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Unaccounted mortality in salmon fisheries:
non-retention in gillnets and effects on estimates of
spawners
Matthew R. Baker*
1
and Daniel E. Schindler
1,2
1
School of Aquatic and Fishery Sciences, University of Washington, Box 355020, Seattle, WA 98195-5020, USA; and
2
Department of Biology, University of Washington, Seattle, WA 98195-1800, USA
Summary
1. Effective and sustainable natural resource management is enhanced when the consequences of
exploitative practices are fully understood and acknowledged. Commercial fisheries devote consid-
erable resources to maximize the harvest of target species and minimize interference with non-target
stocks. Appropriately, bycatch and discard of non-target stocks are recognized as critical economic
and conservation concerns. Few studies, however, have examined non-retention mortality in target
stocks. Non-retention, where fish are engaged by fishing gear but not landed, is rarely quantified
and the effects on stocks are unknown. Mortality due to non-retention may have important effects
on the dynamics of exploited populations.
2. We surveyed spawning populations of sockeye salmon Oncorhynchus nerka that had traversed
commercial fisheries in Bristol Bay, Alaska, to estimate the incidence of non-retention in gillnets
and the severity of injuries associated with entanglement. To better understand how gillnet injury
affects spawning success, we tagged and monitored stream-spawning fish and applied a maximum
likelihood model to mark–recapture data.
3. A substantial portion (11–29%) of spawning sockeye salmon exhibited clear signs of past entan-
glement with commercial gillnets. Survival among such fish was significantly reduced. More than
half of the fish that reach natal spawning grounds with fishery-related injuries fail to reproduce. This
suggests that estimates of spawning stocks are inflated by 5–15% at minimum.
4. Synthesis and applications. Our analyses indicate that non-retention in gillnet fisheries is an
important and under-appreciated consequence of the exploitation of salmon. Stock estimates for
exploited populations that do not account for non-retention mortality overestimate the number of
reproductively viable fish. Unaccounted mortality and interannual variation in the magnitude
of this mortality may prevent accurate estimates of viable spawners, confound our understanding
of the relationship between stock size and recruitment, impede optimal management and obscure
the ecosystem impacts of migratory stocks in coastal watersheds. Given the magnitude of non-
retention in this fishery, explicit consideration of non-retention mortality may be warranted across
a wide range of exploited populations.
Key-words: delayed mortality, ecosystem engineers, fishery-induced injury, mark–recapture
analysis, natural resource management, Pacific salmon, population dynamics, stock-recruit-
ment estimation
Introduction
Fishery-related injury in target stocks is rarely quantified but
may be an important source of mortality in heavily exploited
populations (Alverson 1997; Hall, Alverson & Metuzals 2000).
Both immediate and delayed mortality caused by encounters
with commercial gear is often high (Chopin & Arimoto 1995).
While bycatch, discard and release of non-target species is
often considered (Harrington, Myers & Rosenberg 2005),
damage sustained by target stocks is often ignored. Certain
gear types have low retention rates, enabling a portion of fish
that encounter gear to disentangle or escape, often leading to
delayed mortality. Such delayed mortality may have important
consequences for fisheries management and the sustainability
*Correspondence author. E-mail: mattbakr@u.washington.edu
Journal of Applied Ecology 2009, 46, 752–761 doi: 10.1111/j.1365-2664.2009.01673.x
2009 The Authors. Journal compilation 2009 British Ecological Society
of exploited populations, especially where these stocks are
managed for explicit targets and fishing effort relative to stock
size is variable.
Many Pacific salmon gillnet fisheries are managed according
to escapement targets. These are terminal fisheries, which har-
vest salmon on their return migration to freshwater and are
regulated to ensure that sufficient numbers of adults evade the
fishery and spawn. While most fish intercepted by the fishery
are harvested, many disentangle from nets and continue their
migration to natal spawning areas. Many of these fish sustain
serious injuries. Although counted as part of the aggregate
escapement of viable spawners, fish damaged in the fishery
experience physical trauma, physiological stress, exhaustion
and increased susceptibility to disease (Ricker 1976; Davis
2002). These fish may die prior to spawning or have reduced
spawning success. Such losses have a direct bearing on esti-
mates of spawning adults. If a significant portion of the enu-
merated escapement fails to spawn, escapement estimates will
not accurately reflect the effective population of viable spaw-
ners. This will also confound analyses of the relationship
between spawning stock size and future recruitment to the
population. Where delayed mortality affects a constant per-
centage of escaped stocks, this loss may be implicit in the
stock-recruit function. In most fisheries, however, fishing effort
is variable between years, dependent on the size and timing of
the salmon run. The failure to account for inter-annual vari-
ability in fishery-related injury to spawning stocks may gener-
ate significant errors in stock assessment.
Survival for fish entangled by gillnets is the lowest for all
gear types (ASFEC 1995). With regard to commercial salmon
fisheries, there are no current estimates of gillnet-related injury
in exploited populations nor has there been extensive research
to determine the consequence of these injuries on spawning
success among escaped fish. Studies of mortality associated
with non-retention in salmonids have largely focused on catch-
and-release sport fisheries (Vincent-Lang, Alexandersdottir &
McBride 1993; Booth et al. 1995) or commercial fisheries using
troll and seine gear (Parker, Black & Larkin 1959; Thomas &
Associates Ltd 1997). The few existing studies that address
non-retention mortality in gillnet fisheries either examine the
issue in an experimental context (Thompson, Hunter & Patten
1971; Thompson & Hunter 1973), document outdated harvest
regimessuchashighseasfisheries(Frenchet al. 1970; Ricker
1976), evaluate selective fisheries practices where entangled fish
are deliberately released and revived (Buchanan et al. 2002;
Vander Haegen et al. 2004) or exclude severely damaged fish
from analysis (Thompson & Burgner 1952; Hartt 1963).
The Bristol Bay sockeye salmon Oncorhynchus nerka fishery
is managed to achieve constant annual escapement. Our study
was designed to quantify the impact of gillnet injury on
escaped stocks, given the current operation of the fishery. We
estimated the incidence and severity of injuries in fish returning
to natal streams and the effect of such injuries on pre-spawning
mortality. The findings suggest that gillnet injuries are com-
mon and, in many cases, inhibit spawning. The effects of such
unaccounted mortality may have important implications for
the designation of optimal escapement targets in exploited
populations, the estimation of spawner-recruit relationships,
the understanding of evolutionary processes driven by fishery
selection and the characterization of the ecosystem effects of
spawning activity in coastal watersheds.
Materials and Methods
ESTIMATION OF THE INCIDENCE OF GILLNET INJURY
Analyses were conducted in the Wood River system in south-west
Alaska (see Map Appendix S1, Supporting Information). The Wood
River system is the primary watershed in the Nushagak district of the
Bristol Bay fishery, supporting one of the world’s largest stocks of
commercially exploited sockeye salmon (Hilborn et al. 2003).
Throughout the Wood River system, sockeye salmon gather within a
100 m range of their natal stream for a period of 1 month following
migration through the fishery, entering spawning streams at matura-
tion (Hendry, Berg & Quinn 1999). This behaviour allowed us to sam-
ple discrete populations immediately prior to their entry to spawning
grounds. At Pick Creek, the site of our mark–recapture study, we
used beach seines to sample 200–500 fish each year for three consecu-
tive years (2005–2007) to determine the incidence and severity of gill-
net injuries in the pre-spawning population of sockeye salmon that
had successfully transited the fishery. In 2006 and 2007, we expanded
sampling to include 10 populations throughout the Wood River sys-
tem. All sampling occurred within a 2-week period (12–24 July). We
sampled streams in accordance with historical peak spawning date
(University of Washington, unpublished data), immediately prior to
expected stream entry.
CLASSIFICATION OF GILLNET INJURY
All sockeye salmon were examined for fishery-related injury. Clear
net marks, abrasions, contusions or scale loss spanningthe circumfer-
ence of the fish were considered evidence of gillnet entanglement. Gill-
net marked fish were grouped according to the severity of the injury:
(i) minor injuries included any evidence of gillnet entanglement,
including net marks and ⁄or scale loss; (ii) moderate injuries included
open wounds and ⁄or skin loss on 5–20% of the surface area of the
fish; and (iii) severe injuries included large open wounds, fractured
jaws or gill plates, and ⁄or skin loss on >20% of the surface area of
the fish (Fig. 1).
STREAM RESIDENCE AS AN INDICATOR OF
PRE-SPAWNING MORTALITY
Our analysis sought to determine whether gillnetinjury resulting from
non-retention in commercial fisheries prevents injured fish from
spawning. We examined a stream-spawning population of salmon,
using stream residence as a proxy for successful reproduction. Direct
observation of spawning activity was not possible given the spatial
extent of the survey. Egg retention estimates were compromised by
scavenging gulls Larus glaucescens. Therefore, a mark–recapture
study was conducted at Pick Creek (5933¢00¢¢N, 15904¢18¢¢W) to
determine relative differences in survival and stream residence
between fish with and without fishery-related injuries. A second-order
stream, Pick Creek originates in a series of spring-fed ponds and flows
2 km before entering Lake Nerka. The stream averages 33 cm deep
and 7Æ8 m wide (Hendry 1998) with high water clarity and relatively
constant discharge (Hendry et al. 1999). Spawning occurs at high
densities throughout the lower 2 km of the stream, with an average of
Unaccounted mortality in salmon fisheries 753
2009 The Authors. Journal compilation 2009 British Ecological Society, Journal of Applied Ecology,46,752–761
8000–10 000 adult spawners (Rogers & Schindler 2008) and a spawn-
ing season of c. 40 days. Due to the presumption that mortality of
severely injured fish would increase as a function of distance travelled
from the fishery, we sought to sample a population that represented
the average distance from commercial fishery to natal stream for Bris-
tol Bay stocks. Throughout Alaska, sockeye salmon stocks migrate a
mean distance of 103 ± 70 km (n= 32) to an elevation
72 ± 104 m (n= 32). The average Bristol Bay sockeye migrates
94 km to 28 m (Burgner 1991). With a freshwatermigration of 98 km
to an elevation of22 m (Hendry & Berg 1999), the Pick Creekpopula-
tion is representative of the post-fishery migration in Bristol Bay.
Pre-spawning mortality was assumed to occur where fish failed to
demonstrate sufficient stream residence to allow spawning opportuni-
ties. Although sockeye salmon enter spawning areas at reproductive
maturity, several days in-stream precede successful spawning at high
density sites. The reproductive lifespan (stream entry to senescence)
of Pick Creek fish is 17–20 days (Hendry et al. 1999). All sockeye sal-
mon perish soon after spawning. Typically fish hold in tight schools
during their first days of stream residence and disperse to colonize
spawning habitat within a week of stream entry. Subsequent studies
in Pick Creek indicate females secure territory and spawn towards the
end of the first week of in-stream residence (mean days post-
entry = 8Æ05±5Æ56) and defendtheir redd site until senescence, typ-
ically maintaining a consistent presence for a week or more (mean
days post-spawning = 6Æ93 ± 2Æ37; M. Baker, unpublished data).
While movement does not preclude reproductive success in males,
males establish dominance hierarchies on small spatial scales (Quinn,
Adkison, & Ward 1996) and typically demonstrate strong site fidelity
following a period of initial exploration (Foote 1990; Rich et al.
2006). Competitive advantage among males is driven by prior resi-
dence (Foote 1990) and, as males remain reproductively active until
death, extended stream residence confers greater reproductive oppor-
tunities. Given these conditions, we determined any fish that failed to
demonstrate a minimum stream residence of 3 days failed to spawn
(sensitivityto this threshold value shown in Table 1).
MARK–RECAPTURE SAMPLING AND IN-STREAM
OBSERVATION
From 15 to 17 July 2005, we sampled and tagged pre-spawning adult
sockeye salmon at the mouth of Pick Creek. Fish were capturedusing
a beach seine.A sample of 100 gillnet-marked fish was tagged, includ-
ing 50 with minor injuries, 30 with moderate injuries and 20 with
severe injuries (42 males and 58 females). This distribution of severity
of injury reflects a representative sampling of the injured population
of fish at Pick Creek (n= 1863). A sample of 100 uninjured fish (50
males and 50 females) was also tagged as a control group. Each fish
was anaesthetized with tricaine methanesulphonate (MS-222; Wes-
tern Chemical, Inc., Ferndale, WA), tagged with an external uniquely
coded 3-cm Petersen disc tag (Floy Tag Co., Seattle, WA), rejuve-
nated in cold water and released (Fig. 2). This method of tagging cor-
responds to a well-established procedure that neither accelerates
mortality nor has lasting effects on fish behaviour (Quinn & Foote
1994). Presence and severity of fishery-related injury and presence of
fungal infection (Saprolegnia spp.) was assessed at this stage. Photo-
graphs of all injured fish were reviewed at the conclusion of sampling
to re-evaluate classification and ensure standard ranking overtime.
Visual stream surveys of Pick Creek were conducted every other
day throughout the lifespan of all tagged fish (17 July to 25 August).
Surveys recorded the presence, absence and mortality of tagged fish.
For analysis,each 2 day period was considered a sampling event.
NONPARAMETRIC ESTIMATOR FOR STREAM
RESIDENCE TIME
Survival between sampling occasions and stream residence for each
category of gillnet injury were estimated through a nonparametric
estimator using a maximum likelihood approach. This allowed us to
separately estimate survival and account for failures to detect fish
during stream surveys. A model developed by Lady & Skalski (1998)
was adapted and used to estimate stream residence, following
approaches developed by Cormack (1964) and elaborated by Burn-
ham et al. (1987), whereby conditional survival probabilities are
estimated from one sampling event to the next based on release–
recapture data for marked individuals.
Maximum likelihood estimation (MLE) was used to derive survival
and detection probabilities,using the following function:
LðS;P;kja;cÞ/ Y
K2
i¼1
Svi
i
!
Y
K1
i¼2
Pai
ið1PiÞVi1ai
!
Y
K1
i¼1
vci
i
!
kvK1
where Kis the number of sampling occasions; S
i
is the probabil-
ity that an individual alive at sampling occasion iwill be alive at
sampling occasion i+1; P
i
is the probability that an individual
alive at sampling occasion iwill be detected; kis the product of
final survival and detection probabilities (S
K–1
P
K
); a
i
is the num-
ber of marked individuals detected at sampling occasion i;c
i
is
Fig. 1. Photographs of relative severity of gillnet injury. Note that coloration is dark (red) and scales are absorbed in fish without injury. Fish have
less coloration (red fiblush fisilver) and retain scales as severity of injury increases. Morphological traits associated with sexual maturity in
males (dorsal–ventral expansion and extended kype) are less pronounced among fish with injury. These trends suggest gillnet injury may retard
or inhibit sexual maturation.
754 M. R. Baker & D. E. Schindler
2009 The Authors. Journal compilation 2009 British Ecological Society, Journal of Applied Ecology,46,752–761
the number of marked individuals detected for the last time at
sampling occasion i;v
i
is the number of marked individuals
known to be alive at sampling occasion i+1;v
i
is the probabil-
ity that an individual alive at sampling occasion iwill not be
detected again (v
i
=c
i
⁄a
i
). Ris the number of individuals tagged
at the initial sampling occasion.
where
vi¼RX
i
j¼1
cj
The maximum likelihood estimators for survival parameters (and
their variances and covariances) are derived by Burnham et al. (1987)
and reformulated by Lady & Skalski (1998):
^
S1¼a2v2
Rða2c2Þ
^
Si¼aiþ1ðaiciÞviþ1
aiviðaiþ1ciþ1Þfor i¼2;...;K2
Using these survival probabilities, Lady & Skalski (1998) devel-
oped the following estimator of stream residence time (T), operating
on assumptions that: (i) the distribution of deaths between sampling
periods is uniform and (ii) all individuals die prior to the final
sampling occasion.
^
T¼1
2X
K2
i¼1
ðtiþtiþ1Þð1^
SiÞY
i¼1
j¼1
^
Sj
()
þ1
2ðtK1þtKÞY
K2
j¼1
^
Sj
where t
i
is the time of the ith sampling occasion relative to the
initial sampling occasion, t
1
=0.
Although technically developed to derive estimates of stream resi-
dence time, this model was applied to data on a beach spawning pop-
ulation (Quinn & Foote 1994), where fish were marked and
recaptured at the same location. In our study, fish were tagged at the
stream mouth and surveys were conducted within the main stem of
the stream. We therefore modified the model to estimate separate
probabilities for: (i) whether or not a fish entered the stream and (ii)
its survival and detection within the stream.
In our analysis, the first period describes the probability of stream
entry or the interval between when a fish was marked (tagged at the
stream mouth) and its first recapture (first in-stream observation).
This is defined as the joint probability of survival and stream entry.
The second period describes survival after stream entry, which we
characterize as stream residence. Stream residence was estimated only
for fish that were observed in the stream and initiated at the first
in-stream observation. For integration with the model above, we
arranged the data such that the first in-stream observation (stream
entry) for a given individual is considered the first sampling occasion
(release) for that individual, regardless of calendar date. All sub-
sequent sampling occasions for that individual arerelative to that first
in-stream observation, in effect, modelling stream residence as a first-
order approximation by entry date rather than calendar date. Calen-
dar date of spawning had no influence on the senescence schedule of
fish (Appendix S2).
Table 1. Estimated stream residence time and pre-spawning mortality according to severity of gillnet injury and presence of Saprolegnia spp.
infection
Tagged
fish (n)
Pre-spawning mortality Stream residence time (days)
Threshold for successful
spawning (minimum:
3 days; range: 1–9 days)
Maximum likelihood
estimates
Individual mark–recapture
histories
All fish
Fish observed
in stream All fish
Fish observed
in stream
Gillnet injury
Uninjured 100 6% (2–25%) 10Æ78 11Æ01 14Æ4±8Æ314Æ7±8Æ1
Gillnet injured 100 51% (42–71%) 4Æ54 7Æ82 6Æ1±7Æ810Æ5±7Æ6
Minor 50 16% (8–44%) 8Æ14 8Æ85 10Æ9±8Æ011Æ9±7Æ6
Moderate 30 80% (67–93%) 1Æ37 4Æ11 1Æ7±3Æ75Æ2±4Æ8
Severe 20 95% (90–100%) – – 0Æ4±1Æ40Æ4±1Æ4
Fungal infection (Saprolegnia spp.)
No infection 157 11% (4–35%) 9Æ84 10Æ30 12Æ8±8Æ413Æ4±8Æ1
Fungal infection 43 93% (86–95%) 0Æ53 3Æ83 0Æ7±2Æ55Æ2±5Æ1
Stream residence was calculated for each category of gillnet injury through maximum likelihood estimation methods as a function of sur-
vival probabilities between 2-day sampling periods. Stream residence was also estimated on the basis of individual mark–recapture histo-
ries (±SD). Pre-spawning mortality was assumed in fish that failed to demonstrate in-stream survival over a minimum of two sampling
periods (3 days). Sensitivity to this threshold stream residence is shown as a range of estimated pre-spawning mortality given threshold
values of 1–9 days.
Fig. 2. Fish with Petersen disc tag (photograph: Michael Webster).
Unaccounted mortality in salmon fisheries 755
2009 The Authors. Journal compilation 2009 British Ecological Society, Journal of Applied Ecology,46,752–761
Results
INCIDENCE AND SEVERITY OF GILLNET INJURY
Fishery-related injuries due to gillnet entanglement were evi-
dent in 11% of fish sampled at Pick Creek in 2005. Subsequent
sampling in 2006 and 2007 recorded gillnet injury rates of 29%
and 18% respectively. Fungal infection was strongly associ-
ated with the severity of gillnet injury. No infection was
observed in uninjured fish in 2005. Nearly half (43%) of gill-
net-injured fish were infected, with rates of 6%, 76% and
100% for fish with minor, moderate and severe injuries respec-
tively. Similar patterns were noted in 2006 and 2007.
In multi-year sampling at 10 streams, the incidence of gillnet
injury ranged between 4–37% (mean = 18 ± 13Æ1%) in 2006
and 7–29% (mean = 14 ± 6Æ5%) in 2007 (Fig. 3). Among
injured fish, both sexes exhibited 68% minor injury, 23% mod-
erate injury and 9% severe injury in 2006 and 80% minor
injury, 18% moderate injury and 2% severe injury in 2007.
Fungal infection was associated with severity of gillnet injury
(2 ·3 contingency tables: 2006: v
22
=748Æ20, P<0Æ001;
2007: v
22
=91Æ90, P<0Æ001). Infection rates for fish with
minor, moderate and severe injuries were 9%, 41% and 77%
(2006) and 5%, 33% and 62% (2007) respectively. Although
excluded from our mark–recapture analyses, 2% of sockeye
salmon sampled across 10 streams in both 2006 and 2007 also
exhibited damage from boat propellers.
STREAM ENTRY AND IN-STREAM OBSERVATIONS
Fish must enter and maintain residence in the stream to suc-
cessfully spawn. We tested the independence of severity of
injury and whether or not fish entered the stream and found
significant differences between groups (v
23
=117Æ79,
P<0Æ001). Virtually all (98%) uninjured fish and most (92%)
fish with minor injuries entered the stream in contrast to 33%
of fish with moderate injuries and 10% of fish with severe inju-
ries. The presence of fungal infection was also a strong indica-
tor of whether fish entered the stream (v
21
=130Æ94,
P<0Æ001). Nearly all (96%) fish without fungal infection
were observed in-stream in contrast to a minority (14%) with
infection. Whether or not a fish was observed in-stream was
independent of sex in the control group (v
21
=2Æ04,
P=0Æ153).
Differences were also noted in the date of stream entry. Most
control fish entered the stream 4 days after tagging. Fish with
minor injuries held off the mouth more than twice as long.
Both the mean (t
2,59
=4Æ21, P<0Æ001) and variance
(F
2,97,45
=0Æ327, P<0Æ001) in stream entry date were distin-
guishable from control fish. There was no detectable difference
(t
2,90
=0Æ60, P=0Æ549) in mean stream entry date between
control males (mean days to stream entry = 4Æ4±4Æ8) and
control females (3Æ8±3Æ9). Similarly, no detectable difference
was found (t
2,43
=0Æ22, P=0Æ829) between males with
minor injury (mean days to stream entry = 9Æ4±7Æ8) and
females with minor injury (9Æ0±7Æ6). Few fish with moder-
ate-to-severe injury entered the stream, which prevented accu-
rate estimates.
SURVIVAL AND STREAM RESIDENCE TIME
Survival and detection probabilities
Using the maximum likelihood estimates of survival between
sampling occasions, we calculated cumulative in-stream sur-
vival across sampling intervals as a function of entry date
(Fig. 4). In-stream survival declined precipitously for fish with
moderate to severe gillnet injury. Trends were even more pro-
nounced for comparisons of fish with and without fungal infec-
tion. On any given sampling occasion, the probability of
detecting a control fish known to have entered the stream was
estimated at 0Æ718, taken as an average of MLE estimates over
20 sampling events. No differences were noted between males
(0Æ700) and females (0Æ698). To enable estimation of detection
probabilities independent of survival we also employed the
Manly & Parr (1968) approach and recorded a detection prob-
ability of 0Æ702.
Stream residence by entry date
Maximum likelihood estimates of stream residence time ð^
TÞ
were calculated as a function of survival probabilities between
2-day sampling periods. Gillnet injury had a direct bearing on
stream residence time. We assumed fish that were never
observed in the stream, never entered the stream. Among fish
that entered the stream, uninjured fish had a mean stream resi-
dence of 11Æ01 (95% CI = 9Æ44–12Æ58) days in contrast to 8Æ85
(95% CI = 5Æ85–11Æ84) days for fish with minor injury and
4Æ11 (95% CI = 2Æ28–5Æ95) days for fish with moderate injury.
Too few fish with severe injury entered the stream to estimate
stream residence. Stream residence was also estimated as a
2005 2006 2007
Percentage gillnet injury at natal streams
0
10
20
30
40
Fig. 3. Incidence of gillnet injury averaged across 10 streams in the
Wood River system (2005–2007). Only one site was sampled in 2005
(Pick Creek).
756 M. R. Baker & D. E. Schindler
2009 The Authors. Journal compilation 2009 British Ecological Society, Journal of Applied Ecology,46,752–761
function of all fish in each category (regardless of whether fish
entered the stream) by integrating maximum likelihood esti-
mates of stream residence for fish observed in the stream with
estimates of zero for those never observed.
Longevity and stream residence by calendar date
Due to standardization by stream entry date, our maximum
likelihood estimates do not provide estimates of survival for
individual fish in real time nor allow us to characterize the
number of fish in-stream at any given time. To analyse differ-
ences by calendar date, we estimated longevity for individual
fish on the basis of the last observation for that individual. We
estimated stream residence as the difference between the first
and last in-stream observations. These methods confirmed the
results achieved through maximum likelihood methods
(Table 1).
Longevity (survival in days post-tagging) was greatly
reduced (t
2,146
=15Æ03, P<0Æ001) among moderately and
severely injured fish relative to controlfish.Interestingly,fish
with minor injuries lived somewhat longer than the uninjured
fish (t
2,78
=1Æ36, P=0Æ179; Fig. 5a), but exhibited reduced
stream residence (t
2,94
=2Æ02, P=0Æ046), due to later stream
entry (Fig. 5c). Pair-wise comparisons of stream residence
between categories of gillnet injury confirmed significant
differences between all groups (P<0Æ050) except between
those with moderate and severe injuries (anova,post hoc
Tukey HSD: P=0Æ912). Distinct patterns in longevity
were also noted as a function of fungal infection. Fish
without fungal infections lived more than 15 times longer
(t
2,173
=16Æ95, P<0Æ001; Fig. 5b) and, among fish observed
in-stream, spent more than twice as long in-stream (t
2,6
=3Æ80,
P=0Æ005; Fig. 5d). The longevity of control females
(mean = 19Æ6±7Æ7, n= 50) was significantly longer
(t
2,94
=2Æ50, P=0Æ014) than control males (mean =
15Æ3±9Æ2, n= 49) and among those that entered the stream,
females demonstrated longer stream residence (t
2,95
=2Æ65,
P=0Æ009). Overall, however, males and females displayed
similar patterns of decline in stream residence as a function of
severity of gillnet injury (Fig. 6).
PRE-SPAWNING MORTALITY
The average stream residence for Pick Creek fish not killed
through predation is 10–25 days (Hendry et al. 1999). We
adopted a conservative estimate of pre-spawning mortality,
assumingfishthatfailedtodemonstratein-streamsurvivalfor
a minimum of 3 days failed to spawn. Using maximum likeli-
hood estimates, pre-spawning mortality was calculated as a
function of fish known alive at the second sampling occasion
(v
1
). According to our model, stream entry is considered the
release date for each individual. Subsequent in-stream observa-
tions are in reference to this standardized release. Thus the per-
centage known alive at the second sampling occasion (v
1
),
includes all fish that survive a minimum of two sampling inter-
vals (3 days) from stream entry. Given this criteria, the major-
ity (51%) of fish with gillnet injuries were predicted to fail to
spawn in contrast to 6% of control fish. Nearly all fish (93%)
with fungal infection at the time of tagging failed to spawn
(Table 1).
To account for predation effects, we surveyed all carcasses
to determine the cause ofdeath.BrownbearsUrsus arctos are
a major source of in-stream predation and pre-spawning mor-
tality on sockeye salmon in south-west Alaska (Shuman 1950;
Gard 1971) and are known to preferentially select fish in better
condition in environments that facilitate foraging (Gende,
Quinn & Willson 2001). We noted higher predation on control
fish. Among fish with known fates (n= 76), bear predation
was observed for 31% of uninjured males (n= 17) in contrast
to 17% of gillnet-injured males (n= 7) and in 11% of unin-
jured females (n= 39) in contrast to 8% of gillnet-injured
females (n= 13). While a significant portion of pre-spawning
Fig. 4. Plots of in-stream survival according to severity of injury and presence of fungal infection. These estimates standardize by stream entry
date, such that the plots illustrate total in-stream survival regardless of the timing of stream entry. The first interval reflects the number of fish
tagged and released. The second interval is the percentage estimated to have entered the stream according to in-stream observations. Subsequent
intervals (S1–S18) are calculated as the product of the number alive at the previous period and our MLE estimate for survival between the previ-
ous and the current period (95% confidence intervals are contained within error bars). Fish not observed in the stream were presumed dead.
Unaccounted mortality in salmon fisheries 757
2009 The Authors. Journal compilation 2009 British Ecological Society, Journal of Applied Ecology,46,752–761
mortality in our control group may be attributable to bear pre-
dation, it is unlikely that predation alone accounts for the high
rates of pre-spawning mortality in fish injured through non-
retention in gillnets.
MODEL PERFORMANCE AND ASSUMPTIONS
To analyse model performance, we utilized the release–recap-
ture software SURPH 2Æ1 (Survival Under Proportional Haz-
ards. 2002). To determine whether survival and detection are
the same across treatment groups, we applied TEST 1 devel-
oped by Burnham et al. (1987) and confirmed that survival
parameters differ between fish with and without evident gillnet
injury (v
239
=117Æ73, P=0Æ000). To determine whether sex
impacts survival or detection, we compared males and females
within the control group and found no significant differences
(v
239
=34Æ23, P=0Æ687). Because our analysis standardized
survival estimates according to stream entry date, we tested
whether detection probabilities hold constant across sampling
occasions to ensure different conditions at different sampling
occasions would not bias this approach. Specifically we analy-
sed mark–recapture data by calendar date and compared the
relative performance of: (i) a model assuming unique detection
parameters for each sampling period and (ii) a model assuming
a common detection parameter across sampling periods. On
the basis of the Akaike Information Criterion (Akaike 1973),
wefoundthemodelwithcommondetectionparameterspro-
vided the best fit to the data (Table 2).
Discussion
IMPLICATIONS FOR NON-RETENTION AND DELAYED
MORTALITY IN EXPLOITED STOCKS
Our results suggest that disentanglement from gillnets is a reg-
ular occurrence in commercial fisheries in Bristol Bay, Alaska.
As a consequence, fishery-related injuries are common in
spawning stocks of sockeye salmon. Mark–recapture results
f
Fig. 5. (a–d) Longevity (post-tagging sur-
vival) and stream residence time according to
severity of injury and presence of fungal infe-
ction. These estimates illustrate survival and
stream residence by calendar date. Longevity
estimates include fish known alive at any
given sampling occasion. Stream residence
estimates include fish known alive and
known to have entered the stream.
Fig. 6. Box plots of stream residence time according to sex and sever-
ity of gillnet injury.
758 M. R. Baker & D. E. Schindler
2009 The Authors. Journal compilation 2009 British Ecological Society, Journal of Applied Ecology,46,752–761
demonstrate that survival on the spawning grounds is mark-
edly reduced among gillnet-injured fish and inversely corre-
lated with the severity of injury. Conservative estimates
suggest that more than half of the fish that reach natal spawn-
ing grounds after contracting injuries in the fishery fail to
reproduce. The incidence and severity of gillnet injury also
appear to vary between years, probably as a function of fishing
intensity and run size. Due to constant escapement targets, lar-
ger runs will experience higher rates of exploitation. During
smaller runs managers implement more closures, which inad-
vertently improves the relative condition of the escaped stocks.
Differences in the size of returning fish may also influence
retention, given a relatively constant range of mesh sizes used
in the fishery. For these reasons, distinguishing between total
escapement (all fish that migrate past escapement towers) and
effective escapement (fish that survive the migration and
spawn) should be considered.
There are also broader ecological implications to decreased
spawning activity in coastal watersheds. Recent attention has
focused on the consequences to habitat and community struc-
ture related to the overexploitation of ecosystem engineers by
commercial fisheries (Coleman & Williams 2002). Habitat
modification by spawning salmon alters community organiza-
tion in stream ecosystems and strongly influences the down-
stream flux of nutrients and resource subsidies (Moore,
Schindler & Scheuerell 2004). Non-retention mortality in
spawning stocks will reduce these effects relative to expecta-
tions based on escapement counts.
POTENTIAL FOR UNDERESTIMATING INCIDENCE OF
GILLNET INJURY
Our estimates of the incidence of gillnet injury are almost cer-
tainly lower than actual rates of non-retention in escaped
stocks of spawning salmon. To assess fish from discrete popu-
lations and minimize the inclusion of strays or migrants, our
sampling was conducted at natal streams immediately prior to
stream entry, roughly 2 weeks after stocks had migrated
through the fishery and were enumerated at escapement count-
ing towers. During this period, many injured fish probably do
not survive the challenges associated with migration, osmoreg-
ulation, sexual maturation and maintenance metabolism.
Experimental studies of maturing sockeye salmon disentangled
from gillnets found that 80% died within 1 week (Thompson
et al. 1971; Thompson & Hunter 1973). Our estimates of the
incidence of non-retention fail to account for fish that survive
long enough to migrate past escapement towers but perish
before our sampling occurs at natal streams. It is therefore rea-
sonable to assume our estimate of 11–29% gillnet injury is con-
servative. Actual rates of injury in escaped stocks may be
considerably higher (for further research, see Appendix S3).
PRE-SPAWNING MORTALITY AND PROXIMATE
MECHANISMS
It is clear that virtually all fish with moderate to severe gillnet
injury fail to spawn. In the case of fish with minor injuries, the
delay in stream entry, abbreviated stream residence and the
inhibition of morphological traits associated with sexual matu-
ration (Fig. 1) suggest that even minor injuries retard matura-
tion and reduce reproductive fitness. This delay in maturity
may explain why fish with minor injuries live longer than unin-
jured fish despite reduced stream residence. Pre-spawning mor-
tality was highly correlated with and was likely facilitated by
fungal infection, caused by Saprolegnia spp., a facultative para-
site common in freshwater ecosystems. Saprolegnia spp.causes
tissue damage, loss of epithelial integrity and osmoregulatory
failure (Bruno & Wood 1999). It is associated with damaged
epidermal tissue (Hatai & Hoshiai 1994; Pickering 1994), sug-
gesting fish with gillnet injuries are particularly susceptible to
such infections. Fish with severe infections generally fail to
recover (Pickering & Willoughby 1982). Of 43 fish with fungal
infection at the time of our tagging, only one successfully
spawned. Many injured fish without Saprolegnia spp. at tag-
ging presumably developed infections subsequently. Due to
the close correlation between fungal infection and pre-spawn-
ing mortality, Saprolegnia spp. is likely to be the proximate
cause of pre-spawning mortality in gillnet injured fish.
BROADER APPLICATION OF NON-RETENTION
MORTALITY AND SUSTAINABLE FISHERIES
MANAGEMENT
Commercial gillnet fisheries harvest Pacific salmon on their
return migration and are managed to ensure sufficient numbers
of adults spawn and perpetuate discrete stocks. Complicating
management, many salmon enumerated in escapement counts
suffer injuries in the fishery and fail to spawn. Estimates of
spawning potential based on such escapement counts fail to
consider this loss. Our study indicates that gillnet injury affects
a minimum of 11–29% of escaped fish. Roughly half of the
injured fish fail to spawn. Even minor injuries may lead to
adverse consequences, such as delayed maturation. The
number of viable spawners in escapement counts may be over-
estimated by 5–15%, with repercussions for stock-recruitment
analyses (Fig. 7). Currently, non-retention and delayed mortal-
ity are neither measured nor explicitly incorporated into
stock assessment. The magnitude and inter-annual variation of
non-retention in spawning stocks suggest that this source of
Table 2. SURPH model comparison for unique vs. common
detection parameters appliedacross sampling occasions
Model
No.
parameters
Ln
likelihood AIC
Unique detection parameters
for each sampling occasion
39 )852Æ618 1783Æ24
Common detection parameters
for every sampling occasion
21 )786Æ366 1614Æ73
This analysis confirms our assumption that in-stream detection
remained constant throughout the sampling period. It suggests
that standardizing individual capture histories by stream entry
date (rather than calendar date) did not bias survival estimates.
AIC, Akaike Information Criterion.
Unaccounted mortality in salmon fisheries 759
2009 The Authors. Journal compilation 2009 British Ecological Society, Journal of Applied Ecology,46,752–761
mortality is not adequately considered under current manage-
ment assumptions. This additional unaccounted source of
fishing mortality has not prevented sustainability in the Bristol
Bay fishery due to a precautionary approach to management.
It does, however, suggest that the productivity of these stocks
has been systematically underestimated and indicates a means
to improve efficiency if retention can be increased or mortality
due to non-retention reduced. Management agencies across a
wide range of commercial fisheries should carefully consider
the potential for non-retention mortality in target stocks
and instances where such mortality can be estimated and ⁄or
minimized.
Acknowledgements
We gratefully acknowledge J. Skalski, J. Lady and R. Hilborn for technical
advice and guidance, G. Holtgrieve, T. Reed and T. Branch for review of the
manuscript, managers and biologists at the Alaska Department of Fish and
Game for data, permitting and consultation, and friends and colleagues in the
University of Washington, Alaska Salmon Program for assistance in the field.
Support and funding for this research was provided by the Gordon and Betty
Moore Foundation, the National Science Foundation, the Environmental
Protection Agency STAR fellowship programme, the H. Mason Keeler
Endowment for Excellence, the John G. Peterson Scholarship, the Galen and
Helen MaxfieldFisheries Scholarship, and Alaska salmon processors.
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Handling Editor:Nick Dulvy
Supporting Information
Additional supporting information may be found in the online ver-
sion of this article.
Appendix S1. Map of the Nushagak fishing district and Wood River
system, Bristol Bay, Alaska
Appendix S2. Influence of spawning date on the senescence schedule
of salmon
Appendix S3. Our results in the context of past research
Please note: Wiley-Blackwell are not responsible for the content or
functionality of any supporting materials supplied by the authors.
Any queries (other than missing material) should be directed to the
corresponding author for the article.
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