Download Herring and ICES: a historical sketch of a few

1652
Herring and ICES: a historical sketch of a few ideas
and their linkages
Mike Sinclair
Sinclair, M. 2009. Herring and ICES: a historical sketch of a few ideas and their linkages. – ICES Journal of Marine Science, 66: 1652 – 1661.
This introduction to the Symposium on “Linking Herring” sketches the development of some ideas generated from herring research
within an ICES context. The work of Committee A (1902 – 1908), under the leadership of Johan Hjort, led to a paradigm shift from
“migration thinking” to “population thinking” as the interpretation of fluctuations in herring landings. From the 1920s to the 1950s,
the focus on forecasting services for the herring fisheries, although ultimately unsuccessful, had the unintended consequence of generating ideas on recruitment overfishing and the match– mismatch hypothesis. The collapse of the East Anglian fishery led, in 1956, to
considerable debate on its causes, but no consensus was reached. Three consecutive symposia dealing with herring (1961, 1968, and
1970) reveal a changing perspective on the role of fishing on recruitment dynamics, culminating in Cushing’s 1975 book (“Marine
Ecology and Fisheries”, referred to here as the “Grand Synthesis”), which defined the concept of recruitment overfishing and established the future agenda for fisheries oceanography. The 1978 ICES “Symposium on the Assessment and Management of Pelagic
Fish Stocks” is interpreted as the “Aberdeen Consensus” (i.e. without effective management, recruitment overfishing is to be expected).
In conclusion, herring research within ICES has led to many ideas and two major paradigm shifts.
Keywords: herring, ICES, “migration thinking”, “population thinking”, recruitment overfishing.
Received 15 September 2008; accepted 19 January 2009; advance access publication 30 April 2009.
M. Sinclair: Bedford Institute of Oceanography, Dartmouth, Nova, Scotia, Canada B2Y 4A2;. tel: þ1 902 426 3492; fax: þ1 902 426 8484;
e-mail: [email protected].
Introduction
The following historical sketch links some of the ideas generated
by scientists studying herring fisheries in an ICES context, as background for the “Linking Herring Symposium”. Given the richness
of the topic, my perspective has been selective, focusing on eight
themes and the scientists involved:
(i) Late 1890s: The creation of ICES
(ii) 1902–1908: Committee A
(iii) 1920–1950: Early forecasting services
(iv) 1956: A year of transition
(v) 1961–1970: From entrenchment to doubt
(vi) Mid-1970s: The “Grand Synthesis” and the “Aberdeen
Consensus”
(vii) 1980s: A Northwest Atlantic perspective
(viii) 1990s on: Harvest Control Rules (HCRs) and the Ecosystem
Approach to Management (EAM)
The sketch ends with remarks on the process of the transitions
in thinking about the causes of fluctuations and the impacts of
fishing on recruitment.
Herring and the creation of ICES (late 1890s)
In the 1890s, two major issues affecting European society and its
prosperity led to the creation of ICES: the fluctuations in fisheries
on decadal time-scales, and the concern about overfishing (for
detailed discussions, see Went, 1972; Rozwadowski, 2002). These
two concerns are reflected in the committee structure established
in 1902, in which the (“migration”) Committee A addressed the
causes of temporal fluctuations in landings, and the (“overfishing”) Committee B addressed the issue of overfishing. In terms
of understanding the context and nature of these concerns, and
the associated ideas, the early books on herring (such as Dodd,
1752; Mitchell, 1864; Bertram, 1873; Heincke, 1898) are revealing.
They capture a passion for the subject of herring fisheries and
natural history. Molloy (2006) has called this engagement
“herring fever”. Mitchell (1864) quotes Cuvier as follows:
The coffee bean, the tea leaf, the species of the Torrid Zone,
and the silkworm, have less influence on the wealth of
nations than the herring of the northern seas. Luxury and
caprice may seek those productions, but necessity requires
the other. . . . The greatest statesmen, the most intelligent
political economists, have looked on the herring fishery as
the most important of maritime expeditions. It has been
named the Great Fishery.
Among European fisheries in the 19th century, the herring was of
exceptional importance, with its fluctuations over time having
major economic and social impacts.
The ideas underlying the first societal issue of the 1890s—the
causes of the fluctuations in fisheries—were based to a large
degree on studies of herring. The Polar Migration Theory was
first proposed by Dodd in 1728 and later expanded by Johann
Anderson, a mayor of Hamburg, in 1746 (Heincke, 1898).
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Herring: a historical sketch
This theory was founded on observations that had been accumulated from Iceland to the Bay of Biscay on the timing of arrival of
herring at different locations, their body size, form, and quality
(such as relative fatness). The theory stated that the “home of
herring” was under the northern polar ice, with excess herring
migrating south in search of food and being driven by predators
(predominantly whales). Some reproduction occurred en route,
resulting in variable growth, depending on local conditions. The
interannual and decadal-scale fluctuations observed were attributed to variability in migration patterns. Gilpin (1786) modified the
theory to include transatlantic migrations from the hypothetical
southern endpoint of the European migration to the Northwest
Atlantic, with a return path back to the “polar home” a year
later. There was also criticism, perhaps best articulated by
Mitchell (1864).
In the 1820s, the Royal Scottish Society of the Arts offered a
medal for the best essay “on the natural history of herring, considered in connection with its visits on the Scottish coasts”. The
herring industry, which employed 91 139 people in 1855 (including 39 266 fishers), was critical to the Scottish economy. Mitchell
won the medal in 1827. In his essay, he states 11 points of criticism
and concludes that fisheries are based on more local migrations.
His points, and other criticisms, led to great doubts about the
theory. Still, “migration thinking” was retained as the explanation
for the large fluctuations. Bückmann (1958) captured the nature of
“migration thinking” in a poetic manner. He states that Heincke,
in the latter half of the 19th century, was testing
whether there was one large uniform stock of North Atlantic
herrings, coming from the depths of the Northern waters
and surfing, as it were, against the different coasts of
Northern Europe, attaining these coasts at different times
of year in order to spawn, giving origin at the same time
to different herring fisheries, and ebbing back once more
into the northern deep.
The second societal issue of the 1890s (overfishing) was based
predominantly on flatfish in the southern North Sea. However,
the concept itself had strong links to herring fisheries. As early as
the mid-1700s, Dodd (1752) rejected the concerns that overfishing
of herring had occurred in Great Britain. Bertram (1873) made contradictory statements in his popular treatise, but concludes that “the
pitcher is going too often to the well”. Heincke (1898) quoted
Nilsson’s concerns about overfishing of herring in the Baltic.
Although the specific concerns about overfishing at the time were
related to flatfish, the concept had applications to herring.
At the inaugural meeting of ICES in 1902, Johan Hjort argued
for the need for quick results and for concentrating on two problems of great practical interest (Went, 1972):
1. The migrations of the herring and the cod, and the influence of these migrations on the fisheries in the northern
part of the North Sea (Committee A, with Hjort as
Convener);
2. The question of overfishing, particularly in the Southern
part of the North Sea, and in connection with . . . flatfish
(Committee B, with Garstang as Convener).
In conclusion, the natural history concepts associated with the
societal concerns leading to the creation of ICES were based to a
considerable degree on herring and its “great fisheries”. The
extant paradigm explaining fluctuations by variations in migration
was based on an earlier species concept that emphasized the “ideal
type” (i.e. one homogeneous population) rather than aggregates of
more-or-less isolated populations (Mayr, 1982) and involved
oceanographic variability at large spatial scales. While responding
to the societal concerns was emphasized by Hjort, the visionary
who created ICES was the Swedish oceanographer Otto
Pettersen (Smed and Ramster, 2002). His objective was to
explain the great fluctuations in the Scandinavian fisheries
(including herring). This task, following his vision, required an
international body to carry out extensive oceanographic surveys
at the appropriate spatial scale of the issue (i.e. the North
Atlantic) under “migration thinking”.
Herring and Committee A (1902 –1908)
The work of Committee A (1902–1908) led to a paradigm shift in
the interpretation of decadal-scale fluctuations in fisheries (Hjort,
1914), and thereby solved the practical problem of its remit. This
was of critical importance to ICES in these early years, as the
member countries insisted on quick results. The members were
prominent scientists of that era (e.g. Hjort, Heincke, Petersen,
Redeke, Trybom, D’Arcy Thompson, and Garstang). Heincke, in
particular, brought to the Committee radical thoughts on the
nature of species and races, based on his herring studies
(Heincke, 1898). He had a multidisciplinary and ambitious
vision for the research agenda that complemented the leadership
skills of Hjort. The research component dealing with herring
made a major contribution to the shift from “migration thinking”
to “population thinking”.
Committee A might be viewed as an early GLOBEC. The
studies included large-scale surveys of egg and larval distributions
of commercial species—from Iceland to the Bay of Biscay—to
detect any inherent geographic patterns. This component was
encouraged by Heincke and was based on his herring work in
the Baltic. Oceanographic properties were measured at the same
locations from which the plankton hauls were made. Ageing
studies on herring were initiated at Bergen, again based on
Heincke’s influential ideas. Port sampling of the landings of
diverse fisheries were enhanced, based on protocols developed in
Norway. Additional oceanographic observations were initiated
by the Hydrographic Programme of ICES, with a focus on basinscale influences (such as the role of the Gulf Stream in climate
variability in the Northeast Atlantic).
The syntheses of the first five years (1902–1907) and the first
ten years (1902–1912, which includes follow-up work after the
termination of Committee A) are somewhat paradoxical, given
the breakthrough that was to occur in 1913/1914. Schmidt
(1909) and Damas (1909) proposed a modified version of
“migration thinking” to account for variability in migration patterns. This involved supersensitivity of fish before spawning,
such that each species required specific combinations of temperature, salinity, and oxygen for successful spawning. If these sensitivity criteria were to be understood on a species-specific basis,
the changing spawning patterns (and fluctuations in fishery landings at specific locations) might be linked to oceanographic variability. In retrospect, Schmidt (1917) stated that there was “mere
chaos” in interpreting the results of Committee A’s work under
“migration thinking”. In his 1912 report, Hoek (1913), as
General Secretary, puts a positive spin on what must have
been disappointing progress at the end of the decade of work,
and states:
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M. Sinclair
Although the problem of fluctuations cannot yet be
regarded as solved, the earlier vague conjectures as to occurrence and migration of the fish have taken a clearer and
more certain form.
“Migration thinking” as the interpretation of fluctuations, though
somewhat modified to include supersensitivity of prespawners,
was still well accepted in 1913.
In 1914, Hjort published his lecture, given the previous year,
entitled “Fluctuations of the Great Fisheries”. The key findings
seem to be stated rather blandly when read today:
“the most important results . . . the existence of an intimate
relation between the fluctuations and the numerical value of
stock of fish and the yield of the great fisheries.” and “the
renewal process is of a highly irregular nature”.
Under “migration thinking”, stock abundance was considered to
be relatively constant, with major fluctuations caused by variations
in migration patterns. Under “population thinking”, year-class
variability generates fluctuations within geographically limited
populations. The solution to the fluctuation problems required a
change in the species concept itself. It is to be noted that the “biological species” concept of Ernst Mayr, which was an important
contribution to the so-called “Modern Synthesis” of evolutionary
theory, was not introduced until several decades later. Mayr (1942)
defined species as “groups of actually or potentially interbreeding
natural populations, which are reproductively isolated from other
such groups”. Fishery scientists within the ICES community were
ahead of the broader ecological community in this shift in thinking, from species as “types” to species as aggregates of populations.
Secor (2002) provides an interesting summary of the shift in the
species concept and the relative differences in perspective of
Hjort and Heincke. It is worth noting that the critical-period
hypothesis to account for year-class variability was considered by
Hjort himself to be a second-order finding, not a “key discovery”.
Allen (1914), in his review in Nature, states “There can be little
doubt that this report by Dr. Hjort will mark an epoch in the
history of Scientific investigations”. What happened between the
conclusions of Hoek (1913) and the lecture of Hjort (1914) that
generated such a radical shift in thinking? Hjort’s visit to
Atlantic Canada as the leader of the 1914/1915 Canadian
Fisheries Expedition (Figure 1)—a research initiative in support
of herring fisheries that mimicked the Committee A
programme—provides some insights. His interim report (Hjort,
1915) to the Canadian government was written in essay style
and, as such, provides interesting insights into his thinking at
that time. This report highlights his 1907 London lecture at the
meeting of Committee A as a key turning point by stating:
These discoveries resulted from the endeavour [proposed at
that meeting] to subject the stock of these important fisheries to a similar examination . . . as that universally
adopted for the study of the human populations.
He quotes a passage from the 1907 lecture, explaining the
proposal:
In all expositions of the science of vital statistics . . . a certain
number of individuals are selected who are supposed to
stand for the mass of the people, and attention is directed
to them . . . It seems at first sight a bold suggestion to
propose studying the fish supply on lines like these.
Figure 1. Johan Hjort (left) and Captain Robson on board a vessel
that supported the Canadian Fisheries Expedition in 1914 (photo
from the archives of the St Andrews Biological Station, Canada).
A population can be counted, but who knows how many
fishes are in the sea? And yet it appears to me a project
big with possibility, to regard the discoveries of fishery
research from a stand-point similar to that which has been
adopted in the Science of vital statistics.
In his 1915 essay, Hjort reflects on the lecture and the reaction of
the Committee members:
It must be regarded as a most striking and wonderful fact
that it is possible to collect a sample, say a few hundred herrings, and then to find this sample really giving a representative picture of the composition, with regard to the size and
age, of the whole stock of incalculable millions of spawning
herring in the sea. As I pointed out in my lecture in London,
in 1907, before these investigations started, it seemed at first
a bold suggestion . . . The scientists who took part in this
work hesitated for many years before their definite belief
in the representative character of the results grew so
strong that they dared to regard the method and the
results as sufficiently proved and fully established.
This quote captures Hjort’s excitement concerning his recent discoveries leading to “population thinking”, as well as identifying the
key methodology of applying the “vital statistics” of human populations to fisheries. Saetersdal (2008) and Dragesund et al. (2008)
provide a detailed analysis of the role of Hjort and his team.
The minutes of this 1907 meeting indicate that the lecture was a
long one (1 h and 45 min). His proposal for carrying out an
annual age census of herring, cod, and haddock, with supporting
studies on the appropriate sampling design, was presented under
Agenda Item 3. Heincke supported it, stating that Germany had
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Herring: a historical sketch
already started this kind of sampling. The Committee agreed “to
collect material for the age-census”.
Given Hjort’s quote, it can be inferred that he and Heincke provided the intellectual leadership to ensure that the study was
carried out, despite the majority’s lack of belief. Note that the
sampling would have started in 1907 and was continued up to
1913, the year of Hjort’s synthesis. Therefore, there were observations on the enormous 1904 year class for 7 years. Natural
events were therefore timely tuned to the implementation of the
new approach! The Canadian Fisheries Expedition of 1914/1915
was also fortuitous. It allowed transatlantic comparisons and
strengthened Hjort’s convictions that “population thinking”, and
the associated new interpretation of fluctuations in fisheries, was
robust.
In summary, herring work within Committee A had a major
impact on the paradigm shift of 1914. The key contributions
were from Heincke (ageing, existence of races) and from Hjort
(application of age-census methodology), with Heincke’s
support, as well from the herring itself (the fortuitously large
1904 year class of Norwegian spring-spawning herring was a gift
from nature). The synthesis by Hjort in 1914 is an outstanding
achievement in marine science, although Solemdal (1997)
argues, in a play performed in St Andrews, Canada, at the 1994
Larval Fish Conference, that more credit is due to his herring
research team in Bergen.
ICES early forecasting services for the herring
industry (1920 –1950)
From the 1920s to the 1950s, forecasting for the herring industry
became an innovative research topic. Two examples are addressed:
(i) the use of plankton indicators for setting of nets within a fishing
trip, and (ii) the predictions of fishing success for a herring season
based on age-composition information.
Hardy (1965), looking back to the 1920s, states:
To solve our problems we must have a service of information from the sea like the meteorological observations
from the air . . . to forecast events in the sea a week or two
ahead . . . long enough to be a value in guiding fishing
boats to more economic fishing.
He recalls his early work at the Lowestoft Laboratory, which he
joined in 1921 as an Assistant Naturalist, on the relationship
between plankton and herring. In 1922, because of the lastmoment illness of a senior staff member, Hardy was assigned the
role of chief scientist on a cruise of the RV “George Bligh”. The
aim of the cruise was to relate distributions of young herring to
plankton. Thanks to excellent weather, the cruise was completed
1 d early, and Hardy carried out repetitive sampling at a fixed
station over 24 h and set up a feeding study on deck. He noted
in his catches a high degree of patchiness in the distribution of
zooplankton and young herring, and stated later “it was this
experience on the George Bligh which led me to devise what I
have called the Continuous Plankton Recorder [CPR]”. It also
led to his innovative studies on the food habits of herring and
foodweb analyses, according to a similar statement made in his
keynote lecture at the 1949 ICES Special Meeting on Herring
(Hardy, 1951). A summary of his diverse studies includes 1400
records of plankton tows by fishers before setting their nets.
None of these studies were applied in the long term by the
fishing industry because of the high frequency of false-positives.
Nevertheless, Hardy remained optimistic that new technologies,
such as acoustics, along with plankton sampling, would eventually
provide useful operational forecasts.
The second example involves the use of age-distribution information for annual forecasts. Hjort (1930) uses language similar to
that in Hardy’s quote above. He states:
A biological service must be organized for the regular observation of the age distribution of the stock, and of the relative
numerical strength of year-classes. It will be something like
the meteorological service . . . In the organization of this
biological observation the International Council will have
a task which . . .will repay all the work and expertise that
its existence during the past 30 years has occasioned.
The basic idea was to use year-class tracking as a means of forecasting trends in landings, with the caveat that fishing effort was relatively low and steady (and the species was long-lived).
The forecasts for the East Anglia fishery are well summarized by
Hodgson (1957) in “The Herring and Its Fishery”. He dedicated
this book to Einar Lea of the Bergen team under Hjort, which indicates the links between his forecasting and Committee A’s findings.
This autumn-spawner fishery, which used driftnets at the time of
spawning, had been the largest fishery in the world for many centuries. Herring were partly recruited to the fishery at age 3, and
fully recruited at age 4. The first forecast was made in 1922, and
the press subsequently reported “an expert forecast . . . was
amply fulfilled”. All went well until 1951, when the forecast
turned out to be incorrect (the 1947 year class was not accurately
represented). After a second year of inaccurate forecasting in 1952,
Hodgson discontinued this service to the industry: “The period
1951–52 will go down in history as the end of an epoch, and
also possibly the end of the East Anglia fishery as we have understood it for centuries”. Coincident with the failing forecast were the
developments of an industrial fishery on juvenile herring on the
Bløden Ground and the introduction of trawling on spawning
concentrations. Hodgson proposed two hypotheses for the
decline of the East Anglia spawning stock—overfishing and
oceanographic changes—and leaves the readers to decide which
one they support. However, he leaves no doubt about his own position: that overfishing was primarily responsible. There is sadness
in this book. Hodgson had dedicated his career and heart to fishery
advice and during his “watch”, as it were, the stock collapsed.
The two examples of forecasting for the herring industry both
failed to a large degree. However, they both had unintended but
lasting consequences. The observations with Hardy’s CPR have
led to hypotheses on the processes that generate recruitment variability (match –mismatch). Hodgson’s forecasts, and their failure in
1951/1952, led to the concept of recruitment overfishing.
ICES and herring in 1956: a year of transition
The 1952–1955 decline in the East Anglia fishery generated what
could be seen as a fisheries crisis, perhaps not dissimilar to the
effects of the collapse of the cod stocks off Atlantic Canada in
the early 1990s. As a consequence, 1956 became a hectic year for
ICES herring scientists. This year may also be considered a
turning point regarding the dogma that fishing activities do not
affect recruitment. For the first time, this dogma was questioned
openly, and the debates were to continue for two decades before
consensus was eventually achieved. Scientists at the Lowestoft
Laboratory, especially Cushing and Graham (the Director of the
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Laboratory), made extraordinary efforts to focus the attention of
the ICES herring scientists on the fisheries crisis and asked ICES
to arrange a Special Meeting on the Herring of the Southern
North Sea. ICES responded by arranging to hold the meeting on
28 September, immediately after the symposium—“Special
Meeting on Herring ‘Races’” (which had already been planned).
Copies of an important synthesis paper by Cushing and Burd
(1957), as well as a questionnaire, were distributed well before
the meeting to facilitate discussions. The paper covered the existing data and interpretation in a comprehensive manner. The questionnaire sought comments on the synthesis before the Special
Meeting, as well as requesting any data that had not been considered. The conclusions of the synthesis were threefold: (i) “the
Downs herring is a useful concept representing a possible management unit”; (ii) an advance in maturity (essentially 100% at age 3),
starting with the 1947 year class, had resulted in a reduction in
older age groups and the increase in total mortality had made
the reduction more noticeable; and (iii) fishing had directly
reduced the abundance of older age groups.
The meeting was attended by 39 scientists (including Hempel,
Bückmann, Zijlstra, Popp Madsen, Parrish, Holt, as well as
Cushing and Burd) from 13 countries. Despite the efforts by the
Lowestoft Laboratory, the Special Meeting did not reach a consensus on the role of fishing in relation to the changes in the stock
observed. Without doubt, it was a tense meeting. The Chair stated:
Although the Lowestoft thesis was not refuted on any point
and substantially accepted as a fair explanation of recorded
facts . . . the meeting did not consider the presented evidence as conclusive (Aasen, 1957).
Two statements emerged from the meeting (Aasen and Jones,
1957):
(1) “concern and apprehension for the present state of the
stocks”, and (2) a recommendation for a “co-ordinated programme to determine the relative magnitude of the various
factors affecting the yield” (i.e. the Bløden Ground juvenileherring tagging programme and enhanced recording of
effort data).
Instead of reaching consensus, the meeting initiated what was to be
a 20-year debate on the relative importance of environmental
variability and exploitation on herring recruitment.
The symposium “Special Meeting on Herring ‘Races’” was a
much mellower gathering, with the focus on synthesis of knowledge and generation of research recommendations. In the conclusions, Parrish (1958), who acted as rapporteur, stated:
[The] primary objective of the ‘racial investigations’ is
identification of ‘unit stocks’, constituting distinct ‘management units’, and determining the extent of overlap in time
and space.
As noted above, the synthesis paper by Cushing and Burd (1957)
infers that the key issue of appropriate management units had not
yet been resolved. This major focus raised considerable controversy on the evolutionary status of races.
The Planning Meeting for the tagging programme on 8 –9
November involved Aasen (Chair), Bertelsen, and Cushing. The
goal was to estimate the fishing mortality on young herring in
the “industrial fishery” for fishmeal and fishoil on the Bløden
Ground. The plan was to carry out extensive tagging from
M. Sinclair
a Norwegian purse-seiner (20 000 internal and 5000 external
tags) during summer 1957, as well as to collect detailed catch
and effort statistics for this fishery. Went (1972) highlights this
programme as an important initiative for ICES during its first
70 years. This busy herring year did not result in any specific management actions, but it does mark a turning point as the seed of the
recruitment-overfishing concept was planted. However, the perspectives within the herring research community differed considerably. Hempel, in a 1988 letter (personal archive), stated:
There has always been disagreement between Bückmann
and Cushing. Bückmann was hard working and sometimes
too cautious. He hated any quick conclusions. Cushing was
right in his view regarding the overfishing of herring, but
Bückmann felt the proofs were not sufficient.
The forecasting efforts of Hodgson had ensured that attention
turned rapidly to observed changes in the fishery, but the inertia
of firmly held ideas on the resilience of herring resulted in a
long period of transition.
From entrenchment to doubt: a decade
of transition (1961 –1970)
The term “entrenchment”, with respect to the concept that fishing
had little impact on recruitment, is used to emphasize that other
outlooks did not find much support within the ICES community.
During this decade, three ICES symposia were either wholly or
partly dedicated to herring studies. The 1961 symposium (“The
Herring Symposium”) was broad in scope, covering all aspects
of herring fisheries and ecology. The 1968 “Symposium on the
Biology of Early Stages and Recruitment Mechanisms of
Herring” was more narrowly focused. The 1970 “Symposium on
Fish Stocks and Recruitment” was global in scope and put the
ICES experience with herring within the broader context of population regulation in marine fish. One can track the shift in thinking
within the ICES research community from the introductions and
conclusions of these three events. On aggregate, the papers reflect a
resistance to change in ideas, consistent with Kuhn’s (1962) perspective on the scientific process. Although the 1960s represent a
decade of revolutionary thinking in society at large, there is
limited evidence of radical changes of mind regarding the role of
fishing on recruitment at this time.
Parrish (1963), in his report on the 1961 symposium, provides
an interesting perspective on the unintended consequences of
Hjort’s (1914) synthesis. He states that for herring in particular,
the synthesis inferred that natural processes are more important
than fisheries as causes of fluctuations. Thus, less attention has
been paid “to quantitative problems of abundance estimation
and measurement of fishing effort . . . than for demersal species”,
while the post-war declines in herring fisheries led to increased
attention to “possible importance of man-made factors as major
determinates”. The resultant upsurge in herring studies generated
conflicting interpretations that required synthesis and appraisal in
this symposium. The events of 1956, focusing on the southern
North Sea, were of particular interest, as was the debate on the
relative importance of natural causes and fishing on
Atlanto-Scandian herring. The symposium synthesis is split into
reports on four topical themes, three of which are relevant here.
Popp Madsen (1963), on the subject of the effects of fishing on
adult herring, concludes that for the Downs herring, the observations do not “exclude the fishery as being an important factor
but . . . it also does not exclude the possible influence of other
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Herring: a historical sketch
agents”. Zijlstra (1963), on the subject of recruitment fluctuations
and trends in herring fisheries, concludes:
The concern about the industrial fishery on juvenile herring
in the North Sea and its possible relation to the disturbing
changes experienced in the southern North Sea led to
tagging experiments under the auspices of ICES. The
results . . . indicated that about 18% of the total stock of
immature herring was removed by the industrial fishery
[annually in 1957, 1958]. Therefore most scientists considered that the main changes in the southern North Sea
cannot be attributed to this cause.
Hempel (1963), on the subject of causes of changes in recruitment,
notes that the question of introducing conservation practices in
herring fisheries had not been discussed in much detail. He concludes that “the influence of man on the recruitment of herring
has so far been relatively small”, and that in most fisheries,
“environmental factors seem to be dominant in determining the
strength and pattern of recruitment”. In summary, although
acknowledging that the observations on the Downs herring were
suggestive of a substantial impact of fishing on recruitment, the
consensus was that fishing played a secondary role. Krefft
(1963), at one extreme, presented a hypothesis that attributed
the southern North Sea fishery collapse to natural factors only.
Overall, these events had little impact on the conceptual framework underlying recruitment dynamics in general.
The 1968 “Symposium on the Biology of Early Stages and
Recruitment Mechanisms of Herring” reflects a shift in focus of
research efforts. Saville (1971) states, in his introduction as convener, that the symposium was aimed at clarifying research directions on all aspects relating to the early stages and at identifying
factors regulating year-class strength and recruitment. He links
this aim to Hjort’s (1914) paradigm on the natural causes of fluctuations. Cushing had been on the Planning Committee but surprisingly, given his earlier involvement in this theme, did not
present a paper or have a role in the synthesis. The convener concludes that there is “no direct relationship between spawning
potential of the parent stock and year-class strength” (Saville,
1971). Obviously, the view was still widely accepted that fishing
did not impact recruitment, except under exceptional circumstances (Cushing and Bridger, 1966).
The 1970 “Fish Stocks and Recruitment” symposium, held in
Aarhus and organized jointly with FAO and ICNAF, was global
in scope and was attended by famous ecologists not actively
involved in ICES or herring (e.g. Slobodkin, Ricker, and Larkin).
There is a subtle shift in emphasis when comparing Saville’s
(1971) conclusion 2 years earlier with the statement by Parrish
(1973), in his foreword to the proceedings, that
high in importance . . . is knowledge of factors governing the
magnitude of recruitment to exploited stocks and especially
the relationship between recruitment and parent stock size.
Cushing and Harris (1973) presented an elegant synthesis of
stock– recruitment (S/R) relationships for a wide range of
species, and concluded that: recruitment (of all fish species with
a larval stage) is regulated during larval drift; the capacity for regulation depends on the species’ fecundity; and herring stocks are
more susceptible to extinction than other marine fish species.
However, they did not yet introduce the concept of recruitment
overfishing. Their conclusions are to a large degree reflected in
the foreword by Parrish (1973):
[diverse studies raise] “serious doubts about the validity . . .
of the previously widely held hypothesis that, over the range
of stock sizes encountered in practical fishery situations, the
level of recruitment is mainly independent of spawning
stock size” and “there might be serious dangers in awaiting
final conclusive results of scientific study before management action is taken. There is therefore a new urgency . . .
for taking management decisions”.
The 1956 events in the East Anglia fishery, and comparable
global developments associated with other heavily fished small
pelagics, had enhanced research on S/R relationships and recruitment processes during the 1960s. This did result in a marked
change in tone of the conveners of the 1968 (Saville) and the
1970 (Parrish) symposia, and a considerable shift from entrenchment, as suggested by the conclusions drawn by Popp Madsen,
Zijlstra, and Hempel from the 1961 symposium, to serious
doubt, as expressed by Parrish based on the 1970 symposium.
Cushing’s “Grand Synthesis” (1975) and the
“Aberdeen Consensus” (1978)
The 1970s represent a decade of great change in the ideas about
herring, and more generally within marine ecology. Two highlights
have been selected: the book by Cushing (1975) and the 1978 ICES
Aberdeen “Symposium on the Assessment and Management of
Pelagic Fish Stocks”, referred to as the “Grand Synthesis” and
the “Aberdeen Consensus”, respectively.
The change in Cushing’s thinking from the 1960s to the 1970s is
well illustrated by a comparison of his two books, published in
1968 (“Fisheries Biology: A Study in Population Dynamics”)
and in 1975 (“Marine Ecology and Fisheries”). The former
resulted from a series of invited lectures at the University of
Wisconsin (Cushing, 1968). It does not mention recruitment overfishing, although summarizing well the Harden-Jones (1968)
concept of the migration triangle for the geographic persistence
of populations. Cushing’s statements on the “dogma”, defined as
the independence of recruitment on parent-stock abundance
within the fishable range, is of particular interest. The following
quote suggests that he is either still uncertain or being cautious:
Cushing and Bridger (1966) and Garrod (1967) have published stock vs. recruitment relationships for herring and
cod, respectively, that would deny the dogma if the variations in recruitment were not due to environmental causes.
In his view, the most important theoretical problem needing solution is the dependence of recruitment on parent stock.
The “Grand Synthesis” (Cushing, 1975) has been a watershed
book that focused the global oceanographic and marine-ecology
research community on fisheries problems. University professors
across the globe used this book as content for lectures on fisheries
oceanography (including myself and Bill Leggett at the Université
de Quebec à Rimouski and McGill University, respectively). The
book addressed both the concept of recruitment overfishing and
recruitment processes. A major component of the empirical observations and synthesis was based on herring research within an
ICES context. The recruitment-overfishing concept can be traced
to Hodgson’s forecasts for the East Anglia fishery, and the empirical observations underlying the match– mismatch hypothesis
1658
flowed to a large degree from Hardy’s work on plankton
indicators.
Acknowledging Ricker (1954) as the originator of the concept,
Cushing defines growth overfishing and recruitment overfishing as
follows:
Fish stocks are reduced by fishing in two ways, by growth
overfishing and by recruitment overfishing . . . Herring
and whales suffered from recruitment overfishing, that is,
death by fishing was great enough to reduce recruitment.
He continues:
The problem of growth overfishing was solved in the
yield-per-recruit solution: It is an unhappy accident that
this solution generated the problem of recruitment overfishing and a solution to this problem is needed.
Cushing and Ricker, depicted during a break in the “Herring
Symposium” in Nanaimo, Canada, in 1983 (Figure 2), are
perhaps reflecting on these ideas.
The key observations for his match –mismatch hypothesis are
those of timing of spawning of herring populations and seasonal
cycles of plankton production from the CPR data. These observations were generalized to apply to all fish species with larval
stages. Placing recruitment processes within the broader field of
population regulation in ecology, Cushing concludes that the
M. Sinclair
density-dependent processes of growth and mortality operate
predominantly during the period of larval drift, and states:
during the period of the planktonic life history . . . numbers
are regulated and compensation is established . . . processes
[are] mediated by the availability of food . . . It is not surprising for it is the basis of Lack’s (1954) thesis on the
control of numbers in animal populations.
Interestingly, little mention is made of Andrewartha and Birch
(1954), who had proposed that density-independent processes are
frequently important in the regulation of animal populations.
They had based much of their synthesis on insects, whereas Lack
addressed, to a large degree, birds and mammals. The debate in
the 1950s and 1960s had been heated, and Cushing was clearly
influenced more by Lack than by Andrewartha and Birch.
The final chapter defines the future research agenda in terms of
three ecological topics: (i) more rigorous formulation of the
dependence of recruitment on parent stock; (ii) more comprehensive studies of density-dependent processes of growth and mortality at all life stages; and (iii) ecology of fish larvae, their
growth and survival as they feed. His final words are:
The broader outlook of marine ecology is needed in fisheries
science in order to solve the problems of the generation of
recruitment and those of recruitment overfishing.
His research agenda has been followed to a large degree in subsequent decades (including international programmes, such as
GLOBEC). The ideas that Cushing developed during his ICES
years (late 1940s to mid-1960s) working on herring were generalized for marine fish as a whole.
The 1978 Aberdeen symposium was global in scope, covering
all small pelagics. In his introduction as convener, Saville
(1980a) states that the early to mid-1970s were faced with the collapse of the fisheries for Norwegian spring-spawning herring, two
herring stocks in the Icelandic area, and North Sea herring. He
noted that the scientific community, through ICES, had not
given clear advice to management. The general setting at that
time was the recent collapse of many stocks of small pelagics.
Saville’s (1980b) conclusions were very strong:
(i) essentially all herring stocks had collapsed as a result of
recruitment failure generated by declining spawning–stock
biomass (SSB);
(ii) catchability increased as SSB declined as a result of the
schooling behaviour of small pelagics and the increasing
searching power of fishing fleets;
(iii) the production/biomass (P/B) ratio for herring is low compared with that of demersal species;
(iv) demersal stocks had fared better at comparable levels of
exploitation owing to their higher P/B ratio and the
steeper left-hand limbs of the S/R relationship;
(v) management advice needs to be less “timorous” and must
include a constraint for keeping SSB at some minimum
level to safeguard recruitment.
Figure 2. David Cushing (left) and William Ricker at the 1983
Herring Symposium in Nanaimo, British Columbia, at the time of the
75th anniversary of the Biological Station (photo from the archives
of the Pacific Biological Station, Nanaimo, Canada).
Saville’s final point, in essence, advocates that a “Precautionary
Approach” to the management of fisheries is required. This
concept has become a major focus of ICES advisory services.
Effectively, the conclusions drawn by Hodgson (1957) for the
Downs stock in the late 1950s were generalized for herring and
1659
Herring: a historical sketch
other small pelagics. The “Aberdeen Consensus” was that recruitment overfishing (for pelagics in particular) is to be expected if
management remains ineffective. This change in thinking has
the elements of a paradigm shift, and it signals the end of the
debate initiated by Cushing and Graham in 1956. The possibility
of recruitment overfishing for herring was fully accepted.
A Northwest Atlantic perspective
Derrick Iles, who spent time in Lake Malawi studying the speciation of cichlids (Fryer and Iles, 1972) before joining the herring
team at Lowestoft, had radical ideas on population processes
that were more in line with Andrewartha and Birch (1954). He
became my mentor in 1978 when I started working on herring
stock assessments for the Scotian Shelf and Bay of Fundy area
(only a few weeks after the “Aberdeen Consensus”). The distribution patterns of different life-history stages of herring in the
Northwest Atlantic did not support some of the conclusions that
had been drawn from observations in the Northeast Atlantic
(e.g. migration triangle, match –mismatch). In addition, the explanatory power of these concepts for the differences in mean abundance between herring populations was limited. In conjunction,
modelling of circulation and mixing of shelf seas and the coastal
zone had been improved considerably. Pingree’s application of
the H/u3 parameter, to predict the geographic location of tidally
induced fronts that separated stratified and well-mixed waters
during the spring to autumn period (Pingree and Griffiths,
1978), provided interesting patterns that in some way could be
important to herring. The combination of observations on spawning locations, larval distributions, and fronts led to an alternative
interpretation of population regulation (Iles and Sinclair, 1982;
Sinclair and Tremblay, 1984), based in part on the concept of
larval retention (in contrast to the focus on larval drift in the
Northeast Atlantic). Subsequently, these ideas have been generalized for marine population regulation by Sinclair (1988), under
the rubric of the member/vagrant hypothesis. Secor et al. (2009)
have expanded the conceptual framework in their analysis of
herring as a metapopulation.
The hypothesis provided an interpretation of the differences
between species in their population richness, the spatial patterns
exhibited by different marine fish species, their mean population
abundance, and their interannual variability. The interpretation
provided a mechanism for density-independent regulation, but
did not rule out that density-dependent processes could play a
role. The purpose here is not to evaluate the hypothesis in the
light of the empirical observations available, but rather to make
the point that the ideas were based on herring within an ICES
context. My observation is that the aggregate empirical data available for Atlantic herring are not fully supportive of any of the
diverse interpretations of population regulation for this species.
There is a certain parallel with the unresolved debate between
Lack (1954) on the one hand and Andrewartha and Birch (1954)
on the other. More thinking and synthesis are needed!
Harvest control rules and the ecosystem
approach to management
This final theme briefly addresses some recently emerging ideas. It
is perhaps a stretch to conclude that the idea of HCRs was derived
through herring studies within an ICES context. That said, their
application in practical terms for herring fisheries has been innovative and “closes the loop”, as it were, on the solution of the
recruitment-overfishing problem (as advocated by the “Grand
Synthesis” and the “Aberdeen Consensus”).
Simmonds (2007) provides a neat summary, contrasting the
responses of management to the severe declines of North Sea
herring in 1970 and 1995, respectively. In 1970, the SSB was extremely low. Lacking consensus on the existence of an SSB/R
relationship, ICES provided “timorous” advice (to use Saville’s
term), the management agency lacked authority to set catch
limits, and the stock collapsed. In contrast, in 1995, the SSB was
dangerously low, ICES advice was firm and trusted, the management agency cut the 1996 quota by half within a year after receiving the advice, and the stock decline was at least halted. In 1997, an
ICES team (Patterson et al., 1997) provided the HCRs, which were
adopted subsequently, and the stock recovered. The modelling and
simulations for the HCRs were based on six criteria (four of which
were generic, whereas the other two were specific to North Sea
herring). This example illustrates the strength of ICES by effectively bridging the transition area between scientific research and
advice, a strength that has been a constant factor from Hjort’s
time through to the present.
The second emerging issue for herring research and advice
involves the application of the EAM. Under this approach, conservation objectives have become broader (beyond the target species);
for example, the consideration of impacts on bycatch of other
species, habitat disturbance, and forage-fish issues. Bakun et al.
(2009) address the complex interactions that are of interest, as
do the papers under the theme “Herring in the middle” in this
symposium. Undoubtedly, ideas on herring as a forage species
will be an area of focus for ICES in the coming decade.
Many ideas and two paradigm shifts
Only a small proportion of the ideas generated from herring
studies within an ICES context have been addressed in this
sketch. The broad fields of tagging, acoustics, genetics, and stockassessment methods have not been covered. Stephenson and Clark
(2002) provide a more comprehensive synthesis. Hempel (2002)
also provides a valuable perspective of the debates of the
Herring Committee of ICES from the late 1950s to the early
1980s. Two predominant themes were highlighted: (i) the key
issue of the role of stock identification in the definition of
spatial management units, and (ii) the large-scale migrations of
Atlanto-Scandian spring-spawning herring (including the shift
in their spawning grounds). Saetersdal (2008) covers the latter
theme in considerable detail. This sketch, and other historical
reviews, suggests that herring studies within ICES have been a
rich source for generating concepts. Part of the explanation may
lie in the economic importance of these fisheries to European
society, particularly during the early years, and the urgent need
for scientific advice on societal issues. Another contributing
factor is the persistence of spatial and temporal patterns in their
populations. The observations have been well suited to a comparative approach, perhaps more so than for many other marine
species of commercial importance. The multidisciplinary nature
of ICES, as an organization at the interface of science and
advice, has been important in facilitating this intellectual creativity
during the past century.
Among the many ideas that have emerged, perhaps only two
might be considered as genuine paradigm shifts. The first major
shift was from “migration thinking” to “population thinking” as
an interpretation of fluctuations in fisheries landings (Sinclair
and Smith, 2002). Saetersdal (2008) points out that the practical
1660
implications of this shift were not addressed for several decades
following Hjort’s (1914) classic work. The second shift addresses
the conceptual framework on the effects of fishing on recruitment.
Perhaps an unintended consequence of Hjort (1914), as suggested
by Parrish (1963), was the interpretation that recruitment is essentially independent of population abundance. This “dogma”, to use
Cushing’s (1968) term, was resistant to revision, despite growing
evidence to the contrary. The first strong signal was received in
the early 1950s, yet it took another two decades and several
additional fishery collapses before the dogma was rejected and
replaced by recruitment overfishing as the expectation in the
absence of appropriate management actions. The brief history outlined here suggests that the Kuhn (1962) concept of scientific
resistance to new ideas, rather than the Popper (1968) concept
of falsification as a guiding principle in science, has guided the
process of marine science on these issues.
An additional observation on the scientific process relates to
unintended consequences when tracing the linkages between concepts through time. Two clear examples emerged above: (i) the
plankton indicators aimed at guiding skippers when setting their
nets ultimately contributed to the match –mismatch hypothesis;
and (ii) the fishery forecasts based on age compositions finally
resulted in the recruitment-overfishing concept. “Linkages” are
the overarching theme of this symposium. This sketch illustrates
the complex web of connections through the past century of
herring research within ICES.
I wish to pay a special tribute to David Cushing, in this year of
his passing. During my preparations, I realized what an intellectual
force he was within ICES, from the 1950s to 1970s in particular. He
was active in all aspects of herring research (plankton/fisheries
studies, use of acoustics, definition of management units, stock
assessments, programme planning). His most important contribution, however, was his remarkable capacity for synthesis in
both research papers and books, generalizing many of his ideas
on herring for marine ecology at large. As a “synthesizer”, he
created an ambitious multidisciplinary research agenda in fisheries
oceanography at a global scale, and his intellectual leadership
enriched the marine-science community to an extent well
beyond the herring-minded subset.
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