331 PARADIGMS IN FISHERIES OCEANOGRAPHY WILLIAM C. LEGGETT 1 & KENNETH T. FRANK 2 1 Department of Biology, Queen’s University, Kingston, ON K7L 3N6, Canada E-mail: wleggett@queensu.ca 2 Department of Fisheries and Oceans, Bedford Institute of Oceanography, Dartmouth NS B2Y 4A2, Canada E-mail: FrankK@mar.dfo-mpo.gc.ca Abstract The development of the eld of sheries oceanography over the past century has been heavily inuenced by a relatively small number of paradigms that have shaped thinking, inuenced lines of enquiry and occasionally stalled progress in the eld. This review provides an overview of what are considered to be the most inuential paradigms in the discipline. Each begins with a brief discussion of its origins. Next their respective (and often overlapping) impact on the development of the discipline is discussed and then the evolution of these paradigms as shaped by new advances in approaches and technologies and by direct challenges to their underlying assumptions is reviewed. For each, the endpoint is an overview of the current state of knowledge and thinking and the probable future direction of research in the area. The review concludes with an overview of the probable future directions of research in the discipline as a whole. Introduction The discipline of modern sheries oceanography has its origins in the work of Johan Hjort (1914, 1928), who was the rst to formally hypothesize a link between the dynamics of sh populations and the dynamics of their environment. In his ‘critical period’ paradigm Hjort argued that variabil- ity in food availability during the transition from endogenous to exogenous feeding in larval shes, typically a very narrow time window, was central to the survival of individual larval cohorts. Hjort hypothesized that when food was abundant, survival (and recruitment) would be high, and when food was scarce survival and recruitment would be low. This hypothesis was subsequently general- ized by Cushing (1975) who reasoned, in his ‘match mismatch’ hypothesis, that food availability was linked to the interaction between interannual differences in the timing of spawning/hatching and the timing and magnitude of the primary and secondary production cycles in the ocean. These hypotheses dramatically inuenced the direction of research in the eld by (1) focusing research into the causes of interannual variability in recruitment on the egg and larval stages of shes, (2) provid- ing a simplifying construct within which to explore the causes of temporal changes in the abun- dance of commercially important marine shes and (3) by linking uctuations in the abundance of shes directly to the dynamics of other components of the ocean ecosystem. In hindsight, Hjort’s major contribution appears to have been to awaken thinking and research into the nature of this dynamic interaction between sh and their environment. Prolonged adherence to Hjort’s ideas, and the lure of Cushing’s hypothesis, combined to dominate thinking and research in the eld for most of the twentieth century, some would say negatively (Leggett & DeBlois 1994). As the discipline has advanced several new paradigms have evolved. While originally offered as simplifying constructs, © 2008 by R.N. Gibson, R.J.A. Atkinson and J.D.M. Gordon 332 WILLIAM C. LEGGETT & KENNETH T. FRANK and as the foundation for new studies of important processes governing the dynamics of sh stocks, some of these new paradigms now approach the status of dogma once accorded Hjort’s hypothesis and have the potential, if pursued uncritically, to once again delay progress in the eld. This review examines the major paradigms that have shaped thinking and research in sheries oceanography over the past century and explore how recent research has affected understanding of their validity and usefulness now, and going forward. Table 1 provides an overview of these paradigms ordered hierarchically from individuals to ecosystems. The need for a more holistic and effective approach to the science of sheries oceanography, and of the management strategies applied to marine shes, is evident from the breadth of species now undergoing serious decline, not only worldwide, but also within more restricted ecosystems (Dower et al. 2000, Figure 1). The advent of new methods (ageing techniques for larval shes, the application of biochemical and molecular techniques, the development of instrumentation and computing capacity that has allowed physical oceanographers to measure and model the highly dynamic and variable environ- ment of continental shelf ecosystems, satellite imagery, etc.) have created new opportunities to explore the dynamics of marine shes in relation to the dynamics of their physical environment and the ecosystems they inhabit. Paradigm 1: Spawning stock biomass is a suitable proxy for the reproductive potential of a stock The Hjort and Cushing models focused primarily on the factors determining interannual variability in mortality rates experienced by larvae (the life stage widely believed to be the most vulnerable to environmental variability (reviewed in Leggett & DeBlois 1994). Another highly inuential para- digm holds that it is the product of the number of offspring generated by a spawning stock and the rate of mortality experienced by those offspring until they recruit to the reproducing population that govern the dynamics of sh populations. This thinking is inherent in stock recruitment models (Ricker 1954, Beverton & Holt 1957) that have formed the cornerstone of studies of the recruitment dynamics of shes, and of management based on these studies, for most of the latter half of the twentieth century. These models assume strong density dependence (Figure 2). Fundamental to the practical application of these models has been the assumption that the total spawning stock biomass (SSB) is an acceptable proxy for the reproductive potential of the stock of interest. This assumption is employed because SSB can be readily derived from sheries survey data, whereas total egg production (TEP), a more reliable and realistic indicator of reproductive output is more labour intensive to obtain and, for this reason, does not exist for most stocks. The use of SSB as a proxy for TEP implies that (1) spawner biomass is proportional to the TEP and (2) in lay terms, “an egg is an egg is an egg,” that is, all eggs are equal in their potential to Table 1 Paradigms in sheries oceanography 1. Spawning stock biomass (SSB) is a suitable proxy for the reproductive potential of a stock. 2. Marine sh eggs and larvae are generally designed for dispersion and potential colonization (panmixia). 3. In marine temperate systems, sh spawn in springtime so that peak larval abundance coincides with maximum prey availability (Cushing’s match/mismatch hypothesis). 4. Environmentally based recruitment models, when updated with new data, invariably fail; recruitment prediction is an intractable problem, particularly when it is based on processes associated with the growth and mortality of the early life-history stages. 5. Populations cannot irreversibly collapse/collapsed populations will recover in the absence of shing. 6. Fish stocks can be managed in isolation from their total environment/habitat. 7. Population recovery is synonymous with rebuilding. © 2008 by R.N. Gibson, R.J.A. Atkinson and J.D.M. Gordon 333 PARADIGMS IN FISHERIES OCEANOGRAPHY produce a recruit to the population. However, the variation in SSB is generally insufcient to account for the related variation observed in recruitment in marine sh populations (Shepherd et al. 1984, Wooster & Bailey 1989, Rijnsdorp et al. 1991, Marshall et al. 1998). Notwithstanding this reality, the paradigm that SSB is a suitable proxy for total reproductive effort has persisted and has, in turn, been an important contributor to the persistence of the Hjort and Cushing hypotheses and the focus of research into the causes of recruitment variation in marine shes. This includes the search for ecological and/or environmental factors affecting egg and larval mortality — an approach that has proved challenging and, in only limited cases, successful (see Paradigm 4). This has impeded the development of a coherent understanding of the recruitment dynamics of marine shes in particular and the science of sheries management in general (Rothschild 1986, Hilborn & Walters 1992). plaice 4VT-SSB 1970 1975 1980 1985 1990 Years 1995 2000 plaice 2J3K-SSB cod 3NO spring-SSB cod 2J3KL-Offhore Survey-SSB white hake 4T-SSB thorny skate 4T-SSB cod 4Vn-SSB cod 4X-SSB cod 4T-SSB smooth skate 4T-SSB smooth skate 4VWX-SSB winter skate 4X-SSB little skate 4VWX-SSB turbot 4RST-SSB yellowtail flounder 5Z-SSB herring 4VWX-SSB silver hake 4VWX-SSB cod 5Z-SSB winter skate 4VsW-SSB haddock 4VW-SSB mackerel-SSB winter skate 4T-SSB haddock 4X-SSB plaice 3Ps-SSB haddock 5Z-SSB thorny skate 4VWX-SSB cod 4VsW-SSB pollack 4VWX-SSB Figure 1 (See also Colour Figure 1 in the insert following p. 250.) Ordination of the time of series of spawn- ing stock biomass of various species from scientic surveys conducted throughout the north-west Atlantic, illustrating that the majority of the stocks are at biomass levels well below (red) the long-term average. Intensity of colours is proportional to the magnitude of the standardized anomaly in standard deviation units. Alphanumeric labelling refers to the Northwest Atlantic Fisheries Organization management unit. © 2008 by R.N. Gibson, R.J.A. Atkinson and J.D.M. Gordon 334 WILLIAM C. LEGGETT & KENNETH T. FRANK In the 1990s these assumptions began to come under increasing scrutiny (Lowerre-Barbieri et al. 1998, Marshall et al. 1998, Marteinsdottir & Steinarsson 1998, Marshall & Frank 1999, Marshall et al. 1999). Marshall et al. (1998) were the rst to demonstrate in situ the potential fallacy of the assumption inherent in the use of SSB as a surrogate for TEP. Their work with Barents Sea cod (Gadus morhua) showed that recruitment was positively correlated with the quantity of lipid energy stored in the liver of mature females or, in other words, with female condition. Boyd et al. (1998) observed a similar relationship between parental fat levels and recruitment in Cape anchovy (Engraulis capensis). In cod, total liver energy was proportional to TEP and, like TEP, varied with capelin (Mallotus villosus) abundance (Yaragina & Marshall 2000) such that by either measure the reproductive potential of a xed number of mature females was signicantly higher when the quan- tity of food available to maturing sh was abundant and correspondingly lower when it was scarce. In contrast, cod SSB was found to be not statistically different at high and low prey levels. In short, their study conrmed prior suspicions regarding the paradigm that SSB is an inadequate surrogate for TEP and demonstrated that replacing SSB with more accurate measures of reproductive poten- tial is fundamental to a fuller understanding of the dynamics of recruitment in marine shes. The work of Marshall et al. (1998, 1999) has been an important factor in redirecting the focus of studies into the causes of interannual variation of recruitment in marine sh populations. Their ndings demonstrated that a more successful pursuit of process-oriented models of the recruitment dynamics of marine sh will require integration of the processes affecting reproductive output (growth, production and condition of spawners) with mortality processes affecting egg, larval and juvenile survival (Ulltang 1996, Marshall et al. 2000). Research by Yaragina & Marshall (2000) has demonstrated that the search for a comprehensive understanding of the factors regulating variability in reproductive potential, independent of SSB, may be as complex, and as inextricably tied to environmental and ecological factors, as are the causes of variation in egg and larval survival. For example, their study of temporal variation in the liver condition index (LCI) — an important determinant of reproductive potential (Marshall et al. 1999) — of ve length classes of north-east Arctic cod (Gadus morhua) showed that while varia- tions in the abundance of capelin, a major food source, was the proximate determinant of variation in LCI, an indirect, but perhaps not ultimate, determinant of variation in the index appears to have been the abundance of herring (Clupea harengus), which inuence cod LCI indirectly via their predation on capelin, which in turn are the main prey of cod. Interest in the role and importance of maternal effects as regulators of the recruitment dynamics of marine shes has increased since the publication of these ndings. Scott et al. (2006) modelled the daily reproductive output of a range of simulated age/size-structured populations of Atlantic 0 1 2 SSB 3 20 Recruitment 40 North Sea herring Figure 2 Ricker stock recruitment model t to data for North Sea herring. SSB, spawning stock biomass. © 2008 by R.N. Gibson, R.J.A. Atkinson and J.D.M. Gordon 335 PARADIGMS IN FISHERIES OCEANOGRAPHY cod, created under contrasting stock recruitment scenarios, over an entire spawning season. The objective was to determine the effects of individual female condition and egg quality on stock repro- ductive potential (SRP). Their ndings suggest that, in two populations having equal SSB, the effect of low levels of individual condition in one can lead to almost total reproductive failure for that population. Moreover, the positive effect of increased individual condition was found to depend on the particular population structure designated in the model, a variable that, in situ, can be strongly inuenced by both shing intensity and environment. Indeed, they reported that differences in population size and age structure produced by differences in shing mortalities ranging from 0 to 1.0 could reduce the SRP by 48–74% depending on the related assumptions regarding female con- dition and quality. Any factor, anthropogenic or environmental, inducing changes in mortality of equivalent magnitude would be expected to produce a similarly scaled result. Vallin & Nissling (2000) studied the effect of female age on the survival of cod eggs and lar- vae in the Baltic, where successful spawning is restricted to the deep basins at salinities varying between 11 and 20 ppm. Due to the oxygen depletion commonly prevailing in these areas, neutral egg buoyancies above oxygen-critical depths are important to egg survival. They found that large females produce larger eggs that exhibit neutral egg buoyancy at lower salinities, thereby ensuring egg development in more favourable oxygen conditions. The number of recruited cod (age 2), in the Baltic Sea over two eras characterized by different conditions (1967–1980 and 1981–1994), was found to be positively related to the fraction of eggs produced by older females (5+ yr), implying a strong maternal effect on recruitment. Berkeley et al. (2004) report a similar positive relationship between female age and probability of egg survival in longnose grenadier (Coelorhynchus carmina- tus). Marteinsdottir & Steinarsson (1998) report similar ndings for the egg and early larval stages of cod. The ndings of Vallin & Nissling (2000) also illustrate the potential for negative effects of shery-induced changes in population age structure on population size and persistence. Scott et al. (1999) modelled this shing effect and found that the effects of the loss of more fecund older/larger individuals in the population could lead to overestimation of the number of potential recruits to populations experiencing higher levels of shing mortality by as much as 60%. Environmental variables can also inuence the condition of females and the demographics of populations in ways that can dramatically alter reproductive output independent of SSB. Scott et al. (1999) note that when size- (growth-) related maternal effects on egg viability were incorporated into their shing effect model, the number of potential recruits to heavily exploited populations could be reduced by a further 10%. The work of Choi et al. (2004) illustrates just how profound these environmental inuences can be. In their paper on the devolution of the Scotian Shelf ecosystem off Nova Scotia, Canada, they document declines in growth rates, size at age and age at maturation of the entire benthic sh community that mirror the changes modelled and documented above. These changes occurred pro- gressively over a 45-yr time period (1960–2005), the most dramatic changes occurring in the early 1990s. They resulted in average sizes of mature (age 5) cod, haddock (Melanogrammus aeglenus), pollock (Pollachius virens) and silver hake (Merluccius bilinearis) that were 70–80% of the 1970s levels and remain depressed in spite of a moratorium on shing that began in 1993 (Figure 3). Drinkwater (2002) estimates that approximately 30–50% of the decline in SSB of cod that occurred in the 1980s and early 1990s was linked to these reductions in deep-water temperatures and their depressing effect on growth rates and corresponding sizes at age. Given the strong positive relation- ship between body size and fecundity in these species (Pinhorn 1984, Waiwood & Buzeta 1989), a corresponding decline in per individual reproductive potential, independent of losses due to coinci- dent reductions in the total number of spawners, clearly occurred. © 2008 by R.N. Gibson, R.J.A. Atkinson and J.D.M. Gordon 336 WILLIAM C. LEGGETT & KENNETH T. FRANK Their analysis also revealed that these dramatic changes in reproductive output were not simply the consequence of reductions in the size of reproducing adults (a product of the negative effects that quotas based on biomass and the behaviour of shermen focusing their efforts on the largest sh available; e.g., see Drinkwater 2002). For example, during the 1960s and 1970s the physiologi- cal condition of these shes exceeded the 45-yr norm. However, throughout the 1980s and 1990s physiological condition declined sharply and by 2000 the majority of the sh were in below-average condition. Given the documented impact of female condition on egg quality and recruitment in cod (Marshall et al. 1999), and the evidence of maternal effects on survival linked to female size and condition, it is likely that in this species, and perhaps others, a further reduction in effective reproductive output, independent of SSB, was experienced as a consequence of combined effects of declining size and condition, both of which had an environmental component. There is also evidence that the total metabolic rate of the entire demersal ecosystem was depressed as a consequence of changes in ocean climate. These ocean climate changes included a progressive decline in bottom temperatures, an increase in the volume of the cold intermediate layer, and movement of the Gulf Stream Front to a more offshore position. These changes are judged to have been caused by an increased along-shelf advection from the Gulf of St. Lawrence and south- ern Newfoundland augmented by local, atmospherically induced cooling (Drinkwater et al. 2003). One of the outcomes of this change was a dramatic reduction in the biomass of the once-dominant euphausiid (Euphausia superba) and a corresponding decline in their contribution to the overall diet of the demersal sh assemblage. For example, the contribution of this euphausid species to the diet of pollock and cod declined from >65% by weight in the 1980s to <10% in the 1990s (Hanson & Chouinard 2002, Carruthers et al. 2005). The resulting hysteresis in the structure of the Scotian Shelf ecosystem in the late 1980s pro- duced an ecosystem dominated by smaller pelagic shes and benthic invertebrates (mainly shrimp and crab) in which the once-dominant large-bodied demersal shes now play a relatively minor role. The fact that these once-dominant species have not recovered even in the absence of exploitation, 20 30 40 50 60 70 Length at age 5, cm 1970 1975 1980 1985 1990 1995 2000 Cod Haddock Pollock Silver hake Figure 3 (See also Colour Figure 3 in the insert.) Changes with time in lengths at age 5 for four groundsh species from the eastern Scotian Shelf. © 2008 by R.N. Gibson, R.J.A. Atkinson and J.D.M. Gordon 337 PARADIGMS IN FISHERIES OCEANOGRAPHY as traditional stock recruitment models would predict, suggests that a fundamental change in their tness has occurred. The disjunction between SSB and effective reproductive output appears to be a signicant factor in this change in tness and may have contributed in a major way to the dramatic collapse of these once-dominant demersal species in the early 1990s. Paradigm 2: Marine sh eggs and larvae are generally designed for dispersion and potential colonization (panmixia) Reproduction in commercially exploited marine species generally involves the spawning of billions of tiny eggs that oat in the near-surface waters during the spring of each year. The generality and magnitude of these events were widely considered to be an adaptation to the very high mortality of early life stages caused by the vagaries of the environment (Rothschild 1986, Rothschild & DiNardo 1987). One variable identied as important in this context was ocean currents, often driven by wind, which caused larvae to be transported to regions where food and other factors were less favourable. Several correlation studies reported signicant relationships between larval survival, measured by the abundance of the recruiting year-class, and dispersive events For example, it has been hypothesized that warm core rings (eddies representing instabilities in the Gulf Stream that can entrain large volumes of water from the continental shelf) can transport sufcient numbers of eggs and larvae off the shelf to have a signicant negative impact on recruit- ment. Myers & Drinkwater (1989), who examined this hypothesis using estimates of entrainment from 14 yr of satellite imagery and recruitment estimates for 25 sh and shellsh stocks ranging from the Mid-Atlantic Bight to the southern Grand Banks, found that increased warm core ring activity was associated with low recruitment levels in 17 of 18 groundsh stocks examined. The sole exception was cod on Georges Bank. While the level of signicance related to each stock was low, the collective result was consistent with the original hypothesis. For other examples of the possible link between dispersive effects and recruitment see Carruthers et al. (1951) and Bailey (1981). The ndings of these and other studies led to the view that either excessive dispersion of larvae or dis- placement to areas distant from the nursery ground was a primary cause of the reduced recruitment that resulted when wind strengths and direction were unfavourable. However, in most cases updated analyses of these models have failed to support the relationships originally observed (Myers 1998, see Paradigm 4). The seminal work of Sinclair (1988) showed that many continental shelf spawning locations of marine shes were located in areas characterized by retention features or semipermanent gyres, the current characteristics of which act to minimize the advection of the egg and larval stages and con- sequently their vulnerability to dispersive processes. Many subsequent studies have expanded the suite of species that utilize relatively non-dispersive oceanographic settings for spawning and early larval development (Hinrichsen et al. 2001, North & Houde 2001, Lett et al. 2007). In addition, the advent of technologies allowing high-resolution, discrete-depth sampling of the water column revealed that ontogenetic shifts in depth distributions and vertical migratory behaviour of larvae also serve to minimize dispersion from the spawning areas. These ndings have moderated the belief that the early life stages of marine species were simply passive drifters and that survival was largely dependent on the “mercy” of the currents. One of the most striking examples of this non-dispersive reality involves haddock that spawn on the offshore banks of the Scotian Shelf. Because of the recirculation that occurs around each of these discrete spawning banks there is a strong tendency for the egg and larval distributions of haddock that spawn there to be discrete. And, when larvae metamorphose to the juvenile stage, a development process that takes about 90 days, settlement to the bottom occurs in the same zones in which they were spawned, which now become prime feeding areas for the juvenile and adult stages (Frank et al. 2000). © 2008 by R.N. Gibson, R.J.A. Atkinson and J.D.M. Gordon 338 WILLIAM C. LEGGETT & KENNETH T. FRANK These ndings are consistent with the results of modelling studies of the scales of connectivity in Caribbean reef shes (Cowen et al. 2006). They found that larval dispersal scales for most species were of the order of 50–100 km, much smaller than has generally been assumed. Their analyses also indicate that passive dispersal/retention is insufcient for population replenishment, recruitment levels generated from the use of passive dispersal assumptions in the model being one to two orders of magnitude lower than that required for successful population replenishment. These studies call for a general rethinking of the adaptive character of the spawning behaviour of many marine species from spawning as a vehicle for colonization or bet hedging to one in which the entire early life-history period is viewed as an elegant suite of adaptations to an environment that is highly variable at interannual and smaller timescales but is more predictable in the longer term. However, while this longer-term predictability is reected in adaptations involving both the timing and location of spawning, interannual variability in the ocean environment can result in important disruptions to their efcacy that lead to recruitment variability and even recruitment fail- ure. Well-known examples include the relationship between capelin recruitment and onshore wind discovered by Leggett et al. (1984), the destabilizing effects of warm core rings on the retention dynamics of Scotian Shelf banks (Myers & Drinkwater 1989) and the inuence of upwelling events on recruitment processes along the North African coast (Cury & Roy 1989). Such disruptive events can also lead to the establishment of new subpopulations through colonization of new habitats when environmental conditions permit. Detection of such colonization episodes is most evident when they occur outside the normal range of distribution. The larval drift associated with anomalous oceano- graphic conditions involving the displacement of cod larvae from Iceland to West Greenland — a colonization event covering a distance of almost 1000 km (Frank 1992) — is a striking case in point. A similar displacement, on a much smaller geographic scale, was shown for haddock larvae originat- ing from the eastern Scotian Shelf. Larvae of this species episodically drift downstream to Browns Bank on the western Scotian Shelf. In the case of both cod and haddock, the dispersed larval stages appear to persist and to contribute to the recruiting year-class in the colonized area from which they then make a subsequent return to their spawning area during the maturation phase (Frank 1992, Brickman 2003). Similar events appear to be a characteristic of many Caribbean shes (Cowen et al. 2006). Discovery of this phenomenon has resulted in the need for signicant upward revisions in the estimates of year-class strength at the natal site and a corresponding bonus to the local shery. Its implication for the assessment and management of adjacent stocks is also profound. Paradigm 3: In marine temperate systems, sh spawn in springtime so that peak larval abundance coincides with maximum prey availability (Cushing’s match/mismatch hypothesis) The Hjort and Cushing hypotheses, which were so instrumental in directing the early research into the population dynamics of marine shes, were founded on the dynamic interaction between the temporal and spatial distributions of larval shes and their prey. Leggett & DeBlois (1994) system- atically reviewed the scientic evidence for and against these hypotheses and found Hjort’s hypoth- esis to be wanting. Support for Cushing’s hypothesis was judged equivocal, mainly because of the difculty of adequately operationalising the hypothesis and the technical challenges of assembling data on appropriate time and space scales, realities acknowledged by Cushing himself in his update of the hypothesis (Cushing 1990). An important feature of the Cushing hypothesis was its removal of the restriction inherent in Hjort’s thesis that food-mediated mortality would be restricted to a brief ‘critical’ stage in lar- val development (the transition from endogenous to exogenous feeding). Under the Cushing model © 2008 by R.N. Gibson, R.J.A. Atkinson and J.D.M. Gordon 339 PARADIGMS IN FISHERIES OCEANOGRAPHY recruitment success became associated (at least in theory) with the abundance of food during the entire period of larval development. One of the explicit corollaries of this thinking was the expecta- tion that spawning in north temperate marine shes would be adaptively linked, temporally, to the annual spring (and in some cases fall) production cycle(s) in the sea. This corollary also determined and directed much of the research into the link between ocean physics, primary and secondary production, and the recruitment dynamics of sh populations. Solid evidence of the importance of this link to recruitment has been elusive (Cushing 1990, Leggett & DeBlois 1994). Two papers highlight the contribution of advances in the understanding of physical/biological linkages in the ocean and the availability of more sophisticated sampling technologies, in particular satellite remote sensing, to an understanding of the potential importance of Cushing’s ideas. Mueter et al. (2006) utilized established relationships between the dynamics of the mixed layer and the onset of primary production to develop a 35+-yr time series for the timing of the spring bloom in the Bering Sea in an attempt to explain recruitment variation in walleye pollock (Theragra chalcogramma). This indirect measure of the onset of spring primary production conformed closely to the onset as determined from 6 yr of uorescence data. The production series so developed was then related to indices of walleye pollock survival over the same time interval. The indices were expressed as the residuals from a Ricker stock recruitment model. Walleye pollock survival rates were strongly and inversely related to the timing of the spring bloom dates, a relationship inter- preted by the authors as evidence of the important role of the timing of the spring bloom in relation to the timing of spawning as a determinant of larval survival and recruitment in this species. While possibly a case of overinterpretation due to the use of indirect approximations of the independent and dependent variables, the ndings are nonetheless supportive of the Cushing hypothesis. In a more direct and convincing study, Platt et al. (2003) employed satellite remote sensing to determine the timing of the spring phytoplankton peak on the eastern Scotian Shelf. This they related to peaks in the production of larval haddock. While their data series was short (8 yr) and was divided into two distinct periods (1979–1981 and 1997–2001) their analyses revealed a strong relationship (r 2 = 0.89) between variation in recruitment and variation in the timing of the spring bloom. Unresolved by both studies is the extent to which other components of the ecosystem, perhaps themselves linked to and affected by physical attributes of the ecosystem that are co-related to the timing of the spring bloom (predator abundance and diversity, temperature effects, etc.), might inuence the environment occupied by eggs and larvae (either positively or negatively) and the extent to which this result can be generalized to other areas and other species. In contrast to these ndings, Mousseau et al. (1998), who examined the annual cycles of abun- dance of sh larvae and their zooplankton prey in relation to the biomass and production of phyto- plankton on the Scotian Shelf, discovered that the production of copepod nauplii and copepodites was sustained throughout the year and that sh larvae specializing on copepod prey also occurred year-round. This occurred notwithstanding the fact that the spring bloom of large phytoplankton, normally assumed to form the basis of the food web for larval shes, was restricted to February– April. This year-round food availability was produced by a non-peak food web structured on the large-microphage shunt of the microbial food web (small phytoplankton → appendicularians/ pteropods → sh larvae). Mousseau et al. (1998) concluded that the year-round presence of sh lar- vae and the fact that several of their major prey items exploit the microbial food web challenges the long-standing belief that the feeding of marine sh larvae depends primarily on the reproduction of herbivorous calanoid copepods grazing the spring and autumn blooms of large phytoplankton. De Figueiredo et al. (2005) provide further support for this link between larval feeding and the large microphage shunt of the microbial food web. They found that Protozoa and appropriately sized metazoan prey, previously largely ignored as potential food items, can contribute signicantly to the dietary and energy requirements of larval sh. They conclude that the inclusion of these dietary © 2008 by R.N. Gibson, R.J.A. Atkinson and J.D.M. Gordon 340 WILLIAM C. LEGGETT & KENNETH T. FRANK components into measures of the food resource available to larval shes diminishes the validity of the key assumption underlying the Cushing hypotheses — that is, when, at times other than the spring bloom, food levels in the sea are limiting to larval growth and survival. There is mounting evidence, as well, that at larger scales, water temperature may play a greater role in mediating larval growth and survival than food availability (see Meekan et al. 2003, Takasuka & Aoki 2006). This, too, raises the questions, what other components of the ecosystem (predator densi- ties, types, sizes, feeding rates, etc.) are inuenced by physical factors linked to the timing of the spring bloom, and how do these ecosystem level interactions inuence larval survival and recruitment? A second corollary of the Cushing hypothesis is that larvae that experience superior feeding conditions, by virtue of their association with areas/times of enhanced food abundance, should exhibit faster growth and higher survival, leading ultimately to improved recruitment. This corol- lary, the so-called ‘growth-mortality’ hypothesis (Anderson 1988, Hare & Cowen 1997) is, in fact, comprised of three non-exclusive functional hypotheses: the ‘bigger is better’ hypothesis, the ‘stage duration’ hypothesis and the ‘growth-selective’ hypothesis (Figure 4). Underlying all three hypotheses is the general assumption that following the transition to exog- enous feeding the risk of death to an individual will be inversely related to the quantity and quality of food available and, by extension, to rates of growth and development. The positive effect of high growth and development rates on survival is generally believed to result from the rapid increase in length and/or changes in behaviour related to development during this period that, in turn, differen- tially inuences the susceptibility of individual larvae to predation (reviewed in Litvak & Leggett 1992, Leggett & DeBlois 1994). ‘Bigger is better’ hypothesis The ‘bigger is better’ hypothesis evolved, in large part, from the results of general models that aggregate data at the species level (an approach criticized by Pepin & Miller (1993) for its distorting effects when generalized to intraspecic studies) and, in part, from the results of laboratory studies that showed larger larvae were less vulnerable to predation. However, as demonstrated by Litvak & Leggett (1992) the experimental designs typically used in these studies to assess the relationship between size and vulnerability commonly compounded the effects of age and size by using larvae of different ages to obtain the desired range of sizes investigated. Furthermore, most studies of the effects of size and/or age failed to provide the predator with a choice of prey sizes/ages and there- fore examined only the capture component of the predation act, whereas predation involves three multiplicative probabilities: encounter, attack and capture (reviewed in Litvak & Leggett 1992). Laboratory and in situ mesocosm experiments in which larvae of identical ages but different sizes and of identical sizes but different ages were subjected to predation by both visual and non-visual predators clearly illustrated this bias (Litvak & Leggett 1992). Contrary to the predictions of the big- ger is better model, in predation trials involving experimental cohorts of larvae of identical age, but A Body size Larval mortality Stage duration Growth rate BC Figure 4 Graphical representation of the ‘bigger is better’ (A), ‘stage duration’ (B) and ‘growth-selective’ (C) hypotheses. © 2008 by R.N. Gibson, R.J.A. Atkinson and J.D.M. Gordon [...]... Fisheries and Oceans Canada, Ocean Sciences Division We thank Liam Petrie for his assistance in producing the figures References Anderson, J.T 1 988 A review of size dependent survival during pre-recruit stages of fishes in relation to recruitment Journal of the Northwest Atlantic Fisheries Organization 8, 55–66 Bailey, K.M 1 981 Larval transport and recruitment of Pacific hake, Merluccius productus Marine. .. 2004 Transition to an alternate state in a continental shelf ecosystem Canadian Journal of Fisheries and Aquatic Sciences 61, 505–510 Choi, J.S., Frank, K.T., Petrie, B & Leggett, W.C 2005 Integrated assessment of a large marine ecosystem: a case study of the devolution of the Eastern Scotian Shelf, Canada Oceanography and Marine Biology An Annual Review 43, 47–67 Cowen, R.K., Paris, C.B & Srinivasan,... adaptation? Canadian Journal of Fisheries and Aquatic Sciences 40, 754–762 Frank, K.T & Leggett, W.C 1 985 Reciprocal oscillations in densities of larval fish and potential predators: a reflection of present or past predation? Canadian Journal of Fisheries and Aquatic Sciences 42, 184 4– 184 9 Frank, K.T & Leggett, W.C 1994 Fisheries ecology in the context of ecological and evolutionary theory Annual Review. .. from an individual-based simulation model Canadian Journal of Fisheries and Aquatic Sciences 55, 2244–2254 Magnuson, J.J 1 988 Two worlds for fish recruitment: lakes and oceans American Fisheries Society Symposium 5, 1–6 Marshall, C.T & Frank, K.T 1999 The effect of interannual variation in growth and condition on haddock recruitment Canadian Journal of Fisheries and Aquatic Sciences 56, 347–355 Marshall... fundamental ways to changes in the growth rates, age and size at maturity and even the distribution of many species inhabiting the cold intermediate layer Recent examples of the effect on distribution include the southward extension of Arctic cod from the Labrador Shelf to the southern Grand Banks off Newfoundland and of capelin from the southern Grand Banks to the Scotian Shelf and beyond (Figure 11)... Allee effects and compensatory population dynamics within a stock complex Canadian Journal of Fisheries and Aquatic Sciences 57, 513–517 Frank, K.T & Leggett, W.C 1 982 Coastal water mass replacement: its effect on zooplankton dynamics and the predator-prey complex associated with larval capelin Canadian Journal of Fisheries and Aquatic Sciences 39, 991–1003 Frank, K.T & Leggett, W.C 1 983 Multi-species larval... the winter-time sea-surface pressure difference between Iceland and the Azores The relative strength of this difference varies annually Positive NAO values (associated with years when the Icelandic low deepens and the Azores high 349 © 20 08 by R.N Gibson, R.J.A Atkinson and J.D.M Gordon WILLIAM C LEGGETT & KENNETH T FRANK increases) produce both an intensified latitudinal pressure gradient and westerly... Sciences 54, 781 – 787 Chambers, R.C & Leggett, W.C 1 987 Size and age at metamorphosis in marine fishes: an analysis of laboratory reared winter flounder (Pseudopleuronectes americanus) with a review of variation in other species Canadian Journal of Fisheries and Aquatic Sciences 44, 1936–1947 Chambers, R.C., Leggett, W.C & Brown, J.A 1 988 Variation in and among early life history traits of laboratory-reared... Fisheries Oceanography 15, 230–243 Ottersen, G & Stenseth, N.C 2001 Atlantic climate governs oceanographic and ecological variability in the Barents Sea Limnology and Oceanography 46, 1774–1 780 Pepin P., Dower, J.F & Davidson, F.J.M 2003 A spatially explicit study of prey-predator interactions in larval fish: assessing the influence of food and predator abundance on larval growth and survival Fisheries Oceanography. .. 1 980 1990 2000 Figure 8 Spawning stock biomass (solid line) and landings (dashed line) of cod in nine areas in the north-west Atlantic 1, northern (Northwest Atlantic Fisheries Organization Division 2J3KL); 2, northern Gulf of St Lawrence; 3, southern Gulf of St Lawrence; 4, St Pierre Bank; 5, southern Grand Banks; 6, eastern Scotian Shelf; 7, Gulf of Maine; 8, western Scotian Shelf; 9, Georges Bank . the southern Grand Banks off Newfoundland and of capelin from the southern Grand Banks to the Scotian Shelf and beyond (Figure 11). In general, growth rates, size at maturity and age at maturity. 2000 0 0 100 200 0 100 200 300 400 0 100 200 300 400 0 50 100 0 20 40 60 80 100 150 200 20 40 60 7 8 9 4 5 6 1 2 3 80 20 ousands of metric tonnes ousands of metric tonnes ousands of metric tonnes 10 30 Figure 8 Spawning stock biomass (solid line) and landings (dashed line). southern Grand Banks; 6, eastern Scotian Shelf; 7, Gulf of Maine; 8, western Scotian Shelf; 9, Georges Bank. © 20 08 by R.N. Gibson, R.J.A. Atkinson and J.D.M. Gordon 349 PARADIGMS IN FISHERIES OCEANOGRAPHY argument