Detecting and managing fisheries-induced evolution

Exploitation of fish populations can induce evolutionary responses in life histories. For example, fisheries targeting large individuals are expected to select for early maturation at smaller sizes, leading to reduced fecundity and thus also reduced fisheries yield. These predicted phenotypic shifts have been observed in several fish stocks, but disentangling the environmental and genetic causes behind them has proved difficult. Here, we review recent studies investigating phenotypic shifts in exploited populations and strategies for minimizing fisheries-induced evolution. Responses to selective harvesting will depend on species-specific life-history traits, and on community-level and environmental processes. Therefore, the detection of fisheries-induced evolution and successful fish stock management requires routine population monitoring, and a good understanding of genetics, relevant ecological processes and changing environmental conditions.     

Genetic stock structure of odd-year pink salmon, Oncorhynchus gorbuscha (Walbaum), from Washington and British Columbia and potential mixed-stock fisheries applications

We used electrophoresis to determine the number and characteristics of genetically distinct stocks of odd-year pink salmon in Washington and southern British Columbia. We analysed 5128 fish from 52 collections (taken in 1985, 1987 and 1989). We observed genetic variation at 53 enzyme-coding loci, 19 of which were polymorphic at the P_o-95 level in at least one stock. Genotypic proportions conformed to Hardy-Weinberg expectations in nearly all cases. The genetic profiles of individual populations were generally stable over the three cycle years studied. Significant differences in allele frequencies at sAAT-3* , PEP-LT* and PGDH* for several stocks were, however, noted between this study and previously reported data for pink salmon. We used G-tests and cluster analysis of genetic distances to evaluate genetic interrelationships among collections and to define genetically distinct stocks. Differentiation among stocks exhibited a clear geographic pattern with three major clusters of stocks recognizable: (1) Hood Canal and Washington Strait of Juan de Fuca stocks, (2) Puget Sound, Fraser River, and southern Canada South Coast stocks, and (3) northern Canada South Coast stocks and Canada North Coast stocks. Computer simulations using 14 and 28 loci, and sample sizes of 15C600, demonstrated that accurate estimates of stock-group composition could be obtained for pink salmon fisheries having a considerable range of stock compositions. The simulations revealed that approximately 50% fewer fish were required to obtain a given level of precision of stock group composition estimates with 28 loci as with the set of 14 loci used in previous investigations.     

Effects of access restrictions and stocking on small water body fisheries in Laos

Four different management regimes were identified in small water bodies in Laos: open-access fisheries, both with and without stocking of exotics (mainly Nile tilapia Oreochromis niloticus ); community fisheries with restricted access and regular stocking; and fisheries rented out to corporate entities, based on indigenous stocks only. These regimes represent all possible combinations of the two management measures, access (open/restricted) and stocking of exotic species (no/yes) and a test fishing experiment assessed their effects on stock abundance, richness and diversity. The combination of access restrictions and stocking had a strong positive effect on total standing stocks. Stocks of indigenous fish were significantly increased by access restrictions, while stocking of exotics had no effect on indigenous standing stocks. Community fisheries targeted large sizes of exotic species while reducing the exploitation of smaller size groups, which accounted for much of the indigenous stocks. This suggests that stocking can promote active effort regulation and reduce the exploitation of natural stocks. Data on yields and effort were too limited to allow the use of inferential statistics, but indicated that community fisheries were exploited with much lower effort and gave lower yields than open access fisheries, while providing higher returns to fishing effort. This suggests that active management is effective in increasing standing stocks and the efficiency of exploitation, but does not necessarily increase yields unless optimal management regimes can be identified and implemented by the management institutions. No significant effects on wild stock richness or diversity were detected in the test fishing experiment, but wide confidence limits indicated a low statistical power of the test and therefore no definitive conclusions could be drawn.     

Assessing seasonal changes in stock composition of Atlantic salmon catches in the Baltic Sea with genetic stock identification

The feasibility of using genetic stock identification to analyse seasonal changes in stock compositions of Atlantic salmon catches in the Baltic Sea was examined. The analysis employed seven variable allozyme loci from most of the potentially contributing stocks (16) from Finland and Sweden. Catch samples were collected from Finnish salmon fisheries in the eastern Bothnian Sea during the 1992 fishing season. Simulation studies were used to evaluate the feasibility of identifying Baltic salmon stocks with allozyme data. Special attention was paid to analysing the wild production of salmon stocks. Clear seasonal differences in stock composition were found. The estimates were compared with smolt production and Carlin-tag data. The proportions of the Neva and Oulujoki river stocks could be estimated as individual stocks, whereas the contributions of the remaining stocks were estimated as four composite stock groups. One of the groups consisted of wild stocks from the rivers Kalixälven and Simojoki. Identification of this group, which could be used as an index of wild production in the catches, requires catch sample sizes >300 salmon if <15% error is required.     

Changes in Size and Age of Chinook Salmon Oncorhynchus tshawytscha Returning to Alaska

The average sizes of Pacific salmon have declined in some areas in the Northeast Pacific over the past few decades, but the extent and geographic distribution of these declines in Alaska is uncertain. Here, we used regression analyses to quantify decadal trends in length and age at maturity in ten datasets from commercial harvests, weirs, and spawner abundance surveys of Chinook salmon Oncorhynchus tshawytscha throughout Alaska. We found that on average these fish have become smaller over the past 30 years (~6 generations), because of a decline in the predominant age at maturity and because of a decrease in age-specific length. The proportion of older and larger 4-ocean age fish in the population declined significantly (P < 0.05) in all stocks examined by return year or brood year. Our analyses also indicated that the age-specific lengths of 4-ocean fish (9 of 10 stocks) and of 3-ocean fish (5 of 10 stocks) have declined significantly (P < 0.05). Size-selective harvest may be driving earlier maturation and declines in size, but the evidence is not conclusive, and additional factors, such as ocean conditions or competitive interactions with other species of salmon, may also be responsible. Regardless of the cause, these wide-spread phenotypic shifts influence fecundity and population abundance, and ultimately may put populations and associated fisheries at risk of decline.     

The use of otolith shape to determine stock structure of <Emphasis Type="Italic">Engraulis encrasicolus</Emphasis> along the Tunisian coast

Engraulis encrasicolus is of great economic importance in the Mediterranean. However, little is known about its stock structure. Otolith shape analysis has been successfully used for fish stock identification. In this study, the stock structure of anchovy caught off the open sea and the coastal area of the Gulf of Tunis, lagoon of Bizerte and Lake of Ichkeul were investigated using otolith shape. Otolith shape was determined by Fourier analysis and then compared among specimens sampled from different areas with forward stepwise canonical discriminant analysis. Significant differences in otolith shape between the open sea and inshore anchovy groups were detected. Otolith shape of anchovy collected in the Lake of Ichkeul was distinct from the other groups. This finding suggests a clear discreteness of the open sea and the continental groups. The data highlighted the potential for using otolith shape analysis for anchovy stock identification, as well as the role of oceanographic features in determining stock separation. These findings will have major implications for anchovy fisheries management in Tunisia. By using a precautionary approach and considering the three areas as separate stocks, fisheries management strategies should be adjusted to achieve optimum sustainable production from each stock and to avoid decreases in genetic variety.     

Adaptive changes in harvested populations: plasticity and evolution of age and size at maturation

We investigate harvest-induced adaptive changes in age and size at maturation by modelling both plastic variation and evolutionary trajectories. Harvesting mature individuals displaces the reaction norm for age and size at maturation toward older ages and larger sizes and rotates it clockwise, whereas harvesting immature individuals has the reverse qualitative effect. If both immature and mature individuals are harvested, the net effect has approximately the same trend as when harvesting immature individuals only. This stems from the sensitivity of the evolutionary response, which depends on the maturity state of harvested individuals, but also on the type of harvest mortality (negatively or positively density dependent, density independent) and the value of three life-history parameters (natural mortality, growth rate and the trade-off between growth and reproduction). Evolutionary changes in the maturation reaction norm have strong repercussions for the mean size and the density of harvested individuals that, in most cases, result in the reduction of biomass--a response that population dynamical models would overlook. These results highlight the importance of accounting for evolutionary trends in the long-term management of exploited living resources and give qualitative insights into how to minimize the detrimental consequences of harvest-induced evolutionary changes in maturation reaction norms.     

Ocean Acidification May Aggravate Social-Ecological Trade-Offs in Coastal Fisheries

Ocean Acidification (OA) will influence marine ecosystems by changing species abundance and composition. Major effects are described for calcifying organisms, which are significantly impacted by decreasing pH values. Direct effects on commercially important fish are less well studied. The early life stages of fish populations often lack internal regulatory mechanisms to withstand the effects of abnormal pH. Negative effects can be expected on growth, survival, and recruitment success. Here we study Norwegian coastal cod, one of the few stocks where such a negative effect was experimentally quantified, and develop a framework for coupling experimental data on OA effects to ecological-economic fisheries models. In this paper, we scale the observed physiological responses to the population level by using the experimentally determined mortality rates as part of the stock-recruitment relationship. We then use an ecological-economic optimization model, to explore the potential effect of rising CO₂ concentration on ecological (stock size), economic (profits), consumer-related (harvest) and social (employment) indicators, with scenarios ranging from present day conditions up to extreme acidification. Under the assumptions of our model, yields and profits could largely be maintained under moderate OA by adapting future fishing mortality (and related effort) to changes owing to altered pH. This adaptation comes at the costs of reduced stock size and employment, however. Explicitly visualizing these ecological, economic and social tradeoffs will help in defining realistic future objectives. Our results can be generalized to any stressor (or stressor combination), which is decreasing recruitment success. The main findings of an aggravation of trade-offs will remain valid. This seems to be of special relevance for coastal stocks with limited options for migration to avoid unfavorable future conditions and subsequently for coastal fisheries, which are often small scale local fisheries with limited operational ranges.     

Effects of Management Tactics on Meeting Conservation Objectives for Western North American Groundfish Fisheries

There is considerable variability in the status of fish populations around the world and a poor understanding of how specific management characteristics affect populations. Overfishing is a major problem in many fisheries, but in some regions the recent tendency has been to exploit stocks at levels below their maximum sustainable yield. In Western North American groundfish fisheries, the status of individual stocks and management systems among regions are highly variable. In this paper, we show the current status of groundfish stocks from Alaska, British Columbia, and the U.S. West Coast, and quantify the influence on stock status of six management tactics often hypothesized to affect groundfish. These tactics are: the use of harvest control rules with estimated biological reference points; seasonal closures; marine reserves; bycatch constraints; individual quotas (i.e., ‘catch shares’); and gear type. Despite the high commercial value of many groundfish and consequent incentives for maintaining stocks at their most productive levels, most stocks were managed extremely conservatively, with current exploitation rates at only 40% of management targets and biomass 33% above target biomass on average. Catches rarely exceeded TACs but on occasion were far below TACs (mean catch:TAC ratio of 57%); approximately $150 million of potential landed value was foregone annually by underutilizing TACs. The use of individual quotas, marine reserves, and harvest control rules with estimated limit reference points had little overall effect on stock status. More valuable fisheries were maintained closer to management targets and were less variable over time than stocks with lower catches or ex-vessel prices. Together these results suggest there is no single effective management measure for meeting conservation objectives; if scientifically established quotas are set and enforced, a variety of means can be used to ensure that exploitation rates and biomass levels are near to or more conservative than management targets.     

Contrasting effects of climate change in continental vs. oceanic environments on population persistence and microevolution of Atlantic salmon

Facing climate change (CC), species are prone to multiple modifications in their environment that can lead to extinction, migration or adaptation. Identifying the role and interplay of different potential stressors becomes a key question. Anadromous fishes will be exposed to both river and oceanic habitat changes. For Atlantic salmon, the river water temperature, river flow and oceanic growth conditions appear as three main stressing factors. They could act on population dynamics or as selective forces on life‐history pathways. Using an individual‐based demo‐genetic model, we assessed the effects of these factors (1) to compare risks of extinction resulting from CC in river and ocean, and (2) to assess CC effects on life‐history pathways including the evolution of underlying genetic control of phenotypic plasticity. We focused on Atlantic salmon populations from Southern Europe for a time horizon of three decades. We showed that CC in river alone should not lead to extinction of Southern European salmon populations. In contrast, the reduced oceanic growth appeared as a significant threat for population persistence. An increase in river flow amplitude increased the risk of local extinction in synergy with the oceanic effects, but river temperature rise reduced this risk. In terms of life‐history modifications, the reduced oceanic growth increased the age of return of individuals through plastic and genetic responses. The river temperature rise increased the proportion of sexually mature parr, but the genetic evolution of the maturation threshold lowered the maturation rate of male parr. This was identified as a case of environmentally driven plastic response that masked an underlying evolutionary response of plasticity going in the opposite direction. We concluded that to counteract oceanic effects, river flow management represented the sole potential force to reduce the extinction probability of Atlantic salmon populations in Southern Europe, although this might not impede changes in migration life history.     

Ecological and evolutionary patterns of freshwater maturation in Pacific and Atlantic salmonines

Reproductive tactics and migratory strategies in Pacific and Atlantic salmonines are inextricably linked through the effects of migration (or lack thereof) on age and size at maturity. In this review, we focus on the ecological and evolutionary patterns of freshwater maturation in salmonines, a key process resulting in the diversification of their life histories. We demonstrate that the energetics of maturation and reproduction provides a unifying theme for understanding both the proximate and ultimate causes of variation in reproductive schedules among species, populations, and the sexes. We use probabilistic maturation reaction norms to illustrate how variation in individual condition, in terms of body size, growth rate, and lipid storage, influences the timing of maturation. This useful framework integrates both genetic and environmental contributions to conditional strategies for maturation and, in doing so, demonstrates how flexible life histories can be both heritable and subject to strong environmental influences. We review evidence that the propensity for freshwater maturation in partially anadromous species is predictable across environmental gradients at geographic and local spatial scales. We note that growth is commonly associated with the propensity for freshwater maturation, but that life-history responses to changes in growth caused by temperature may be strikingly different than changes caused by differences in food availability. We conclude by exploring how contemporary management actions can constrain or promote the diversity of maturation phenotypes in Pacific and Atlantic salmonines and caution against underestimating the role of freshwater maturing forms in maintaining the resiliency of these iconic species.     

L'otolithe: la ≪ boîte noire ≫ des Téléostéens

Calcified structures such as otoliths have been used successfully for estimating the age of teleost fishes for many years. Otoliths record age as well as annual and/or seasonal events in the lives of fish and they are an important source of life history information. Otoliths have been found to contain characteristics that are stock specific. Elemental composition might be useful for identifying non-mixing groups of fish that may be regarded as separate stocks for fisheries management. Examination of otolith microstructure has been used to study early life history. Papers describe the use of otolith microstructure combined with chemical analysis to assess the relative significance of environmental variables: feeding frequency, photoperiod and temperature, migration from freshwater to marine water, pollution, etc. Otoliths are the first calcified structures that appear during the early development of fish and they provide a more adequate record of the growth history than scales. Otoliths represent the black box of teleost fish.     

Exploited marine invertebrates: genetics and fisheries

The application of genetic techniques to invertebrate fisheries is in many ways essentially similar to that in vertebrate (i.e. finfish) fisheries, for which there is already an extensive body of published data. However, there are also relative differences which lead to particular problems in the use of genetic data to study commercially important invertebrate species. The main role for genetics of both vertebrates and invertebrates has been, and is likely to continue to be, the identification of groups of interbreeding individuals as the basis for a fishery. It is in the identification of the breeding unit that the genetic differences between vertebrates and invertebrates can be of practical significance. The genetic breeding unit, usually called a 'stock' in fisheries biology, generally shows a certain uniformity of size in most marine fish which have been studied. Smaller or less mobile fish (e.g. flatfish) may only range a few tens of kilometres to their breeding grounds, whilst in more mobile, particularly migratory pelagic species (e.g. Scombridae), the area occupied by a stock is likely to be far greater and for a few (e.g. large pelagic elasmobranchs), a single unit of stock may be almost circumglobal. However, marine fish generally, particularly those large or plentiful enough to be of commercial interest, are likely to be fairly mobile and in many cases the order of mobility is likely to be in the region we might predict from our knowledge of the biology and habits of the species. In the genetic assessment of `stocks' for invertebrate fisheries, we face a number of additional problems, mostly related to the large evolutionary range of invertebrates exploited and their widely different biology. Although in Europe and North America marine invertebrate fisheries may be thought of as being mainly for decapod crustaceans and bivalve molluscs, globally commercially important marine invertebrate fisheries range from sponges to squid and include such diverse groups as sea cucumbers, barnacles, krill, octopuses, cuttlefish, sea anemones, ascidians, polychaetes, sea urchins, gastropods and jellyfish. An obvious feature of many of these invertebrates is that the adult (i.e. commercial) stage of the life cycle is sessile (e.g. barnacles, sponges, ascidians) or of very limited mobility (e.g. sea anemones, sea urchins, bivalves, gastropods), with the result that the dispersive phase of the life cycle is the larva. Other groups (e.g. krill, jellyfish) are planktonic or nektonic and may cover very large distances, but, unlike fish, have little control over the distance or direction of travel, whilst some of the open ocean pelagic squid are more mobile than most fish and may migrate thousands or kilometres to spawning grounds. The very low mobility of both larva and adult in some invertebrates indicates that dispersal, and hence stock size, is likely to be low and that, therefore, stocks are far more vulnerable to overfishing than in most fish species. An additional difficulty is that genetic studies to date indicate a remarkably high incidence of cryptic speciation in marine invertebrates, sometimes even in comparatively well studied commercially important species. Thus, although to date marine invertebrate fisheries have not received the same level of attention from geneticist as finfish fisheries, it is clear that for invertebrate fisheries genetic data are relatively far more important if a fishery is to be exploited without being endangered.     

Probabilistic maturation reaction norms assessed from mark–recaptures of wild fish in their natural habitat

Reaction norms are a valuable tool in evolutionary biology. Lately, the probabilistic maturation reaction norm approach, describing probabilities of maturing at combinations of age and body size, has been much applied for testing whether phenotypic changes in exploited populations of fish are mainly plastic or involving an evolutionary component. However, due to typical field data limitations, with imperfect knowledge about individual life histories, this demographic method still needs to be assessed. Using 13 years of direct mark–recapture observations on individual growth and maturation in an intensively sampled population of brown trout (Salmo trutta), we show that the probabilistic maturation reaction norm approach may perform well even if the assumption of equal survival of juvenile and maturing fish does not hold. Earlier studies have pointed out that growth effects may confound the interpretation of shifts in maturation reaction norms, because this method in its basic form deals with body size rather than growth. In our case, however, we found that juvenile body size, rather than annual growth, was more strongly associated with maturation. Viewed against earlier studies, our results also underscore the challenges of generalizing life‐history patterns among species and populations.     

Evolution of growth by genetic accommodation in Icelandic freshwater stickleback

Classical Darwinian adaptation to a change in environment can ensue when selection favours beneficial genetic variation. How plastic trait responses to new conditions affect this process depends on how plasticity reveals to selection the influence of genotype on phenotype. Genetic accommodation theory predicts that evolutionary rate may sharply increase when a new environment induces plastic responses and selects on sufficient genetic variation in those responses to produce an immediate evolutionary response, but natural examples are rare. In Iceland, marine threespine stickleback that have colonized freshwater habitats have evolved more rapid individual growth. Heritable variation in growth is greater for marine full-siblings reared at low versus high salinity, and genetic variation exists in plastic growth responses to low salinity. In fish from recently founded freshwater populations reared at low salinity, the plastic response was strongly correlated with growth. Plasticity and growth were not correlated in full-siblings reared at high salinity nor in marine fish at either salinity. In well-adapted lake populations, rapid growth evolved jointly with stronger plastic responses to low salinity and the persistence of strong plastic responses indicates that growth is not genetically assimilated. Thus, beneficial plastic growth responses to low salinity have both guided and evolved along with rapid growth as stickleback adapted to freshwater.     

The role of marine reserves in achieving sustainable fisheries

Many fishery management tools currently in use have conservation value. They are designed to maintain stocks of commercially important species above target levels. However, their limitations are evident from continuing declines in fish stocks throughout the world. We make the case that to reverse fishery declines, safeguard marine life and sustain ecosystem processes, extensive marine reserves that are off limits to fishing must become part of the management strategy. Marine reserves should be incorporated into modern fishery management because they can achieve many things that conventional tools cannot. Only complete and permanent protection from fishing can protect the most sensitive habitats and vulnerable species. Only reserves will allow the development of natural, extended age structures of target species, maintain their genetic variability and prevent deleterious evolutionary change from the effects of fishing. Species with natural age structures will sustain higher rates of reproduction and will be more resilient to environmental variability. Higher stock levels maintained by reserves will provide insurance against management failure, including risk-prone quota setting, provided the broader conservation role of reserves is firmly established and legislatively protected. Fishery management measures outside protected areas are necessary to complement the protection offered by marine reserves, but cannot substitute for it.     

Population dynamics and potential of fisheries stock enhancement: practical theory for assessment and policy analysis

The population dynamics of fisheries stock enhancement, and its potential for generating benefits over and above those obtainable from optimal exploitation of wild stocks alone are poorly understood and highly controversial. I review pertinent knowledge of fish population biology, and extend the dynamic pool theory of fishing to stock enhancement by unpacking recruitment, incorporating regulation in the recruited stock, and accounting for biological differences between wild and hatchery fish. I then analyse the dynamics of stock enhancement and its potential role in fisheries management, using the candidate stock of North Sea sole as an example and considering economic as well as biological criteria. Enhancement through release of recruits or advanced juveniles is predicted to increase total yield and stock abundance, but reduce abundance of the naturally recruited stock component through compensatory responses or overfishing. Economic feasibility of enhancement is subject to strong constraints, including trade-offs between the costs of fishing and hatchery releases. Costs of hatchery fish strongly influence optimal policy, which may range from no enhancement at high cost to high levels of stocking and fishing effort at low cost. Release of genetically maladapted fish reduces the effectiveness of enhancement, and is most detrimental overall if fitness of hatchery fish is only moderately compromised. As a temporary measure for the rebuilding of depleted stocks, enhancement cannot substitute for effort limitation, and is advantageous as an auxiliary measure only if the population has been reduced to a very low proportion of its unexploited biomass. Quantitative analysis of population dynamics is central to the responsible use of stock enhancement in fisheries management, and the necessary tools are available.     

The anatomy of a shrike bite: bill shape and bite performance in Loggerhead Shrikes

There is evidence that fisheries are altering the phenotypic composition of fish populations, often in ways that may reduce the value of fish stocks for the exploiters. Despite the increasing number of theoretical and field studies, there is still debate as to whether these changes are genetic, can be reversed, and are occurring rapidly enough to be considered in fisheries management. We review the contribution that selection experiments have already provided with respect to the study of the evolutionary effect of fisheries, identify issues that still require more study, and outline future directions for doing so. Selection experiments have already been crucial in showing that harvesting can lead to phenotypic and genetic evolution over relatively short time frames. Furthermore, the experiments have shown the changes involve many other traits than those under direct selection, and that these changes tend to have population‐level consequences, including a decreasing fisheries yield. However, experiments focused on fisheries‐induced evolution that fulfil all our requirements are still lacking. Future studies should have more controlled and realistic set‐ups and assess genetic changes in maturation and growth (i.e. traits most often reported to change) to be more relevant to exploited populations in the wild. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 485–503.     

Discovery and characterization of single nucleotide polymorphisms in two anadromous alosine fishes of conservation concern

Freshwater habitat alteration and marine fisheries can affect anadromous fish species, and populations fluctuating in size elicit conservation concern and coordinated management. We describe the development and characterization of two sets of 96 single nucleotide polymorphism (SNP) assays for two species of anadromous alosine fishes, alewife and blueback herring (collectively known as river herring), that are native to the Atlantic coast of North America. We used data from high‐throughput DNA sequencing to discover SNPs and then developed molecular genetic assays for genotyping sets of 96 individual loci in each species. The two sets of assays were validated with multiple populations that encompass both the geographic range and the known regional genetic stocks of both species. The SNP panels developed herein accurately resolved the genetic stock structure for alewife and blueback herring that was previously identified using microsatellites and assigned individuals to regional stock of origin with high accuracy. These genetic markers, which generate data that are easily shared and combined, will greatly facilitate ongoing conservation and management of river herring including genetic assignment of marine caught individuals to stock of origin.