Introduction
Worldwide, the population depletion of many marine species by overfishing threatens the sources of jobs and food security of many regions where fishing is one of the main economic activities (FAO, 2020). In Mexico, fishing is an important activity that generates direct and indirect jobs and is a source of protein for more than 11 000 coastal communities (SAGARPA, 2017). In 2018, fishing production in Mexico reached 2,159,650 tons and an average national consumption per capita in the last five years of 18.24 kg (SAGARPA, 2020), which places Mexico among the 15 leading fish producers in the world (FAO, 2020). In Mexico, a total of 551 marine invertebrates and fishes are recorded that are relevant for small-scale and industrial fisheries for consumption or ornament purposes (DOF, 2000). The main key species are abalones, clams, squids, octopus, scallops, shrimps, lobsters, conchs, sea urchins, elasmobranchs, small pelagic fishes, coastal and demersal fishes, and tunids (DOF, 2018). The Mexican fishing fleet includes 2,020 larger vessels and 74,286 small (coastal) vessels, and a record of more than 238,000 people in the fishing sector (DOF, 2020). Fishing is carried out with a wide variety of fishing gear, including purse seines, gillnets (bottom and surface set), longlines (bottom and surface set), handlines, trawl lines, pots, traps, diving, and manual gathering (DOF, 2012; DOF, 2018). Invertebrates and fishes are sold fresh, frozen, or live (filleted or whole) or processed (e.g., dried, salt dried, canned, cooked, smoked) (DOF, 2010a; DOF, 2012; SAGARPA, 2021). The fishery products are sold in the domestic markets (with high national consumption) and international markets, with more than 350,000 t exported in 2019, mainly to the United States of America, Hong Kong, Japan, Spain, and China (SAGARPA, 2021).
Fisheries management in Mexico is administered by the General Law of Sustainable Aquaculture and Fisheries (LGPAS, by its Spanish acronym) (DOF, 2007). The LGPAS establishes the national policy for regulating the fisheries via the Official Fisheries Mexican Standards (NOM-PESC), which describe the specific management measures by species or group of species. The National Fisheries Charter (CNP) is another legally binding instrument used in Mexico to manage all the fisheries in Mexico with yearly updates (DOF, 2007). Developed by the National Fisheries and Aquaculture Institute (INAPESCA), the CNP indicates the strategies and actions that must be fulfilled to regulate fishing in Mexico, including information related to the fishing sites and gears, the status of the stocks, and fishing effort (DOF, 2007; DOF, 2018). In addition, researchers from INAPESCA elaborate and update the fisheries management plans (FMP) approved by CONAPESCA. The fisheries management plans include actions aimed at developing the fishing activity sustainable and are based on biological, ecological fishing, environmental, economic, cultural, and social knowledge. Of a total of 36 main fisheries, 27 (75%) of these fisheries are at the level of maximum sustainable yield, seven are in deterioration, two with development potential, and only 13 (36%) have a management plan (DOF, 2018).
Given the growing concern about invertebrate and fish populations’ status and the increased demand for marine products, initiatives have been developed to inform consumers about the production processes (Roheim, 2003; FAO, 2010). The development of environmentally responsible fishing standards has been highlighted through the certification of fisheries and recommendations for the consumption of seafood (Ward and Phillips, 2008; Kirby et al., 2014). These standards have been recognized by the Committee on Trade and Environment of the World Trade Organization as environmental policy instruments (Maneiro Jurjo and Burguillo Cuesta, 2007) and represent a great opportunity and frame of reference towards the development of sustainable fisheries in Mexico. There are different eco-labels or programs based on sustainability schemes, among which some stand out on a global scale for incorporating rigorous aspects of social, political, economic, and ecological issues. The Marine Stewardship Council (MSC), Seafood Watch (SFW), and Fair-Trade USA (FT) are three of the organizations that have boomed in the last decade because they show robust and sustainable principles (CEA, 2020).
However, organizations such as the MSC have recognized that certification procedures and standards are more challenging for fisheries in developing countries, especially small-scale fisheries with poor and limited data. For the above, the MSC developed a methodology to evaluate data-deficient fisheries following the ecological risk assessments framework to generate critical information for fisheries (Ponte, 2012). Ecological risk assessments have been developed in recent years as an alternative to conventional stock assessments, which require a large amount of information (Carruthers et al., 2014). Within the framework of ecological risk assessments, there is the semi-quantitative Productivity and Susceptibility Analysis (PSA), in which the relative vulnerability of a particular stock to fishing is estimated by analyzing the interaction of fishing with the stock (susceptibility) and the capacity of the species to face the impacts of fishing through its biological characteristics (productivity) (Hobday et al., 2011; Cortés et al., 2015).
The National Commission for the Knowledge and Use of Biodiversity (CONABIO) developed the Responsible Seafood Consumption Guide (RSCG) in Mexico. This RSCG includes advice and recommendations for a total of 615 species of fish and invertebrates in a colored guide system (Green = Recommended, Yellow = Not recommended or in moderation, and Red = Avoid) to create awareness of sustainably managed fisheries and encourage the consumers about the sustainable seafood consumption and behavioral changes that could reduce fishing pressure on vulnerable species (Gulbrandsen, 2009; Vázquez-Rowe et al., 2013; Fernández-Rivera Melo et al., 2018). The RSCG considers the following criteria to issue a seafood purchase recommendation: a) fishing origin (e.g., domestic or imported), b) status of the populations based on the official information on current fisheries published in the National fisheries charter ( (DOF, 2010a; DOF, 2012; DOF, 2018), c) species at risk based on the Official Mexican Standards for Species at Risk (NOM-059-SEMARNAT-2010) and the Red List of the International Union for Conservation of Nature (IUCN), d) type of ban available, and e) the catch selectivity. However, there is no information on the population status of many species due to the lack of biological and fishing information necessary to assess the populations using traditional quantitative methods. Hence, the impact of extractive activities on many species is unknown (Arreguín-Sánchez and Arcos-Huitrón, 2011; Saldaña-ruiz et al., 2017), and it is not possible to issue a seafood purchase advice or recommendation. In this study, we estimate the relative vulnerability of invertebrates, elasmobranchs, and bony fish of commercial importance to fishing activities in Mexico, using the MSC’s version of the productivity and susceptibility analysis (MSC, 2014) for data-limited fisheries.
Discussion
In the present study, more invertebrates were highly vulnerable, followed by elasmobranchs and bony fishes. Although in the elasmobranch group, we identified the species with the lowest biological productivity (I. oxyrinchus) among all the evaluated species and the highest proportion of species with high and moderate vulnerability. The high vulnerability of the invertebrates is associated with the life traits of some species such as clams, abalones, and sea cucumbers (e.g., P. generosa, P. globosa, Haliotis corrugata, H. cracherodii, H. sorenseni, and Holothuria casoae) that are relatively long-lived (Andrews et al., 2013; Suárez-Moo et al., 2013). Three of the sea cucumbers species are listed as critically in danger and one species as Data Deficient by the IUCN red list (Samyn, 2013; Peters and Rogers-Bennett, 2021a; Peters and Rogers-Bennett, 2021b; Peters and Rogers-Bennett, 2021c). Furthermore, these and other lobster, clams, and shrimp species (e.g., Panulirus sp., Rangia sp., Rimapenaeus sp., Sicyonia sp., and Penaeus sp.) have a high fisheries susceptibility due to their narrow habitat range, low mobility and high gear selectivity of the fisheries that catch them (Briones Fourzán, 1995; Ramírez-Rodríguez et al., 2000; Wakida-Kusunoki and MacKenzie, 2004; Hendrickx, 2016). Many invertebrate species are manually harvested through diving, resulting in a high selectivity (Melchor-Aragón et al., 2002). Sessile or slow-moving invertebrates have a limited capacity to flee or seek refuge from divers and active fishing gears (Menge and Lubchenco, 1981; Levitan and Genovese, 1989; Hunt et al., 2020); thus, a high proportion of species (82%) caught by dive fisheries resulted with high vulnerability. Furthermore, the tendency of several sessile marine invertebrate species to assemblage (Osman, 2015) increases the possibility of the fishing gear encountering a higher density of organisms. Nevertheless, this grouping feature and the proximity of the invertebrate species with the fishing communities has made possible the establishment of adequate and effective measures for their management through functional management units (e.g., marine protected areas, areas of repopulation, monitoring, and surveillance by fishers), and abundance estimations as a baseline for harvest strategies (Defeo and Castilla, 2005; López-Rocha et al., 2021).
More than half of the evaluated elasmobranch species resulted with moderate vulnerability to fishing activities despite the widely documented low biological productivity for this group (Stevens et al., 2000). The above is because elasmobranch species with low productivity have low susceptibility and, high susceptible species have moderate productivity. In our analysis, we identified elasmobranchs that, unlike invertebrates, have wider geographic distribution, significant mobility through the water column, and are highly migratory species (e.g., Alopias sp., Carcharhinus falciformis, C. longimanus, P. glauca, and Aetobatus narinari), thus, a reduced overlap with fishing activities (Camhi et al., 1998). Furthermore, among the 17 species (including both elasmobranchs and bony fishes) that are fished in all the regions of the Mexican EEZ, only four resulted in high RV to fishing. These are highly migratory pelagic sharks and bony fishes (e.g., Alopias sp., C. falciformis, C. longimanus, C. leucas, Galeocerdo cuvier, I. oxyrinchus, P. glauca, Sphyrna sp., Thunnus albacares, Istiophorus platypterus, and Xiphias gladius). Nevertheless, it is essential to acknowledge that the distribution of these highly migratory pelagic shark and bony fishes (e.g., tunas and billfishes) overlaps with fishing fleets from other countries in both the Pacific and the Atlantic (Calich et al., 2018; White et al., 2019). This study focuses on evaluating the RV only for Mexican fisheries. Thus, for highly migratory species management and conservation measures, besides the negotiations among jurisdictions, should consider a better understanding of their distribution, habitat use over large spatial scales, overlap patterns between species distribution and fishing fleets across borders, and the effect of these fisheries on the species (Pons et al., 2018; White et al., 2019). On the other hand, several elasmobranch species resulted highly susceptible to fishing activities (e.g., Mustelus canis, M. henlei, M. lunulatus, Nasolamia velox, Negaprion brevirostris, Squatina cubensis, S. californica, S. dumeril, Gymnura marmorata, Myliobatis goodei, Pseudobatos productos, and Beringraja inornata); however, their biological productivity is moderate. The bonnethead shark (Sphyrna tiburo) was the only one with low vulnerability among elasmobranchs, mostly due to their high biological productivity (Parsons, 1993; Ebert et al., 2013; Frazier et al., 2014). Other PSA analyses in Mexico reported low vulnerability for the bonnethead shark, however, is classified as Critically Endangered by the IUCN red list (Furlong-Estrada et al., 2014; Pollom et al., 2020). In the Mexican Pacific, this species is reported as possibly extirpated (Pérez-Jiménez, 2014; Saldaña-ruiz et al., 2017). For the above, studies are needed to clarify the population status of the bonnethead shark in the Pacific and identify the cause of its possible absence. Most of the elasmobranchs in this analysis resulted with moderate RV to fishing activities in Mexico. However, future analysis should consider that species may be subject to other sources of pressure (e.g., overlapping with fishing fleets from other countries, oil spills, climate change, and habitat loss) (Calich et al., 2018; Osgood et al., 2021; Yan et al., 2021; Romo-Curiel et al., 2022). Moreover, half of the evaluated elasmobranchs in this study belong to extinction risk categories of the Red List of Threatened Species of the International Union for Conservation of Nature (IUCN) of Critically Endangered, Endangered, and Vulnerable (Supplementary Table S3). For all the above, elasmobranch’s research and management efforts should consider the complexities of the factors influencing their overall vulnerability.
In our study, more than half of the evaluated species (57%) had low vulnerability to fisheries, mostly bony fishes with high biological productivity. Most bony fish are called “r” strategists due to their high biological productivity and large interannual variation in recruitment related to climate-oceanic changes (Musick, 1999; King and McFarlane, 2003). These characteristics allow this group to recover their populations from fishing extraction rapidly; however, it is not an intrinsic characteristic of all bony fish species, and proper management tools are necessary to maintain healthy populations. For example, scorpionfishes of the Sebastes genus resulted with moderate to low productivity due to their reproductive strategy and great longevity (Echeverria, 1987; Reilly et al., 1994; Cailliet et al., 2001; Munk, 2001; Love, 2012; Berkel and Cacan, 2021). Also, we identified several species (e.g., Hypsopsetta guttulata, Kyphosus azureus, Mycteroperca jordani, Sebastes atrovirens, S. chrysomelas, S. miniatus, S. rastrelliger, S. rosenblatti, S. rufus, S. semicinctus, S. serranoides, S. serriceps, S. simulator, S. umbrosus, and Semicossyphus pulcher) with limited geographic distribution, increasing their encounterability with the fishing activities (Eschmeyer et al., 1983; Williams and Ralston, 2002; Fricke et al., 2021). There are endemic invertebrate and fish species in Mexico with significantly restricted distribution to the Northern Gulf of California, like the sandy clamp (Chione cortezi), the gulf croaker (Micropogonias megalops), and the gulf corvina (Cynoscion othonopterus) (Villarreal-Chávez et al., 1999; Garcés-Rodríguez et al., 2018). Another critical issue for these species is the habitat loss due to the disruption of the Colorado River that once flowed into the Northern Gulf of California (Rowell et al., 2005; Rodríguez-Quiroz et al., 2010). In this study, these species resulted with high RV, and the data quality was poor for the sandy clamp and the gulf croaker. For all the above, its prioritization for future evaluations to identify the status of the populations is highlighted.
This vulnerability analysis was specific to a particular fishery and fishing gear type in this study. However, it is important to consider the multi-species and multi-gear character of the fisheries in Mexico (Arce-Acosta et al., 2018). Evaluating the cumulative effects of multiple fisheries affecting one species was beyond our scope. However, further evaluations focused on evaluating the impacts that multiple fisheries may have on individual species should be considered. The most vulnerable species identified in this study could provide the basis for prioritizing future research along these lines. In Mexico, there are 21 fisheries management plans, nine in the Mexican Pacific (Region 1 and 2) and 12 in the Gulf of Mexico and the Caribbean Sea (Region 3) (Peña-Puch et al., 2020). Among the evaluated species in this study, only 33 have a fisheries management plan (e.g., Octopus bimaculatus, O. Maya y O. Vulgaris, O. hubbsorum, Megapitaria squalida, Centropomus viridis, Lutjanus colorado, Thunnus orientalis, T. albacares, Paralabrax nebulife, Dosidicus gigas, Xiphopenaeus kroyeri, Penaeus brasiliensis, P. aztecus, P. setiferus, P. duorarum, Sicyonia brevirostris, Fasciolaria tulipa, Strombus costatus, S. pugilis, Melongena melongena, M. corona, Cynoscion othonopterus, Callinectes spp., Panulirus argus, Mugil cephalus, M. curema, E. morio, Entropomus undecimalis, and several sardines, anchovies, and mackerel species). Despite having management plans, there is no robust assessment of the population status for many of these species. Through this study, future research efforts can be prioritized to evaluate the populations of the species and to review the established management tools. Regarding the main information gaps detected, there are very few studies focused on evaluating selectivity and post-capture mortality, and there are mainly focused on incidentally caught elasmobranch species (Poisson et al., 2014; Hutchinson et al., 2015; Eddy et al., 2016). The complexity of many Mexican fisheries, in which various species are caught using various gear-types, makes it difficult to evaluate the selectivity and post-capture mortality of the species (Castillo-Géniz et al., 1998; Pérez-Jiménez et al., 2005). This study identifies data gaps about the area overlap between the species and the fisheries for many species. Knowing the degree of area overlap of the species distribution with the fishery is essential to determine the species’ susceptibility to the fisheries; a greater overlap indicates highest susceptibility (Patrick et al., 2010; Hobday et al., 2011). Understanding the spatial dimensions of fishing activities in relation to the distribution of the species is critical to improve the management of complex multi-gear and multi-species Mexican fisheries (Salas et al., 2007; Moreno-Báez et al., 2010). For most of the invertebrate species, there is no data about the depensatory effects on the resilience of marine invertebrates to fishing mortality Various studies indicate that abiotic factors mainly influence fluctuations in invertebrate species abundance (e.g., temperature and precipitation); Villalejo-Fuerte et al., 2000; Houlahan et al., 2007; Gonzalez and Loreau, 2009). Trophic ecology studies were also very scarce for many species, especially invertebrates; thus, data on the trophic level were obtained mainly from Fishbase. In Fishbase, the trophic position is calculated with diet and food information based on prey lists or stomach content studies, which gives high uncertainty to the value of trophic level used. In this data-limited context, the PSA in this study is an effective risk-based approach to estimate the potential vulnerability of the species to fishing. Nevertheless, we acknowledge the subjectivity of elements of the PSA analysis (Hordyk and Carruthers, 2018). For example, this analysis calculates the relative vulnerability for each species based on productivity and susceptibility attributes scores (1, 2, or 3) derived from source data that range from highly precise (e.g., age determination study using otoliths) to imprecise data (e.g., adopting age from a species in the same genus or family). However, having the quality scores of the data used for the analysis allows us to identify the reliability of the RV results and help us with the interpretation (Patrick et al., 2009). The PSA also has limitations in assessing a cumulative vulnerability of a species to multiple fisheries (Griffiths et al., 2019), which would be especially useful in the specific case of the multi-species Mexican fisheries. However, the PSA is useful to prioritize species needing research and management attention despite data limitations. Although the PSA does not replace a robust population assessment, is a valuable tool to identify priority species for future research, biological and fishery data gaps, and set the baseline for future research efforts toward the sustainability of fisheries. Implications of the Productivity and Susceptibility Analysis results in the responsible seafood consumption.
Fisheries certification and eco-labeling have been promoted in the past three decades as a useful market-based instrument to encourage sustainable fisheries operations worldwide (Ward and Phillips, 2008). Within fishery certification schemes such as the Marine Stewardship Council, the Seafood Watch, and Fairtrade USA (fisheries), PSA analysis is used in cases where there is no quantitative stock assessment available to determine species vulnerability to fishing pressure (USA, 2017; MSC, 2020; Watch, 2020). The MSC has become the most influential fisheries certification entity globally (Le Manach et al., 2020). Nevertheless, the MSC certification process is not suitable for fisheries in developing countries (Pérez-Ramírez et al., 2016), including those located in Latin America and the Caribbean like Argentina (Pérez-Ramírez et al., 2012a), Chile (MSC, 2019), and several fisheries in Mexico (Pérez-Ramírez et al., 2012b). This high underrepresentation of the MSC in developing countries is due to the lack of reliable scientific data to address the state of their fisheries and species populations, necessary for the certification process (Gulbrandsen, 2009). Due to the above, the MSC developed a risk-based framework (RBF), the PSA, to assess the vulnerability of species impacted by fishing activities in small-scale and data-deficient fisheries to inform the certification process (Howes, 2008; Ponte, 2012). This RBF is used to address deficiencies in the ecological principles for sustainable fisheries (i.e., Principle 1: stock status and Principle 2: minimizing environmental impacts) in the preliminary review of the MSC to identify if the fishery is ready to enter full assessment (Mohamed et al., 2018; MSC, 2020). However, the effectiveness of the MSC’s risk-based framework to increase the number of certified fisheries in developing countries will need to be evaluated, and actions are still needed to improve the capacity to initiate, develop and sustain the certification processes (Ponte, 2012; Stratoudakis et al., 2016). Furthermore, the limitations and uncertainty associated with the PSA should be further explored and evaluated to improve the analysis (McCully Phillips et al., 2015). Like other risk-based approaches, this analysis does not replace standard stock assessments but rather evaluates the relative vulnerability to becoming overfished (Patrick et al., 2010; Hobday et al., 2011). Moreover, these vulnerability results do not indicate levels of sustainability since this analysis does not consider inputs from the management and socio-economic aspects of the analyzed fisheries (Hilborn et al., 2015; Astles and Cormier, 2018). It is important to consider that the results of this analysis cannot be used directly in future pre-assessments of the MSC since specific characteristics of the fishery to be evaluated must be looked upon (e.g., evaluation of susceptibility to different fishing gear types to those evaluated in this study). However, this is a straightforward approach that can be used in a data-poor environment that provides a preliminary screening of the many species of commercial importance potentially affected by fisheries. As a result, it represents a potential means to advance progress towards reducing some barriers to certification of fisheries in developing countries. The market-based approaches within the eco-labeling initiatives, like the RSCG, use a seafood-ranking guides system to inform consumers on the purchasing choices providing information about the origin and sustainability of fishery products (Kaiser and Edwards-Jones, 2006; Gulbrandsen, 2009). The RSCG include information about certified fisheries (e.g., the MSC and FT), fisheries that follow responsible fishing practices (e.g., Seafood Watch and the Fishery Improvement Project), the status of the species populations, according to Mexican regulations (e.g., the National fishery charter and the normative instrument that defines the risk categories for the Mexico flora and fauna species; DOF, 2010b; DOF, 2018), and the global conservation status of species of the Red List of Threatened Species by the International Union for Conservation of Nature. The eco-labeling implementation and success of approaches like the RSCG to promote sustainable fisheries will depend on many factors, including the level of concern for sustainable fisheries by the consumers, the evaluation of the economic benefits for the fishers, and the effective monitoring of the certified fisheries (Kaiser and Edwards-Jones, 2006). However, these results set the baseline for future research efforts to improve the biology data and the interaction of the species with the fisheries. Also, the vulnerability results can be incorporated in the RSCG to improve the guidance and recommendations to help consumers choose seafood from sustainably Mexican fisheries, which is critical in a country where fisheries play a key role in livelihoods and food security and well-being of many coastal communities.