
P. Lestenkof of Central Bering Sea Fishermen’s Association. Partial
funding for this project was provided by the Aleutian Pribilof Island
Community Development Association, Central Bering Sea Fishermen’s
Association, Exxon Valdez Oil Spill Trustee Council, the International
Pacific Halibut Commission, the North Pacific Research Board, the
U.S. Geological Survey–Alaska Science Center and the University of
Alaska Fairbanks College of Fisheries and Ocean Sciences.
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How to cite this article: Seitz AC, Farrugia TJ, Norcross BL,
Loher T, Nielsen JL. Basin- scale reproductive segregation of
Pacific halibut (Hippoglossus stenolepis). Fish Manag Ecol.
2017;24:339–346. https://doi.org/10.1111/fme.12233