Article

Movement patterns of a Critically Endangered elasmobranch (Dipturus intermedius) in a Marine Protected Area

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Abstract

• Marine Protected Areas (MPAs) are widely used in marine management, but for mobile species understanding the spatio-temporal scale of management measures that is required to deliver conservation benefits depends on a detailed knowledge of species’ movements that is often lacking. This is especially the case for species of skate (Rajidae) for which relatively few movement studies have been conducted. • In Scotland, the Loch Sunart to the Sound of Jura MPA covering 741 km² has been designated for the conservation of the Critically Endangered flapper skate (Dipturus intermedius), but fine-scale movements within this area remain poorly understood. • A passive acoustic telemetry study which coupled acoustic tagging of 42 individuals and a static array of 58 receivers was conducted from March 2016 to June 2017. Using acoustic detection time series, angler capture–recapture data and depth time series from archival tags, fine-scale movements of individuals were investigated. • Overall, 33 of the 42 tagged individuals were detected. Residency, site fidelity and transiency were documented. Residency around receivers, lasting from 3 to more than 12 months, was documented in 16 acoustically detected individuals (48%) and all life-history categories, but was most noticeable among females. Acoustic detections were associated with depth, salinity and season, but there was no evidence that individuals formed close-knit groups in the areas in which they were detected. • Taken together with historical occurrence records of flapper skate, the prevalence and scale of residency documented here suggest that the MPA is sufficiently large to benefit a notable percentage (38 [24–52]%) of skate found in the study area over monthly and seasonal timescales. This result strengthens the case for the use of MPAs to support the conservation of flapper skate and other skate species that display similar movement patterns in areas of high local abundance.

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... The flapper skate (Dipturus intermedius) is a Critically Endangered benthic elasmobranch 33 that is found off the west coast of Scotland where data from animal-borne tags have been collated to guide management of a 741 km 2 Marine Protected Area (MPA) established for its conservation [34][35][36][37][38][39][40][41][42] . Since the 1970s, a wealth of citizen-science mark-recapture data has been assembled from a recreational catch-and-release sport fishery that principally targets skate from anchored charter vessels over areas of relatively deep (> 100 m) water [34][35][36][37][38][39][40] . ...
... The flapper skate (Dipturus intermedius) is a Critically Endangered benthic elasmobranch 33 that is found off the west coast of Scotland where data from animal-borne tags have been collated to guide management of a 741 km 2 Marine Protected Area (MPA) established for its conservation [34][35][36][37][38][39][40][41][42] . Since the 1970s, a wealth of citizen-science mark-recapture data has been assembled from a recreational catch-and-release sport fishery that principally targets skate from anchored charter vessels over areas of relatively deep (> 100 m) water [34][35][36][37][38][39][40] . More recently (2016-17), the flapper skate became the focus of a major electronic tagging and tracking project that deployed passive acoustic telemetry and archival tags [39][40][41]43 . ...
... Since the 1970s, a wealth of citizen-science mark-recapture data has been assembled from a recreational catch-and-release sport fishery that principally targets skate from anchored charter vessels over areas of relatively deep (> 100 m) water [34][35][36][37][38][39][40] . More recently (2016-17), the flapper skate became the focus of a major electronic tagging and tracking project that deployed passive acoustic telemetry and archival tags [39][40][41]43 . Collectively, these data provide a novel opportunity to develop the use of benthic species as animal oceanographers and support model validation across a central portion of the WeStCOMS domain. ...
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Developments in animal electronic tagging and tracking have transformed the field of movement ecology, but interest is also growing in the contributions of tagged animals to oceanography. Animal-borne sensors can address data gaps, improve ocean model skill and support model validation, but previous studies in this area have focused almost exclusively on satellite-telemetered seabirds and seals. Here, for the first time, we develop the use of benthic species as animal oceanographers by combining archival (depth and temperature) data from animal-borne tags, passive acoustic telemetry and citizen-science mark-recapture records from 2016-17 for the Critically Endangered flapper skate (Dipturus intermedius) in Scotland. By comparing temperature observations to predictions from the West Scotland Coastal Ocean Modelling System, we quantify model skill and empirically validate an independent model update. The results from bottom-temperature and temperature-depth profile validation (5,324 observations) fill a key data gap in Scotland. For predictions in 2016, we identified a consistent warm bias (mean = 0.53 °C) but a subsequent model update reduced bias by an estimated 109% and improved model skill. This study uniquely demonstrates the use of benthic animal-borne sensors and citizen-science data for ocean model validation, broadening the range of animal oceanographers in aquatic environments.
... (Neat et al., 2015). Flapper skate demonstrated high occupancy of the deep water (100-150 m) within the NCMPA (Lavender et al., 2021a) in the summer months with more movement into shallower areas during the winter Lavender et al., 2021b). A second, smaller (6.05 km 2 ) urgent NCMPA The split of the species complex into flapper and common blue skate (Iglésias, Toulhoat & Sellos, 2010) has resulted in difficulty in interpreting earlier literature regarding the reproductive biology of the species. ...
... However, a successful conservation strategy requires protection across all life history stages of a species (Kinney & Simpfendorfer, 2009), particularly strongly K-selected species such as flapper skate (Ellis et al., 2021). Off the west coast of Scotland, flapper skate show high levels of site affinity to particular areas (Neat et al., 2015;Lavender et al., 2021a); therefore if areas containing habitats important for all life history stages (eggs, juveniles and adults) could be identified and protected, this could deliver important conservation benefits for the species. Thus far, an egg nursery or juvenile nursery have not been identified within the Loch Sunart to the Sound of Jura NCMPA which was designated for the presence of adult skate. ...
... Thus far, an egg nursery or juvenile nursery have not been identified within the Loch Sunart to the Sound of Jura NCMPA which was designated for the presence of adult skate. While flapper skate are capable of making long-range movements (Little, 1995;Lavender et al., 2021a) ...
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This study provides the first report of an egg nursery for the Critically Endangered flapper skate Dipturus intermedius and a description of the habitat, thus contributing towards our understanding of essential habitats for the species. In total, 1,395 flapper skate egg cases were recorded (accounting for overlapping surveys) in two egg case collection dives (n = 67 egg cases), one photogrammetry dive (n = 10 egg cases), 509 drop‐down video (DDV) camera drifts (n = 510 egg cases) and 18 remote operated vehicle (ROV) flights (n = 1,031 egg cases), carried out in the Inner Sound on the west coast of Scotland from 2018 to 2021. All of the egg cases were found on a shallow bedrock plateau between the Isle of Scalpay and a deep (>100 m) water channel between the Isle of Longay and the Crowlin Islands. Egg cases were observed on a cobble/boulder reef between 25 and 58 m depth, with a modelled annual temperature range of 9–12 °C, modelled current speeds up to 0.2 m−1, a rugosity index of 1.7 and low levels of sedimentation. Flapper skate egg cases are large and the incubation period is protracted (18 months), making them potentially vulnerable to anthropogenic disturbance. A description of the habitat where egg cases were observed in this study will help inform the search for egg nurseries for this Critically Endangered species elsewhere. Targeted DDV, ROV and scuba diving surveys will support this search in areas where suitable bathymetric and hydrodynamic conditions are identified. Safeguarding egg nurseries is essential for successful conservation. Protection should involve the designation of egg nurseries as Marine Protected Areas where activities that are likely to damage or alter seabed habitats are managed.
... The three main angling sites (Kerrera, Insh and Crinan) are noted in bold. Points mark recreational angling and scientific tagging events recorded in the capture-recapture (n = 1,166) and Movement Ecology of Flapper Skate archival (Star Oddi milli-TD) tagging (n = 45) databases, as described in Lavender et al. (2021a). Stars mark capture events associated with archival data used in this study (n = 26). ...
... Lavender et al. Behavioural Responses to Catch-and-Release three areas over relatively deep (> 100 m) water (Lavender et al., 2021a) ( Figure S1). Water temperature varies seasonally from a minimum of approximately 7.5°C in March to a maximum of 16.0°C in September, with the surface waters warming by 1-2°C more than the layers below in summer. ...
... In the MPA, 45 individuals were caught and tagged with Star Oddi milli-TD archival tags in March 2016-April 2017 ( Table S1) as part of research conducted by the Movement Ecology of Flapper Skate project on depth use (Thorburn et al., 2021), vertical movement (Lavender et al., 2021b) and residency (Lavender et al., 2021a). Skate were caught from two anchored charter vessels using 50-80 Ib class rods with lever drag multiplier reels. ...
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Selective pressures driving dispersal in vagile species often differ between males and females, resulting in sex-biased dispersal. Male-biased dispersal is common in mammals, where there is greater reproductive investment by females, and there is emerging evidence for a similar pattern in elasmobranchs. We examine the population structure of the short-tail stingray (Bathytoshia brevicaudata), a large, viviparous coastal species common in southern hemisphere waters. Using 11 nuclear (nDNA) microsatellite markers from 202 individuals in comparison to mitochondrial (mtDNA) data reported by Le Port and Lavery (J Hered 103:174–185, 2012), we elucidate patterns of dispersal at both southern hemisphere and New Zealand scales. At a global scale, estimates of population differentiation were comparable across marker types (microsatellite FST = 0.148, p < 0.001, mtDNA ϕST = 0.67, p < 0.001). In contrast, New Zealand structure was much weaker for microsatellite markers (FST = 0.0026, p > 0.05) than for mtDNA (ϕST = 0.054, p < 0.05). Female-only data displayed a greater degree of population differentiation from both nDNA and mtDNA compared to male-only data, and population assignment tests indicated that males were significantly more likely to be immigrants to the population from which they were sampled. We estimate that within New Zealand, male-mediated gene flow is at least fivefold greater than female-mediated gene flow. This molecular evidence for sex-biased dispersal in a batoid species adds further support to male-biased dispersal as a recurrent pattern in viviparous elasmobranchs. Many elasmobranch species are vulnerable to extinction, and understanding movement patterns is crucial to management of threatened populations.
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Bycatch in fisheries can have profound effects on the abundance of species with relatively low resilience to increased mortality, can alter the evolutionary characteristics and concomitant fitness of affected populations through heritable trait-based selective removals, and can alter ecosystem functions, structure and services through food web trophic links. We challenge current piecemeal bycatch management paradigms, which reduce the mortality of one taxon of conservation concern at the unintended expense of others. Bycatch mitigation measures may also reduce intraspecific genetic diversity. We drew examples of broadly prescribed ‘best practice’ methods to mitigate bycatch that result in unintended cross-taxa conflicts from pelagic longline, tuna purse seine, gillnet and trawl fisheries. We identified priority improvements in data quality and in understanding ecological effects of bycatch fishing mortality to support holistic ecological risk assessments of the effects of bycatch removals conducted through semi-quantitative and model-based approaches. A transition to integrated bycatch assessment and management that comprehensively consider biodiversity across its hierarchical manifestations is needed, where relative risks and conflicts from alternative bycatch management measures are evaluated and accounted for in fisheries decision-making processes. This would enable managers to select measures with intentional and acceptable tradeoffs to best meet objectives, when conflicts are unavoidable.
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Marine protected areas (MPAs) are increasingly advocated for the conservation and management of sharks and rays. However, substantial uncertainty remains regarding which species can benefit from MPAs. Meanwhile, area-focused protection targets have spurred recent and rapid gains in the creation of large MPAs, many of which carry vague objectives set by a diverse group of stakeholders with potentially different notions of "success." Here, we capture and critically evaluate current views on the use of MPAs for shark and ray conservation. Through interviews with scientists, MPA managers, fisheries experts, conservation practitioners, advocates and policy experts (n = 53), we demonstrate a variety of perspectives regarding: (a) the effectiveness of MPAs as a tool for shark and ray conservation; (b) which factors influence the success of MPAs for sharks and rays; and (c) the desired outcomes of these MPAs. While MPAs created specifically for sharks and rays were viewed to be slightly more effective than regular MPAs as a tool for shark and ray conservation, both were generally considered insufficient in isolation. Despite greater emphasis on social success factors (e.g., local support) over biophysical success factors (e.g., size), biological outcomes (e.g., increased abundance) were prioritized over social outcomes (e.g., livelihood benefits). We argue that a stronger focus on achieving social outcomes can enhance the potential for MPAs to benefit sharks and rays. In revealing current thinking regarding the drivers and indicators of MPA success for sharks and rays, the results of this study can inform efforts to conserve and manage these species. K E Y W O R D S effectiveness, factors, marine protected areas, outcomes, shark and ray conservation, success
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• Flapper skates (Dipturus intermedius) were once widespread in European shelf waters but are currently classified as critically endangered by the International Union for Conservation of Nature due to historical overexploitation. Novel monitoring approaches are needed to assess the efficacy of management measures, such as dedicated marine protected areas, for the conservation of relict skate populations. • Flapper skates possess distinctive dorsal spot patterns, which could potentially be used for individual recognition using photo‐identification (photo‐ID) approaches. This study assessed the potential of photo‐ID as a method for individual recognition of a relict population of skates within a dedicated marine protected area in western Scotland (UK), which has long been targeted by directed recreational angling. A collection of 486 photographs of 373 separate skate capture events from 2011 to 2016, taken with standard mobile phones and compact cameras, was studied using visual pairwise comparison methods to determine number of individuals and recapture rates. • Results indicated that adult flapper skates were individually recognizable with a high degree of certainty through comparison of spot patterns, assuming appropriate lighting conditions. A total of 226 individuals were identified, of which 77 (34%) were recaptured at least once. The average recapture interval was 308 days (SE: 29.4 days), with the longest recapture interval to date being 4.4 years. Spot patterns among recaptured tagged or otherwise uniquely identifiable skates were found to remain stable over timescales of months to >1 year. • Results indicate that photo‐ID, based on photographs sourced through citizen science approaches, can provide a low‐cost alternative means of monitoring flapper skate presence and distribution for the purposes of underpinning management decisions.
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Background: Central place foragers (CPF) rest within a central place, and theory predicts that distance of patches from this central place sets the outer limits of the foraging arena. Many marine ectothermic predators behave like CPF animals, but never stop swimming, suggesting that predators will incur 'travelling' costs while resting. Currently, it is unknown how these CPF predators behave or how modulation of behavior contributes to daily energy budgets. We combine acoustic telemetry, multi-sensor loggers, and hidden Markov models (HMMs) to generate 'activity seascapes', which combine space use with patterns of activity, for reef sharks (blacktip reef and grey reef sharks) at an unfished Pacific atoll. Results: Sharks of both species occupied a central place during the day within deeper, cooler water where they were less active, and became more active over a larger area at night in shallower water. However, video cameras on two grey reef sharks revealed foraging attempts/success occurring throughout the day, and that multiple sharks were refuging in common areas. A simple bioenergetics model for grey reef sharks predicted that diel changes in energy expenditure are primarily driven by changes in swim speed and not body temperature. Conclusions: We provide a new method for simultaneously visualizing diel space use and behavior in marine predators, which does not require the simultaneous measure of both from each animal. We show that blacktip and grey reef sharks behave as CPFs, with diel changes in activity, horizontal and vertical space use. However, aspects of their foraging behavior may differ from other predictions of traditional CPF models. In particular, for species that never stop swimming, patch foraging times may be unrelated to patch travel distance.
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Numerous studies over the last decades have focused on marine protected areas (MPAs) and their effects on fish communities. However, there is a knowledge gap regarding how species that live associated with soft-substrates (e.g., sand, mud) respond to spatial protection. We analyzed abundance, biomass and total lengths of the soft-bottom fishes in a multiple-use MPA in the north-eastern Atlantic, the Luiz Saldanha Marine Park (Portugal), during and after the implementation of its management plan. Data were collected by experimental fishing in areas with three different levels of protection, during the implementation period and for three years after full implementation of the MPA. Univariate analysis detected significant biomass increases between the two periods. Fish assemblages were mainly structured by depth and substrate, followed by protection level. Community composition analyses revealed significant differences between protection levels and between the two periods. Species exhibited a broad variation in their response to protection, and we hypothesize that factors such as species habitat preferences, body size and late maturity might be underlying determinants. Overall, this study provides some evidence of protection effectiveness in soft-bottom fish communities, supported by the significant increase in biomass in the protected areas and the positive trends of some species.
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Significance The occupation of progressively deeper waters with increasing size and age of fish is common among commercially exploited species, a behavior attributed to evolved ontogenies. Recently deepening has been attributed to ocean warming. We evaluated the possibility, ignored in previous analyses, that these patterns result from selective exploitation of larger individuals. We found that size-selective exploitation accounted for >70% of the deepening of cod on the Scotian Shelf (Northwest Atlantic). This deepening declined dramatically when exploitation was banned. Ontogeny contributed to the remaining variance. The claim that deepening can be used as an index of ocean warming should be exercised with caution; the overarching effect of exploitation should be specifically addressed in all such analyses.
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Scientific monitoring has recorded only a recent fraction of the oceans’ alteration history. This biases our understanding of marine ecosystems. Remote coral reef ecosystems are often considered pristine because of high shark abundance. However, given the long history and global nature of fishing, sharks’ vulnerability, and the ecological consequences of shark declines, these states may not be natural. In the Chagos archipelago, one of the remotest coral reef systems on the planet, protected by a very large marine reserve, we integrated disparate fisheries and scientific survey data to reconstruct baselines and long-term population trajectories of two dominant sharks. In 2012, we estimated 571,310 gray reef and 31,693 silvertip sharks, about 79 and 7% of their baseline levels. These species were exploited longer and more intensively than previously thought and responded to fishing and protection with variable and compensatory population trajectories. Our approach highlights the value of integrative and historical analyses to evaluate large marine ecosystems currently considered pristine.
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Diel vertical migration (DVM) is a widespread behaviour among many pelagic species, from zooplankton to sharks, and has been widely studied in both marine and freshwater environments. Usually, DVM comprises repeated daily vertical movements through the water column, from shallower at night to deeper during the day. Consequently DVM is perhaps unexpected in benthic predators, nonetheless, DVM has been observed in benthic sharks and freshwater teleosts, where it comprises inshore-offshore migrations over the substrate. However there is no clear evidence of this behaviour in large temperate benthic predators, such as skates. Here we present new observations of DVM in 4 species of skate (Raja brachyura, R. clavata, R. microocellata and R. montagui) that identify it as a general behaviour in this clade. Analysis of 89 depth recording archival tags yielded 674 clear DVM events where skate left daytime deeper waters for shallower night time areas before returning to within 2.5 m of starting depths. Interestingly, these events closely resemble those of central place foragers, where shallow areas are foraging and deeper areas are refuging locations. Behaviour such as this has not been previously recorded in marine benthic predators and the findings suggest DVM might occur in many other benthic species. A broader understanding of DVM in benthic animals will be important in the design of effective boundaries for marine protected areas. These findings also have implications for trophic coupling between deep and shallow benthic zones. Further characteristics of this unexpected behaviour are presented and hypotheses for its occurrence are discussed.
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There is a growing need to understand the inter-annual movements of mobile marine species of conservation concern to inform the design and placement of Marine Protected Areas (MPAs) to maximise their conservation potential. We use satellite telemetry data from 36 basking sharks (Cetorhinus maximus) tracked in 2012, 2013 and 2014 (cumulative total: 1598 days; median: 44 days; range: 10–87 days) to quantify movements in coastal waters off the west coast of Scotland within the Sea of the Hebrides proposed MPA. Sharks exhibited seasonal residency to the proposed MPA, with a mean of 84% of filtered best daily locations occurring within its boundaries (2012 = 80%, 2013 = 90% and 2014 = 74%). Three long-term tracked basking sharks demonstrated inter-annual site fidelity, returning to the same coastal waters in the year following tag deployment, with two returning to within the boundaries of the proposed MPA. These data likely suggest the area experiences favourable conditions and/or resources for basking sharks across years and, if designated, coupled with appropriate management, could afford protection during summer months.
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Animal movements, in particular residency or return migrations (collectively defined as ‘philopatry’), can shape population structure and have implications for management. This review examines the evidence for philopatry in batoids, which are some of the least understood and most threatened vertebrates, and updates a prior review of the same in sharks. Evidence for philopatry in batoids was found in 46 studies, including 31 species that involve 11 species complexes. Batoid philopatry research has lagged behind shark philopatry research, with the annual publication rate of shark philopatry studies in the last 5 yr (17 yr-1) being more than twice that of batoids (7 yr-1). Philopatry research on both sharks and rays is taxonomically skewed: <50% of elasmobranch families are represented. Research is also skewed towards charismatic megafauna (white sharks, whale sharks, and manta rays), while the batoid philopatry literature is biased towards ‘Near Threatened’ species, even though approx. 47.5% of batoids are considered to be ‘Data Deficient’ by the IUCN. Limited evidence was found for residency in batoids, contrary to popular assumptions that they are sedentary, and there was limited evidence for sex-differentiated movements. Hypothesis-driven research, longer study durations, more taxon and life stage diverse studies, and consistent use of philopatry terminology are needed to advance the fields of batoid philopatry and conservation. Given strong evidence of philopatry in some species of batoids, management should proceed at the local scale until more studies are conducted.
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A sympatric assemblage of morphologically similar predators is expected to exhibit fine-scale habitat segregation, or resource partitioning, to reduce the effects of direct competition. This principle has been well studied for predators in terrestrial ecosystems. In the marine environment, the fine-scale spatial segregation of sympatric species of large predators is poorly understood because detailed movement and behavioural data are often not available across multiple species within the same timeframe. The ways in which co-occurring congeneric predators separate spatially is even less well understood. Medium-sized species of skates (genus Raja) co-occur in temperate habitats of the north-east Atlantic Ocean, share similar morphologies and have distributional ranges that overlap significantly in the western English Channel ecosystem. In the present study, detailed depth time series retrieved from 89 electronic data storage tags attached to 4 species of skate were analysed to determine preferred depth ranges. The 4 species were found to segregate spatially into 2 groups, with one group having a significantly shallower core annual depth range than the other. To our knowledge, fine-scale segregation by depth has not been observed previously. Interestingly, the members of each species group appeared complementary, each group comprising species with different dietary preferences and with a larger and smaller body size. An understanding of how core depth ranges differ and how these species utilise vertical habitat could potentially enable geographic ranges around the coast to be predicted, with important implications for how these species interact with fisheries and Marine Protected Areas.
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• Knowledge of vital data such as growth and age at maturity is necessary to develop effective management strategies for endangered species. The Critically Endangered flapper skate (Dipturus intermedius) is the largest skate in the North Atlantic and growth information, necessary to assess key life-history traits, populations’ growth rates and anticipate their response to management measures, is still lacking. • While classical age estimation methods used in fish generally require the analysis of calcified structures, destructive methods are incompatible with conservation objectives for this species. Taking advantage of the high recreational value of the flapper skate, this study uses citizen-science data originating from photo-identification of trophy pictures and tag–recapture data supported by anglers to estimate growth in this Critically Endangered species. Using the growth increments measured between recapture events, an individual-based Von Bertalanffy growth model was fitted to the data using Bayesian inference. • The results confirm that the flapper skate is a long-lived species with ages estimated as >40 years for the largest individuals captured. Despite this longevity, the model reveals a relatively fast initial growth but relatively late ages at maturity and significant sex-related differences in both growth rate and maximum size. • These results suggest that population growth rate, and therefore recovery, might be much slower than previously reported. By using citizen science this study provides the necessary information to begin understanding population dynamics and monitor the recovery of an iconic Critically Endangered species.
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This review represents a comprehensive analysis on pollutants in elasmobranchs including meta-analysis on the most studied pollutants: mercury, cadmium, PCBs and DDTs, in muscle and liver tissue. Elasmobranchs are particularly vulnerable to pollutant exposure which may pose a risk to the organism as well as humans that consume elasmobranch products. The highest concentrations of pollutants were found in sharks occupying top trophic levels (Carcharhiniformes and Lamniformes). A human health risk assessment identified that children and adults consuming shark once a week are exposed to over three times more mercury than is recommended by the US EPA. This poses a risk to local fishing communities and international consumers of shark-based products, as well as those subject to the widespread mislabelling of elasmobranch products. Wider screening studies are recommended to determine the risk to elasmobranchs from emerging pollutants and more robust studies are recommended to assess the risks to human health.
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The protection of sensitive species from overfishing is a key aspect of the ecosystem approach to fisheries management. We use life history parameters and knowledge of fish shape and habitat to estimate the sensitivity of 270 species in the Northeast Atlantic to demersal trawling and compare sensitivity to the most recent IUCN categorization. Species classified as threatened were on average significantly more sensitive to trawling than other species. Using trawl surveys in European Atlantic waters from 36oN to 62oN, we estimated indicators of abundance of 31 highly sensitive species and compared changes in abundance to sensitivity, management measures and value of landings. The abundance of 23 of the 31 sensitive species increased after year 2000 with 14 of the species showing increases significant at the 5% level. The increases were not due to specific management measures, as less than half of the species were covered by catch limits. Further, sensitivity or value of landings were not related to trends in abundance. Three species (Atlantic wolf‐fish, tusk and starry ray) declined significantly. These species are all at their southern distributional limit in the North Sea. Synthesis and applications. We recommend monitoring the development of sensitive species to identify species under pressure and allow rapid management actions before species enter the IUCN threatened category. Further, we recommend taking precautions where species are under combined pressure from climate change and fishing.
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Knowledge of skate ecology must be improved to ensure their effective protection. This study represents the first description of diet composition for one of the largest European rajid, the blue skate Dipturus cf. flossada . A total of 346 specimens collected in Celtic Sea from 2012 to 2015 were analysed for their gut content, with respect to individual total length, maturity stage and sex. Overall, blue skate diet mainly consisted of shrimps and prawns, crabs and teleost fishes. Non‐metric multidimensional scaling and ANOSIM analyses revealed major ontogenetic shifts in feeding strategy that were related to size and maturity, but not to sex. Shrimps and prawns, mostly composed of Crangon allmanni , dominated the diet of small and immature individuals, while mod‐size skate primarily preyed on crabs. The prevalence of crustaceans decreased with size and maturity and was gradually replaced by teleost fishes in large mature individuals. A concomitant increase of the trophic level with size revealed that large blue skate become a top predator within the ecosystem. These results highlight the need to include the ontogenetic changes in the diet description. As individuals grow and mature, blue skates can play a fundamental role in the structure of the Celtic Sea food web. This article is protected by copyright. All rights reserved.
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MPAs are expected to improve the conservation status of rare and important habitats and species. However, the reduction in anthropogenic pressure due to such management measures is rarely estimated. Although MPA networks may cover a large proportion of the seabed, designated areas that prohibit damaging fishing activity are often much smaller. This case study compares fishing pressure inside and outside areas covered by Scottish MPAs and MPA management measures, further relating its distribution to bottom ruggedness, which influences benthic communities and their exposure to mobile bottom fishing. While 7% of the study region was found to be within MPA boundaries, only 2.5% of the region was subject to management measures that restrict mobile bottom fishing. Taking historical levels of fishing as a benchmark, management measures have been applied to <0.6% of the swept area of existing mobile bottom fishing activity. This may be explained by the higher average seabed ruggedness within MPA management measures, which was also where some key species of conservation interest were found. These findings suggest that protection has been focussed in areas that already act as natural refugia for sensitive benthic species and lie away from the majority of fishing activity. While the measures do not reduce fishing pressure markedly, they do protect relatively pristine habitats from future fishing impacts. MPA management measures had higher average seabed ruggedness, suggesting a bias in protection for species and habitats within such areas.
Article
Often the ecology of a commercially fished species and the behaviour of the fishers are inextricably linked. An understanding of both species ecology and fisher behaviour are therefore fundamental for effective fisheries management. In Europe, Rajidae are commercially fished species that are vulnerable to overfishing, have historically been grouped in landings data and declines have been reported to the point of local extinction in some species. Management of these species is therefore important, however an understanding of species ecology and the way they interact with the fishery is lacking. Here we investigate how the differing ecology of four species affects interactions with the fishery by considering gear types, Marine Protected Areas, location of capture and geographic displacements. Our results demonstrate that the four species interacted differently with the fishery, for example Raja clavata were more commonly captured by static nets (69 % of recaptures) and Raja brachyura more commonly by trawlers (77 %). There were clear differences in the location of capture, depths and displacements of the four species resulting in differing interactions with existing management in the form of Marine Protected Areas. For example 53 % of R. clavata recaptures were within the boundaries of an MPA compared to 18 % for R. brachyura. These results provide important differences among species that are generally grouped by current management, emphasising the need for further species specific research to ensure effective management.
Article
No-take marine protected areas (MPAs) are a commonly applied tool to reduce human fishing impacts on marine and coastal ecosystems. However, conservation outcomes of MPAs for mobile and long-lived predators such as sharks are highly variable. Here, we use empirical animal tracking data from 459 individual sharks and baited remote underwater video surveys undertaken in 36 countries to construct an empirically supported individual-based model that estimates the conservation effectiveness of MPAs for five species of coral reef-associated sharks (Triaenodon obesus, Carcharhinus melanopterus, Carcharhinus amblyrhynchos, Carcharhinus perezi, and Ginglymostoma cirratum). We demonstrate how species-specific individual movement traits can contribute to fishing mortality of sharks found within MPAs as they move outside to adjacent fishing grounds. We discovered that the world's officially recorded coral reef-based managed areas (with a median width of 9.4 km) would need to be enforced as strict no-take MPAs and up to 5 times larger to expect protection of the majority of individuals of the five investigated reef shark species. The magnitude of this effect depended on local abundances and fishing pressure, with MPAs required to be 1.6-2.6 times larger to protect the same number of Atlantic and Caribbean species, which occur at lower abundances than similar species in the western Pacific. Furthermore, our model was used to quantify partially substantial reductions (>50%) in fishing mortality resulting from small increases in MPA size, allowing us to bridge a critical gap between traditional conservation planning and fisheries management. Overall, our results highlight the challenge of relying on abundance data alone to ensure that estimates of shark conservation impacts of MPAs follow the precautionary approach.
Article
The implementation of spatial protection measures is currently a priority in batoid species' conservation strategies, but their spatial ecology remains largely unknown. We provide some preliminary insights into the movement patterns of the white skate (Rostroraja alba), a batoid classified as Critically Endangered in European waters. Three individuals (two females: one mature, one immature; and one immature male) were monitored with acoustic telemetry in a marine protected area (Portugal). The mature female remained present in the study area throughout the whole monitoring period (20 months). Residency analyses revealed this specimen spent more than 70% of the time within this coastal marine park. The immature female and the immature male were only detected during three and four months, respectively. Whether the uncovered movement patterns are common within the population remains unclear, but the present study provides useful information to better plan future research on the movement ecology of a rather unstudied species.
Article
Despite increased focus on ascertaining the status of elasmobranch fish, the stock units for many species are uncertain. Data from mark-recapture tagging studies undertaken from 1959–2017 were analysed for 13 batoid species. Data were most comprehensive for skates (Rajidae), with 22,374 released and 3342 (14.9%) returned. Most data related to thornback ray Raja clavata , blonde ray R. brachyura and spotted ray R. montagui . Tags were generally returned from areas less than 50 km from their release, and usually from the ICES Division in which they were released. However, straight-line distances travelled of up to 910 km ( R. brachyura ) and 772 km ( R. clavata ) were recorded, highlighting that individual skates are capable of longer-distance movements. The maximum time at liberty was 16.6 years ( R. clavata ). Whilst mark-recapture data indicated that the current stock units used by ICES are broadly appropriate, southward movements of several skate species tagged off Northern Ireland (Division 6.a) to the Irish Sea (Division 7.a) were observed. In contrast, skates tagged in the Irish Sea and Bristol Channel (Division 7.f) generally remained in that area, with only occasional recaptures from Division 6.a.
Article
Tope (Galeorhinus galeus) is a highly mobile elasmobranch in the temperate to subtropical northeast Atlantic. It is highly migratory and has been shown to display complex movement patterns, such as partial migration, in the southern hemisphere. In the northeast Atlantic, previous mark-recapture studies have struggled to identify movement patterns and the species behavior is poorly described, yet identification of migratory behaviors and habitats of importance for the species is of paramount importance for effective management. Here, we combined fisheries independent survey data with mark-recapture (MR) data to investigate the distribution of different age classes of tope across the northeast Atlantic. We further investigated depth use in detail with archival electronic tags and a pop-up satellite archival tag (PSAT). We suggest previous studies struggling to find consistent movement patterns using MR data were confounded by a combination of site fidelity, partial migration by females, and increasing depth and home range of juveniles. Survey and MR data showed immature tope <40 cm were caught exclusively in continental shelf waters <45 m deep, showing a significant relationship between habitat depth and total length. Immature individuals seemed to remain on the continental shelf, while mature tope of both genders were caught in both shelf and offshore waters. This use of deeper water habitats by mature tope was further supported by archival tags, which indicated individuals use both shallow (<200 m depth) and deep-water habitats, diving to depths of 826 m; the deepest record for this species. The PSAT tag tracked the horizontal movements of an adult male, which confirmed utilization of both shallow inshore and deep offshore habitats. Most tope remained within 500 km of their tagging site, although some mature females had a larger, more southerly range, including connectivity with the Mediterranean. This study clearly demonstrates the highly migratory habits of tope, and suggests larger individuals divide their time between shallow and deep-water habitats. It shows the northeast Atlantic tope population should benefit from consistent management throughout its range.
Article
Batoids (Chondrichthyes: Batoidea; e.g. stingrays, skates, and guitarfish) comprise more than 55% of elasmobranch taxa and represent ecologically important predators in benthic and pelagic habitats. Although overexploitation and habitat degradation are the two biggest threats to batoid populations, coastal and oceanic pollution is also a pervasive potential threat. In this systematic review, we compile published scientific literature on trace metals and persistent organic pollutants (POPs) contamination in elasmobranch species of the Batoidea superorder and present contamination patterns, exposure effects, and potential human exposure risks to most reported contaminants. We found batoids to accumulate a wide range of trace metals, including mercury (Hg), arsenic (As), lead (Pb), copper (Cu), cadmium (Cd) and zinc (Zn). Accumulation of POPs is reported for chlordanes, dichlorodiphenyltrichloroethane (DDT), polychlorinated biphenyl (PCB), dieldrin, Heptachlor epoxide, hexachlorobenzene and perfluoroalkyl substances (PFAS). Hg levels in muscle tissue were significantly different among oceanic basins and habitats, consistent with previous global assessments of Hg oceanic background levels. Some batoid species presented Hg levels higher than large pelagic teleost fishes and comparable to sharks. Ecological traits such as, bottom feeding, upper trophic position and elasmobranch-specific physiology and metabolism are discussed as potential factors associated with Hg uptake and accumulation in batoids. Some species exceeded USEPA's maximum contamination safety limits in edible tissues for Hg, As and ΣPCBs. For most trace metals and POPs, there is a lack of studies focusing on contamination levels in batoids. We recommend future research increasing reporting on POPs and trace metals besides Hg in batoids to further investigate the role of Elasmobranch as a bioindicator for marine pollution.
Article
Skates (class Chondrichthyes; subclass Elasmobranchii; order Rajiformes; family Rajidae) comprise one quarter of extant chondrichthyans, yet have received little attention in the scientific literature likely due to their relatively low economic value and difficulties in species identification. The absence of species-specific information on catch, life history and migration of skates has often precluded the development of single-species stock assessments and led to the use of cursory multispecies assessments, which lack the ability to track species-specific catch and abundance trends. This has resulted in undetected local extirpations, as has been previously reported for common (Dipturus batis, Rajidae), white (Rostroraja alba, Rajidae), and long-nose (Dipturus oxyrhinchus, Rajidae) skates in the Irish Sea. Here, we (1) use case studies to illustrate how the perception of skate population structure and stock status has historically been masked through multispecies assessment and management practices; (2) review current information on the movement of skates and identify gaps in knowledge; and (3) identify biases associated with the use of various tagging technologies, which have confounded our understanding of movement and migration ecology of skates. Considering that over 40% of extant Rajidae species are listed as ‘Data Deficient’ by the International Union for Conservation of Nature, we illustrate a critical need to broaden the current understanding of skate life history, movement, and migration ecology by providing recommendations on the further application of electronic tags and biogeochemical natural tags in movement studies, and highlight the benefits that studies using these approaches have for novel management frameworks.
Article
PCB—still a problem Until they were recognized as highly toxic and carcinogenic, polychlorinated biphenyls (PCBs) were once used widely. Their production was banned in the United States in 1978, though they are still produced globally and persist in the environment. Persistent organic compounds, like PCBs, magnify across trophic levels, and thus apex predators are particularly susceptible to their ill effects. Desforges et al. looked at the continuing impact of PCBs on one of the largest marine predators, the killer whale. Using globally available data, the authors found high concentrations of PCBs within killer whale tissues. These are likely to precipitate declines across killer whale populations, particularly those that feed at high trophic levels and are the closest to industrialized areas. Science , this issue p. 1373
Article
Habitat mapping is an important tool for marine spatial planning and is required for most ecosystem-based management approaches. The Firth of Lorn Special Area of Conservation (SAC), west Scotland, was originally designated for its rocky reef habitat but it is also an area of high importance for the Flapper skate (Dipturus intermedius) and Harbour porpoise (Phocoena phocoena). Here we present an improved predictive habitat map for the SAC utilising multibeam backscatter and bathymetry data collected as part of the Ireland, Northern Ireland and Scotland Hydrographic Survey Project. Backscatter, bathymetry and bathymetric derivatives were analysed using Principal Component Analysis (PCA) and acoustic signatures were created from drop-down video habitat location data. A predictive habitat map was created from Maximum Likelihood Classification using the PCA. Dominant habitat types identified included; moderate energy circalittoral rock (CR.MCR), sublittoral mixed sediment (SS.SMx) and sublittoral sand and muddy sand (SS.SSa). Drop down video showed variable accuracy with 0–100% correctly classified habitats due to the small sample size. The initial validation points were added and the model was rerun. In areas with no previous sea truthing points, some predictions changed to SS.SMx at depths > 100 m and SS.SSa in depths < 50 m, suggesting that the model can be improved with a greater depth-range of sea truthing data. Modern acoustic surveys undertaken for other purposes, such as navigational charting, can thus be used to generate broad-scale predictive habitat maps in a cost and time effective manner. Such maps have the potential for a wide range of use by marine stakeholders, in particular, for establishing environmental baselines for long term monitoring of benthic habitats. Given the high costs of surveying, such an approach supports the rationale of “Collect once and use many times”.
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