Fitness landscape of Atlantic cod shaped by harvest selection and natural selection

Harvesting may lead to evolutionary changes in life histories on a contemporary time scale, changes that could be maladaptive in natural contexts. However, our understanding of the strength and direction of harvest-induced selection versus natural selection is still limited, partly due to the difficulty of tracking the fate of individuals in the wild. Here, we present direct estimates of harvest mortality, natural mortality and site fidelity of coastal Atlantic cod (Gadus morhua) from the Norwegian Skagerrak coast. Furthermore, we present standardised selection differentials for fish body size. Estimates are obtained from acoustic telemetry, where we continuously monitored fish (n = 60) within a semi-sheltered area using a network of 25 listening stations. To obtain additional information about harvested cod, all fish (body size: 30–66 cm) were also tagged with traditional T-bar tags with a printed reward of 500 NOK (60 E). We estimate that 75% of the fish died within the study area during 1 year. Fishing mortality was markedly higher than natural mortality. Together, recreational fishers and commercial fishers caught at least 50% of the tagged fish during 1 year. Standardised selection differentials showed that fisheries targeted larger fish (i.e. favoured the survival of smaller fish), while natural selection favoured the survival of larger fish. Albeit on a small scale, we provide empirical evidence that harvesting can have a dominant influence on the fitness landscape experienced by a marine fish such as the Atlantic cod. We suggest that no-take marine reserves may help to counter evolutionary impacts of harvesting in the ocean.     

Harvest selection on Atlantic cod behavioral traits: implications for spatial management

Harvesting wild populations may contrast or reinforce natural agents of selection and potentially cause evolutionary changes in life-history traits such as growth and maturation. Harvest selection may also act on behavioral traits, although this field of research has so far received less attention. We used acoustic tags and a network of receivers to monitor the behavior and fate of individual Atlantic cod (Gadus morhua, N = 60) in their natural habitat on the Norwegian Skagerrak coast. Fish with a strong diel vertical migration, alternating between shallow- and deep-water habitats, had a higher risk of being captured in the fishery (traps, gillnet, hand line) as compared to fish that stayed in deeper water. There was also a significant negative correlation between fish size (30-66 cm) and the magnitude of diel vertical migration. Natural selection on behavior was less clear, but tended to favor fish with a large activity space. On a monthly time scale we found significant repeatabilities for cod behavior, meaning that individual characteristics tended to persist and therefore may be termed personality traits. We argue that an evolutionary approach to fisheries management should consider fish behavior. This would be of particular relevance for spatial management actions such as marine reserve design.     

A century of fish growth in relation to climate change,population dynamics and exploitation

Marine ecosystems, particularly in high‐latitude regions such as the Arctic, have been significantly affected by human activities and contributions to climate change. Evaluating how fish populations responded to past changes in their environment is helpful for evaluating their future patterns, but is often hindered by the lack of long‐term biological data available. Using otolith increments of Northeast Arctic cod (Gadus morhua) as a proxy for individual growth, we developed a century‐scale biochronology (1924–2014) based on the measurements of 3,894 fish, which revealed significant variations in cod growth over the last 91 years. We combined mixed‐effect modeling and path analysis to relate these growth variations to selected climate, population and fishing‐related factors. Cod growth was negatively related to cod population size and positively related to capelin population size, one of the most important prey items. This suggests that density‐dependent effects are the main source of growth variability due to competition for resources and cannibalism. Growth was also positively correlated with warming sea temperatures but negatively correlated with the Atlantic Multidecadal Oscillation, suggesting contrasting effects of climate warming at different spatial scales. Fishing pressure had a significant but weak negative direct impact on growth. Additionally, path analysis revealed that the selected growth factors were interrelated. Capelin biomass was positively related to sea temperature and negatively influenced by herring biomass, while cod biomass was mainly driven by fishing mortality. Together, these results give a better understanding of how multiple interacting factors have shaped cod growth throughout a century, both directly and indirectly.     

The effects of body mass and feeding on metabolic rate in small juvenile Atlantic cod

Apparent specific dynamic action (SDA) amplitude in young juvenile Atlantic cod Gadus morhua (1 to 8 g wet mass), fed a standardized meal and then exercised in a circular swimming respirometer at a constant swimming speed of 0·5 ± 0·3 body lengths s^-1, occurred within l h after feeding in all juveniles. SDA amplitude were 1·4 to 1·8 times higher in fed fish compared to unfed fish, and rates of oxygen consumption decreased as body mass increased. SDA duration had a tendency to decrease with increasing body mass and was shortest, at 6 h, in the smallest fish (1–1·5 g), but increased to 10–11 h in the largest fish. Apparent SDA in fed fish ( R _r) scaled with a mass exponent of 0·89, while maximum metabolic rate ( R _max) determined by chasing fish to exhaustion and then measuring oxygen consumption for 12 h, and unfed routine metabolic rate (R_r) scaled with a mass exponent of 0·79 and 0·76 respectively. Relative aerobic scope ( R _max– unfed R _r) did not appear to vary over the 1 to 8 g increase in wet mass. These results show that as body mass increased in young juvenile Atlantic cod: (1) apparent SDA ( R _f) increased more rapidly than R _max, and (2) apparent SDA took up >98% of the relative aerobic scope and that young Atlantic cod allocated most of the energy to growth, and left little for other metabolic activities.     

Prehistoric versus modern Baltic Sea cod fisheries: selectivity across the millennia

Combining Stone Age and modern data provides unique insights for management, extending beyond contemporary problems and shifting baselines. Using fish chronometric parts, we compared demographic characteristics of exploited cod populations from the Neolithic Period (4500 BP) to the modern highly exploited fishery in the central Baltic Sea. We found that Neolithic cod were larger (mean 56.4 cm, 95% confidence interval (CI)+/-0.9) than modern fish (weighted mean length in catch =49.5+/-0.2 cm in 1995, 48.2+/-0.2 cm in 2003), and older (mean ages=4.7+/-0.11, 3.1+/-0.02 and 3.6+/-0.02 years for Neolithic, 1995, and 2003 fisheries, respectively). Fishery-independent surveys in 1995 and 2003 show that mean sizes in the stock are 16-17 cm smaller than reflected in the fishery, and mean ages approximately 1-1.5 years younger. Modelled von Bertalanffy growth and back-calculated lengths indicated that Neolithic cod grew to smaller asymptotic lengths, but were larger at younger ages, implying rapid early growth. Very small Neolithic cod were absent and large individuals were rare as in modern times. This could be owing to selective harvests, the absence of small and large fish in the area or a combination. Comparing modern and prehistoric times, fishery selection is evident, but apparently not as great as in the North Atlantic proper.     

The stress and metabolic responses of juvenile Atlantic cod Gadus morhua L. to an acute thermal challenge

Survival, oxygen consumption (     ), total plasma cortisol and glucose levels and gill heat-shock protein 70 (hsp70) expression were measured in 10 and 50 g juvenile Atlantic cod Gadus morhua during an acute temperature increase (2° C h⁻¹) to their critical thermal maximum. Ninety three per cent of the fish in both size classes survived to 24° C; however, mortality was 100% within 15 min of reaching this temperature. The     for both size classes increased significantly with temperature, reaching peak values at 22° C that were c. 2·8-fold those of control (10° C) fish. Resting plasma cortisol and glucose levels were lower in 10 g as compared to 50 g fish. Plasma glucose levels were highly variable in both size classes, and significant increases were only seen at >22° C for the 10 g fish. In contrast, plasma cortisol showed an exponential increase with temperature starting at 16° C in both size classes, and reached maximum levels at 22° C that were 19-fold (10 g fish) and 35-fold (50 g fish) higher than their respective control groups. Both the constitutive (73 kDa) and inducible (72 kDa) isoforms of hsp70 were detected in both size classes using the widely utilized mouse monoclonal antibody. Expression of these isoforms, however, did not change when Atlantic cod were exposed to elevated temperature, and the 72 kDa isoform was not detected using salmonid-specific antibodies. These results indicate that juvenile Atlantic cod are very sensitive to acute increases in water temperature. In addition, they (1) show that     and plasma cortisol, but not plasma glucose or gill hsp 70 levels, are sensitive indicators of thermal stress in Atlantic cod and (2) support previous reports that the upper critical temperature for this species is 16° C.     

Behavioral responses of Atlantic cod to sea temperature changes

Understanding responses of marine species to temperature variability is essential to predict impacts of future climate change in the oceans. Most ectotherms are expected to adjust their behavior to avoid extreme temperatures and minimize acute changes in body temperature. However, measuring such behavioral plasticity in the wild is challenging. Combining 4 years of telemetry‐derived behavioral data on juvenile and adult (30–80 cm) Atlantic cod (Gadus morhua), and in situ ocean temperature measurements, we found a significant effect of sea temperature on cod depth use and activity level in coastal Skagerrak. During summer, cod were found in deeper waters when sea surface temperature increased. Further, this effect of temperature was stronger on larger cod. Diel vertical migration, which consists in a nighttime rise to shallow feeding habitats, was stronger among smaller cod. As surface temperature increased beyond ~15°C, their vertical migration was limited to deeper waters. In addition to larger diel vertical migrations, smaller cod were more active and travelled larger distances compared to larger specimens. Cold temperatures during winter tended, however, to reduce the magnitude of diel vertical migrations, as well as the activity level and distance moved by those smaller individuals. Our findings suggest that future and ongoing rises in sea surface temperature may increasingly deprive cod in this region from shallow feeding areas during summer, which may be detrimental for local populations of the species.     

Persistent growth effects of temperature and photoperiod in Atlantic cod Gadus morhua

Short-term environmental manipulations during the early juvenile stage have a large impact on harvesting size of Atlantic cod Gadus morhua nearly 3 years later. A group of juvenile Atlantic cod (initial mass 9·5 g) were reared for 3 months under simulated natural photoperiod or continuous light, and a range of temperatures (7, 10, 13 and 16° C, and a group called T-step, i.e. with temperature reduced successively from 16 to 13 and 10° C). After termination of the laboratory trial, the fish were moved to sea pens and reared at ambient conditions for 30 months before harvesting in June 2006. Observed growth gain from the 3 month laboratory trial was still persistent following the 30 months of sea-pen ongrowing. The T-step group displayed 15, 13, 1 and 10% superior mass gain respectively than the groups initially at 7, 10, 13 and 16° C at harvest in June 2006. Similarly, rearing under continuous light during the initial 3 month period during the early juvenile stage resulted in 1–9% larger size at harvesting compared to fish reared at simulated natural photoperiod. Gonado-somatic and hepato-somatic indices were similar in all groups. Contribution to the understanding of the mechanism behind size variation in adult fish can have wide range applications for Atlantic cod fisheries and aquaculture.     

Ticket to spawn: Combining economic and genetic data to evaluate the effect of climate and demographic structure on spawning distribution in Atlantic cod

Climate warming and harvesting affect the dynamics of species across the globe through a multitude of mechanisms, including distribution changes. In fish, migrations to and distribution on spawning grounds are likely influenced by both climate warming and harvesting. The Northeast Arctic (NEA) cod (Gadus morhua) performs seasonal migrations from its feeding grounds in the Barents Sea to spawning grounds along the Norwegian coast. The distribution of cod between the spawning grounds has historically changed at decadal scales, mainly due to variable use of the northern and southern margins of the spawning area. Based on historical landing records, two major hypotheses have been put forward to explain these changes: climate and harvesting. Climate could affect the distribution through, for example, spatial habitat shifts. Harvesting could affect the distribution through impacting the demographic structure. If demographic structure is important, theory predicts increasing spawner size with migration distance. Here, we evaluate these hypotheses with modern data from a period (2000–2016) of increasing temperature and recovering stock structure. We first analyze economic data from the Norwegian fisheries to investigate geographical differences in size of spawning fish among spawning grounds, as well as interannual differences in mean latitude of spawning in relation to changes in temperature and demographic parameters. Second, we analyze genetically determined fish sampled at the spawning grounds to unambiguously separate between migratory NEA cod and potentially smaller sized coastal cod of local origin. Our results indicate smaller spawners farther away from the feeding grounds, hence not supporting the hypothesis that harvesting is a main driver for the contemporary spawning ground distribution. We find a positive correlation between annual mean spawning latitude and temperature. In conclusion, based on contemporary data, there is more support for climate compared to harvesting in shaping spawning ground distribution in this major fish stock in the North Atlantic Ocean.     

Sea surface temperature dictates movement and habitat connectivity of Atlantic cod in a coastal fjord system

While movements of organisms have been studied across a myriad of environments, information is often lacking regarding spatio‐seasonal patterning in complex temperate coastal systems. Highly mobile fish form an integral part of marine food webs providing linkages within and among habitats, between patches of habitats, and at different life stages. We investigated how movement, activity, and connectivity patterns of Atlantic cod (Gadus morhua) are influenced by dynamic environmental conditions. Movement patterns of 39 juvenile and subadult Atlantic cod were assessed in two coastal sites in the Swedish Skagerrak for 5 months. We used passive acoustic telemetry and network analysis to assess seasonal and spatial movement patterns of cod and their relationships to different environmental factors, using statistical correlations, analysis of recurrent spatial motifs, and generalized linear mixed models. Temperature, in combination with physical barriers, precludes significant connectivity (complex motifs) within the system. Sea surface temperature had a strong influence on connectivity (node strength, degree, and motif frequency), where changes from warmer summer waters to colder winter waters significantly reduced movement activity of fish. As the seasons changed, movement of fish gradually decreased from large‐scale (km) linkages in the summer to more localized movement patterns in the winter (limited to 100s m). Certain localized areas, however, were identified as important for connectivity throughout the whole study period, likely due to these multiple‐habitat areas fulfilling functions required for foraging and shelter. This study provides new knowledge regarding inshore movement dynamics of juvenile and subadult Atlantic cod that use complex, coastal fjord systems. The findings show that connectivity, seasonal patterns in particular, should be carefully considered when selecting conservation areas to promote marine stewardship.     

Variability in the summer diets of juvenile polar cod (<Emphasis Type="Italic">Boreogadus saida</Emphasis>) in the northeastern Chukchi and western Beaufort Seas

Polar cod (Boreogadus saida) is an important link between top predators and lower trophic levels in high-latitude marine ecosystems. Previous findings describe differences in its diet throughout the western Arctic; however, the causes of this variation are not well known. This study examined the diets of juvenile polar cod collected via demersal trawling methods over three summers in the northeastern Chukchi Sea (2010–2012) and one summer in the western Beaufort Sea (2011) to determine the amount of variability explained by biological, spatial, and interannual factors. Prey were identified, measured for length, and aggregated by percent mean weight into taxonomically coarse prey categories for analysis. Within seas, variation in juvenile polar cod diet composition was significantly related to body size, latitude, longitude, depth, and interannual (Chukchi Sea only) factors. Canonical correspondence analysis indicated body size was the most important factor contributing to the total variance in juvenile polar cod diet in the Chukchi and Beaufort Seas. Body size-based diet differences between the Chukchi and Beaufort Seas were evaluated using non-metric multidimensional scaling. This method revealed that similar-sized polar cod consumed similar-sized prey in both seas, but their diets were more benthically influenced in the Chukchi Sea and more pelagically influenced in the Beaufort Sea. Juvenile polar cod diet compositions vary by body size and region of inhabitance throughout their distribution. Here, we show that body size was the primary factor explaining variation in the summer diet of juvenile polar cod within the Chukchi and Beaufort Seas.     

Cod Gadus morhua L. populations as behavioural units: inference from time series on juvenile abundance in the eastern Skagerrak

Abundance and distribution of cod Gadus morhua in various size intervals and age groups between 2000 and 2005 were followed in coastal trawl surveys. In spite of a reduction in fishing pressure in recent years and high cod recruitment in the Skagerrak region in 2001 and 2003, no recovery could be evidenced. The survey data clearly showed that low cod density areas were not recolonized, even though abundance of juvenile cod remained high for about a year after the recruitment episodes. Increased abundance of fish >400 mm total length was only discernible at some scattered locations where other studies also have suggested local populations still to be present. The intermittent high recruitment has been linked to an inflow of egg and larvae from the North Sea, a theory which also has gained support from genetic studies. It was thus argued that the disappearance of the juvenile cod from the inshore is an effect of a migratory behaviour; the fish of offshore origin eventually leave the coast for the open Skagerrak or the North Sea. These findings support a view on cod populations as essentially behavioural entities, whereas dispersal of early life stages may be less important as a structuring mechanism.     

Maternal Influences on Variation in Egg Sizes in Temperate Marine Fishes

SYNOPSIS. We examine the variation in egg sizes of marine teleostsand evaluate the maternal contribution to this variability.At the species level, egg sizes in 309 North Atlantic fishesrange from 0.3 to 18.0 mm diameter (median = 1.1), size at hatchingvaries directly with egg size, and large adult size is associatedwith large eggs but the relationship is weak. Within populations,egg sizes are distributed normally with a median coefficientof variation of 4% (n = 56 species). Egg size varied among femalesin all cases for which female-level data were found. Estimatesof the variance components of egg size due to females were foundfor three species and, as a percentage of total variance, are71 % for capelin, Mallotus villosus, 46% for winter flounder,Pleuronectes americanus, and 35% for Atlantic cod, Gadus morhua.For cod, which spawn multiple egg batches per year, an additionalbatches-within-females component was estimated to be 26%. Sizeat hatching also differs among sibgroups and is generally directlyrelated to egg size at the individual level. We modelled fishgrowth by allowing individuals to grow at exponential ratesfrom a normal distribution of initial sizes. Comparing sizevariation in model fish to empirical evidence suggests thatvariation in initial sizes, propagated by growth, could accountfor a large fraction of the size variation observed months afterhatching in natural populations. We view size variation in youngmarine fishes to be largely of maternal origin and environmentallymodulated, which if true has special consequences for fisheriesand aquaculture.     

Conserving marine biodiversity: insights from life-history trait candidate genes in Atlantic cod (Gadus morhua)

Recent technological developments have facilitated an increased focus on identifying genomic regions underlying adaptive trait variation in natural populations, and it has been advocated that this information should be important for designating population units for conservation. In marine fishes, phenotypic studies have suggested adaptation through divergence of life-history traits among natural populations, but the distribution of adaptive genetic variation in these species is still relatively poorly known. In this study, we extract information about the geographical distribution of genetic variation for 33 single nucleotide polymorphisms (SNPs) associated with life-history trait candidate genes, and compare this to variation in 70 putatively neutral SNPs in Atlantic cod (Gadus morhua). We analyse samples covering the major population complexes in the eastern Atlantic and find strong evidence for non-neutral levels and patterns of population structuring for several of the candidate gene-associated markers, including two SNPs in the growth hormone 1 gene. Thus, this study aligns with findings from phenotypic studies, providing molecular data strongly suggesting that these or closely linked genes are under selection in natural populations of Atlantic cod. Furthermore, we find that patterns of variation in outlier markers do not align with those observed at selectively neutral markers, and that outlier markers identify conservation units on finer geographical scales than those revealed when analysing only neutral markers. Accordingly, results also suggest that information about adaptive genetic variation will be useful for targeted conservation and management in this and other marine species.     

Seasonal distribution of juvenile Atlantic cod in the southern Gulf of St Lawrence

Seasonal changes in the geographic distribution of juvenile (ages 1–4) Atlantic cod Gadus morhua were determined from research surveys conducted in the southern Gulf of St Lawrence during 1986–87, 1990–91, and 1994. From late June to early October, juvenile cod were most abundant in shallow water (<50 m deep). By early November, all age groups (adults and juveniles) had migrated to deep (>100 m) offshore waters for the winter. For most juveniles, this represented a minimum migration of >225 km (each way). Age 3 and 4 cod migrated greater distances than age 1 and 2 fish. Some age 3 and 4 cod migrated as far as 650 km from their summer and early autumn areas. Although there was partial geographic segregation of juvenile and adult fish during summer and winter, all age groups were found together during the migration. No cod were present in the shallow waters (<80 m deep) of the south-western Gulf during April due, in part, to later than average ice-melt. Large numbers of all age-classes were present in most of the south-eastern Gulf by mid-May.     

A preliminary study on quantitative relations among growth,reproduction and mortality in fishes

As a quantitative approach to the life histories of fishes, the present paper attempted to predict a relation among reproduction, growth and mortality numerically with a technique of control theory, the discrete maximum principle. A method for predicting the relation was derived on the postulate that natural selection maximized the net reproductive rate subject to a few constraints. The derived method was applied to Atlantic cod and Atlantic herring populations in the Southern Gulf of St. Lawrence as numerical examples. The examples demonstrated that the theoretical reproductive effort and body weight were well consistent with the observed ones every age but the theoretical survival rates were slightly different from the observed ones. For the reasons mentioned below, however, it should be interpreted that the examples rather support the adopted postulate to a certain degree. First, in general, it is very difficult to obtain good estimates of the rates with traditional methods. Second, intense fishing pressure possibly changes the life history parameters to some extent in fish populations. Moreover, the examples also suggested that, to examine the postulate in further detail, similar analyses had to be made with the data of many fish populations on which intense fishing pressure had not been exerted.     

Disentangling structural genomic and behavioural barriers in a sea of connectivity

Genetic divergence among populations arises through natural selection or drift and is counteracted by connectivity and gene flow. In sympatric populations, isolating mechanisms are thus needed to limit the homogenizing effects of gene flow to allow for adaptation and speciation. Chromosomal inversions act as an important mechanism maintaining isolating barriers, yet their role in sympatric populations and divergence with gene flow is not entirely understood. Here, we revisit the question of whether inversions play a role in the divergence of connected populations of the marine fish Atlantic cod (Gadus morhua), by exploring a unique data set combining whole‐genome sequencing data and behavioural data obtained with acoustic telemetry. Within a confined fjord environment, we find three genetically differentiated Atlantic cod types belonging to the oceanic North Sea population, the western Baltic population and a local fjord‐type cod. Continuous behavioural tracking over 4 year revealed temporally stable sympatry of these types within the fjord. Despite overall weak genetic differentiation consistent with high levels of gene flow, we detected significant frequency shifts of three previously identified inversions, indicating an adaptive barrier to gene flow. In addition, behavioural data indicated that North Sea cod and individuals homozygous for the LG12 inversion had lower fitness in the fjord environment. However, North Sea and fjord‐type cod also occupy different depths, possibly contributing to prezygotic reproductive isolation and representing a behavioural barrier to gene flow. Our results provide the first insights into a complex interplay of genomic and behavioural isolating barriers in Atlantic cod and establish a new model system towards an understanding of the role of genomic structural variants in adaptation and diversification.     

The influence of variability in species trait data on community‐level ecological prediction and inference

Species trait data have been used to predict and infer ecological processes and the responses of biological communities to environmental changes. It has also been suggested that, in lieu of trait, data niche differences can be inferred from phylogenetic distance. It remains unclear how variation in trait data may influence the strength and character of ecological inference. Using species‐level trait data in community ecology assumes intraspecific variation is small in comparison with interspecific variation. Intraspecific variation across species ranges or within populations may lead to variability in trait data derived from different scales (i.e., local or regional) and methods (i.e., mean or maximum values). Variation in trait data across species can affect community‐level relationships. I examined variability in body size, a key trait often measured across taxa. I collected 12 metrics of fish species length (including common and maximum values) for 40 species from literature, online databases, museum collections, and field data. I then tested whether different metrics of fish length could consistently predict observed species range boundary shifts and the impacts of an introduced predator on inland lake fish communities across Ontario, Canada. I also investigated whether phylogenetic signal, an indicator of niche‐conservativism, changed among measures. I found strong correlations between length metrics and limited variation across metrics. Accordingly, length was a consistently significant predictor of the response of fish communities to environmental change. Additionally, I found significant evidence of phylogenetic signal in fish length across metrics. Limited variation in length across metrics (within species), in comparison with variation within metrics (across species), made fish species length a reliable predictor at a community‐level. When considering species‐level trait data from different sources, researchers should examine the potential influence of intraspecific trait variation on data derived by different metrics and at different scales.     

Regime shifts in exploited marine food webs: detecting mechanisms underlying alternative stable states using size-structured community dynamics theory

Many marine ecosystems have undergone ‘regime shifts’, i.e. abrupt reorganizations across trophic levels. Establishing whether these constitute shifts between alternative stable states is of key importance for the prospects of ecosystem recovery and for management. We show how mechanisms underlying alternative stable states caused by predator–prey interactions can be revealed in field data, using analyses guided by theory on size-structured community dynamics. This is done by combining data on individual performance (such as growth and fecundity) with information on population size and prey availability. We use Atlantic cod (Gadus morhua) and their prey in the Baltic Sea as an example to discuss and distinguish two types of mechanisms, ‘cultivation-depensation’ and ‘overcompensation’, that can cause alternative stable states preventing the recovery of overexploited piscivorous fish populations. Importantly, the type of mechanism can be inferred already from changes in the predators'' body growth in different life stages. Our approach can thus be readily applied to monitored stocks of piscivorous fish species, for which this information often can be assembled. Using this tool can help resolve the causes of catastrophic collapses in marine predatory–prey systems and guide fisheries managers on how to successfully restore collapsed piscivorous fish stocks.