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Fisheries Research 219 (2019) 105314

Contents lists available at ScienceDirect

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

The state of Canada’s iconic Northern cod: A second opinion T



George A. Rose , Carl J. Walters
Institute for the Oceans and Fisheries, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada

A R T I C LE I N FO A B S T R A C T

Handled by A.E. Punt Canada’s Northern cod stock (NAFO Divisions 2J3KL), once one of the world’s most important stocks, declined
Keywords: rapidly in the early 1990s and remains at historically low biomass despite a recent comeback. In contrast to
Northern cod many studies, recent stock assessments based on a new state-space model (hereafter Canada Department of
Stock assessment Fisheries and Oceans, or NCAM model) concluded that natural (M) and not fishing mortality (F) was the main
VPA cause of stock depletion and has kept it at low levels since. Here we offer a second opinion on those conclusions,
M and F mortality using the same catch and survey data, but based on a VPA model that allows for variability in M and unreported
Recruitment overfishing catch. This model posits that the biomass, both total and spawning from the NCAM model, is overestimated
(35%), that fishing mortality was a major contributor to the early 1990s decline and slow rebuilding, and that
the decline began in the late 1980s and was not as knife-edged as suggested by the NCAM. In agreement with the
NCAM results, M has been variable and episodically elevated, but much less than suggested by the NCAM. VPA
using a non-variable M did not fit well. In addition, the stock recruitment relationship suggests an asymptote at
near 106 t, similar but slightly higher than the current limit reference point for spawning biomass. Of im-
portance, the present analyses suggest that fishing has impacted rebuilding and will slow achievement of a
spawning biomass that avoids recruitment overfishing.

1. Introduction 2014; Mullowney et al., 2019).


Following the decline in the early 1990s and until the mid-2000s,
Canada’s Northern cod stock (NAFO Divisions 2J3 K L, Fig. 1) was the formerly dominant offshore components of the Northern cod stock
once one of the world’s largest and most important fish stocks (Rose, complex (Templeman, 1966) or metapopulation (Smedbol and
2007). After being fished commercially and for the most part sustain- Wroblewski, 2002), showed only limited stock growth and highly
ably since the late 1400s, the stock suffered a massive decline as a result contracted size and age distributions (DFO, 2016). The sole exception
of rampant over-fishing by foreign fleets in the 1960s. After a slight was a robust overwintering and spawning group located in the coastal
reprieve in the late 1970s and early 1980s with imposition of an Ex- fjord of Smith Sound (Rose, 2003; Rose et al., 2011). The dispersal of
clusive Economic Zone in 1977, the stock declined again to un- the Smith Sound cod from 2006 to 2009 very likely contributed to the
precedented low biomass in the early 1990s. The cause of the decline in increase in numbers and age distribution in the adjacent Bonavista
the 1960s has been universally attributed to over-fishing during a Corridor where offshore rebuilding was first apparent (Mello and Rose,
period of strong productivity, but the causes of the later decline have 2009; Rose et al., 2011; Cadigan, 2016; Rose and Rowe, 2018; Neville
been more controversial. Initial evidence of spatial and productivity et al., 2018). From 2007–2015, the offshore groups were estimated to
declines in a cooling environment (deYoung and Rose, 1993d) were have grown at an average rate of about 30% per year with redistribu-
countered by arguments that over-fishing was the sole factor re- tions occurring to the northern ranges off Labrador in keeping with
sponsible for the decline (e.g., Hutchings and Myers, 1994). More re- historic stock distribution (Rose and Rowe, 2015, 2018; DFO, 2016,
cently, most all studies have concluded that declining productivity 2018).
(growth and recruitment), and perhaps increases in natural mortality The underlying drivers of the population dynamics of the Northern
from starvation or predation, exacerbated the over-fishing that no cod remain controversial, not just with respect to the stock collapse in
doubt elevated removals well above productivity and led to inevitable the early 1990s, but since then. The prolonged slow recovery has been
decline (Rice, 2006; Shelton et al., 2006; Rose, 2007; Rothschild, 2007; attributed to several factors, including continued fishing (Shelton et al.,
Lilly, 2008; Hilborn and Litzinger, 2009; Etchegary, 2013; Buren et al., 2006), the decline in availability of the stock’s main food source,


Corresponding author.
E-mail address: g.rose@oceans.ubc.ca (G.A. Rose).

https://doi.org/10.1016/j.fishres.2019.105314
Received 26 April 2019; Received in revised form 12 June 2019; Accepted 17 June 2019
0165-7836/ © 2019 Elsevier B.V. All rights reserved.
G.A. Rose and C.J. Walters Fisheries Research 219 (2019) 105314

Fig. 1. Map of the range of the Northern cod (NAFO Divisions 2J3KL) off Newfoundland and Labrador.

capelin (Mallotus villosus) (Rose and O’Driscoll, 2002; Buren et al., and its productivity, the roles of the fishery and natural mortality in
2014), increased predation rates from harp seals (Lilly, 2008), genetic regulating stock dynamics, and the future of the stock under differing
or life history changes (Hutchings, 1999; Olsen et al., 2004), depensa- management strategies.
tion (Shelton and Healey, 1999) and potential combinations of these
factors. Most recently, however, stock assessments conducted by the 2. Methods
Canadian Department of Fisheries and Oceans (DFO) have suggested
that natural mortality alone has been the major driver of the population 2.1. VPA model for Northern cod
dynamics, including the collapse of the stock in the early 1990s, with
fishing relatively unimportant (DFO, 2016, 2017, 2018). The inference In a stock synthesis approach for reconstructing population age
that fishing has had little impact on stock growth has likely influenced structure given seasonal harvesting (as for the Northern cod after
recent management measures to allow increased removals despite the 1989), we would predict numbers at age forward in time using
stock being well below the most recently determined precautionary
lower limit for spawning stock biomass (ca. 800,000 t). The conclusion Na+1,t+1=(Na,t-Ca,t)e−Mt, (1)
that fishing played only a minor role in the collapse of the Northern cod
for ages a = 1,…,A and years t = 1,…,T, where N is numbers at age, C
and its stock dynamics since then was inconsistent with most published is predicted catch (from annual fishing rate Ft and age vulnerability
studies (summarized in Rose et al., 2019), even those strongly ad-
va,t), and Mt is the time-varying natural mortality rate. This structure is
vocating environmental influences. likely more realistic than the Baranov (continuous fishing and natural
In this paper, we offer a second opinion on the state of the Northern mortality) equation used in DFO assessments, at least for 1990 and
cod and its stock dynamics since the early 1980s. Our objective is to later, when fishing has been highly seasonal.
provide a constructive second opinion on the state of this highly im- If we insist (through estimation of fishing rates Ft and vulnerabilities
portant stock to Canada, and in particular to Newfoundland and at age and time va,t) that the synthesis model closely predicts observed
Labrador. Our view is based on the same data used by the DFO in their catches at age, then we can replace Eq. (1) with the backward time or
formal assessments (DFO, 2016, 2017, 2018; Brattey et al., 2018), but VPA recursion
using a more traditional VPA model, in contrast to the space-state
model (NCAM) used by DFO (Cadigan, 2016; Brattey et al., 2018). We Na,t=Na+1,t+1eMt+Ca,t (2)
intend to provide an alternative view of the state of the Northern cod
using observed rather than predicted catches at age. This formulation

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G.A. Rose and C.J. Walters Fisheries Research 219 (2019) 105314

avoids having to estimate most of the time-varying Ft and va,t para- with alternative assumptions about how variable M may have been. We
meters, and also avoids having to estimate initial age structure (Na,1) do not pretend that σ2m is estimable from the data.
and recruitments over time (N1,t) as unknown parameters. But we must Potentially estimable parameters for the model structure and data as
provide estimates instead of the terminal numbers at age in the last described above include the “leading” set {U*T,m1983…m2016, σ2m, v2…
year, Na,T, and numbers in the last age, NA,t for t < T. To provide these v4, and Mo}. Additionally, we obtain analytical estimates of the survey
estimates, we use a modification of the VPA approach of Walters and catchabilities qB for biomass and qa for cpue at age “for free”, along
Punt (1994). In that approach, NA,t for t < T is estimated as with observation variance estimates σ2B, σ2a for the survey data, by
evaluating these at their conditional maximum likelihood values given
NA,t = CA,t/U*t, (3)
the other parameters, as recommended in Walters and Ludwig (1994).
where U*t is the sum over fully vulnerable ages less than A (7–13 in the The VPA reconstruction is of course highly sensitive to the assumed
Northern cod case) of catches at age divided by the sum over ages of base natural mortality rate Mo and the annual mt multipliers, which are
numbers at age < A from Eq. (2). To begin this backward calculation, only estimable for 1983 and later (for which mortality rate changes
we need to provide estimates of the numbers at age for all (including A) might be “visible” in the survey cpue at age). For most estimation tests,
fully vulnerable ages in the last year, and we do this using Eq. (3) by instead of trying to estimate Mo we set it to the average 0.26 of M
treating the fully vulnerable exploitation rate U*T for the last year as an estimates for Gadus morhua from Fishbase. Higher estimates (around
unknown parameter to be estimated by fitting to time series survey 0.37) were obtained when we included Mo in the estimation parameter
data. To provide initial numbers at age in the last year for fish not fully set, but such higher values are not consistent with the overall mortality
vulnerable (a < 7), we use the survey catch per unit effort (cpue) ca,t for rate (Z) apparent from catch at age data prior to 1983. When we al-
year T and “lock” the Na,T to exactly predict those survey cpue’s, that is lowed the survey q2…q4 to vary, we obtained higher values for q2 and
we estimate Na,T for a < 7 as q3 than estimated by DFO, most likely because the VPA estimates for
N2,t and N3,t are likely biased downward because of failing to account
Na,T=[ca,t/(q*va)]et*MT+Ca,t, (4) for likely higher M of younger fish.
where va is survey vulnerability of age a fish, t* is time from start of the For some estimation trials, Eq. (2) was modified by multiplying the
fishery to the survey time, and q* is the sum of cpue’s ca,T over fully catches Ca,t by annual multipliers for most years based on estimates
vulnerable ages divided by the sum of Na,T for those fully vulnerable used by NCAM (1.1–1.5 for 1983–1990; 1.1–1.6 for 1995–2016 which
ages where Na,T=Ca,T/U*T. Eq. (4) is basically a way to avoid the would include unreported recreational catches; Brattey et al., 2018).
problem of estimating fishery vulnerabilities for younger fish in the last For the years 1991–1994 we used the same bottom limit but raised the
year. upper limit to 10 to allow an accounting for possible unprecedented
There are two minor wrinkles for the Northern cod data, namely the increases in unreported catch in those years when NCAM suggested that
earlier data contain estimates of catch for a “plus group” of age 15 and natural mortality was extremely high. At the suggestion of Jeff
older fish, and catches were spread over the year before 1990. To avoid Hutchings, we also let ages 2–4 take different values than older fish (for
unnecessarily complicating the VPA equations for age 14 and 15+, we the years 1991–1994) in an additional model run. In that run, the catch
estimate abundance of these older fish for earlier years (mainly before multipliers were higher for ages 2–4 than for older fish in 3 of 4 years,
1980) as simply N15+,t=C15+,t/U*t using the fully vulnerable U*t as in which suggests discarding of smaller fish. Nonetheless, the overall re-
Eq. (3), while assuming A = 14 in Eq. (3). To account for year-round sults were very similar to those using an age independent multiplier,
fishing before 1990, we used Pope’s approximation to the backward hence the results are not shown. The ct were included in the estimation
solution of the Baranov equation, i.e. multiplied Ca,t in Eq. (2) by eMt/2, as unknown parameters. This approach essentially assumes that any
for years before 1990; this caused modest increases in estimated unreported catches had the same age composition proportions as esti-
abundances for earlier years. mated for the reported catch. Total unreported catches could then be
If the survey vulnerability estimates va in Eq. (4) are assumed estimated and compared with possible sources of such catches. Of
known from other assessment approaches, the VPA stock reconstruction particular interest was the potential impact of the Spanish hake fleet
problem then reduces to estimation of only the terminal U*T and the that was expelled from Namibian waters in 1990 when Namibia
time-varying natural mortality rates Mt. For this estimation, we mini- achieved independence. This fleet arrived on the Grand Banks begin-
mize a negative log likelihood function with three components: ning in the late 1980s (Emery, 1996; Comeau and Cook, 2003), which
coincided with the onset of a massive decline in the stock. Data on the
(1) Log-normal deviations of predicted from annual relative survey capacities of that fleet and potential catches were obtained from the
biomass estimates (estimated as a sum over ages of survey cpue’s FAO databases and reports from Namibia, in addition to reported cat-
times observed mean body weights), divided by a single assumed ches to FAO, the Northwest Atlantic Fisheries Organization (NAFO) and
survey catchability q, using predicted survey biomass equal to the DFO surveillance. In addition, the catches in the since the mid-1990s
sum over ages of vulnerabilities va times predicted biomasses at age might also have been under-reported, as the recreational fishery was
at the time of the survey calculated as the sum over ages of ob- not accounted for in catch records in most years and the commercial
served mean weights at age times numbers at age (Na,t-Ca,t)e−Mtt*, stewardship fishery was another potential source of some unreported
i.e. numbers at age corrected for fishing and natural mortality be- catch (Brattey et al., 2018).
tween start of the fishing season and the survey time t*.
(2) Log-normal deviations of age-specific cpue’s from predicted values, 3. Results
with the predicted values being a catchability coefficient times
vulnerabilities va times (Na,t-Ca,t)e−Mtt*. 3.1. VPA
(3) A quadratic prior term for deviation of Mt from some base value Mo,
i.e. for log-normal variation in mt. An excellent fit to the VPA model was obtained when natural
mortality rates and/or unreported catches were assumed to have varied
The Mt are parameterized as Mt=Momt, where mt is an annual M over time (Fig. 2A). When M was assumed to be constant, the fit was
multiplier (constrained to be greater than 0.5). Assuming lognormal very poor, being inconsistent with the survey data for the late 1980s
variation in mt, the quadratic penalty term is then just 0.5 times the and early 1990s. The VPA biomass estimates were about 35% lower
sum over time of ln(mt)2.σ−2 2 than DFO’s NCAM estimates (DFO, 2018), mainly as a result of higher
m plus n/2 ln(σm), where alternative choices
of σm (the “variance” of mt treated as a random effect) allow estimation
2 estimates of fishing mortality (F) in the VPAs (Fig. 2B) and lower es-
timates of natural mortality (M) for most years (Fig. 2C). Likelihood

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G.A. Rose and C.J. Walters Fisheries Research 219 (2019) 105314

Fig. 2. Estimates of historical changes in stock biomass and mortality rates from the VPA models, with comparisons to the Brattey et al. (2018) state-space model
NCAM. a) trends in biomass; b) trends in fishing mortality rate; c) trends in natural mortality rate M.

profiles for Mo (Fig. 3A) show the best base estimate (0.31) to be close and in DFO assessment reports (DFO, 2016, 2018). The present analyses
to the average of 0.26 for Gadus morhua reported in Fishbase. The VPA suggest that recovery began earlier from a very low spawning biomass,
fit to survey catch at age was reasonably good for ages 2–10 (Fig. 4). with starts and stops, probably because the Smith Sound fish, which
When a variable for unreported catches was included in the esti- near tripled in biomass from 1995 to the early 2000s, were considered
mation, the VPA abundance pattern was indistinguishable from that to be part of the stock (as in Cadigan (2016) and Brattey et al. (2018)).
shown in Fig. 2A, but the estimated M’s for that period decreased The resultant biomass estimates indicate a general pattern of log-linear
dramatically (Fig. 2C). The best fit to the survey data estimated un- (exponential) population recovery beginning in 1995, punctuated by
reported catches from 1991 to 1994 to average 73,000 t per year, two short periods (2001-3 and 2009-11) of declining abundance with
peaking at about 150,000 t in 1992 (Fig. 5). possibly a third period beginning in 2016-2017. High natural mortality
The VPA estimates of the terminal exploitation rate (U2017) were rates Mt > 0.4 are estimated for these periods by both the VPA and
about 0.18 for the variable-M model and 0.14 for the model with un- NCAM models. But averaging over these periods, the stock has appar-
reported catch, but these estimates are quite uncertain as indicated by ently been increasing at an average rate (population “r”) of around 17%
likelihood profiles (Fig. 3B). Nonetheless, the estimates are much per year, despite continued fairly high fishing mortality rates. Direct
higher than obtained with the NCAM model (Brattey et al., 2018). calculations of the population r value corrected for catch removal (as ln
A key point to note in Fig. 2A is that the survey data do not indicate [(Bt+1+Ct+1)/Bt]) from the survey data indicate that r averaged
a substantial delay after 1994 before recovery began, followed by rapid around 0.37 during the periods between the high Mt “events”. These
recovery as suggested by the arithmetic scale biomass plots in Rose and spurts in r are somewhat higher than the average long-term intrinsic
Rowe (2015), which pertain only to the offshore portion of the stock, growth rate of 0.28 for the population estimated by Rose (2004).

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G.A. Rose and C.J. Walters Fisheries Research 219 (2019) 105314

3.4. Recovery scenarios

The stock-recruitment relationship in Fig. 7 was used in an age-


structured model to predict future biomass recovery and to examine
how recovery might have proceeded after 1994 if there had been no
fishing (Fig. 8). Relatively slow recovery rates were predicted, with the
spawning stock not to exceed 106 mt until at least 2030 even with no
fishing and M remaining near Mo. Continued fishing at the VPA F2017
(0.16) is predicted to delay the recovery to healthy levels until at least
2040. The retrospective simulation of complete fishery closure after
1994, but including estimated Mt and recruitment anomalies over
1995–2017, indicated that the stock would have been substantially
higher by 2017 and could have reached 106 mt by about 2025.

4. Discussion

The present VPA-based analyses of the state of the Northern cod


stock since the early 1980s differ substantially from that of current DFO
assessments. Specifically, the present analyses suggest that stock bio-
mass growth has not been as great as reported in DFO (2018), such that
the rebuilding total biomass is estimated to have peaked in 2015 at
about 320,000 t and to have declined somewhat since (DFO, 2018 in-
dicates a total post-fishery biomass > 500,000 t in 2015). The present
estimate of end of year biomass is more closely aligned with in-
dependent acoustic-trawl surveys reporting a biomass of 310,000 t in
the major areas of distribution in the spring of 2015 prior to that year’s
fishery (Rose and Rowe, 2018). Moreover, the VPA biomass estimates
for the years 2012–2015, when the spring surveys were conducted,
correspond closely with the results of these surveys (Fig. 9).
Fig. 3. Likelihood profiles for the base natural mortality rate Mo (a) and VPA The differences between the present VPA-based and DFO’s NCAM-
terminal exploitation rate U2017 (b). Relative likelihoods are values of the based analyses are for the most part based on higher fishing mortality
maximum likelihood for the data (Appendix eq. A1) given a range of fixed Mo or rates (F) and lower natural mortality (M) from the VPA. Jeff Hutchings
U2017 values, scaled by the maximum likelihood when Mo or U2017 is included in his review of the present analyses pointed out that massive short-
in the fitting. term increases in M, as suggested by NCAM in the early 1990s, are
biologically unreasonable with no evident hypothesis put forth to ex-
Hutchings (1999) emphasized that stochasticity in r might increase as a plain how this might occur. The NCAM model used tagging data to
population declines and that deterministic estimates of r will be lower assist in the estimation of F and hence M. This suggests that the higher
than stochastic estimates. The present results are consistent with those biomass (and lower F) estimates from NCAM have come at least partly
expectations. from low recovery rates in the tagging data which results in lowering
estimates of F and inflating M and modeled biomass. NCAM apparently
assumes relatively low tag loss mortality rates and perhaps inflated
3.2. Survey catchability (q) reporting rates; for example, when the much lower initial tag survival
rate (27%) estimated by Brattey (2013) for acoustic tags is used for
Somewhat different patterns of apparent variation in survey catch- analysis of the conventional tag data therein, estimates of exploitation
ability (q) were evident from the survey biomass and cpue-at-age data rate similar to those from the VPA are obtained, i.e. nearly three times
(Fig. 6). The apparent survey qa for age data showed a low period over the exploitation rates reported in Brattey (2013).
1995–2005, possibly because the survey biomass estimates were cor- Despite the differences between NCAM (Brattey et al., 2018; DFO,
rected upward for that period by including the Smith Sound survey 2018) and present VPA results, there were notable consistencies. Both
estimates, but the survey cpue’s at age were not similarly corrected. suggest that the stock has grown considerably over the past decade and
Also evident in the relative catchability estimates are the high q for the that natural mortality (M) has been higher than average, somewhat
1986 survey, and also for the 2008 survey. sporadically, since the early 1990s. The present likelihood profiles for
Mo (0.31) were close to the average of 0.26 for Gadus morhua reported
in Fishbase. Nonetheless, variations in M were required to obtain a
3.3. Stock recruitment reasonable VPA model fit to the survey data. Under an assumption that
catches were accurate as reported, the patterns of variation in M from
Estimates of the stock-recruitment relationship from the VPA results VPA were similar to those from NCAM, but lower in the early 1990s and
(Fig. 7) show an essentially log-linear pattern, with the Beverton-Holt in most years since. Allowing the model to adjust the reported catches,
model fit indicating flattening of recruitment only at spawning stock however, resulted in much lower but still elevated estimates of M
sizes exceeding 106 mt. The Beverton-Holt slope parameter estimate during the early 1990s that continued in episodes to 2017. The possible
implies relatively weak recruitment compensation (Goodyear compen- causes of elevated M have been dealt with previously and most likely
sation ratio 9.24, steepness h = 0.7), and this estimate is not sensitive relate to poorer condition resulting from environmental changes that
to assumptions about mean historical M (higher M simply implies both have led to a decline in capelin which is a key food source of this stock
higher absolute recruitment and higher absolute spawning stock bio- (Rose and O’Driscoll, 2002; Buren et al., 2014, 2019), and possibly
mass). Such weak compensation, in combination with recent historical related increased predation. We stress that in keeping with much re-
vulnerabilities at age such that some immature fish are vulnerable to search on the dynamics of this stock showing that productivity (growth
harvest, implies low Fmsy in the range 0.15–0.2. and recruitment) declined in the late 1980s and early 1990s (e.g.,

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G.A. Rose and C.J. Walters Fisheries Research 219 (2019) 105314

Fig. 4. Comparison of observed and predicted survey catch per effort at age for the VPA model with variable M over time. Missing observations for ages 9–10 in the
1990s are for years when survey cpue was zero.

deYoung and Rose, 1993d; Hilborn and Litzinger, 2009), likely con- consequence of the increase in catch allowed in 2016-2017. An increase
tributing to rapid stock decline under what was unrelenting fishing in M in the most recent years is consistent with NCAM results, but the
pressure, the present results assign important mortality to fishing and to VPA results suggest a lower M than with NCAM, and that fishing has
unspecified (natural) causes. Both appear to be important in explaining been an important mortality factor that has limited stock growth. The
the rapid decline in the early 1990s and relatively slow rebuilding present results suggest that a restriction on fishing effort and catch
since. should enable stronger stock growth, with at least a cessation of the
That the terminal Fs indicated under assumptions of variable M and major stock decline reported in Brattey et al. (2018).
unreported catches were substantially higher than indicated with The sources of putative large unreported catches in the early 1990s
NCAM suggests that the survey decline in 2017 could at least partly be a cannot be confirmed. There are at least two likely sources. Firstly, there

Fig. 5. Unreported catch estimated with the VPA model by including annual catch multipliers on the catch at age data (see text for details; 3 term moving average).

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G.A. Rose and C.J. Walters Fisheries Research 219 (2019) 105314

Fig. 6. Apparent variation in survey catchability over time from VPA, in survey cpue at age (dark line) and for survey biomass (lighter line).

flag. FAO reports suggest that the Spanish fleet caught only about
15,000 t of cod in the entire Northwest Atlantic in 1991, with NAFO
recording only about 8300 t from NAFO Divisions 3L (Northern cod)
and 3M (Flemish Cap) combined. In contrast, Canadian surveillance
estimates used by DFO in stock assessments for Northern cod are about
50,000 t for 1991 and could have been as much as 94,000 t (Shelton and
Lilly, 2000), which is not inconsistent with the average VPA estimates
for these years. In addition, FAO and Namibian data indicate that the
Spanish fleet had more than sufficient capacity to be responsible for the
estimated unreported catches of the early 1990s. That fleet in the late
1980s, prior to being ejected from the Namibian hake fishery, caught up
to 185,000 t annually. In summary, there is evidence that the un-
reported catches indicated by the present model in the early 1990s were
at least plausible, and at best probable.
In addition to unreported catches of foreign fleets, discarding of
small fish by Canadian vessels may also have contributed to mortality in
Fig. 7. Stock recruitment estimates from the VPA model, with solid line
the early 1990s (Myers et al., 1997). The present analyses cannot par-
showing best fit to Beverton-Holt stock-recruitment model assuming log-normal
tition F into discards and catch, but it is likely that discards by this fleet
variation in recruitment around the model predictions.
contributed to the increased mortality in the early 1990s. In contrast,
unreported catches and discarding from the early 2000s to the present
is evidence that catches from the foreign fleets fishing on the northern in Canadian inshore fisheries are almost certainly small in comparison
Grand Banks in the early 1990s, both Northwest Atlantic Fisheries to those of the early 1990s, because of much lower fishing effort and
Organization (NAFO) members and non-NAFO and flag-of-convenience power. The present analyses suggest an average of about 2500 t per
vessels, were grossly under-reported (Emery, 1996; Shelton and Lilly, year was unreported from 2006 to 2016 which is not inconsistent with
2000; Rose, 2007). Moreover, there is little agreement in the various the range of proportions of unreported to reported catches indicated in
catch statistics from these fleets during these years, which is itself a red Brattey et al. (2018).

Fig. 8. Historical spawning stock biomass from VPA and rebuilding scenarios based on fishing mortality extended from 2017 (dark line), no fishing from 2018
onward (light line), and if no fishing had taken place after 1995 (dotted line).

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G.A. Rose and C.J. Walters Fisheries Research 219 (2019) 105314

Fig. 9. A comparison of total biomass from VPA with unreported catch and variable natural mortality with springtime trawl acoustic surveys conducted from 2012 to
2015 (from Rose and Rowe, 2018).

The low estimated survey catchability (q) from 1995 to the mid- present analyses are in full agreement that natural mortality has been
2000s, which thereafter increased and peaked in 2008, is likely a high episodically during this period (to 0.4 or more), but in contrast
consequence of changing distributions within the stock during these indicate that fishing mortality has also been a major, and perhaps
years. From 1995 to 2006, a major component of the stock biomass dominant, contributing factor.
occurred in Smith Sound and would not have been available to the The science underpinning recent management, which enabled a
trawl survey, resulting in lower survey q, followed by likely dispersal to tripling of reported catch from 2015 to 2017, was largely based on
the offshore which likely peaked in 2008 (Rose et al., 2011; Cadigan, recent DFO assessments. In keeping with a precautionary approach,
2016; Brattey et al., 2018). Dispersal would have resulted in an ap- DFO science recommendations (DFO, 2017, 2018) were “to keep re-
parent high survey q. Accounting for such variations may have resulted movals at the lowest possible level”, but do not state what that level
in slight over- and under-estimations by the VPA of abundances at age might be, enabling much management leeway based on the somewhat
during those years. contradictory assessment conclusions that fishing has had little impact
The stock recruitment relationship indicated by the present results is on stock dynamics. This leeway no doubt contributed to re-
nearly linear over the range of stock sizes since 1962, the most linear of commendations from the Newfoundland and Labrador Groundfish
any major cod stock (Rose et al., 2019), and consistent with earlier Industry Development Council (2019) to increase quotas, and resultant
analyses (e.g., Cushing, 2010). We used age 2 to assess this relationship management policies that have enabled catch increases, despite the
to be consistent with current DFO practice (e.g., DFO, 2016) which may stock being well below the prescribed precautionary lower limit for SSB
have contributed to the suggested linearity. The asymptote to the re- set by DFO, or the similar limit to curtail recruitment overfishing sug-
lationship appears to occur at spawning stock biomass (SSB) ap- gested in the present analyses.
proaching 106 mt (the DFO 2018 estimate is similar, at approximately In conclusion, we believe that alternative model approaches benefit
0.8 × 106 mt), which indicates that the stock has been subject to re- the assessment of any fish stock. In this paper, an alternative re-
cruitment overfishing (sensitive dependence of recruitment on SSB) for construction of the stock dynamics of the Northern cod suggests that the
most years since 1962. Moreover, the productivity suggested by this total and SSB are somewhat less than suggested by the stock assessment
relationship is low compared to other major stocks, also consistent with of the DFO (2018) based on the NCAM model. Moreover, according to
other longer-term modeling (Rose, 2004; Rose et al., 2019) and com- the present analyses, the fishery prosecuted on and off since the early
parisons among stocks (Dutil and Brander, 2003). Low productivity 1990s has negatively impacted rebuilding with fishing mortality sub-
indicates that sustainable annual harvest rates are equally low com- stantially higher than concluded in recent stock assessments. Of note,
pared to other major stocks, presumably < 20% of SSBs that exceed the the present reconstruction does not support the conclusion (DFO, 2018)
lower SSB limit, and considerably less, as now, when the stock is less that natural mortality is mostly responsible for the decline in the early
abundant. 1990s and the slow rebuilding thereafter – although in agreement that
An important outcome of the present analyses is the conclusion that natural mortality was elevated during that period and has undergone
the fisheries for Northern cod, including recreational and commercial substantial variability since, with its causes bearing further scrutiny and
since the early 1990s, have contributed to the slow average rate of research.
rebuilding. At least one previous study came to similar conclusions A few final words pertaining to management and rebuilding of this
(Shelton et al., 2006). This contrasts with recent stock updates and iconic fish stock are thought warranted. It is almost axiomatic that
assessments (DFO, 2017, 2018; Brattey et al., 2018) reporting that successful management requires as wide a range of science-based in-
fishing has had little impact on the stock trajectory, or on the rapid formation as possible. It would be optimal and reassuring if differing
decline that occurred in the early 1990s. The DFO reports attribute the model approaches gave similar results, but when they do not, as here, it
decline and slow rebuilding almost totally to natural mortality. The calls for increased management caution, especially when estimates of

8
G.A. Rose and C.J. Walters Fisheries Research 219 (2019) 105314

SSB and fishing mortality differ substantially, and all indications are Author statement of contributions
that the stock is well below the SSB required to avoid recruitment
overfishing. For the Northern cod, plans to increase fisheries should be Both authors contributed equally to data curation, formal analyses,
tempered with the knowledge that although growing, the stock may not methodology and writing.
be as strong as the DFO assessment suggests, and production, and
therefore sustainable catch, will be impeded until SSB increases sub- Acknowledgments
stantially. Fishing more now means a longer rebuilding timeframe by
slowing stock growth. We are well aware that management decisions We thank Jennifer Gee and Pierre Maudoux (FAO Rome) and Carola
often have, and should have, socio-economic inputs that influence Kirchner (Namibian fisheries consultant) for providing information on
fishery policies and rebuilding strategies. We stress that we support the Namibian Spanish hake fleet. The catch and assessment data used
redevelopment of fisheries as the stock rebuilds, but it is self-defeating were made available through FAO, NAFO records and DFO documents
if these fisheries harm long-term sustainable harvests by overly (no appropriate tagging data were available). We also thank Jeff
prolonging recruitment overfishing. In closing, we hope that the present Hutchings and Jake Rice for stimulating and challenging reviews.
results, that offer an alternative reconstruction of the Northern cod Nonetheless, we take full responsibility for the interpretations of all
stock over the past few decades to that of recent assessments, assist data and analyses reported here. This research did not receive any
management rebuild this iconic stock and its fishery. specific grant from funding agencies in the public, commercial, or not-
for-profit sectors.

Appendix A. Negative log likelihood function for model fitting

Following the recommendation of Walters and Ludwig (1994), we minimized a condensed negative log likelihood function (nll) of the form

n ll = (ny /2)ln[ ∑ (zt − z¯y )2 ] + (nay /2)ln[ ∑ (zat − z¯ay )2 ] + (0.5/σ 2 m) ∑y ln(mt)2 + (ny /2)ln(σ 2 m ).
t t (A1)
Here, ny is the number (35) of years with survey data, and nay is the number (342) of non-zero survey cpue at age observations. The last two terms
involving σ2m and mt represent assumed log-normal, time-independent variation in the annual natural mortality rate multipliers m. The z̄y and z̄ ay are
arithmetic means of the “z-statistics” zt and zat; z̄y is the conditional maximum likelihood estimate of ln(qB), the survey catchability coefficient for
biomass, and z̄ ay is the conditional maximum likelihood estimate ln(qa), the catchability coefficient for cpue.
In A1, the first sum of squares represents deviations of observed from predicted total survey biomass, assuming log-normal survey variation,
where the z-statistic zt for each year is given by

zt = ln[∑acatwat/∑ava(Na,t-Ca,t)e−Mtt*Wat] (A2)

where va is survey vulnerability at age, cat is survey cpue at age, wat is mean observed weight at age, and Nat is the VPA estimated numbers at age.
The numerator sum is the observed survey biomass cpue, and the denominator sum is the predicted survey biomass. In the second sum of squares in
A1, the z-statistic for each age-year cpue at age observation again assuming log-normal survey variation is given by

zat=ln[cat/(va(Na,t-Ca,t)e−Mtt*)]. (A3)
−M
The (N-C)e terms in A2 and A3 represent prediction of numbers still alive at the fall survey time, from preharvest numbers N and year-specific
natural mortality rates evaluated over the time t* from the start of fishing to the fall surveys.
The two ln(SS) terms in A1 represent evaluation of the normal likelihood function at the conditional maximum likelihood estimates of the
observation error variances σ2B and σ2a, i.e. they are the components of the normal negative log-likelihood function that do not depend only on
additive constant factors (like the number of observations). So as the nonlinear search aiming to minimize nll in A1 proceeds, the survey catch-
abilities (q’s) and variance estimates are “automatically” adjusted so as to always be evaluated at their conditional maximum likelihood estimates
given the other parameters that result in changes in predictions of Na,t.

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