Sustainable Management Plans in Fisheries and Genetic Tools: An Overview of the Challenge in Invertebrates’ Fisheries at the Central Area of the Southern Bay of Biscay, Spain

Abstract

The fishing and aquaculture sectors are an important source of development around the globe. In Asturias (Spain), the diversity and richness of the fishing grounds of the Cantabrian Sea favored the historical settlement of a large number of communities closely linked to the marine environment and fishing resources, forming an integral part of the region’s cultural and natural heritage. However, aquatic ecosystems are facing, nowadays, important threats from anthropogenic activities. To address these problems and avoid their impact on fishing activities, it is essential to know the ecological and genetic status of the species. Despite this, the application of genetic tools is still incipient in many species of commercial interest; however, its use can help to generate data that allow better regulation and fisheries planning. Here, the use of genetic markers and educational strategies in the management of some shellfish species of great commercial and cultural value in Asturias are reviewed. Moving toward sustainable fisheries management is a priority that can only be achieved through R + D + i, educational strategies, and the development and implementation of a regional strategy oriented toward the sustainable management and exploitation.

1. Introduction

In 1984, the United Nations (UN) established an independent group of 22 individuals from member states and charged them with identifying long-term environmental strategies for the international community [1]. In the resulting report of the World Commission on Environment and Development, entitled Our Common Future—also known as the Brundtland Report [2], the term “sustainable development” was used extensively and defined as “development that meets the needs of the present without compromising the ability of future generations to meet their own needs.”

The fisheries, seafood, and aquaculture sectors are an important source of food and income for millions of people around the world [3]. Addressing the problems associated with fisheries is an essential purpose, not only in the development of marine conservation policies but also for the achievement of the sustainable development goals (SDGs) of the 2030 Agenda, a major agreement that was signed in 2015 among 193 countries [4]. The achievement of these SDGs should have a strong influence on the governance of sustainable fisheries and aquaculture, ensuring that fisheries and aquaculture adapt to the impacts of climate change and improve the resilience of food production systems [3].

In addition, aquatic ecosystems face today significant threats from anthropogenic activities. In global ocean systems, concerns include climate change, overfishing, dispersal of invasive species, fertilizer runoff, plastic pollution, ocean acidification, and general defaunation [5, 6, 7, 8, 9, 10]. Only 65.8% of fish stocks are currently classified as being exploited within biologically sustainable levels, continuing a downward trend that has been occurring since 1974. Similarly, underexploited species account only for 6.2% –steadily declining from 1974 to the present—whereas stocks exploited at maximum sustainable levels account for 59.6% [11].

It has been demonstrated that when fisheries are properly managed, there are significant decreases in fishing pressure and important increases in stock biomass, with some stocks having reached biologically sustainable levels, underscoring the relevant role of fisheries managers and governments when willing to take strong action [12]. The UN Code of Conduct for Responsible Fisheries states that in adopting management measures, the “best available scientific data should be used to assess the state of fishery resources” [13]. However, most exploited stocks globally are classified as data-poor stocks [14] and their status, although highly uncertain, is generally considered to be worse than that of data-rich stocks [15]. Recently, it has been argued that stock estimates based primarily on historical catch series performed on average 25% better than a random estimate; but in turn, these methods assigned fisheries the wrong FAO status category 57% of the time [16]. Substantial improvements in estimates of the state of exploited stocks worldwide depend on the expansion of new information and efficient use of existing data [16].

The use of molecular genetic techniques in fisheries research has increased dramatically in recent decades, paralleling the awareness of the value of genetic data and mainly due to the increased number of techniques available and improvements in computer technology [17, 18]. However, the application of genetic techniques to invertebrate fisheries or related problems has been remarkably scarce. Thus, most of the invertebrate groups of fishery interest have been the subject of little or no genetic study in relation to these fisheries [19].

We reviewed here the use of genetic markers as well as educative strategies in the fisheries management of some shellfish species with great commercial and cultural value in Asturias, the central area of the southern Bay of Biscay, Spain, to move forward with the relevant aim of generating data to support the design of sustainable fisheries management plans.

2. Fisheries in the central Cantabrian Sea: evidence, needs, and actions aimed at reaching sustainable exploitation levels

2.1 Fisheries in the principality of Asturias

The Principality of Asturias is an autonomous community located in northern Spain (SW Europe) bordered by the Cantabrian Sea to the north and the autonomous regions of Castilla y León, Cantabria, and Galicia to the south, east, and west, respectively. The Cantabrian Sea is the transition from the Atlantic Ocean to the Bay of Biscay, between Spain and France. The coast of Asturias covers about 30% of the Cantabrian coast and presents a general E-W trend along approximately 335 km. In general, this coastline is eminently rocky and abrupt—with a predominance of north-facing cliffs, dotted with small coves, beaches, and dune systems associated with the wider beaches [20].

Currently, the coast of Asturias is one of the most populated areas in the region, which is linked to the presence of industrial activity, such as fishing industry, factories, and ports, and to the tourist exploitation of natural resources. The historical settlement of a large number of coastal communities strongly linked to the marine environment and fishing resources was favored by the diversity and richness of the Cantabrian fishing grounds [20, 21]. These regional fishing grounds have been recently redefined and mapped, totaling 226 and occupying 984,038 hectares.

Fishing is a traditional activity linked to the Asturian coast since prehistoric times, as evidenced by archeological excavations in which numerous mollusks, crustaceans, salmonids, and other marine remains have been found [22, 23, 24, 25, 26, 27]. Nineteen fishing seaports currently operate along the entire coast, and all of them are strategically located taking advantage of the sheltered location of the cliffs. These ports differ in terms of total landings, species marketed, and number of vessels. Of the total number of fishing ports, 17 of them record sales for at least 6 months of the year [21]. The National Strategic Plan of the European Fisheries Fund established that of the total number of councils that form the Asturian coastal belt, only Muros, Castrillón, and Caravia do not depend on fishing activity [28].

In Asturias, specialists agree in considering artisanal vessels registered in the category of the national census of the operational fishing fleet of “minor gears” [29], and, in 2010 there were 233 vessels registered in that category. However, according to the data collected in the Census of the Fishing Fleet registered in Asturias, in 2016 the number had decreased to 202 and, although at present (latest data from 2021) the total number of artisanal vessels totals 192—out of a total of 248 active vessels—distributed in 19 ports—representing 77.4% of the total fishing fleet with home port in Asturias –, the downward trend in the fleet of minor gears is not so pronounced, even stabilizing.

In terms of fishing strategies, most of this regional artisanal fleet switches between different gears throughout the year and exploits areas that can be reached in a few hours from fishing ports. Although the landings of the artisanal fleet—in kilograms—only represent around 10% of the total regional catch, they account for approximately 30% of the total economic value generated by the landings, due to the higher first sale price of these catches (high-value seafood products) compared to those of other fleet segments—average 4.25 €/kg compared to 1.68 €/kg –. The regional artisanal fleet targets many species, including high-value species, and landings are characterized by quality, freshness, and higher first-sale profit. This partly compensates for the lower weight of landings and lower fishing power [21, 30]. The main species landed by the Asturian artisanal fleet are hake (Merluccius merluccius), mackerel (Scomber scombrus), conger eel (Conger conger), sea bass (Dicentrarchus labrax), and octopus (Octopus vulgaris), in addition to the shellfishing of stalked barnacle (Pollicipes pollicipes). Eel (Anguilla anguilla) fishing, and other fishing activities, such as stalked barnacle (P. pollicipes) harvesting, play a fundamental role as alternative fishing activities during certain periods when it is difficult and unprofitable to carry out other activities, that is, the first months of the year when many fishing activities cannot be carried out due to bad weather conditions [30].

Artisanal fisheries have traditionally received less research effort than industrial fisheries and have generally received little attention in Europe [31, 32]. This lack of information has reduced the potential for developing effective and integrated management measures aimed at improving the long-term sustainability of artisanal fisheries, considering the complex interactions and linkages between the human and natural dimensions within these fisheries [33]. Despite the comparatively low volume of catches and its economic relevance, artisanal fisheries are important in terms of employment and must be considered in economic terms at the local level. It contributes to strengthening people’s attachment to their territory, increasing social stability in rural and peripheral areas [32].

2.2 Traceability as a cornerstone of sustainable fisheries management in Asturias: a case study on scallops (family Pectinidae)

The UN Code of Conduct for Responsible Fisheries stated in 1995 that the “best available scientific data for assessing the state of fishery resources” should be used for effective fisheries management measures [13]. Traditionally, fisheries conservation and management have been conducted on the basis of abundance data, productivity estimates, and information on stock dynamics—that is, an intraspecific group of randomly mating individuals with temporal and spatial integrity [34, 35, 36, 37]. However, managers need to be aware that the implementation of legislation, stocking strategies, and other management activities affect the genetic composition of populations [38, 39, 40]. Genetic factors play a role in the conservation of fishery resources because fishery resources are the product of their genes, the environment, and the interactions between them [41]. Although understanding of the state of global fisheries has now improved over the last decade, there is a consensus that data remain incomplete, with most of the world’s fish stocks lacking formal statistical assessments [16]. In addition, this lack of biological data is compounded by the fact that not all fishery catches are properly reported or recorded by governmental or non-governmental agencies. These unreported catches may be illegal, of unregulated species, or simply not monitored due to logistical barriers [42]. Mislabeling, inaccurate species identification in landings [43, 44], or the modification of the catch area are other factors that also contribute to the unreported exploitation of stocks and the consequent reduction of fishery resources.

The Common Market Organization (CMO) for fishery and aquaculture products is laid down in Regulation (EU) No 1379/2013 of the European Parliament. In Article 35, the commercial designation of the species and its scientific name (among other relevant data) are included as mandatory information on the relevant labeling. Furthermore, Article 37 stipulates that the Member States shall draw up and publish a list of the commercial designations accepted in their respective territories, together with their scientific names [45]. Informative labeling is particularly important for processed products, as any recognizable external morphological characteristics are often removed, so consumers rely on product labeling for information about the contents of the product.

In recent years, molecular biology techniques—based on DNA and sequencing—have gained notoriety in the study of mislabeling and food fraud, allowing species identification even if the product under suspicion is highly processed [46, 47]. A combined assessment of the levels of fraud in the commercialization of fresh and processed specimens of the family Pectinidae, both in retail establishments and restaurants, has been carried out using genetic methods based on mtDNA—16S rRNA gene–and taxonomic methods in Asturias [48]. That research showed that out of 148 samples of 15 commercial products analyzed, 73 samples (49%) and 9 (60%) of the 15 commercial products studied were mislabeled. In the case of the 20 samples purchased in 20 restaurants, all specimens labeled with the common name “zamburiña” were assigned to the Pacific scallop (A. purpuratus), resulting in 100% substitution fraud in the samples analyzed. These results are in agreement with the numerous works previously carried out that used molecular markers as an effective tool for the identification of species—both in fresh and frozen products as well as in highly processed ones—that, in many cases, were impossible to identify without the use of this type of tools [49, 50, 51, 52]. At the same time as Parrondo et al. study [48] was published, Klapper and Schröder report the development of a multiplex qPCR assay using a TaqMan probe that allowed the rapid and reliable identification of three commercially important scallop species in German supermarkets and fishmongers—the scallop (P. maximus), the Atlantic scallop (Placopecten magellanicus), and the Japanese scallop (Patinopecten yessoensis) [53]. Using this new tool, Klapper and Schroeder revealed a mislabeling rate of 48%—especially high for products purchased in fish shops. Furthermore, they showed that only 18 out of 33 (52%) samples were correctly labeled and in 12 (36%) samples the scientific name was not provided. Where appropriate, the rate of mislabeling in supermarkets was relatively low (5 out of 21, 24%) compared to fishmongers (8 out of 10, 80%) and restaurants (2 out of 2, 100%) [53]. Despite differences in methodology and target species, the results obtained for Germany by Klapper and Schröder are consistent with the data produced by Parrondo et al. [48] for Asturias.

These investigations join those previously presented by other authors, both in the development or use of forensic biology techniques and in the creation of a threshold of knowledge in the study of mislabeling and fraud of fishery products from marine invertebrates, specifically scallops [54, 55, 56, 57, 58, 59]. Despite the difficulty in making accurate estimates of the extent of mislabeling, especially in invertebrates due to lack of data and bias toward certain taxa and geographical areas [60], the high percentages of errors in product labeling found in Parrondo et al. [48] are not unusual in other European countries, such as Iceland, Finland, or Germany, where similar results of between 40 and 50% were obtained [51]. These percentages are alarming if we take into account that most of the samplings carried out for these studies (including the present one) lack temporality, being performed only once in a specific locality, so the approximations tend to be always conservative [49].

Research regarding mislabeling and food fraud in seafood products are increasingly extensive at all levels of the production chain [49, 50, 61], the urgent need for control measures throughout marketing to avoid consumer confusion, mislabeling, or potential health problems—such as allergies due to substitutions [62]—is evident. It is worth mentioning that, in general, there is an increased awareness of the industry to improve the transparency of the food chain, as well as the growth in the number of inspections put in place by European official control bodies, which have achieved a significant reduction in the number of incidences of misdescriptions [63]. This lack of monitoring plays an important role in threatening the sustainability of fisheries, despite international efforts, and may even imply the eventual extinction of more vulnerable overfished species [64].

In Asturias, the existing regulation gives legal and regulatory support to food quality—especially to differentiated quality and organic production—and establishes regulation of infractions and sanctions, with the aim of tackling intrusion and fraud [65]. However, the Asturian law is framed within Community regulations and applies European legislation on labeling. That is why, from a legislative point of view, Article 35 of Regulation (EU) No 1379/2013 of the European Parliament should be amended to include the fishery and aquaculture products listed in points h) and i) of Annex I to that Regulation, which refers to “prepared or preserved fish; caviar and caviar substitutes prepared from fish eggs” and “crustaceans, molluscs, and other aquatic invertebrates, prepared or preserved.” It is indisputable that to implement correct management and planning of the exploitation of marine resources and to watch over the rights of consumers, it is necessary to increase routine controls and sanctions—both on fishery products and those prepared and processed throughout the whole production chain—with emphasis on those stages where there is greater evidence of fraud and on those species to which, perhaps, less attention has been paid, such as marine invertebrates.

2.3 Sustainable fisheries management, certifications, and the scarcity of biological data in Asturias

2.3.1 The MSC octopus fishery in western Asturias: dilemma and challenges

Labeling to provide additional ecological information about a product is usually voluntary. FAO recognized that it could contribute to improved fisheries management and convened a technical consultation in 1998, which led to the development of the “Guidelines for the Ecolabeling of Fish and Fishery Products from Marine Capture Fisheries” [66]. Since then, numerous programs have been proposed for ecolabelling seafood products in an effort to encourage fisheries managers to create sustainable fisheries. One of the most recognized today is the Marine Stewardship Council (MSC)—created in 1997, thanks to a collaboration between the World Wildlife Fund (WWF) and Unilever, a multinational company that markets several international brands [67]. The aim of these initiatives is to provide a market-based incentive for sustainable fisheries management. Processors, wholesalers, and retailers who purchase products from these accredited fisheries may acquire the right to affix an eco-label, informing consumers that the product has been caught in a sustainable fishery. Hypothetically, if there were a demand for environmental quality, consumers would respond by purchasing those products with an eco-label, thereby reducing demand for those without and causing price devaluation on unlabeled products. This may result in fishermen putting pressure on fishery managers to achieve sustainability accreditation and thus receive a higher percentage of the price [67].

In February 2016, the MSC awarded the Tapia, El Porto, Ortigueira, and Veiga fishermen’s associations the first certification for the octopus fishery worldwide. O. vulgaris (Cuvier, 1797) is the cephalopod species with the largest landings in Asturias, being this resource of great importance for the artisanal fleet of the region [68]. This fishery operates with a “management plan for the common octopus (O. vulgaris) in the Principality of Asturias,” developed by the Directorate General of Maritime Fisheries of the Government of Asturias with the collaboration of the fishermen’s guilds, which is revised every year [69]. From that moment on, all octopus caught by certified vessels is eligible to display the blue MSC ecolabel, allowing consumers to enjoy this species with the security that it comes from a sustainable and environmentally friendly fishery [70]. The MSC report accrediting such sustainability highlighted some weaknesses in certifying this fishery, warning that “biological information on the resource was still scarce” and explicitly recommending that “information on the knowledge of octopus stocks should be improved.” This means that relevant parameters, such as maximum sustainable yield and stock definitions, were still lacking or incomplete for octopus fisheries.

Stock assessment is crucial, being an integral part of fisheries management. However, it can be challenging due to the methodological difficulties arising from marine monitoring using traditional methods—such as individual capture (with trawls, nets, or traps) or visual identification of species based on their distinctive morphological characteristics—and the amount of time consumed. Moreover, its financial cost is high, and, in some cases, it is simply unfeasible. The need to overcome these impediments has stimulated the search for new tools and approaches to integrate different environmental dimensions into decision-making in a data-driven policy approach [71].

Since 2016, improvements have been made in those areas where information was lacking for the management of the octopus fishery in Asturias. Particularly important has been the development of a model for octopus stock assessment, and the determination of annual reference points for the fishery, allowing the estimation of an annual TAC per campaign that responds to the situation of the octopus stock in the area [72], as well as making it possible for octopus fished with traps in western Asturias to have achieved—in this year 2021 and for five more years—the recertification of this MSC ecolabel. This work is part of a research project (ECOSIFOOD; MCI-20-PID2019-108481RB-100) funded in 2020 by the Spanish National State Program of Research and Development oriented to the challenges of society.

This last research project is also included as a target to work on obtaining new molecular traceability matrices based on new genomic and environmental DNA (eDNA) data from octopus and their application in temporal and spatial samples to help in detection, quantification, defining historic and contemporary patterns of genetic variation data, stocks and management units. The concept of the biological stock as the basic population unit of exploited species is fundamental to the management of wild fisheries. The delimitation of appropriate conservation units—which is the core of short-term management programs—is also a difficult task in marine systems that have traditionally been characterized as genetically undifferentiated populations [73] due to the large population size, high dispersal potential, and high fecundity of these species [74, 75].

The collection and analysis of water samples for eDNA has, in many cases, proven to be a cost-effective, sensitive, and noninvasive method for species presence/absence surveys, in contrast to established monitoring techniques that rely on the capture of whole organisms [76, 77, 78]. Studies now abound listing the many qualities of eDNA analyses for aquatic species detection and distribution assessment using DNA released into the environment by marine organisms, both vertebrates [79, 80, 81] and invertebrates [82, 83, 84]. The development of more reliable and cost-effective procedures for monitoring commercial species populations may, therefore, improve stock assessment [85]. An eDNA-based method was developed for stock assessment of O. vulgaris, pioneering work in the use of this methodology to estimate the sustainability of common octopus fisheries [86]. Furthermore, in that work it was found a positive and significant correlation—Pearson correlation coefficient 0.38627, p-value = 0.01261—between octopus biomass and eDNA abundance detected in tank experiments [86]. These results are in agreement with previous studies that showed a strong linear relationship in aquaria: Takahara et al. found that eDNA concentration was positively correlated with carp biomass in both aquaria and experimental ponds, furthermore, they used this method to estimate carp biomass and distribution in a natural freshwater pond [87]; Maruyama et al. examined the effect of the developmental stage of sunfish (Lepomis macrochirus) on environmental DNA release rate, finding a positive relationship between fish size and eDNA release rate [88]; and Klymus et al. used controlled laboratory experiments to measure the amount of eDNA that two invasive carp species (Hypophthalmichthys nobilis and Hypophthalmichthys molitrix) shed into the water, finding a positive relationship with fish biomass by finding that fed fish, compared to non-fed fish, excrete more eDNA [89].

Other authors have found this relationship to be less pronounced [90, 91, 92] or even nonexistent [93] in natural ecosystems. However, in more recent studies, Spear et al. have shown that pikeperch density explains most of the variance in eDNA recovered in lake surface waters in natural systems [94]. Quantification of eDNA abundance is based on the assumption that local population size can be inferred by measuring eDNA concentration at a given locality and that this estimate represents the quantitative relationship between eDNA concentration and underlying population size [95]. However, such a relationship may not always be true, or even present in most cases. The results of Mauvessau et al. [86] show significant variations in the amounts of eDNA detected in the different sampling points located in the Cantabrian Sea. In any case, the observed variation in the amount of eDNA may be due to different and even unknown factors. Compared to eDNA sampling in river systems—which also poses its own set of problems, often difficult to address—factors such as tides, currents, large depths, and rapid movements of individuals in three dimensions may affect the collection of unbiased samples [71, 96].

The results presented by Mauvisseau et al. [86] were obtained using species-specific primers and the qPCR technique using the SYBR Green compound—double-stranded DNA-binding dye that allows the detection of the PCR product as it accumulates during PCR, as it is a simple, easy, and economical option. However, other types of technical approaches are now common, such as qPCR using TaqMan probe or recently digital droplet PCR (ddPCR) [97]. More recently, intraspecific diversity assessments have been performed in several species [98, 99], finding multiple haplotypes that had previously been identified from tissue-derived DNA by Sanger sequencing. This is a revolutionary tool for fisheries and population management, as the use of eDNA could allow detection, quantification, and estimation of diversity with minimal sampling efforts.

The use of environmental DNA-based tools to quantify commercial species populations is of great interest to fisheries managers and policy makers, as stock assessment is a central component of any management and/or conservation program [71]. There is a strong need to inform researchers, advisors, managers, and other stakeholders about the many challenges (and opportunities) associated with the application of environmental DNA analyses in routine marine fisheries management [85].

2.3.2 Getting data from a potentially eco-certifiable fishery in Asturias: the highly valued goose barnacle P. pollicipes

The stalked barnacle fishery in Western Asturias has been co-managed by the fishermen’s guilds and the Center for Fishing Experimentation (General Directorate of Maritime Fisheries of the Principality of Asturias) since the eighties. On the west coast of Asturias, harvesting is not open, but rather each fishery guild or group of guilds is granted the right to exclusively exploit barnacles in a strip of the coast, a system known as “exploitation plans.” In exchange, the guilds commit to exploiting the barnacle in a sustainable manner (complying with the rules established in the exploitation plan) and to report in minute detail the date, place, and amount of barnacle extracted, which is an extraordinary source of information for research and management [100]. In these systems, fishermen become co-responsible for management, intervening in the design of the exploitation plans. The DGP collects and analyzes the data on daily catches per shellfish gatherer and extraction area collected by the authorized fish rangers in each exploitation plan. At the same time, in collaboration with shellfish harvesters and fish wardens, the total and partial closed seasons and areas for each season are evaluated and proposed.

The potential of genetic approaches for the identification of fish stocks has long been recognized. However, in practice, stock assessments for management purposes often do not incorporate information on the biological stock structure because genetic and biological data are unavailable or ambiguous [101]. Even today, the isolation and characterization of new molecular markers remain difficult and costly for many non-model species [102]. Although microsatellite markers—and now also SNPs—are increasingly available for more species, studies on most marine organisms are still limited by marker availability and biased toward those of greatest commercial interest. A good example of this could be the barnacle fishery, which has an annual economic value of 10 million euros, with about 500 t of landings and 2100 professional fishermen involved [103] and yet has hardly been studied from a genetic point of view [100, 104, 105]. Although this may be alarming due to their importance, crustaceans—and other marine invertebrates as well—still lack genetic and genomic resources compared to other widely studied groups [106, 107]. The research projects PERCEBES (PCIN-2016-120) (funded by the EU Biodiversa call in 2016) and ECOSIFOOD (MCI-20-PID2019-108481RB-100) have targeted this objective of developing new genetic tools (microsatellites and SNPs) to assess genetically the fishery stocks of the stalked barnacle P. pollicipes.

Microsatellites are established as the most popular and versatile marker type [17]. Their hypervariable nature confers sufficient power to compare gene pools between populations, as unique alleles appear at low frequencies that are useful for discriminating populations. Under a standard set of parameters that includes 20 highly mutational microsatellite loci and approximately 50 individuals from each of the subpopulations to be sampled, the power to detect deviations from panmixia is very high—even with high gene flow [73]. This is the case of barnacle populations, where patterns of spatial and temporal structuring have been observed at a scale where variability should be homogenized by gene flow through larval dispersal and coined as chaotic genetic patchiness (CGP) [108, 109, 110].

The detection of genetic differences between samples far apart in space or time implies the existence of some level of demographic independence and the presence of separate populations [34, 73, 111]. The ongoing analyses carried out with 20 new microsatellite loci aimed to define, with greater precision, the spatiotemporal evolution of the genetic structure of the barnacle P. pollicipes [112]. Preliminary results using microsatellites pointed out a population dynamics where P. pollicipes displays high genetic diversity along the Iberian Peninsula, which is attributable to large effective population sizes representing a well-connected network of local populations. However, temporal and spatial genetic differentiation of populations over regional scales, on one hand, and a significant reduction in genetic diversity in juveniles, on the other hand, clearly indicate that patterns of exchanges together with seasonal wind-induced upwelling may induce genetic differences between settlers throughout generations. Such patterns of chaotic genetic patchiness are likely due to sweepstake reproductive success with possible collective dispersal or episodic self-recruitment events [112]. In the specific case of the barnacle fishery, the future use of SNP markers would allow a more precise review of concepts such as population structure—which has been described as patchy [112]—and larval connectivity—which on the Asturias coast seems to take place on a small scale [100]; also if there are differences or not between the phenotypes considered of better and worse quality—in previous reports, these differences were not significant [113]—or how landscape components affect the resource on its quality [114]; allowing to know the evolutionary forces that drive the spatio-temporal heterogeneity of barnacles, and thus being able to assess and preserve the evolutionary potential of this fishery resource in a context of global change. Although these boundaries are usually spatially defined, they may also have a temporal component [115].

2.3.3 The management of declining or depleted stocks in Asturias: restock or restore? The sea urchin case study

Paracentrotus lividus is a sea urchin with an important ecological role in the Cantabrian Sea ecosystem. In the same context of global change and triggered in recent decades by overfishing, there has been a definitive decline in sea urchin (P. lividus) populations on the Asturian coast. Among the measures to mitigate this population collapse, the Government of Asturias decided to establish a year-round ban on the capture of this species and to undertake a population restoration experience with the aim of preserving this marine resource. However, these practices may entail a series of genetic risks that are widely recognized and documented in the literature and that can be summarized as follows: (i) loss of genetic diversity, (ii) loss of fitness, (iii) change in population composition, and (iv) change in population structure. Moreover, although adverse genetic impacts on wild populations are recognized and documented, little effort is devoted to their actual monitoring [116]. Because of this, these practices are highly controversial [117] and their utility is not always clear to fisheries and conservation goals [118]. Genetic monitoring of P. lividus populations in the central Cantabrian Sea (Asturias) was carried out using the mitochondrial DNA cytochrome B gene and microsatellite markers previously described by Calderón et al. [112, 119].

The results of a genetic diversity study based on mtDNA on this marine invertebrate show that the Asturian populations could constitute, at present, a peculiar and so far, undiscovered management unit (MU) of the Bay of Biscay, separate from that of the Atlantic populations. Microsatellite marker data—which reflect recent processes of population dynamics—did not reveal controversial results. However, both markers suggested genetic heterogeneity in the Mediterranean and Candás samples [112]. These results are fundamental, as an essential requirement for sustainable exploitation is the adequacy of biologically relevant processes and the scale of management: mismatches between the two often occur [120]. The P. lividus fishery in Galicia has been an example of how the mismatch between biological, fishery, and management scales causes governance failures, leading to overexploitation. P. lividus is spatially distributed in nested biological units: patches, micropopulations, local populations, and metapopulations. Fishing operations are local and exploit micro-stocks; however, management units in Galicia often comprise more than one local population. This pattern allowed the depletion of several micro-stocks with no short-term signs in exploitation rates across the managed territory [121]. Identification of MUs is fundamental for the management of natural populations and is crucial for controlling the effects of human activity on species abundance [122]. Local sea urchin populations may be more isolated than suggested by larval dynamics [123, 124, 125, 126, 127].

The number of broodstock used in the sea urchin restocking experience carried out so far in Asturias—average number of spawners per event = 14.42—has been clearly far from what is desirable and from the recommended minimum number of broodstock [112]. This causes certain alleles and haplotypes to be overrepresented in the new population, leading to a reduction in the effective population size [128]. Besides this, microsatellite markers used indicated that juvenile individuals used for supplementation were genetically different from wild populations [112]. This means a poor representation of the wild gene pool in broodstock as a result—among other factors—of the low number of individuals used as broodstock since, in the particular case of marine invertebrates, they present a very high fecundity associated with a large variance in reproductive success [129], resulting in small Ne in cultured populations.

In Parrondo et al. [112] work, at least 3.5% overall of the total recaptured sea urchins with hatchery origin were found by randomly sampling 100 juveniles from each of the two restocked localities. Comparison of recapture rates is complicated for pilot studies [118], as they may depend on the objective of the experiment, the number of releases and size of individuals at the time of release, sampling effort, as well as the length of the experimental period and areas surveyed, and also the variance between studies. Despite the already commented previous findings, genetic monitoring of the restocked localities showed that they currently do not differ from the rest of the Asturian localities in terms of genetic diversity using both genetic markers, with no evidence of the Ryman-Laikre effect in the restocked populations [112]. Similar results were found in the P. maximus breeding program in Brest Bay (France), which had no effect on genetic diversity [130] and no R-L effect was detected [131]. Even if the reduction in allelic diversity and the alteration of allele frequencies were limited, they could accumulate over generations, gradually eroding the genetic variability of P. lividus, so long-term monitoring of these populations is proposed as standard practice.

Habitat restoration—taking into account that kelp forests are in serious decline due to, among other factors, the increase in temperature in the Cantabrian sea that has been occurring since the beginning of the 21st century, the increase in the intensity of storms or the limitation of available nutrients due to changes in the frequency of coastal upwelling [132], the construction of shelters against waves, which also seem to be effective in promoting the colonization of kelp [133], as well as the establishment of marine protected areas (MPAs)—which would allow maintaining the supply of larvae—may be other options to be considered to improve sea urchin populations. In some cases, translocation of adult sea urchins could also be considered; however, translocation can have an impact on the “host” population, so it is necessary to manage the stock of animals to be translocated [133]—many of these measures have been successfully implemented in Japan. The integration of aquaculture-based enhancement with habitat restoration presents a notable opportunity for future research and development [134].

2.3.4 Facing biological invasions and their threat to Asturias exploited fishery resources. The Crepidula case study in the Bay of Biscay

Biological invasions are a key component of the ecological and biodiversity conservation crisis. One of the main threats caused by introduced species is the alteration of the structure of host communities -both terrestrial and aquatic- and the modification of ecosystem functioning [135, 136]. Although only a small fraction of the many species introduced outside their native range are able to thrive and invade new habitats, their impact can be dramatic [9, 137]. The invasion process unfolds as a multistage operation involving the acquisition of a propagule in its native range, the transport of that propagule to the new range, and the introduction, establishment, and spread of the invader in the new habitat [138].

Accurate analysis and effective modeling of current and future distributions of invasive alien species (IAS) are highly dependent on the availability and accessibility of occurrence data and information on the natural history of the species [139]. Because conventional sampling techniques often have very low probabilities of detecting rare species in aquatic ecosystems [140], such as the initial stages of invasion processes, not being really effective until the population is established—years after the first introduction—[141], tools that favor immediacy are necessary to combat the spread and establishment of invasive species, carrying out strategies of “early detection and rapid response” (EDRR).

Early detection is a vital step for the effective management of invasive species. The species-specific molecular markers for C. fornicata presented by Miralles et al. can be used to detect the early stages of invasions due to their sensitivity, low cost, and ease and speed of laboratory testing [142]. The results of that research demonstrate the presence of C. fornicata in close proximity to the M. gigas culture facilities operating in the Eo estuary. This oyster is very robust, with great physiological tolerance and an enormous reproductive potential, qualities that favor its cultivation and that have allowed it to become naturalized in all continents, making its eradication a complex task when it reaches high densities. In addition, it is an engineering species that generates important structural changes in the ecosystems it colonizes. M. gigas is also responsible for the global dissemination of many harmful species and pathogens, as is the case of C. fornicata [143]. This is why intensive sampling is necessary, as well as management measures to prevent the spread of C. fornicata, as M. gigas has been previously found in the region [144] even attached to floating marine debris [145], demonstrating its potential disperser of biological invaders [146, 147, 148].

2.4 Marine citizenship for the new generations in Asturias? Education as tools for a sustainable fishing strategy

There is a need for an education strategy at all levels for sustainable development that provides knowledge, skills, attitudes, and values to enable citizens to make informed decisions to take responsible action for environmental integrity. Environmental education is necessary to foster behavioral changes in the population that lead to a “citizenship of the sea.” People who contribute to this “citizenship of the sea” show awareness and concern for the ocean and are motivated to take personal action to contribute to its protection [149]. The number of youth conservation movements is increasing around the world, for example, Fridays for Future—as the younger generations are more aware of the environmental issues affecting the planet. Consequently, young people seem to play a key role in the development of successful conservation programs. However, other avenues need to be developed to bridge the gap between positive attitudes and a real commitment to conservation and sustainable management [150].

The use of games as tools to enhance the acquisition of technical knowledge has long been studied as a powerful tool for learning, engaging, and tackling complicated tasks [151]. Sustainable sea is a strategy game developed for educational purposes in which players assume the role of fishermen while learning concepts related to the sustainable management of fishery resources [152]. Despite the small sample size, the board game provides information that can be useful for teaching fisheries management. According to the results of the pre- and post-tests, regardless of educational level, all groups improved their knowledge of specific topics after the activity. Knowledge gained by playing an educational game seems to be more effective because it is acquired through hands-on learning [153]. This not only raises awareness of the marine environment and its issues but also encourages a change in values to take personal responsibility for protecting the ocean [154].

The board game can be used to enhance the learning of technical concepts related to marine conservation, fisheries, and sustainable management of marine resources, being an alternative to conventional methods and a more useful educational resource, if possible, in the current context. In 2020, as the COVID-19 pandemic spread across the globe, most countries announced temporary school closures, affecting more than 91% of students worldwide—in April 2020, nearly 1.6 billion children were out of school - [155]. This board game can be very helpful tool when developing Information, Education, and Communication (IEC) activities by teachers. It can be played both in the classroom and among household members, the latter option being interesting because parents/guardians have greater responsibility for making decisions about household practices and this requires greater attention to be paid to how adults and children respond to environmental messages [156]. Marine issues are partly rooted in individual behavioral choices, which, either directly or indirectly through the global marketplace, have the potential to make a significant impact on the marine environment, such as through food choices – choosing correctly labeled or eco-labeled seafood – waste – reducing plastic use – and products [150, 154]. The development of learning can be seen as an intergenerational and multidirectional process that includes (but is not limited to) the information that children bring to families through educational formats for sustainability [156]. In addition, the game can be adapted to other fishing and marine resource scenarios, which are close to the players, as well as different educational levels. In the case of the board game, taking into account its low reproduction cost, it is an affordable tool for schools of all educational levels, as well as for anyone who may be interested in working on the goals of the 2030 Agenda.

3. Take home messages while moving forward to a regional strategy for the management of exploited invertebrates’ marine stocks in Asturias

The work summarized in this chapter suggests that advancing toward a sustainable fisheries management that guarantees both, the employability and profitability of the sector, as well as the cultural and natural heritage in the region, is a priority that can only be achieved through R + D + i and educational strategies—which require funding—and the development and implementation of a regional strategy oriented toward sustainable management and exploitation.

3.1 Traceability and control over the products from fishing activities marketed in Asturias are still deficient and must be improved

Irregularities in labeling and high levels of substitution fraud have been found in the analysis of scallops marketed with different degrees of processing and acquired in different establishments. The most processed products are those with the highest proportion of incorrect labeling. There is a need to carry out a review of the legislation and control methodologies—routine inspections, sanctions, etc.—that guarantee consumer rights, as well as the reliability of the databases on the first sale of fishery products on which fishery statistics are based and, therefore, fishery management, so that they become an efficient tool for the establishment of sustainable development strategies in the region.

3.2 Design and establishing of new coastal marine protected areas (MPAs) in Asturias is necessary

MPAs favor the conservation of biodiversity; the protection of critical habitats; the increase of fisheries productivity through the regeneration of populations; the increase of knowledge of the marine environment; the refuge and protection of genetic diversity; and the protection of heritage and cultural diversity [157]. The implementation of Marine Protected Areas (MPAs) in Asturias coasts under the umbrella of Ecosystem-Based Management (EBM) and Integrated Coastal Zone Management (ICZM) has been suggested by different fields, as they are subordinated to the wider ecological, social, economic, and political context of the coastal and oceanic zones of which they form part. The sustainable management and, therefore, the preservation of such relevant natural resources of the region as barnacles, sea urchins, and octopus, would benefit significantly from this. Ecosystem-based management (EBM) and Integrated coastal zone management (ICZM) based on knowledge of fish stocks and the implementation in Asturias of possible marine protected areas (MPA) closer to or including the coast is necessary to ensure an efficient larval supply. On the other hand, it seems advisable to establish the figure of technical personnel to assist in fisheries management in the fishery associations, similar to the existing one in Galicia.

3.3 Start as soon as possible new eco-labeling certification processes for Asturias fisheries

The fishermen’s guilds that are part of the co-managed barnacle extraction schemes of central-western Asturias could proceed with an application for MSC eco-sustainability certification. Previous studies endorse the high levels of sustainability of this fishery [103], which are managed through TURFs where fishermen actively participate in all aspects of management and share responsibilities with the administration in decision-making. However, among the disadvantages of this certification are the high costs derived from the external audits necessary to carry out its implementation, as well as the successive recertifications. The standards of this type of certification, which incorporate many aspects that were not considered in traditional management, can be incorporated into the management plans of artisanal fishing resources, being the Administration itself the one that requires them to obtain the “privilege” of exploiting a resource. The application of these sustainability standards to management has been very positive in the octopus experience, so they could be adapted to other well-controlled fisheries, such as stalked barnacles or the extraction of Gelidium sp.

3.4 Prevent ecosystem damages due to restocking strategies and think about ecosystem restoration

Mitigation and restoration strategies for the decline of exploited marine populations require genetic control and monitoring programs to confirm that hatchery individual truly represent the wild gene pool and for early detection of possible adverse effects on genetic diversity. Moreover, the mitigation of population decline with autochthonous individuals—as it is being done—is the only possible option, because the use of allochthonous individuals—even those coming from any other population of Atlantic origin—could negatively affect the genetic diversity of wild populations since the new variants could displace the autochthonous ones and affect the adaptability and fitness of local populations. It has become evident that it is extremely important to increase the number of broodstock used to obtain these juveniles. In addition, it is recommended to evaluate the implementation of a habitat restoration plan for sea urchins in Asturias, since this type of combined strategy has proven to be more effective in the recovery of populations.

3.5 Generalize the use and application of genetic tools in the management strategies of the Asturias fisheries

Genetics offers a diverse collection of versatile and useful tools to inform fisheries management on biologically based issues. However, the application of genetic tools is still incipient in many species of fishery interest. Genetic data need to be integrated into the management of fishery resources in Asturias, as they can address issues of direct relevance to the management of these resources; therefore, the implementation of routine genetic studies in management plans is recommended, always from a collaborative approach with managers and taking full advantage of new genetic technologies. The genomic era and the use of eDNA are still waiting to be effectively implemented in the management of marine invertebrates in Asturias.

3.6 Educating new generations in “sustainability” will be a keystone in the Asturias 2030 fisheries development strategy

There is an urgent need to bridge the gap between positive attitudes and real engagement of children and youth in ocean conservation, helping to foster real “citizenship of the sea.” Gamification can be an efficient alternative learning method that establishes new knowledge, attitudes, and commitment of the new generations with sustainability in the exploitation of marine resources in Asturias.

Acknowledgments

This work is based on the PhD dissertation “Genetic tools for the implementation of sustainable management plans in fisheries” defended by M. Parrondo on December 3, 2021 at the University of Oviedo (Spain). This work was funded by the projects GRUPIN-IDI_2021_000040 and ECOSIFOOD (MCI-20-PID2019-108481RB-I00/AEI/10.13039/501100011033). This is a contribution of the Marine Observatory of Asturias (OMA) and the Biotechnology Institute of Asturias (IUBA).