A review of the application of molecular genetics for fisheries management and conservation of sharks and rays

Since the first investigation 25 years ago, the application of genetic tools to address ecological and evolutionary questions in elasmobranch studies has greatly expanded. Major developments in genetic theory as well as in the availability, cost effectiveness and resolution of genetic markers were instrumental for particularly rapid progress over the last 10 years. Genetic studies of elasmobranchs are of direct importance and have application to fisheries management and conservation issues such as the definition of management units and identification of species from fins. In the future, increased application of the most recent and emerging technologies will enable accelerated genetic data production and the development of new markers at reduced costs, paving the way for a paradigm shift from gene to genome-scale research, and more focus on adaptive rather than just neutral variation. Current literature is reviewed in six fields of elasmobranch molecular genetics relevant to fisheries and conservation management (species identification, phylogeography, philopatry, genetic effective population size, molecular evolutionary rate and emerging methods). Where possible, examples from the Indo-Pacific region, which has been underrepresented in previous reviews, are emphasized within a global perspective.     

Methodologies and special considerations for environmental risk analysis of genetically modified aquatic biocontrol organisms

Genetic biocontrol of invasive aquatic species proposes to introduce, for control purposes, a genetically modified (GM) version of an invasive fish species to a targeted aquatic environment. Safe deployment and long term use of such technologies will depend on identifying and managing possible unintended effects to the natural environment. Environmental risk analysis (ERA) is a method for identifying the likelihood and consequences of unintended impacts, and for developing risk management strategies. For the unique situation of genetically modified biocontrol organisms (GMBOs), we review the latest thinking in ERA methodologies for GM fish and explore how terminology and assumptions from ERAs of traditional, non-modified biocontrol organisms and GM fish will need to be recast in ERAs of GMBOs. We also outline some special considerations that an ERA of a GMBOs will have to contend with: non-intuitive potential hazards; uncertainty introduced by extrapolating from domestic systems to natural ecosystems; redundancy in risk management options; and challenges of stakeholder engagement related to new technologies.     

Spatial Heterogeneity in Fishing Creates de facto Refugia for Endangered Celtic Sea Elasmobranchs

The life history characteristics of some elasmobranchs make them particularly vulnerable to fishing mortality; about a third of all species are listed by the IUCN as Threatened or Near Threatened. Marine Protected Areas (MPAs) have been suggested as a tool for conservation of elasmobranchs, but they are likely to be effective only if such populations respond to fishing impacts at spatial-scales corresponding to MPA size. Using the example of the Celtic Sea, we modelled elasmobranch biomass (kg h⁻¹) in fisheries-independent survey hauls as a function of environmental variables and ‘local’ (within 20 km radius) fishing effort (h y⁻¹) recorded from Vessel Monitoring Systems data. Model selection using AIC suggested strongest support for linear mixed effects models in which the variables (i) fishing effort, (ii) geographic location and (iii) demersal fish assemblage had approximately equal importance in explaining elasmobranch biomass. In the eastern Celtic Sea, sampling sites that occurred in the lowest 10% of the observed fishing effort range recorded 10 species of elasmobranch including the critically endangered Dipturus spp. The most intensely fished 10% of sites had only three elasmobranch species, with two IUCN listed as Least Concern. Our results suggest that stable spatial heterogeneity in fishing effort creates de facto refugia for elasmobranchs in the Celtic Sea. However, changes in the present fisheries management regime could impair the refuge effect by changing fisher''s behaviour and displacing effort into these areas.     

Forecasting elasmobranch survival following exposure to severe stressors

Current fishing practices and habitat degradation in most of the world's oceans pose significant threats to marine fish including elasmobranchs. The accurate prediction of survival probability for elasmobranchs subjected to prolonged immobilisation and diminished oxygen availability during capture and a vulnerable state post-release, is reliant on selecting a reliable set of biomarkers to profile as well as using them to design pre-release interventions which minimise elasmobranch death. The purpose of this review is: i) to make a case for the need to develop new biomarkers to use in conjunction with blood chemistry; ii) to briefly present the survival strategies used by other vertebrates subjected to diminished oxygen iii) to discuss new approaches to forecasting the effect that altered physiological and biochemical markers have on long-term survival with a particular emphasis on oxidative stress, the adenylate energy charge, heat shock protein expression and the capacity for repair, so that a more detailed profile of the qualities of elasmobranch survivorship can be constructed. In addition, the review will discuss the relevance of biomarkers to field samples as well as their incorporation into laboratory based research, aimed at providing physiological and biochemical data to inform conservation management.     

Molecular phylogeny of elasmobranchs inferred from mitochondrial and nuclear markers

The elasmobranchs (sharks, rays and skates) being the extant survivors of one of the earliest offshoots of the vertebrate evolutionary tree are good model organisms to study the primitive vertebrate conditions. They play a significant role in maintaining the ecological balance and have high economic value. Due to over-exploitation and illegal fishing worldwide, the elasmobranch stocks are being decimated at an alarming rate. Appropriate management measures are necessary for restoring depleted elasmobranch stocks. One approach for restoring stocks is implementation of conservation measures and these measures can be formulated effectively by knowing the evolutionary relationship among the elasmobranchs. In this study, a total of 30 species were chosen for molecular phylogeny studies using mitochondrial cytochrome c oxidase subunit I, 12S ribosomal RNA gene and nuclear Internal Transcribed Spacer 2. Among different genes, the combined dataset of COI and 12S rRNA resulted in a well resolved tree topology with significant bootstrap/posterior probabilities values. The results supported the reciprocal monophyly of sharks and batoids. Within Galeomorphii, Heterodontiformes (bullhead sharks) formed as a sister group to Lamniformes (mackerel sharks): Orectolobiformes (carpet sharks) and to Carcharhiniformes (ground sharks). Within batoids, the Myliobatiformes formed a monophyly group while Pristiformes (sawfishes) and Rhinobatiformes (guitar fishes) formed a sister group to all other batoids.     

Environmental risk assessment of GE plants under low-exposure conditions

The requirement for environmental risk assessment (ERA) of genetically engineered (GE) plants prior to large scale or commercial introduction into the environment is well established in national laws and regulations, as well as in international agreements. Since the first introductions of GE plants in commercial agriculture in the 1990s, a nearly universal paradigm has emerged for conducting these assessments based on a few guiding principles. These include the concept of case-by-case assessment, the use of comparative assessments, and a focus of the ERA on characteristics of the plant, the introduced trait, and the receiving environment as well as the intended use. In practice, however, ERAs for GE plants have frequently focused on achieving highly detailed characterizations of potential hazards at the expense of consideration of the relevant levels of exposure. This emphasis on exhaustive hazard characterization can lead to great difficulties when applied to ERA for GE plants under low-exposure conditions. This paper presents some relevant considerations for conducting an ERA for a GE plant in a low-exposure scenario in the context of the generalized ERA paradigm, building on discussions and case studies presented during a session at ISBGMO 12.     

Diet,trophic interactions and possible ecological role of commercial sharks and batoids in northern Peruvian waters

The Peruvian sea represents one of the most productive ocean ecosystems and possesses one of the largest elasmobranch fisheries in the Pacific Ocean. Ecosystem-based management of these fisheries will require information on the trophic ecology of elasmobranchs. This study aimed to understand the diet, trophic interactions and the role of nine commercial elasmobranch species in northern Peru through the analysis of stomach contents. A total of 865 non-empty stomachs were analysed. Off northern Peru, elasmobranchs function as upper-trophic-level species consuming 78 prey items, predominantly teleosts and cephalopods. Two distinctive trophic assemblages were identified: (a) sharks (smooth hammerhead shark Sphyrna zygaena, thresher shark Alopias spp. and blue shark Prionace glauca) that feed mainly on cephalopods in the pelagic ecosystem; and (b) sharks and batoids (Chilean eagle ray Myliobatis chilensis, humpback smooth-hound Mustelus whitneyi, spotted houndshark Triakis maculata, Pacific guitarfish Pseudobatos planiceps, copper shark Carcharhinus brachyurus and school shark Galeorhinus galeus) that feed mainly on teleosts and invertebrates in the benthonic and pelagic coastal ecosystem. This study reveals for the first time the diet of T. maculata and the importance of elasmobranchs as predators of abundant and commercial species (i.e., jumbo squid Dosidicus gigas and Peruvian anchovy Engraulis ringens). The results of this study can assist in the design of an ecosystem-based management for the northern Peruvian sea and the conservation of these highly exploited, threatened or poorly understood group of predators in one of the most productive marine ecosystems.     

Annotated reference compilation: Conducting qualitative and quantitative ecological risk assessments at hazardous waste sites

As the field of ecological risk assessment (ERA) broadens, scientists from various disciplines are called upon to become assessors at hazardous waste sites. Although a United States Environmental Protection Agency (USEPA) Framework for ERAs exists, the guidance is unlike the detailed USEPA guidance available for human risk assessments. Currently, the quality of an ERA is dependent upon the assessor's scientific acumen, professional experience, and recognized reference documents. This annotated reference compilation encompasses published documents which have provided useful and important information for qualitative and quantitative ERAs.     

Risk-Based Approaches to Managing Contaminants in Catchments

Risk-based methods promise improved decision-making for managing of contaminants, such as salinity, sediments, nutrients, and toxicants, that can adversely affect the ecological condition of aquatic ecosystems. Two aspects of ecological risk assessment (ERA) and management—stakeholder involvement and more quantitative approaches to risk analysis—are particularly challenging. Stakeholder involvement is crucial both in the risk assessment process and the development, acceptance, and implementation of a risk management plan. Additionally, a number of quantitative approaches (particularly Bayesian approaches and multi-criteria decision-making) have been identified as having the potential to include expert-based inputs into risk-based decision-making. These offer promise for better inclusion of stakeholder knowledge and preferences into the decision-making process, and for improving the links between stakeholder inputs and potential risks to the ecological condition of the system. A major challenge for ecologists and natural resource managers is to make the ERA process more quantitative. Most ERAs conducted to date have been qualitative assessments that suffer from a number of deficiencies, the most serious being the lack of transparency and a reliance on subjective judgments. This article argues that the most productive way forward may be to use Bayesian methods to couple existing process-based models, empirical relationships based on good data, and expert opinion, to make the analysis of ecological risks more robust, consistent, and repeatable.     

Stable isotopes and elasmobranchs: tissue types, methods, applications and assumptions

Stable-isotope analysis (SIA) can act as a powerful ecological tracer with which to examine diet, trophic position and movement, as well as more complex questions pertaining to community dynamics and feeding strategies or behaviour among aquatic organisms. With major advances in the understanding of the methodological approaches and assumptions of SIA through dedicated experimental work in the broader literature coupled with the inherent difficulty of studying typically large, highly mobile marine predators, SIA is increasingly being used to investigate the ecology of elasmobranchs (sharks, skates and rays). Here, the current state of SIA in elasmobranchs is reviewed, focusing on available tissues for analysis, methodological issues relating to the effects of lipid extraction and urea, the experimental dynamics of isotopic incorporation, diet-tissue discrimination factors, estimating trophic position, diet and mixing models and individual specialization and niche-width analyses. These areas are discussed in terms of assumptions made when applying SIA to the study of elasmobranch ecology and the requirement that investigators standardize analytical approaches. Recommendations are made for future SIA experimental work that would improve understanding of stable-isotope dynamics and advance their application in the study of sharks, skates and rays.     

Effects of biological traits on capture-induced parturition in a freshwater stingray and perspectives for species management

Elasmobranchs are particularly vulnerable to overexploitation and population depletion, especially due to their life-history traits, such as low reproductive output and slow growth. Given that capture-induced parturition (abortion or premature birth) is a common consequence of fisheries in elasmobranchs, but still little studied, we investigated how the abortion/premature birth process varies in response to reproductive traits in a freshwater stingray, Potamotrygon amandae. Our results revealed that capture-induced parturition was affected by reproductive traits, such as litter size (one to seven) and gestation stage. The event occurred faster in pregnant females with high litter size during late pregnancy. Also, as found in other elasmobranchs, litter size was positively correlated with maternal size. These findings indicate that larger pregnant females in late pregnancy are more vulnerable to capture-induced parturition. This study improves our understanding of the capture-induced parturition process in stingrays, and provides useful information for management strategies and future recommendations for elasmobranch conservation.     

Integration of Ecosystem Services into Ecological Risk Assessment for Implementation in Ecosystem-Based River Management: A Case Study of the Yellow River,China

Ecological risk assessment (ERA) is a scientific tool used to support ecosystem-based management (EBM), but most current ERA methods consider only a few indices of particular species or components. Such limitations restrict the scope of results so that they are insufficient to reflect the integrated risk characterization of an ecosystem, thereby inhibiting the application of ERA in EBM. We incorporate the concept of ecosystem services into ERA and develop an improved ERA framework to create a comprehensive risk map of an ecosystem, accounting for multiple human activities and ecosystem services. Using the Yellow River as a case study, we show how this framework enables the implementation of integrated risk characterization and prioritization of the most important ecological risk issues in the ecosystem-based river management of the Yellow River. This framework can help practitioners facilitate better implementation of ERA within EBM in rivers or any target ecosystem.     

Approaches to Ecological Risk Characterization and Management: Selecting the Right Tools for the Job

Chemical-specific hazard quotient (HQ) risk characterization in ecological risk assessment (ERA) can be a value-added tool for risk management decision-making at chemical release sites, when applied appropriately. However, there is little consensus regarding how HQ results can be used for risk management decision-making at the population, community, and ecosystem levels. Furthermore, stakeholders are reluctant to consider alternatives to HQ results for risk management decisions. Chemical-specific HQs risk characterization should be viewed as only one of several approaches (i.e., tools) for addressing ecological issues; and in many situations, other quantitative and qualitative approaches will likely result in superior risk management decisions. The purpose of this paper is to address fundamental issues and limitations associated with chemical-specific HQ risk characterization in ERA, to identify when it may be appropriate, to explore alternatives that are currently available, and to identify areas that could be developed for the future. Several alternatives (i.e., compensatory restoration, performance-based ecological monitoring, ecological significance criteria, net environmental benefit analysis), including their limitations, that can supplement, augment, or substitute for HQs in ERA are presented. In addition, areas of research (i.e., wildlife habitat assessment/landscape ecology/population biology, and field validated risk-based screening levels) that could yield new tools are discussed.     

Considerations Regarding the Use of Reference Area and Baseline Information in Ecological Risk Assessments

There has been debate in the recent literature as to whether a reference assessment should be included in ecological risk assessments (ERAs) of contaminated sites, and if so, how such an evaluation can be incorporated in a way that aids in decision making. It is our view that an assessment of reference conditions can be useful in the ERA process, for both prospective and retrospective ERAs, given adequate resources and acknowledgement and understanding of the limitations and uncertainties associated with this information. Suggestions and considerations for incorporating reference area information into an ecological risk assessment are discussed.     

The importance of considering genetic diversity in shark and ray conservation policies

Many populations of elasmobranchs (sharks and rays) are experiencing severe declines due to the high demand for shark fins in Asia, the activities of unregulated fisheries, and increases in shark and ray catches. Recently, the effects of the decline in the populations of marine fish species on genetic diversity have drawn increasing attention; however, only a few studies have addressed the genetic diversity of shark and ray populations. Here, we report the results of a quantitative analysis of the genetic diversity of shark and ray species over the past 20 years and discuss the importance and utility of this genetic information for fisheries management and conservation policies. Furthermore, we suggest future actions important for minimizing the gaps in our current knowledge of the genetic diversity of shark and ray species and to minimize the information gap between genetic scientists and policymakers. We suggest that shark and ray fisheries management and conservation policies consider genetic diversity information, such as the management unit, effective population size (Ne), haplotype and nucleotide diversity, observed heterozygosity, and allelic richness, because the long-term survival of a species is strongly dependent on the levels of genetic diversity within and between populations. In addition, sharks and rays are a group of particular interest for genetic conservation due to their remarkable life histories.     

The physiological response to anthropogenic stressors in marine elasmobranch fishes: a review with a focus on the secondary response

Elasmobranchs (sharks, rays, and skates) are currently facing substantial anthropogenic threats, which expose them to acute and chronic stressors that may exceed in severity and/or duration those typically imposed by natural events. To date, the number of directed studies on the response of elasmobranch fishes to acute and chronic stress are greatly exceeded by those related to teleosts. Of the limited number of studies conducted to date, most have centered on sharks; batoids are poorly represented. Like teleosts, sharks exhibit primary and secondary responses to stress that are manifested in their blood biochemistry. The former is characterized by immediate and profound increases in circulating catecholamines and corticosteroids, which are thought to mobilize energy reserves and maintain oxygen supply and osmotic balance. Mediated by these primary responses, the secondary effects of stress in elasmobranchs include hyperglycemia, acidemia resulting from metabolic and respiratory acidoses, and profound disturbances to ionic, osmotic, and fluid volume homeostasis. The nature and magnitude of these secondary effects are species-specific and may be tightly linked to metabolic scope and thermal physiology as well as the type and duration of the stressor. In fishes, acute and chronic stressors can incite a tertiary response, which involves physiological changes at the organismal level, thereby impacting growth rates, reproductive outputs or investments, and disease resistance. Virtually no studies to date have been conducted on the tertiary stress response in elasmobranchs. Given the diversity of elasmobranchs, additional studies that characterize the nature, magnitude, and consequences of physiological stress over a broad spectrum of stressors are essential for the development of conservation measures. Additional studies on the primary, secondary, and tertiary stress response in elasmobranchs are warranted, with particular emphasis on expanding the range of species and stressors examined. Future studies should move beyond simply studying the effects of known stressors and focus on the underlying physiological mechanisms. Such studies should include the coupling of stress indicators with quantifiable aspects of the stressor, which will allow researchers to test hypotheses on survivorship and, ultimately, derive models that effectively link physiology to mortality. Studies of this nature are essential for decision-making that will result in the effective management and conservation of these species.     

基于生态系统服务的生态风险评价研究进展

生态风险评价对科学管理与保护生态系统具有重要的意义,为弥补传统生态风险评价方法的不足和提高风险管理的效率,将生态系统服务引入生态风险评价中进行发展和完善,成为了当前生态风险评价研究的前沿和热点。系统分析了生态系统服务在生态风险评价中的应用,指出生态系统服务在问题形成阶段中可明确保护对象和属性,在风险分析阶段可联系生态系统结构过程作用,在风险表征阶段及后续阶段能可提供清晰明确的评价结果,加强风险交流和管理,能有效地改进生态系统传统生态风险评价。在实践上,基于生态系统服务的生态风险评价可从3个不同层面开展:一是针对外界压力对某类特定功能或者系统中某些服务功能的影响,构建基于某种特定服务的实体属性评价方法;二是针对外界压力作用下生态系统结构与过程变化下对功能影响,构建基于复杂生态系统作用的评价方法,实现对生态风险的模拟评价;三是评价社会生态系统下外界驱动对人类福祉的影响时,可将DPSIR(Drive-Pressure-State-Impact-Response)理论模型运用到生态风险管理中,也可基于景观生态系统服务与压力源的空间作用关系,实现社会生态系统风险评价与管理。作为生态风险表征手段,可基于生态系统服务损失与不利服务进行表征,也可选取热力学等指标作为评估量纲。从理论、评价方法、风险管理等方面对基于生态系统服务生态风险评价给予展望。     

The Changing Focus of the Ecological Risk Assessment of Aquaculture Operations: From Local to Cumulative Risk Assessment

Ecological risk assessment (ERA) methodologies must be continually improved so that resource managers, activity proponents, and stakeholders can better manage the environmental impacts of human activities. One of the largest challenges facing ERA methodologies and approaches is to develop the ability to encompass cumulative and far-field effects of human activities. It is argued here that the ERAs of industrial aquaculture activities have been an example of where ERA practitioners and researchers have responded to the challenge of managing the cumulative risks of a new and rapidly growing industry by developing innovative ERA approaches that can be applied elsewhere.     

Distribution of skates and sharks in the North Sea: 112 years of change

How have North Sea skate and shark assemblages changed since the early 20th century when bottom trawling became widespread, whilst their environment became increasingly impacted by fishing, climate change, habitat degradation and other anthropogenic pressures? This article examines long‐term changes in the distribution and occurrence of the elasmobranch assemblage of the southern North Sea, based on extensive historical time series (1902–2013) of fishery‐independent survey data. In general, larger species (thornback ray, tope, spurdog) exhibited long‐term declines, and the largest (common skate complex) became locally extirpated (as did angelshark). Smaller species increased (spotted and starry ray, lesser‐spotted dogfish) as did smooth‐hound, likely benefiting from greater resilience to fishing and/or climate change. This indicates a fundamental shift from historical dominance of larger, commercially valuable species to current prevalence of smaller, more productive species often of low commercial value. In recent years, however, some trends have reversed, with the (cold‐water associated) starry ray now declining and thornback ray increasing. This shift may be attributed to (i) fishing, including mechanised beam trawling introduced in the 1960s–1970s, and historical target fisheries for elasmobranchs; (ii) climate change, currently favouring warm‐water above cold‐water species; and (iii) habitat loss, including potential degradation of coastal and outer estuarine nursery habitats. The same anthropogenic pressures, here documented to have impacted North Sea elasmobranchs over the past century, are likewise impacting shelf seas worldwide and may increase in the future; therefore, parallel changes in elasmobranch communities in other regions are to be expected.     

Elasmobranchs of the Persian (Arabian) Gulf: ecology, human aspects and research priorities for their improved management

Given widespread concern about the status of elasmobranch fishes globally, information on this group in the Persian (Arabian) Gulf is reviewed comprehensively for the first time. The Arabian region may be of overlooked significance to elasmobranch biogeography, and the environmentally unique Gulf has some highly distinctive elements of biodiversity: an endemic and critically endangered rajid skate, a rarely recorded carcharhinid shark, and preliminary molecular studies which indicate intriguing levels of distinctness from conspecifics elsewhere in the Indo-Pacific. Elasmobranchs also have a long history of association with, and exploitation by, humans around the Gulf. Despite this, Gulf elasmobranchs have been poorly researched, probably due to their low esteem as food. Information is scattered through a variety of literature, and only a handful of published works have been primarily concerned with aspects relevant to management. Key areas of concern include large reported landings by Iran; the export of fins to east Asian markets (particularly through the United Arab Emirates); potentially increasing demand for elasmobranchs for pharmaceutical products and human consumption; a reported change in elasmobranch community structure along the Iranian coast; and major degradation of the Gulf’s shallow, semi-enclosed environment. Priorities for research in the near future should include: resolution of taxonomic issues; species-level monitoring and reporting of fisheries landings by all Gulf states (including the species, pathways and fisheries involved in the fin trade locally); establishing the degree of connectivity of Gulf populations to those in adjacent waterbodies; and identification of key spatio-temporal sensitivities.