A sea change: Johan Hjort and the natural fluctuations in the fish stocksSchwach, Vera
doi: 10.1093/icesjms/fsu108pmid: N/A
That recruitment of juveniles to the stocks of fish is subject to natural variations is considered a scientific truth, if not a truism, in marine science. However, in 1914, when the zoologist Johan Hjort (1869–1948) published the notion, it meant a basic change in the understanding of the biology of the sea fish. A century later, his insight is a topic still at the centre of interest in fish biology. Hjort based his concept largely on investigations of herring (Clupea harengus) and cod (Gadus morhua) in the North Atlantic. He was the mastermind, but worked with a small group at the Directorate of Fisheries in Bergen, Norway, and in cooperation with the International Council for the Exploration of the Sea (ICES). The theory of natural fluctuations prompted an important step from migration thinking to population thinking, and gave the emerging fish biology and multidisciplinary marine science a theoretical basis. The article aims to explore the set of important facts and reasoned ideas intended to explain the causes for variations in year classes, and in this the fluctuations in the recruitment to the stocks. It argues that in addition to scientific factors, economic and political circumstances had an important say in the shaping of the understanding of stock fluctuations. The mere existence of a theory does not alone account for a breakthrough, and the article draws attention to the acceptance of scientific results.
Johan Hjort: The Canadian Fisheries Expedition, International Scientific Networks, and the challenge of modernizationHubbard, Jennifer
doi: 10.1093/icesjms/fsu086pmid: N/A
Abstract By leading the Canadian Fisheries Expedition of 1914–1915 Johan Hjort took the opportunity to do far more than just survey herring, other fish stocks, and the hydrography of Canadian Atlantic waters. He also attempted to improve the backward fish-processing technologies used in the local fisheries, an agenda blocked by the Canadian government. Hjort did succeed markedly, however, in introducing Canadian scientists to the International Council for the Exploration of the Sea's new scientific methods for fisheries research. He and his colleagues offered training in the new dynamic oceanography as well as population demographic studies and biometrics for studying fish populations, races, and other units. His extroverted leadership-initiated lasting linkages between Canadian and Scandinavian scientists, and created an international network of fisheries biologists. Introduction The 2008 celebration of the hundredth anniversary of Canada's St Andrews Biological Station (formerly the Atlantic Biological Station) was marked by presentations of histories of its many research programmes. A running theme in the papers was the role of Johan Hjort's Canadian Fisheries Expedition of 1914–1915 (Hubbard et al., in press). Hjort amply merited this recognition, as his contributions were foundational to Canadian fisheries biology and oceanography as focused scientific disciplines. The Canadian government had funded Canada's first permanent marine research facility in St Andrews in 1908, but the university-based volunteer researchers conducting summer investigations were capable of only a parochial treatment of fisheries issues. Few had any Maritime background, and while several biologists enthusiastically researched fisheries problems, they lacked the experience to create coherent or long-range research programmes. When, in 1914, the Biological Board of Canada requested Hjort to lead the Canadian Fisheries Expedition, the stated intent was to have this Norwegian scientist locate and identify herring “races” and assess the potential for exploiting existing and as yet unidentified stocks. The scientists' deeper agenda was to have Hjort train Canadian expedition participants in advanced fisheries research methods that he and others were developing under the auspices the International Council for the Exploration of the Seas. Indeed, they hoped to hire the 46-year-old “greatest living authority on fish and the fish industry” permanently (Macallum, 1914). Although this was not to be, Hjort's leadership of the Canadian Fisheries Expedition was indeed seminal in establishing a solid fisheries research programme in Canada, one that flourished for decades thereafter under the auspices of the Biological Board of Canada (after 1937, the Fisheries Research Board of Canada). Beyond this, Hjort instilled a culture of modernization within Canadian fisheries science, and his dynamic leadership led Canadian scientists to establish and develop contacts in Scandinavia and the United States, beyond traditional British imperial links. Hjort drew Canadian scientists into the international research network that he and other ICES scientists were nurturing as they developed the nascent discipline of fisheries biology. Hjort and the Backward Canadian Atlantic Fisheries Hjort led the Canadian Fisheries Expedition on the heels of publishing his seminal Fluctuations in the Great Fisheries of Northern Europe in 1914. In part he was building on earlier oceanographic studies: in 1910 he and Sir John Murray had used the S.S. Michael Sars—the research vessel of the Board of Fisheries in Bergen, Norway—to survey Northwest Atlantic waters. But when Hjort, who served as Director of the Fisheries Directorate in Bergen, requested the Norwegian government for a leave of absence in 1914, his stated aim was verifying his year-class theory of stock fluctuations beyond Eastern Atlantic waters. Adverse research conditions in Norway following the outbreak of the First World War, and Canadian government funding for the project, contributed to the Norwegian government's willingness to grant him this leave. Hjort arrived in October and carried out an energetic 2-month survey of fisheries and fish-processing practices. He travelled northward along the coast, starting from Boston, Massachusetts and visiting fishing ports in New Brunswick, Nova Scotia, the Magdalen Islands, and Newfoundland and Labrador. He collected scale samples to analyse the growth rings of samples from the fish catch, and thereby determine the age structure of the inshore fished populations; he observed working fisheries, examined local fishing gear, and talked to fishers and businessmen. Proceeding to Toronto, he remained until early January collating and analysing the samples and data thus obtained. His expenses for this preliminary work were covered by the Biological Board of Canada. Hjort was not impressed by primarily coastal or inshore nature of the fisheries, carried out through gillnets. He advised Canadian scientists and bureaucrats that Canada should develop an offshore driftnet fishery for herring that would at the very least provide the Grand Banks schooner fleet with much-needed bait for the cod fishery (Hjort, 1914a). From his preliminary survey, he recommended a full oceanographic expedition for the following year, while conducting experimental fishing using nets capable of catching a full range of age classes of herring and other fish. He proposed to discover “whether the sea off the coasts of Canada and Newfoundland has these immense riches yet untouched by the Canadian fishermen”, and thus if a new kind of herring fishery would be possible in Canadian waters (Hjort, 1914a). Hjort did not comment on the parallels he must have seen between the Canadian and Norwegian fisheries. While he was particularly distressed by the backward fish-processing techniques and poor quality of Canadian fresh and frozen fish, he would have found the levels of fishing technology familiar. Neither Norway nor the Canadian Atlantic had any significant industrialized fisheries until after the Second World War (Schwach and Hubbard, 2009). The fishers of both nations relied mainly on sail and traditional fishing methods. Perhaps because of their similarities, he thought he had some insights into how to improve the profitability of Maritime fisheries. About a third of his proposal was focused on using the expedition to train fishers in the use of a new, and patented, Norwegian fast-freezing method—the Ottesen method. Newfoundland fishers, he noted, waited until the first frosts to freeze herring, limiting supplies of this product as bait. He considered improving fish preservation by freezing “of the greatest importance for the establishment of an enlarged herring fishery” (Hjort, 1914a). Hjort promoted this idea with fishing industry leaders, and this proposal was strongly endorsed by the Halifax, N. S. Board of Trade (1914). The Department of Marine and Fisheries would have none of this, however. Hjort was so upset by the rejection of what he saw as an essential component of the whole programme that he almost cancelled the expedition (Hjort, 1914b). What Hjort failed to realize was that Norwegian and Canadian markets for fish were vastly different. In Norway the fisheries were an important component of the economy and the Norwegians relied heavily on seafood in their diet. In Canadian and US urban centres and inland markets, people had a low regard for sea protein, preferring the New World's affordable beef, pork, and chicken. The backwardness in fish handling that he witnessed was a product of this weak demand for fresh or processed fish, which meant that the major markets for Atlantic Canadian and Newfoundland dried and salted cod, and other pickled and smoked fish, were located in the West Indies and Brazil and South America, with some markets in Catholic European countries like Spain and Italy (Grant, 1934). There was a limited North American market for canned seafood, but these products were generally locally caught before canning and the Canadian product had problems that could not be addressed by fast-freezing methods. The Atlantic fisheries were not highly regarded as a source of wealth. Canadian fisheries officials were content to encourage the industry by training fishers to adopt the best practices of long-established methods; they believed that emergence from its primitive conditions would only come when the Maritime fishing industry adopted British industrial fishing technologies such as steam-powered vessels that would enable fishers to capture better quality offshore fish (Mills, 2009). In the meantime, Department of Marine and Fisheries officers gave Maritime fishers demonstrations of superior versions of traditional methods, such as Scottish smoke cures for salmon and haddock, or Norwegian methods for pickled herring. Since 1904 it had hired several experienced Scottish fisheries overseers to establish a voluntary programme to help Maritime fishers learn to make tightly coopered fish barrels and to train them in improved smoking, pickling, salt-cure and dry-cure methods (Hubbard, 2006). This programme made little headway. Unlike the conservative Canadian bureaucracy, Hjort was an ardent modernizer who demanded that fisheries science provide practical outcomes for the fishing industry. In Norway, he promoted new fishing methods and expanded the number of species exploited by Norwegian fishers, himself pioneering Norway's first shrimp fishery and developing a new net design to facilitate this (Søndergaard and Schwach, 2009). While Canada's Commissioner of Fisheries, Edward Ernest Prince (1858–1936), who was Chair of the Biological Board of Canada, and Archibald Byron Macallum (1858–1934), its Secretary Treasurer, both endorsed promoting the Ottesen fast-freezing method to fishers, the Department of Marine and Fisheries saw no value in this work, and flatly rejected it. Hjort continued to plead for his scheme, telling Prince: “I am convinced that an effort to solve the great actual practical questions must embrace their most important sides” (Hjort, 1914b). He contended that he could not carry out an expedition if it did not “correspond [...] to the lines expected by the supporters: the Board of Trade of Halifax. I do therefore prefer the scheme to be withdrawn to endangering the possibilities of the success of the expedition” (Hjort, 1914b). J.G. Desbarats, the Deputy Minister of Fisheries, turned a deaf ear to these pleas. Officials at the Department of Marine and Fisheries held fast to the English-speaking world's cultural opposition to commercial applied science (Lucier, 2012): fisheries science to determine the racial characteristics, demographics, geographical distribution, and fluctuations of commercial fish was “pure” and deserved support. But demonstrating new fish-processing methods for commercial ends, no matter how scientific the spirit, was not the proper role of scientists. Desbarats even squashed Hjort's later attempts to carry out in Halifax demonstrations of superior salt-cure methods (Hjort, 1915c, 1915e; Desbarats, 1915). Ironically, while Canadian civil servants were unimpressed by Hjort's practical approach to fisheries problems, he had the opposite impact on the scientists with whom he interacted. The Department of Marine and Fisheries gave an annual allocation to the Biological Board of Canada to run its Pacific and Atlantic Biological Stations, with no proviso other than that at least some of the volunteer scientists devote time to practical fisheries problems. Later, after the First World War, scientists at these stations began investigating fish-processing problems; in 1919 Archibald Patterson Knight (1848–1935) took on the problem of deterioration in canned lobsters, for example, developing improved canning methods he helped to disseminate among Atlantic Canadian lobster canners. Knight became the Board's Chair in 1921 and reoriented it in a more practical direction. Hjort inspired Archibald Gowanlock Huntsman (1883–1973), the young curator of the Atlantic Biological Station, to incorporate fish-processing problems into the station's programme; Huntsman, with the support of the Halifax Board of Trade, and Knight as the Biological Board's Chair, created a new research station in Halifax dedicated entirely to fish-processing issues. The Fisheries Experimental Station was inaugurated in 1924. A sister station for fish-processing research, the Fisheries Experimental Station (Pacific), was also established in British Columbia in 1924 (Hubbard, 2006; Stewart and Safer, 2005). Biological Board scientists took up this aspect of fisheries science too late to help Canadian troops in the First World War, who were condemned to rations of Canadian frozen fish—oozing water, with a cardboard-taste and texture—but they made great strides in improving Canadian products during the 1920s and 1930s. Huntsman himself took up the problem of fast-freezing fish so as to leave it in a near-fresh state once cooked: his “Ice Fillets” were a hit on the Toronto market in 1928, and beat Clarence Birdseye's development of a similar product to the market by 1 year. The Department of Fisheries, however, disallowed the scientists from marketing their product after the initial experiment, as it did not want to be seen as competing with private industry. Frozen fish remained a product before its time, however, until refrigeration technology became widespread after the Second World War. Huntsman, while developing flash-frozen fish, also addressed a problem he was encountering in existing refrigeration technology, and invented “jacketed cold storage”: this new freezer design sealed the coolant pipes behind steel plates, and became standard in North American railway refrigeration cars (Hubbard, 2006). Hjort, despite being thwarted in carrying out fast-freezing demonstrations, inspired a flowering of Canadian practical research to improve nets and gear and fish-processing techniques. The Department of Marine and Fisheries's opposition to his holistic programme proved to be no barrier to Hjort promoting the importance of this work to his receptive Canadian scientific hosts and disciples. Hjort and the Canadian fisheries expedition in 1915: biology and oceanography Hjort's 1910 and 1914 surveys had pointed to the possible existence of several herring races in the waters of Canada, New England, and Newfoundland. Once back in Norway in January 1915 he proposed to return to Canada to conduct a sea-going expedition in the waters between Newfoundland and the Atlantic Provinces and into the Gulf of St Lawrence. He outlined a number of questions: did growth rates vary in herring from different coastal waters, or by race? Did herring stock fluctuations mirror those of European herring? Where were exploitable concentrations of herring located? He would require two sea-going vessels equipped with Norwegian purse-seines and driftnets and other scientific equipment, to carry out a series of three hydrographic cruises, one each in May and June and a final cruise at the end of July and beginning of August; one ship would focus on the Gulf of St Lawrence, the other would make stations to the east of Nova Scotia, and north to Newfoundland. Both would search for spawning grounds and document growth, migrations, fish distributions, water conditions, plankton, etc. Each cruise was to follow the same course to enable comparisons of conditions (Hjort, 1915a). He wished to have the help of Dr Paul Bjerkan, Hjort's long-time assistant and collaborator, and of an experienced Norwegian herring captain, Thor Iversen, captain of the Norwegian Board of Fisheries' ship “Michael Sars” since 1902. These proposals were eagerly supported both by Prince and Macallum at the Biological Board and by Canadian fisheries technocrats. Individuals such as J.J. Cowie, the Chief Inspector of Fisheries, hoped that if the expedition found evidence for commercial concentrations of fish stocks in areas off Nova Scotia and between Newfoundland and the Maritimes, that the Maritime fishing industry would abandon its antiquated, traditional fishing techniques and develop offshore fishing capabilities using more efficient technologies (Mills, 2009). The quickly-approved Canadian Fisheries Expedition disappointed Hjort only in his inability to demonstrate superior fish preservation methods. Nevertheless, while in general the expedition accomplished its scientific objectives, there were several set-backs. The hydrographic equipment was delayed in arriving from Norway due to the war (Hjort, 1915b). The late arrival of spring and ice conditions led to a delayed start to the hydrographic and fisheries surveys, as did the death a commander of one of the survey ships (Hjort, 1915d). The primary vessels used were the Halifax-based Canadian Government Ship (CGS) Acadia—which the Canadian Hydrographic Survey had commissioned in 1913, and loaned to the expedition—and the Canadian Coast Guard steamer Princess, a former fisheries cruiser purchased in 1906. Princess was to be based out of the expedition headquarters in Souris, Prince Edward Island. Princess' commander, William Wakeham (1844–1915), an experienced Canadian fisheries inspector, had led several expeditions into the Hudson Bay beginning in 1897; acting for the Canadian government he had proclaiming Canadian sovereignty over Baffin Island and the Arctic Archipelago in 1897. Officially retired in 1909, he returned to duty at the Canadian government's request (Mimeault, 1998). Unfortunately, during the first cruise of Princess, he became seriously ill; refusing to end the work, in the end he collapsed, and the cruise was cut short to bring him home to the Gaspe (Hjort, 1915e), where he died on 20 May. Because of these delays and set-backs, only two of the proposed cruises for the Gulf of St Lawrence were carried out. The cruises were staggered: Princess had begun its aborted trip in the Gulf of St Lawrence on 10 May. Hjort embarked on the Acadia on 29 May for a fast survey that ended on 4 June. Princess conducted its first proper survey from 9 to 15 June, followed by Acadia's second cruise from 21 to 29 July. Finally Princess's second cruise was from 3 to 12 August. Additional information and samples were gathered by the Canadian government's herring “steam drifter” 33 which conducted experimental fishing in the Gulf of St Lawrence. James Playfair McMurrich supervised a 10-day expedition on the Biological Board's small research vessel, Prince, in the Bay of Fundy. Altogether, Acadia and Princess made 162 stations (Figure 1), and Prince made 9 stations. Hjort (Figure 2, with Acadia's Captain Robson to his right) assisted by Canadian and Norwegian scientists, measured hydrographic conditions and took samples of water, plankton, food fish eggs, and larvae, in the hopes of linking local oceanographic features with fish productivity. With Hjort's leadership, this was the first such work conducted under Canadian auspices, involving Canadian scientists, in Canadian waters. Hjort directed the initial preparation and collation of samples at the two-story wooden house set up as a laboratory in Souris, Prince Edward Island. His assistant Paul Bjerkan titrated water samples to determine salinities, using standard water samples from the ICES Central Laboratory in Copenhagen to calibrate the measurements. Huntsman and Dr Arthur Willey (Chair of the McGill University zoology department) did preliminary work on the plankton and fish eggs samples, but Hjort found the equipment in the temporary lab to be too primitive for its successful completion (Hjort, 1915f). The preserved biological material was mostly worked up by Canadian and Scandinavian scientists in university and fisheries biology laboratories after the expedition's completion. Figure 1. Open in new tabDownload slide Hjort and Captain Robson aboard Acadia, Canadian Fisheries Expedition 1915. Figure 1. Open in new tabDownload slide Hjort and Captain Robson aboard Acadia, Canadian Fisheries Expedition 1915. Figure 2. Open in new tabDownload slide Cruises and stations of Princess and Acadia, May–August 1914. Figure 2. Open in new tabDownload slide Cruises and stations of Princess and Acadia, May–August 1914. The Canadian Fisheries Expedition's final report had a tortuous preparation and was not published until 1919, after the war, as materials and drafts had to criss-cross the Atlantic. Challenges arose in part because it was prepared by a combination of Norwegian experts and two Canadian neophytes. Huntsman wrote two of the nine “memoirs”, one on herring growth in the Bay of Fundy and one on a quantitative and qualitative study of eastern Canadian plankton. Willey prepared a report on the copepods obtained in the Gulf of St Lawrence and adjacent seas. Unfortunately, an American participant, James Mavor, could not complete his cod growth studies before the 1919 report was published. A glaring flaw in the publication is that each report was seemingly prepared without knowledge of information in other reports, and Hjort failed to synthesize the material in his overview. The expedition had used methods developed by plankton expert H.H. Gran of the King Frederik's University in Kristiania (Oslo), and the material was turned over to him for analysis. He wrote the report on the productivity of Gulf of St Lawrence and adjacent waters. Hjort turned over the herring year class and population structure work to his assistant Einar Lea, although he did assist Lea in examining scale rings to measure the age of the fish sampled, and taking biometric measurements to distinguish different herring races. Lea wrote the report. Fish egg and larvae samples were handed to Alf. Dannevig, Hjort's colleague who managed the Flødevigen Utklekningsanstalt fish hatchery in Norway. Dannevig's ‘memoir’ on this subject was probably among the most puzzling of the contributions. While the samples indicated billions of cod eggs and other gadoid eggs being present in the Gulf of St Lawrence, there were very few larvae of these species. For Hjort this raised a problem: why would so many cod spawn in a region in which billions of eggs would be doomed for destruction? With no material from other years for comparison with the 1915 samples, he could not determine if this was an anomaly, but the questions raised certainly showed the urgent need for more surveys and sampling (Hjort, 1919). For the hydrographic work, no Canadian was competent to analyse the samples and data or write the report. Therefore, Paul Bjerkan reported on hydrographic observations and salinities, while J.W. Sandström, a Swedish pioneer of the new dynamic oceanographic approach that later revolutionized physical oceanography in the twentieth century, reported on the region's currents, water movements, and hydrography. His report included a 46-page introduction to the new dynamic oceanography that, according to historian of oceanography Eric Mills, he intended to serve as a basic training manual for Canadian oceanographers (Mills, 2009). Einar Lea's “Report on the ‘Age and Growth of the Herring in Canadian Waters’” similarly began with a 39-page discussion of Lea's scale-ageing methods, also most likely intended to proselytize the methods developed by ICES scientists and to serve as a beginner's manual for Canadian scientists interested in using these methods (Hubbard, 2006). The consequences for Canadian fisheries science Perhaps Hjort's most important objective in undertaking the Canadian Fisheries Expedition was to introduce ICES-style fisheries biology to Canada; this truly international expedition—with the above-mentioned experienced professional participants from Norway and Sweden assisting those from Canada and the United States—served as an intensive training course for the North American participants, whose approach until then resembled natural history studies of the nineteenth century. The Canadian participants, who in effect became Hjort's students in an intensive fishery biology “course”, included Huntsman and McGill University embryology professor Dr Arthur Willey (who much earlier completed his doctorate under the tutelage of E. Ray Lankester), and University of Toronto anatomy professor James Playfair McMurrich (who later became Chair of the Biological Board of Canada). His American collaborator and student was James W. Mavor, a Harvard graduate who served as Atlantic Biological Station curator in 1913 and 1917, and who soon after the expedition became a professor at Union College in Schenectady, New York. After the expedition, Mavor worked on problems of fish growth and hydrography during summers at St Andrews, abandoning his earlier parasitology research (Hubbard, 2006). Among the quantitative methods Hjort introduced were those developed in the previous 15 or so years by German scientists: Dr Friedrich Heincke's approach to distinguish fish races using biometric measurements such as fin ray counts, vertebrae counts, and other measures; C. Hoffbauer's method of counting growth rings on scales to determine fish age; Johannes Reibisch's use of vertebrate and otolith growth rings for the same purpose; and his own use of a combination of these, in tandem with fisheries statistics, fish population vital statistics, and studies of fish migration. His educational goal was a familiar one for Hjort. As a scientist from a small nation, Hjort shared the eagerness of other Norwegian natural scientists to participate in Scandinavian and international collaborative research, as the quality of their science was highly dependent on their ability to partake in exchanging data and discussing, presenting, and diffusing their results internationally. Through ICES, Norwegian marine scientists could rapidly spread their methods, new instruments, and results from ongoing research; they also organized annual 2-month courses in Bergen from 1903 until 1913, and trained roughly 175 participants (Schwach, 2000). Hjort's most important Canadian student was Huntsman (Figure 3), who until his first encounters with Hjort in November, 1914, had made ascidian taxonomy his research focus. Huntsman, newly appointed as the Atlantic Biological Station's first permanent curator—and who was in 1916 to become its first full-time director—was chosen by Prince and Macallum to assist Hjort in working up the scale samples from Hjort's travels from New England to Newfoundland. Huntsman immediately spied a flaw in this method—and exasperated Hjort by pointing out that “the scales could not be growing proportionately to the whole fish, since in the small herring, of which [he] … had one preserved in a bottle, the scales did not touch each other, while in a large herring, they overlapped greatly” (Huntsman, 1951). Annoyed, Hjort declared Huntsman unfit to work with scales; Huntsman nevertheless became Hjort's primary Canadian assistant during the 1915 expedition. Hjort switched Huntsman to counting vertebrae and studying plankton, and introduced Huntsman to the basics of European fish population analysis, plankton studies, and hydrography, the main components of ICES research. Despite their initial clash, both held each other in great respect and corresponded on various issues for the rest of Hjort's life. His encounter with Hjort led Huntsman to abandon ascidian taxonomy and embrace all aspects of fisheries biology. Within 3 years after the expedition, he published articles on methods in fisheries biology (Huntsman, 1918a), hydrography (Huntsman, 1918b), and the fish scale method—with proposed improvements (Huntsman, 1918c). He also published the world's earliest mathematical model of showing the effects of fishing on fish populations size and age structure (Figures 4 and 5). His graph showed the shrinking numbers of older year classes, and comparative expansion of young fish in fished populations (Huntsman, 1918d). Unfortunately, this analysis appeared in the Biological Board's first Bulletin, directed at fishers, and escaped wider scientific attention at that time. Nevertheless, fisheries biologist and historian Tim. D. Smith believes that Huntsman's ideas influenced W.F. Thompson's epochal work for the Pacific Halibut Commission in the 1920s and 1930s (Smith, 1994), and his re-analysis of this material in the late 1940s had important influences on later theory of fishing population models (see Hubbard, in press). Huntsman continued to teach during the fall and winter as a tenured professor at the University of Toronto after being hired as the Biological Board of Canada's first full-time fisheries biologist and director of the Atlantic Biological Station in 1915. Although he was not paid by the University of Toronto, his position there enabled him to train a generation of Canadian graduate students as fisheries biologists; Hjort, through Huntsman, was therefore instrumental in the new discipline's emergence as a leading scientific sector in Canada. Figure 3. Open in new tabDownload slide Archibald Gowanlock Huntsman, the Canadian scientist who adopted Hjort's and ICES’ methods and who trained subsequent generations of Canadian fisheries biologists and promoted Canadian oceanography. Figure 3. Open in new tabDownload slide Archibald Gowanlock Huntsman, the Canadian scientist who adopted Hjort's and ICES’ methods and who trained subsequent generations of Canadian fisheries biologists and promoted Canadian oceanography. Figure 4. Open in new tabDownload slide Huntsman's graph showing the age structure of unfished plaice populations in three regions around the Maritime Provinces. Figure 4. Open in new tabDownload slide Huntsman's graph showing the age structure of unfished plaice populations in three regions around the Maritime Provinces. International networks Beyond the lasting changes that Hjort wrought through launching the new ICES-developed version of fisheries research in Canada, his enthusiasm for the project had another vital outcome, in the shape of the many lasting linkages he forged between American, Canadian, and Norwegian scientists. One of these connections was an accident of war. Wartime hostilities delayed the Atlantic crossing of Captain Iversen and the Norwegian hydrographic and fisheries equipment. Hjort, searching for alternative gear, turned to Dr Henry B. Bigelow (the future founding director of the Woods Hole Oceanographic Institution), who was then engaged in hyrographic and fisheries investigations in the Gulf of Maine for the United States Bureau of Fisheries. His gear was housed at Harvard University between research seasons, and Hjort, accompanied by his wife, set off to meet Bigelow and arrange to have the gear sent north. Tremendously impressed by Bigelow, he lingered for a few days to learn about conditions off Nova Scotia, which had been the focus in 1912 and 1913 of hydrographic surveys—including the earliest American quantitative plankton sampling, using Victor Hensen's methods—by Bigelow and the US Bureau of Fisheries (Hubbard, 2006). Bigelow's and the Biological Board's resulting mutual awareness was to blossom into close ties in the early 1920s, when Huntsman helped instigate the formation of the North American Council on Fisheries Investigations (NACFI); and Bigelow and Huntsman both served as scientific representatives and officers for this organization. Huntsman and Bigelow had many arguments about oceanography and fisheries science in their resulting spirited correspondence, and a lifelong friendship arose. Hjort also had to call upon other Norwegian and Swedish scientists to help write the reports, as Canada at that time lacked experts capable of preparing reports according to the latest methods. New dynamic oceanographic methods had been developed in Norway by Vilhelm Bjerknes (1862–1951), and made practical by Bjørn Helland-Hansen (1877–1959) and Johan Sandström (1874–1947). Therefore, Bjerkan, Hjort's assistant, and Sandtröm were brought in to report on the Canadian Fisheries Expedition's hydrographic work. Hjort also appointed the professor of botany at the University of Oslo, Haaken Hasberg Gran (1870–1955), to work up and report on the plankton collections. Huntsman and Bigelow in the early 1930s were to hire Gran and his student, Trygve Braarud (1903–1985) as his assistant, to come to St Andrews and work as plankton experts for the International Passamaquoddy Fisheries Commission in 1931 and 1932—a scientific commission appointed by NACFI for the Canadian and US governments to determine the environmental effects of building hydroelectric tidal-power dams between Passamaquoddy Bay and the greater Bay of Fundy. Hjort, then, through his dynamic and extrovert personality, forged ties between Canadian, American, and Scandinavian scientists who were to influence the course of fisheries biology. His influence in Canada, in this respect, was especially important as it drew Canadians beyond their traditional British, and occasionally American, scientific role models and into a wider international community. Conclusion Unfortunately for the Canadian government, poor economic conditions, not lack of fish, were holding back the fisheries' economic development: the Canadian Fisheries Expedition was a complete failure if measured by its immediate consequences for the Canadian Atlantic fisheries. For Hjort, one of the great rewards from leading the Canadian Fisheries Expedition was having his year-class theory further vindicated. The survey's experimental fishing and sampling revealed strongly dominant year classes: in the waters off Newfoundland, as in North Atlantic waters closer to Europe, this was the 1904 year class. One finding particularly pleasing to Hjort was that each of the four “races” or distinct groups of herring identified seemed to have a unique pattern of year-class abundance, reinforcing his theory that there were different “tribes” of herring; the 1903 and 1908, 1909–1910 year classes dominated in herring in Nova Scotian and Bay of Fundy waters. For Canadian fisheries biology, the Canadian Fisheries Expedition's results were dramatically more important. In the wake of this expedition, several researchers, especially Huntsman, were motivated to adopt the ICES approach to fisheries studies, though limited by small research vessels and limited equipment and funding. Huntsman was profoundly influenced by the demonstrated importance of studying oceanographic conditions to understand how these affect fish populations. It was due to his insistence and persistence that Canada's first full-time oceanographer, Harry B. Hachey, was hired to work at the Atlantic Biological Station in 1928 (Mills, 2003). Huntsman led several smaller expeditions in the Bay of Fundy, Annapolis Basin, the Miramichi estuary on the Northern New Brunswick coast, and Gaspé region during the following years (Figure 5). These culminated in one major international expedition, the Strait of Belle Isle Expedition, in 1923, under the auspices of NACFI, with British, American, and French participation. As increasing numbers of Canadian researchers and even some US researchers fell under Huntsman's sway, the stamp of ICES fisheries research was apparent in the annual and long-term research programmes being fielded by the Biological Board of Canada, reflected in the organization's name change to the Fisheries Research Board of Canada in 1937. International networks were formed as scientists across the Atlantic and across nations sought to investigate and understand the resources of the borderless oceans. Hjort and his Canadian Fisheries Expedition transformed, permanently, Canadian fisheries biology and oceanographic science and made it a part of a global marine science enterprise that he also helped to create. Figure 5. Open in new tabDownload slide Huntsman's graphical representation of the effects of fishing on Maritime plaice populations. Figure 5. Open in new tabDownload slide Huntsman's graphical representation of the effects of fishing on Maritime plaice populations. References Desbarats G. J.. , 1915 Letter to J. Hjort, 6 May 1915. Libraries and Archives Canada, RG 23 Vol. 1204, File 726-2-4 [1] Grant R. F.. , The Canadian Atlantic Fishery , 1934 Toronto Ryerson Press (pg. 17 - 23 ) Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Halifax, N. S. Board of Trade , 1914 Resolution. 1 December. Libraries and Archives Canada, RG 23 Vol. 1204, File 726-2-4 [1] Hjort J.. , 1914a Letter to A.B. Macallum, 25 November. Libraries and Archives Canada, RG 23 Vol. 1204, File 726-2-4 [1] Hjort J.. , 1914b Letter to E.E. Prince, 31 December. Libraries and Archives Canada, RG 23 Vol. 1204, File 726-2-3 [1] Hjort J.. , 1915a Atlantic Herring Investigations. Details of Scheme. 16 March 1915. 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Fra fisheriundersøkelser til et havforskningsinstitutt [The Sea, the fish and the science. From fishery investigations to an institute for marine research] , 2000 Bergen Havforskningsinstituttet/Grieg grafisk produksjon (pg. 116 - 121 ) Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Schwach V., Hubbard J.. Johan Hjort and the Birth of Fisheries Biology: the construction and transfer of knowledge, approaches and attitudes, Norway and Canada, 1890–1920 , Studia Atlantica , 2009 , vol. 13 (pg. 22 - 41 ) Google Scholar OpenURL Placeholder Text WorldCat Smith T.. , Scaling Fisheries: the Science of Measuring the Effects of Fishing 1855–1955 , 1994 Cambridge, MA Cambridge University Press (pg. 205 - 208 ) Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Søndergaard M. K., Schwach V.. 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Johan Hjort's impact on fisheries science: a bibliometric analysisAksnes, Dag W.; Browman, Howard I.
doi: 10.1093/icesjms/fsu147pmid: N/A
We analyse how Johan Hjort's publication, “Fluctuations in the great fisheries of northern Europe, viewed in the light of biological research” (Hjort, 1914), has been cited in the subsequent scientific literature. In the context of this special issue commemorating the 100th anniversary of Hjort's seminal publication, our objective is to provide insights into how his work has penetrated the literature and influenced the development of fishery science. We also tracked Hjort's related article, “Fluctuations in the year classes of important food fishes” (Hjort, 1926). We present the citation life cycles of these articles and analyse various characteristics of the publications that cite them. The importance of Hjort (1914) is reflected in the large number of citations that it has accrued (908), and by the 40–50 citations that it continues to receive every year. This is exceptional for a 100-year-old scientific article, in any field. Hjort (1926) initially received as many cites as Hjort (1914), but the latter subsequently became the paradigmatic article. Hjort (1914) has been cited in 162 different journals and by scientists in 53 countries—Hjort's work has had a broad and global impact on fisheries research. The contextual analysis demonstrated that Hjort (1914) is considered a seminal, novel, and paradigm setting study—the core research questions addressed by Hjort (1914) remain unsolved and several of his hypotheses continue to drive fisheries science to this day.
Autumn bloom phenology and magnitude influence haddock recruitment on Georges BankLeaf, Robert T.; Friedland, Kevin D.
doi: 10.1093/icesjms/fsu076pmid: N/A
The haddock (Melanogrammus aeglefinus) stock on Georges Bank in the Northwest Atlantic is characterized by extremely large recruitment events relative to spawning-stock biomass. Recent work has indicated that the dynamics of the preceding autumn bloom may have explanatory power to describe these events. In this paper, we examine the hypothesis that autumn phytoplankton dynamics affect the recruitment of haddock, examine the temporal and spatial characteristics of the autumn phytoplankton bloom on Georges Bank, and correlate individual sex-specific condition measurements of haddock made in spring to recruitment patterns. Autumn bloom characteristics vary considerably across Georges Bank with earlier-occurring and larger-integral blooms occurring on the northern flank. On average, autumn blooms start on day 273 (29 September) and persist ∼50 days. There was a significant negative correlation detected between bloom start date and recruitment and a significant positive correlation of bloom integral and recruitment. The survivor ratio loge(R/SSB) was positively and significantly correlated with individual condition of females in spring. The analysis of autumn bloom on Georges Bank provides a predictive index for recruitment strength of haddock and has utility for the assessment of this stock.
North Sea herring (Clupea harengus L.) recruitment failure may be indicative of poor feeding successLusseau, Susan Mærsk; Gallego, Alejandro; Rasmussen, Jens; Hatfield, Emma M. C.; Heath, Mike
doi: 10.1093/icesjms/fsu070pmid: N/A
Recruitment of the 2002–2012 year classes to the North Sea herring stock has been below expectations given the spawning biomass, due to exceptionally low overwinter survival of larvae. Here, we investigate whether changes in survival of larvae in the northwestern North Sea could be attributed to changes in parasite prevalence or feeding conditions. We used a method that combined particle tracking models and survey data to estimate survival, and microscopic examination of gut contents of archived samples of larvae collected in February each year between 1995 and 2007 to investigate parasite prevalence and feeding. We deduced that we can use the incidence of tetraphyllidean parasites as an index of the cumulative feeding history of the larval population. We found that the prevalence of larvae of a tetraphyllidean cestode in the gut contents varied significantly between years and was positively correlated with feeding success. High feeding success, indicated by high prevalence of tetraphyllideans, influenced survival by offsetting the effect of a second parasite type, a digenean trematode. We suggest that variability in cumulative food intake over the lifespan up to February is a significant determinant of variability in survival.
Poor taxonomical knowledge of larval fish prey preference is impeding our ability to assess the existence of a “critical period” driving year-class strengthRobert, Dominique; Murphy, Hannah M.; Jenkins, Gregory P.; Fortier, Louis
doi: 10.1093/icesjms/fst198pmid: N/A
Despite 100 years of research testing the link between prey availability during the larval stage and year-class strength, field-based evidence for Hjort's “critical period” hypothesis remains equivocal. Here, we argue that a minority of past studies have relied on sufficient taxonomical knowledge of larval fish prey preference to reveal the potential effects of variability in zooplankton prey production on larval vital rates and year-class strength. In contrast to the juvenile and adult stages, larval fish diet and prey field are often poorly resolved, resulting in the inclusion of zooplankton taxa that do not actually contribute to the diet as part of the prey field considered by fisheries scientists. Recent studies have demonstrated that when accounting for prey selectivity, the expected positive relationships between preferred prey availability and larval feeding success, growth and survival are revealed. We strongly recommend that laboratories conducting research on larval fish trophodynamics take prey selectivity into account and acquire the necessary taxonomic expertise for providing valid assessments of the influence of prey availability on larval vital rates. We make the prediction that the proportion of studies supporting the existence of a “critical period” will increase proportionally to the progress of knowledge on prey preference during the early larval stage.
Making use of Johan Hjort's “unknown” legacy: reconstruction of a 150-year coastal time-series on northeast Arctic cod (Gadus morhua) liver data reveals long-term trends in energy allocation patternsKjesbu, Olav Sigurd; Opdal, Anders Frugård; Korsbrekke, Knut; Devine, Jennifer A.; Skjæraasen, Jon Egil
doi: 10.1093/icesjms/fsu030pmid: N/A
Abstract Hidden within the seminal 1914 publication by Johan Hjort, we find what is probably one of the first comprehensive teleost time-series ever published. The series is liver size and fat content of northeast Arctic (NEA) cod measured during the traditional winter fishery in Lofoten, Northern Norway, in 1880–1912 and 1883–1913, respectively. The data were collected well before the advent of the great industrialized fisheries in the 1930s. The raw data used by Hjort originate from annual reports of the Lofoten fishery, initiated by Member of Parliament and pioneer fishery inspector of Northern Norway, Ketil Motzfeldt, in 1859. Based on these reports and following various calibration exercises, we present robust estimates of the hepatosomatic index (HSI) from 1859 to 2012 (except 1863), i.e. over 153 years—extending Hjort's analysis both backwards (1859–1879) and forwards (1913–present). This series of bulk HSI contained five major periods: 1859–1880, 1881–1919, 1920–1974, 1975–2003, and 2004–2012; the highest HSI was recorded 1920–1974, whereas the lowest was from the most recent period. Despite variability, total length was a significant predictor of HSI, 1932–2012. A weak but significant relationship existed with both total-stock biomass and ocean temperature, as well as with the North Atlantic Oscillation winter index under a 1-year lag. The present exceptionally long HSI series will give an excellent opportunity for further research on the “quality of the cod” in a historic perspective. Introduction The importance of Johan Hjort's pioneering efforts for the development of marine biology generally and fisheries biology especially can hardly be overstated (Sinclair, 1997; Houde, 2008). Today, his main legacy includes “the critical period hypothesis” for first-feeding larvae, drift (advection) of early life stages including mortality, the formation of strong and weak year classes, spawning migration routes, and finally, stock variability linked to ecological conditions. His main species of interest were Atlantic herring (Clupea harengus) and Atlantic cod (Gadus morhua). Above all, his seminal book “Fluctuations in the Great Fisheries of Northern Europe Viewed in the Light of Biological Research” (Hjort, 1914) stimulated research all over the world and remains integral to modern fisheries management, i.e. this ICES volume is still frequently cited 100 years after its release. Perhaps less known is the fact that Hjort showed one of the first, if not the first, comprehensive time-series on a marine fish with his presentation of data on commercial liver landings of northeast Arctic (NEA) cod from the Lofoten area, the largest coastal fishery in Norway, in the period from 1880 to 1912. The corresponding fat content was also reported for the years 1883–1913. These efforts should not be considered an original approach, since several of his contemporaries were completing similar studies of annual variations in biological traits, e.g. the fat content in Atlantic herring and European sprat (Sprattus sprattus; see figures and references in Hjort, 1914). What was novel was the markedly longer length of his established time-series compared with others that existed in this period and that he placed his findings within the context of population dynamics. However, Helland-Hansen and Nansen (1909) were apparently the first to put up an ecological framework by relating “physical conditions” (ocean temperature) with “biological conditions”, here studying a limited subset (1899–1906) of the same liver (and roe) data as used by Hjort (1914). Today, time-series analyses are essential in a broad range of monitoring programmes and analytic assessments, but also to disentangle and show complex causal links, like that of climate (e.g. Ottersen et al., 2010; Petitgas et al., 2013) and fisheries-induced evolution (e.g. Rijnsdorp, 1993; Heino and Godø, 2002) on teleost traits. Several studies on the monthly resolved Russian NEA cod liver data (1927–present) from the Barents Sea (Sandeman et al., 2008; Yaragina, 1996, 2010), as well as other related studies, including experimental (Skjæraasen et al., 2009), have provided a large amount of knowledge of factors affecting this stock's investment in liver energy storage. In particular, the close link between relative liver size (hepatosomatic index; HSI) and liver energy content (Lambert and Dutil, 1997; Skjæraasen et al., 2010), but also with the abundance of the main prey, Barents Sea capelin (Mallotus villosus), as well as environmental temperature (Sandeman et al., 2008) stand out as important (Marshall et al., 1998). However, as the earlier part of the Barents Sea liver data (1927–1966) is incomplete or grouped by fish weight instead of length, Sandeman et al. (2008) restricted their statistical analyses from 1967 onwards. Hjort was mainly motivated by the importance of the liver as a commercial product in its own right, but also by the association between liver size and “the quality of the cod”, or more specifically, “its condition in point of nourishment” (sic) (Hjort, 1914). Condition is here analogous with “the percentage in volume of the oil”. The main finding was, in his own words, “the remarkable cyclicity of liver landings”, which was accompanied by a similar co-variation in liver fat content (Figure 1). In this article, we revisit Hjort's original time-series and supplement his data with both newer and older data on liver landings (Figure 2). The existence of older, similar data (1859–1879) was somewhat unexpected because there is no specific mention of them in Hjort (1914). The primary source of data was the yearly reports and catch statistical time-series from the Lofoten fisheries (e.g. the Official Fisheries Statistics). Their origin can be traced back to the onset of a government initiated regulation of fisheries in Northern Norway, passed as an amendment to the existing Law of Lofoten (from 1816) in 1858. The intent of the amendment was to shift regulatory power from private proprietors to federal authorities. A significant political advocate for the making and passing of this amendment was Member of Parliament, Ketil Motzfeldt, who, in the following year, became the first Fishery Inspector of Northern Norway and initiated what would become the regular status report series of the Lofoten fisheries, although named differently over time (Anon, 1859–2012). Hence, Hjort could access annual and seasonal information from “the Fisheries Inspectors telegraph” on the “average quantity” of “skrei” and the corresponding amount of liver (and occasionally roe; Hjort, 1914). “Skrei” is from old Norse and means to move or to travel, cf. the long spawning migration route of NEA cod from the Barents Sea to the Norwegian coast. The report series, including catch statistics, was primarily intended as a bookkeeping system for social costs and services, as well as, for example, commercially relevant parameters such as weekly turnover, landings, production, and bait prices. In its original form, the reports included no account of biological or ecological aspects. Its biological negligence is exemplified by the common gauge for “quality” being the number of cod required to fill a barrel with the liver. Naturally, Hjort was bound to the same coarse metrics as applied there, i.e. bulk volumetric landings of the liver (initially number of 116 l barrels and later hectolitres), and total number of landed cod (Figure 2). Since Hjort (1914) also contains records of body weights, the “bulk HSI”, a term used by us, could be estimated. Figure 1. Open in new tabDownload slide Redrawn plot of Hjort's Figure 107 (Hjort, 1914) showing hectolitres of liver per thousand fish (dark circles) and the corresponding liver fat content (grey circles) for northeast Arctic cod in the Lofoten fishery, 1880–1912 and 1883–1913, respectively. Figure 2. Open in new tabDownload slide Overview of data sources from the annual Lofoten cod fishery and research monitoring programme. Upper panel shows Fisheries Statistics data of the relative amount of liver, including the data consulted by Hjort (1914), presented either in litre of liver per thousand fish or litre of liver per kilo gutted weight, the recent Råfisklaget series, reporting kilo of liver per kilo gutted weight, and the research survey data, reporting kilo per kilo whole weight. Lower panel shows supplementary data sources on gutted weight and total length. The primary task of our work was to expand as far as possible Hjort's liver data both backwards and forwards in time in a coherent way to obtain (i) a better insight into the “condition” of NEA cod at the time of his seminal research, and (ii) a long-term proxy of the dynamics of liver size and thereby energy allocation patterns in this stock. In the analysis, we opted for HSI as the universal expression of investment in liver size vs. body size. We consulted recent publications on the relationship between fat content and HSI, as well as fisheries-independent annual values on the mean HSI, to ground-truth as much as possible the present series on bulk HSI. Finally, we examined the whole time-series in terms of general trends and shorter oscillations, concentrating on investigations into broad mechanisms that might be responsible for the observed patterns in HSI. Material and methods General overview Commercial landings Commercial landings of NEA cod were restricted to be from within the same geographical area during the spawning season, i.e. the Lofoten area. This defines the main spawning time and ground of this major gadoid stock. Immature fish and fish that skip spawning were unaccounted for because they rarely undertake such migrations to the Norwegian coast and therefore remain in the Barents Sea feeding area (Trout, 1957; Jørgensen et al., 2006; Yaragina, 2010; Skjæraasen et al., 2012). Some large immature specimens might, however, show extended winter migrations to the coast, i.e. so-called “dummy runs”, and thereby appear close to the spawning ground (Trout, 1957; Woodhead and Woodhead, 1965). The main part of the data were from the long-running report series established by the Norwegian authorities in 1859, initially named “Om Lofotfiskeriet”, but renamed “Lofotfiskeriet” in 1879, “Lofotfisket” in 1922, and then “Melding fra utvalgsformannen for Lofotfisket” in 2000. However, this report series discontinued their account of landed quantities of the liver in 1990 and data for the latter period (1991–2012) was therefore obtained through Norges Råfisklag (http://www.rafisklaget.no/), commonly called “Råfisklaget” (Figure 2). Råfisklaget is the largest fishers' sales organization in Norway, administrating, among other tasks, all catches and catch statistics of cod from local landing ports under strict governmental laws and regulations. Research survey data A fisheries-independent liver series of NEA cod, established as part of the Institute of Marine Research (IMR) statutory acoustic spawning migration survey in the Lofoten area in March–April 1997–2013, was included to be contrasted with the corresponding commercial series in overlapping years (Figure 2). Whole body weight and liver weight were measured onboard to the nearest gramme using a motion compensated balance. Bulk measures from the Lofoten fishery Data presented in the yearly Official Fisheries Statistics (Anon, 1859–2012), hereafter referred to as the Fisheries Statistics, including those of Hjort (1914), were collated from bulk measures of landed cod and liver during the Lofoten fishery. To establish a coherent extension of Hjort's original time-series, the same source was consulted for 1859–1990, whereas after 1990, analogous data had to be obtained from landings data recorded by Råfisklaget (Figure 2). For the earlier period, the Lofoten area was defined by the principal communities used in the Fisheries Statistics. These included Flakstad, Moskenes, Vestvågøy, Værøy, Vågan, Røst, and Lødingen. Only NEA cod caught in the period of the Lofoten fishery, i.e. January to April, were considered. For total landings of NEA cod, the Fisheries Statistics denote numbers of landed individuals (thousands) from 1859 to 1937 (Figure 2). In an overlapping period from 1929 to 1937, total landings were recorded both in numbers and in tonnes gutted weight, whereas after 1937, total landings were only available in tonnes gutted weight (Figure 2). Here, gutted weight excludes the head, guts, roe, and liver. Liver quantities before 1881 were logged as the number of barrels (á 116 l), whereas from 1881 to 1990, total quantities were expressed in hectolitres (100 l). The statistics from Råfisklaget used for the remaining period (1991–2012) were given in tonnes, both for the amount of cod liver and gutted weight. Standardization of commercial Lofoten data Hjort's (1914) original time-series on the amount of landed liver of NEA cod (1880–1912) used hectolitres/1000 fish (Figures 1 and 2). This was a convenient measure at the time because catch statistics of liver landings were recorded in volumetric units and fish in numbers. However, when extending the time-series forward in time, we found that the Fisheries Statistics switched to cod landings in gutted weight, not numbers, and this practice continued with Råfisklaget. We believe that it is more biologically meaningful to divide liver size by total body weight, i.e. to adopt the common HSI (see formal definition below). From fish numbers to weight For the period when gutted weight was available together with the amount of liver collected (1929–2012; Figure 2), gutted weights were multiplied by 1.5, which is the common conversion factor used to calculate total (“round” or whole) weight from gutted weight in the Norwegian cod fisheries (http://www.fiskeridir.no/fiske-og-fangst/omregningsfaktorer). For the earlier period (1859–1928), only numbers of landed cod were available in combination with the liver data. However, for the larger part of this period, matching information on fish size was found in Rollefsen (1953), who presents official catch statistics of mean gutted weight of commercially landed NEA cod in Lofoten from 1883 to 1953. Hence, numbers of cod could be converted to total weight in the period 1883–1928 using the corresponding data in Rollefsen (1953; Figure 2). However, for the years 1859–1882, data on cod size were unavailable and a proxy of bulk HSI was estimated from a linear regression (see Section “Turning hectolitres of liver into HSI”) based on the period where data for both the number of fish and mean gutted weight were available (1883–1937). From liver volume to weight While data on liver landings from Råfisklaget (1991–2012) were presented in weight, the Fisheries Statistics (1859–1990) used volumetric measurements (Figure 2). To calculate HSI, liver volume had to be converted to liver weight. The specific density of a liver will vary due to variations in its content of fat, water, and protein, with the latter constituent exhibiting less variation (Lambert and Dutil, 1997; Skjæraasen et al., 2010). A liver containing no fat is expected to have a specific density of ≈1 g ml−1, i.e. only water and minor amounts of protein, whereas a liver containing only fat would have a specific density of ≈0.9 g ml−1, i.e. only fat and minor amounts of protein. In reality, neither extreme is likely (e.g. a fat liver will also contain some water) and the range of possible density values is therefore limited. We used a specific density of 0.96 g ml−1 for all years in question based on the available liver proximate composition data on captive spawning individuals of cod in moderate to good condition (Kjesbu et al., 1991). Hence, liver weight was estimated as 0.96 × liver volume. Turning hectolitres of liver into HSI For the period 1883–2012, the standard formula used to estimate the bulk hepatosomatic index (HSIBulk) was: HSIBulk=100×totalamountoflivertotalamountoffish,(1) where both the denominator and the numerator are the measures of mass presented in kg. For the earliest part of the Fisheries Statistics time-series (1859–1882), where systematic information on NEA cod body size was lacking, we applied a somewhat different procedure to get HSIBulk. Because there exists an overlapping period in the Fisheries Statistics (1883–1937) where liver quantities are available in both l/1000 fish (denoted as Hectolitres1000 fish) and l/kg gutted fish (Figure 2), we utilized the linear relationship between these two measures (Figure 3) to estimate HSIBulk for the earliest period without fish weight (1859–1882): HSIBulk= 2.40+1.236×Hectolitres1000fish,(2) where radjusted2=0.89 (d.f. = 54 and p < 0.0001). Within this particular period, observed values of Hectolitres1000 fish ranged from 2.00 to 4.22 (Figure 3). For the sake of readability, HSIBulk will from here on be referred to only as HSI, or bulk HSI if necessary to avoid confusion with individual HSI. Figure 3. Open in new tabDownload slide Linear regression between the measured amount of hectolitres of liver per thousand fish vs. the correspondingly estimated bulk HSI from the Lofoten northeast Arctic cod fishery, 1883–1937. Black solid line, regression line; grey solid lines, 95% confidence band; grey broken lines, 95% prediction band. Vertical lines show the range of values used in the prediction for the period 1859–1882. Exploratory analyses Fat content vs. HSI As the fat content data in Hjort (1914) were limited, similar data from the Barents Sea and Lofoten area in 2007/2008 were consulted in Skjæraasen et al. (2010) to statistically relate HSI to liver “condition”. In Hjort (1914), no clear statements on which methods were used to extract the fat were given, only that the content of “medicinal oil” was reliably estimated by a person named Mr P. M. Heyerdahl, personally observing “the course of the fishery”. Skjæraasen et al. (2010) used a standard laboratory techniques of today, including extraction by ethyl acetate and spectrophotometric determination of triplicates. In our analysis, four outliers (out of 91 observations) were deleted; see applied statistical tests in Skjæraasen et al. (2010). Note that in Skjæraasen et al. (2010), data were presented as somatic HSI values, i.e. HSI = 100 × liver weight × (total fish weight - gonad weight)−1, whereas in the present study the same data are presented as percentages of total weight, i.e. HSI = 100 × liver weight × total fish weight−1 [Equation (1)], to allow for direct comparisons with data from Hjort (1914). To investigate whether a change-point existed in liver fat percentage for a given HSI value, piecewise linear regression was used, where the inflection point was presumed unknown (estimated). The regression and 95% bootstrap confidence intervals (CIs) were fit using the SiZer package (Sonderegger, 2012) in R (R Development Core Team, 2013). Piecewise linear regression estimates one, abrupt change in the slope, but the data suggested that the change might be better fit by a curve. Therefore, a bent-cable regression for independent data was also fit, using the bentcableAR package (Chiu, 2012). Trends in HSI Basic statistics on HSI from the Lofoten fishery were reported in three different ways: (i) the HSI for each year based on the total amount of landings of cod and liver in that year (see above), (ii) the smoothed 9-year average of bulk measures (the level of smoothing was based on trials to properly account for interannual variability), and (iii) the grand mean of HSI measures for a specific time segment (change-point analysis). Change-point analysis was used to identify the location of multiple change-points, or abrupt changes in the mean level, within the HSI series. For the change-point analysis, a Segment Neighbourhood algorithm (Auger and Lawrence, 1989) was chosen because it does not sacrifice accuracy (Killick and Eckley, 2013). Thereafter, the Akaike Information Criterion (AIC) was consulted (changepoint package in R; Killick and Eckley, 2013) to assess a penalty for the number of segments used to describe the data and thus prevent overfitting. Trends in bulk HSI were tested with the earlier mentioned piecewise linear regression package using the complete dataseries from 1864 onwards; no data existed for 1863. The annual mean HSI from the fisheries-independent survey data were compared with the commercial bulk HSI. Predictors of HSI Our inclusion of biometric predictors was limited to total length (TL), which is believed to have the main effect on the HSI (Yaragina, 1996, 2010; Sandeman et al., 2008). Reports on TL were taken from the IMR commercial catch sampling programme, conducted between January and May in the Lofoten area from 1932 (Figure 2). To reflect the protocol of the corresponding bulk liver sampling programme, we combined TL information from all types of gears, but only used specimens classified by otolith expert readers as “certain skrei”, i.e. NEA cod from the main Barents Sea area (Rollefsen, 1933, 1934). TL information was lacking for 7 years in the 1970s. The 1989 estimated length (67 cm) was omitted from the analysis as it appeared to be an outlier. Change-point analysis was performed to identify the location of changes in mean TL. The maximum number of change-points used was four based on the inspection of segment length. Other factors that might explain the dynamics in the HSI were also investigated. The influence of ocean temperature (Sandeman et al., 2008), represented by the Kola transect temperature series (hereafter Kola temperature) from the Barents Sea (0–200 m depth, 70°30′–72°30′N 33°30′E) (Boitsov et al., 2012), was chosen because of its influence on prey abundance and individual growth and condition. Temperature, categorized as high (warm) or low (cold) within a year, was defined in relation to the average Kola temperature for 1900–2012, i.e. Δtemp = annual temperature - mean Kola temperature. Also consulted was Godø's (2003) definition of warm and cold periods, largely based on Kola temperature, especially before 1900 when only anecdotal information on temperature was available. The North Atlantic Oscillation (NAO) winter index, established from 1899 (Hurrell et al., 2003), was also included. When the NAO is in a positive phase, oceanic responses in the Barents Sea are reinforced; this typically results in increased Atlantic Water inflow, which increases both the temperature and the influx of zooplankton prey into the Barents Sea. The principal component-derived index was used instead of the station-based index because it is considered a more optimal representation of the full NAO (Hurrell et al., 2013). Total spawning-stock biomass (TSB, i.e. mass of specimens aged 3 years and older) and spawning-stock biomass (SSB, i.e. mass of maturing, spawning, or spent specimens) were selected to investigate the effect of density-dependence on HSI; series for both indices were available from 1900 (Hylen, 2002; ICES, 2012). However, because of collinearity, only a few of these factors were included in the final model; TL and TSB were significantly correlated (r = 0.39, p = 0.0005), as were TSB and SSB (r = 0.53, p < 0.0001), and Kola temperature and NAO (r = 0.36, p < 0.0001). Only TL and SSB were uncorrelated (r = 0.05, p = 0.689). Due to the collinearity of possible explanatory factors (noted above), only those that were not correlated but believed to have a relationship with the HSI were included in the same model. The effects of TSB and Kola temperature (including a lagged effect, investigated a posteriori) on the HSI were investigated using a GAM (Generalized Additive Model) with a Gaussian error structure and identity link. Kola temperature was included in the final multivariate model, not the NAO index because regional or local environmental effects were expected to have a greater direct effect on cod than large-scale atmospheric factors. The effect of the NAO on the HSI was investigated separately, using again a GAM with Gaussian error structure and identity link. Both the HSI and NAO data were standardized to a mean of zero and a standard deviation of one before the analysis to put the indices on a common scale. A plot of the HSI and NAO indicated a slight non-linear effect. Because this could be the result of a lagged effect in the predictor variable, the effect of a 1-year lag was also investigated a posteriori. GAMs were run in R (R Development Core Team, 2013) using the mgcv package (Wood, 2011). All remaining data explorations were done either with Microsoft Office Excel 2007, Systat® 13 or SigmaPlot® 12. Results Fat content vs. HSI The combination of recent and historical liver fat data indicated a markedly lower HSI-specific liver fat content in Hjort (1914) than today (Figure 4). No statistical test was performed because the raw data were different in nature, i.e. bulked and individual data, respectively. Hjort's HSI data were also very restricted in range (1.6 ≤ HSI ≤ 7.0) compared with the present-day HSI values (1.5 ≤ HSI ≤ 16.0). Although both Hjort (1914) and Skjæraasen et al. (2010) reported the same minimum HSI, in terms of liver fat, the minimum content observed in the two studies was very different; 12 and 30%, respectively. The maximum liver content was also dissimilar; 59 and 79%, respectively. Figure 4. Open in new tabDownload slide Relationship between historical (filled circles) and recent (open circles) HSI and liver fat content of northeast Arctic cod. Grey line is the bent-cable regression fit, while the black line is the piecewise linear regression. Use of the individual data from Skjæraasen et al. (2010) showed an inflection point, where the growth in the percentage of liver fat reached an asymptote at ∼70% (Figure 4). Both the piecewise linear regression and the bent-cable regression model indicated a change in slope (inflection point) at HSI = 7.0 (liver index = 65.4% at this point). However, the bootstrapped 95% CIs of the inflection point were wide for both models; 3.8–9.0 for the piecewise linear regression and 4.2–9.6 for the bent-cable regression model. Trends in the HSI The collation of information from the Lofoten fishery (Figure 2) made it possible to establish a 153-year long HSI time-series for NEA cod from 1859 to 2012 except for 1863, where no record on liver landings was found (Figure 5). These reports on the bulk HSI were centred on ≈6 (grand mean: 5.89; 95% CI: 5.70—6.09), but annual fluctuations were evident; the CV (coefficient of variation; s.d./mean) was estimated at 0.20. The most recent HSI values were comparable with the low values seen at the end of the 19th/beginning of the 20th century (Figure 5). Fisheries-independent data from the period 1997–2012 (Figure 2) were similar to the commercially based HSI and showed no evidence of contrasting values (p = 0.063, Wilcoxon signed-rank test), except in 2011 and 2012, when the research survey series had markedly higher values (≈1.5 per cent points; Figure 5). Excluding these 2 last years from the test, the p-value changed to 0.198. Furthermore, the mean HSI from the 2013 research survey was as high as 5.64 (Figure 5). This marked contrast with the commercial HSI series might indicate that there are differences in how livers are currently processed. Figure 5. Open in new tabDownload slide Annual variation in the northeast Arctic cod bulk HSI from the Lofoten fishery (1859–2012; circles) and the mean HSI (diamonds) from the Institute of Marine Research (IMR) Lofoten research survey (1997–2013). Values for 1859–1876 were estimated and include the 95% CI of the estimates. Black circles indicate the period of Johan Hjort's investigations. The dotted line (HSI = 7.0) is the inflection point from the piecewise and bent-cable regressions (see Figure 4). Minimum and maximum HSI values spanned a broad range of ocean temperatures. Using mean Kola temperature as reference point (1900–2012: 3.99°C), the lowest value, found within “Hjort's time-series”, i.e. 1.6 in 1903, occurred when ocean temperatures were below average (Δtemp = −0.91°C). The second lowest HSI value of 2.7 in 1883 occurred before the Kola series began, but was most likely during a period of ocean cooling (Godø, 2003). The next three lowest HSI values appeared both during warm and cold ocean periods: 2012 (HSI = 3.3, Δtemp = 1.37°C), 1904 (HSI = 3.4, Δtemp = −0.43°C), and 2011 (HSI = 3.5, Δtemp = 0.38°C). The maximum HSI appeared in 1953 with a record of 9.1, but this was during a cool ocean phase (Δtemp = −0.20°C). Although the HSI oscillated considerably over the time-series, some broader patterns were discernible after smoothing (Figure 6), the HSI declined from the start of the time-series in 1859 until the 1880s, when it remained low. Then, the HSI increased noticeably from the 1920s up to the 1950s, after which it remained relatively high until the mid-1970s before decreasing. The change-point analysis on the complete HSI series identified five different periods (Figure 6), the respective grand means being: (i) 1859–1880: 6.1; (ii) 1881–1919: 5.0; (iii) 1920–1974: 6.8; (iv) 1975–2003: 5.5; (v) 2004–2012: 4.4. Exclusion of predicted values (1859–1882) from the analysis did not affect the location of the four later segments. Figure 6. Open in new tabDownload slide Temporal trends in 9-year smoothed HSI (solid line) and Kola temperature (broken line). Horizontal lines are the grand mean HSI for a specific period (segment) located by change-point analysis. Kola temperature and the HSI, both smoothed over 9 years, varied in close synchrony until the 1970s, but then the Kola temperature increased with no comparable response in the HSI (Figure 6). From the mid-1980s, the two series have trended in opposite directions. The piecewise linear regression analysis (1864−) showed a change in the annual trend in the HSI in 1954 (97.5% CI: 1951–1966), which occurred shortly after a decline in the Kola temperature (1950–pre-1990). Predictors of the HSI The body size of NEA cod fluctuated markedly (Figure 7a), and this dynamic had a significant effect on the HSI (Figure 7b; radjusted2=0.25,p < 0.0001, linear regression). Change-point analysis indicated four periods in TL size [grand mean (cm): (i) 1932–1946: 86.1; (ii) 1947–1965: 90.2; (iii) 1966–1986: 81.8; (iv) 1987–2012: 79.0 (Figure 7a)]. Generally, the HSI increased with the mean TL, but the last 2 years (2011 and 2012) had the lowest recorded HSI, although the mean TL in these years was not atypical (grand mean entire period = 83.7 cm). Figure 7. Open in new tabDownload slide Variation in northeast Arctic cod (a) mean TL, 1932–2012 and (b) the resulting relationship with the HSI. Horizontal coloured lines are the average TL per period identified by change-point analysis, whereas the solid black line is the linear relationship with the 95% confidence band (shaded area). Grey circles in both panels are the years 2011 and 2012. Symbol colour in (b) corresponds to segment line colour in (a). Large symbols in (b) are the mean HSI for each period as defined in (a). From 2010, TSB has been high but within the normal range seen within the time-series, whereas SSB has been at a historical high (above 1.2 million tonnes; Figure 8a). No evidence of a relationship between HSI and SSB was present. Both TSB and Kola temperature were positively related to the HSI, but each factor explained less than the mean TL, and their contribution was insignificant (p > 0.05) if combined with TL. TSB regressed on the HSI showed an radjusted2 of 0.13 (p < 0.0001, linear regression; Figure 8b), whereas the % deviance explained for HSI vs. Kola temperature was 10.3 [GCV (Generalized Cross-Validation) score = 1.44, p = 0.03, GAM; Figure 8c]. Kola temperature appeared to be positively related to the HSI at temperatures below 4°C, but negatively above 4°C, i.e. there were weak indications of a convex response curve (Figure 8c). Time-lags were investigated, but lagged temperature was not found to be significantly related to changes in the HSI. In the multivariate model, the HSI was positively related to both TSB (p < 0.0001) and Kola temperature (p = 0.009) but a large amount of variability was left unexplained by the GAM (% deviance explained = 24.2, GCV score = 1.29), indicating that other factors may be important. The winter NAO index did not predict changes in the HSI (p = 0.10) but there was a marginally significant linear relationship (p = 0.045) at a lag of 1 year (Figure 8d). Figure 8. Open in new tabDownload slide Trends in (a) total-stock (black columns) and spawning-stock biomass (grey columns) of northeast Arctic cod, (b) HSI vs. total-stock biomass (TSB), (c) HSI and Kola temperature, and (d) standardized HSI vs. standardized NAO winter index (lagged by 1 year). Line in (a) refers to the maximum spawning-stock biomass through 2009, i.e. 1.2 million tonnes. Lines in (b)–(d) are the fitted regression or GAM models, whereas the shaded areas are the 95% confidence band. Grey circles in (b)–(d) indicate the low HSI from years 1903, 1904, 2011, and 2012. Discussion One might wonder if Johan Hjort, when collating and interpreting his liver time-series (1880–1912) on NEA cod from the Lofoten area, was aware that Ketil Motzfeldt's initiative of Fisheries Statistics records (1859–1879) existed. If Hjort had elongated his time-series to cover 54, instead of 33, years, he might have been in a better position to fully judge the “condition” of NEA cod within his period of interest. Condition was generally on the poor side over the longer period, i.e. not only in 1903 as stated in his book, and included much larger interannual variability. The year 1903 is worth special attention for both biological and social reasons; the “revolt in Finnmark” (Northern Norway) took place that year, when angry fisher attacked the local whale oil factory and blamed this industry for the poor cod fishery (Hanssen, 1963). The more likely reasons for the failure in the cod fishery were a collapse in the capelin stock and invasion of seals to the coast (Hanssen, 1963). In other words, a situation resembling “the ecological crisis in the Barents Sea” seen in the late 1980s (Hamre, 1994). The extremely low HSI of 1.6 in 1903 could be argued to be unrealistically low (Figure 5), but such values are also detected in more recent articles, for both individuals (Skjæraasen et al., 2010) and length classes of smaller cod (TL ≤ 80 cm; Sandeman et al., 2008; Skjæraasen et al., 2012). Likewise, the fat content of 12% in 1903 is probably not a reporting mistake (Kjesbu et al., 1991), especially after accounting for the inefficient fat extraction procedure at Hjort's time, where it was several per cent points less effective than in today's laboratory (Figure 4). Extreme low HSI values appear when spawners are both small in size and in poor condition (Hjort, 1914), and high HSI values result when the opposite is the case (Marshall et al., 1998). Note also that the 1903 HSI value was linked to an extremely cold year, which may have influenced individual size and condition in that year. A useful cut-off between relatively poor and good condition for NEA cod might be the threshold HSI = 7, i.e. the inflection point in the liver fat content curve (Figure 4). However, this point value should not be taken too literally as the statistical analyses showed that variance in liver fat content at this threshold was moderately large. Furthermore, the average HSI is typically around 6; higher average values are rare and were found mainly in the 1920–1950s in some of the years (Figure 5). Taken together, one's perspective regarding trends and magnitude of change is very much dependent upon the length of the time-series, but extreme values are important to address and clarify main causal factors. The liver data in the 1914 publication of Johan Hjort inspired us to establish the current series; his data formed a natural “bridge” between the earliest and the latest Fisheries Statistics data. The presented biological series, 1859–2012; 153 years (no data in 1863), is probably one of the longest in the world, although there are examples of others, e.g. White Sea herring (Clupea pallasi marisalbi) catch statistics that go back to the 1780s (Lajus et al., 2007). This statement ignores species of no commercial interest, as well as proximate (e.g. Øiestad 1994), anecdotal information (Kurlansky, 1997) and limited or non-sequential data. To create this long series, we had to assume that the manner and frequency of how liver was extracted from and landed together with cod were similar throughout the time-series. This latter view was challenged by the introduction of the fisheries-independent HSI series; relatively less liver is probably landed when the fishing ground is densely packed with spawners, as seen in recent years (see below). This issue should be looked into more closely in future studies. Although we focused on a characteristic life-history metric, i.e. it's liver size, of a capital spawner (Alonso-Fernandez and Saborido-Rey, 2012), the Fisheries Statistics have also been used to document the loss of spawning fields in southern Norway, i.e. a northerly shift, over time (1866–1969; Jørgensen et al., 2008; Opdal, 2010). The Fisheries Statistics also form a central input in the unique series of NEA cod population dynamics (1900-present; Hylen, 2002), which shows large fluctuations in stock size and recruitment. Furthermore, series from stock assessments (ICES, 2012) clarify that both the SSB and TSB of today are among the highest in history, particularly for SSB, which is the highest recorded. This high biomass (Figure 8a) appeared in exceptionally warm waters (Figure 6), although the causal mechanisms are obviously complex. The temperature series used in our analyses was chosen because of its high quality (length and completeness) and relevance (reflecting both temperature per se and advection of Atlantic water masses; Boitsov et al., 2012). The same argument applies to the NAO index, although reflecting instead westerly wind in the North Atlantic, which is known to influence multiple factors that might affect fish population dynamics (Hurrell et al., 2003). The lack of any potentially suitable explanatory time-series before 1900 makes any advanced exploratory analysis for the whole length of the present NEA cod liver index series highly challenging or speculative. However, for the sake of clarity metrological data as such can be traced several hundreds of years back in time (Parker et al., 1992), but is difficult to compile such series for the area near Northern Norway. We therefore restricted the analysis to a limited number of series, all commencing around 1900, i.e. Kola temperature, SSB, TSB, and the NAO index, which starts before our series and continuing up today. A long list of other less data-rich covariates, not considered here, may also be expected to influence the HSI, such as sex ratio (Marshall et al., 1998; Yaragina, 2010), length and age at maturity (Jørgensen, 1990; Nash et al., 2010), capelin abundance (Marshall et al., 1998; Sandeman et al., 2008), migration distance (Jørgensen et al., 2008; Opdal, 2010), and, possibly, fisheries-induced evolution (Heino et al., 2002; Olsen et al., 2004; Jørgensen et al., 2007, 2009). The HSI vs. Kola temperature analysis (Figure 8c) resembles a “dose–response curve”, as seen in physiology; however, only a small amount of the deviance was explained, which indicates that other factors might be responsible for the observed changes. Because individual HSI can change rapidly with food consumption and is heavily influenced by fish size, care must be taken not to over-interpret these results. Nevertheless, Kola temperature has been shown to not always have a positive effect on the HSI (Sandeman et al., 2008), whereas we have shown that large-scale atmospheric factors (that influence many other factors) do not appear to play a strong role in determining HSI. Godø (2003) grouped temperature into likely warm and cold periods, beginning in 1866 (see also Opdal, 2010). The last cold period ended in the mid- to late 1980s and the Barents Sea is currently in a warm period. The higher HSI was typically associated with warm periods, and cold periods with a lower HSI, but the recent HSI values are surprisingly low, contradicting this pattern. TSB, but not SSB, appeared to have a weak relationship with the HSI. This result may be an artefact of the strong correlation between TSB and TL, which has a strong relationship with the HSI. TL clearly began to decline after 1965 (Figure 7a), but the HSI began its downwards trend in 1954, although still being reasonably high up to the mid-1970s (Figure 6). Several things were happening in this period that might be responsible for the trends. The temperature in the Barents Sea was declining and cold periods appear to indicate the lower HSI. But perhaps more importantly, the effects of industrialized fishing began to change the demographic structure of the cod population (Jørgensen, 1990). With declining fish size, the HSI continued to decline. Hence, the remarkably close association seen between HSI and Kola temperature, provided smoothing both dataseries (currently over 9 years), from 1900 and up to this time vanished. Because the relationship between size and HSI is much stronger than that with temperature, the HSI continued to decline with size even after temperature shifted to a warm phase. The effects of temperature on the HSI are weak and the conclusions drawn regarding its effects are, at best, speculative, therefore we argue that the link between size and HSI appears currently to be the key to HSI dynamics. What causation that is behind this association is an interesting topic for future work. In summary, we have successfully established an extremely long time-series but firm conclusions regarding potential environmental stressors, demographic factors, or evolutionary effects influencing HSI must be postponed until more in-depth analyses. The use of commercial catch statistics obviously has great merits because of their uninterrupted annual resolution and massive collection programme within a rather restricted season and geographical area. Acknowledgements We are most grateful to the secretariat at Norges Råfisklag (Råfisklaget), in particular Gunnar Johnsen, for providing us with NEA cod catch metrics over the last decades, and to Knipovich Polar Research Institute of Marine Research and Oceanography (PINRO), Murmansk, Russia, for giving us access to the Kola temperature time-series. Thanks also go to the librarians Wencke Vadseth (retired) and Brit Skotheim at the Directorate of Fisheries' Library, Bergen, for helping us locating Fisheries Statistics reports and other historical literature. 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