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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). # 2009 International Council for the Exploration of the Sea. Published by Oxford Journals. All rights reserved. For Permissions, please email: [email protected] 1653 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: 1654 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 1655 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 1656 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 1657 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). 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