INTRODUCTION:Over the last century, sea surface temperatures have increased by more than 0.5°C, with predictions suggesting an increase of 1-4°C by 2100. Oceanic warming poses significant challenges to marine species, particularly those with physiological and developmental processes that are tightly linked to environmental conditions. In cartilaginous fishes, including sharks, the brain grows continually throughout life, supported by the capacity for lifelong neurogenesis. This feature suggests that the nervous system - both peripheral (sensory) and central (brain) - of sharks may be highly plastic and able to adapt dynamically to a changing environment. METHODS:We investigated the effects of elevated rearing temperature on brain development in the epaulette shark (Hemiscyllium ocellatum), a species known for its tolerance of environmental fluctuations in intertidal habitats. Eggs (n = 12) were sourced from a breeding stock at the New England Aquarium and reared in either ambient (27°C) or elevated (31°C, 4°C above ambient) seawater temperatures until 2 months post-hatch. Using histological analyses, we compared the relative volume of the nose (olfactory rosette), total brain, and major brain regions between treatment groups. RESULTS:Despite this species' natural exposure to temperature variability, generalized linear models revealed that elevated temperature significantly altered the volume of the olfactory sensory epithelium, olfactory bulbs, and medulla oblongata after accounting for overall brain size. Analyses of proportional brain region volumes also showed that elevated temperature was associated with reduced olfactory bulb size and increased subpallial volume relative to total brain size. These differences may suggest potential changes in cognitive capacity related to olfactory processing as well as sensory and/or motor functions at elevated temperatures. CONCLUSIONS:While short-term studies, such as this one, cannot capture long-term adaptive potential, understanding the impacts of elevated temperature on brain phenotypes provides critical insights into how elasmobranchs may cope with changing ocean conditions. Such knowledge will be vital for predicting the resilience of these ecologically important species to future environmental stressors.
Reproduction in chondrichthyan fishes (sharks, rays, skates, and chimaeras) is generally assumed to be a long-term, energetically costly process, given their slow generation times. However, metabolic costs of reproduction remain poorly understood due to a lack of direct, non-lethal measurements. To address this, we investigated metabolic and physiological changes during oviparous reproduction in five female epaulette sharks (Hemiscyllium ocellatum). We tracked oxygen uptake rates - a proxy for metabolic rate - across a 3-week cycle, capturing data before, during, and after egg case encapsulation and oviposition. We also measured reproductive hormones (testosterone, 17β-estradiol, progesterone) and hematological parameters (hematocrit, hemoglobin concentration). Results revealed a positive but non-significant relationship between metabolic rate and body mass, and contrary to expectations, metabolic rate did not significantly change throughout the 19-day cycle. Hormone levels remained stable, except for a transient testosterone peak early in the cycle, and hematological parameters showed no significant variation. These findings tentatively suggest epaulette sharks maintain reproductive effort without marked increases in metabolic or physiological costs. Continued research under seasonal environmental variation could clarify reproductive energetics in chondrichthyans further. This study provides the first direct measurement of metabolic effects of oviparous reproduction in chondrichthyans, challenging assumptions about energetic demands in this taxon.
ObjectiveA recent expansion of the northern stock of Black Sea Bass Centropristis striata into the northern Gulf of Maine raises questions about this species' movement and population dynamics in this region. Determining the origin of these fish is essential, as dramatic changes in migration patterns or current population boundaries could have profound effects on stock assessment estimates and subsequent management regulations.MethodsIn this study, we measured otolith core concentrations of stable isotopes (delta 18O, delta 13C) and trace element:calcium ratios (Mg:Ca, Mn:Ca, Cu:Ca, Zn:Ca, Ba:Ca, Sr:Ca) to assess the natal origin of Black Sea Bass that were caught off the coast of Maine. Spawning condition adults from southern New England (SNE) and the mid-Atlantic Bight (MAB) were used to characterize the chemical fingerprint of these known spawning regions.ResultUnique chemical fingerprints were identified for fish from SNE and the MAB, with high reclassification success using random forest analysis (16% error rate). The classification of Black Sea Bass of unknown origin that were caught in Maine waters indicated that 85% of the samples matched to SNE and 13% to the MAB, whereas one sample remained unclassified.ConclusionResults from this study support the current management population separation of the northern stock of Black Sea Bass between SNE and the MAB and lends additional information to the understanding of this species' movement into the northern Gulf of Maine. As fish stocks around the world continue to shift into new regions due to climate change, knowledge of their natal origin will be critical to long-term sustainable management of this species. Determining which population Black Sea Bass located in Maine came from helps scientists understand how these fish migrated there, their potential for success, and their expected growth and maturity. If this species becomes more abundant in the region, this information could help inform regulation surrounding conservation and fishing practices.Impact statement
Body condition is an important proxy for the overall health and energetic status of fishes. The classically used Fulton's condition factor requires length and mass measurements, but mass can be difficult to obtain in large species. Girth measurements can replace mass for wild pelagic sharks. However, girth-calculated condition has not been validated against Fulton's condition factor intraspecifically, across ontogeny or reproduction, or in a controlled setting. We used the epaulette shark (Hemiscyllium ocellatum), because they are amenable to captive reproduction, to track fine-scale body condition changes across life stages, oviparous reproduction and between condition indices. We measured four girths, total length and mass of 16 captive epaulette sharks across 1 year and tracked female reproduction daily. We also collected length and mass data from an additional 72 wild-caught sharks and 155 sharks from five previous studies and two public aquaria to examine the relationship between length and mass for this species. Even though data were derived from a variety of sources, a predictable length-mass relationship (R-2 = 0.990) was achievable, indicating that combining data from a variety of sources could help overcome knowledge gaps regarding basic life history characteristics. We also found that condition factor decreased during early life stages, then increased again into adulthood, with predictable changes across the female reproductive cycle. Finally, we determined that both Fulton's and girth condition analyses were comparable. Outcomes from this study uniquely provide body condition changes across the complete life history, including fine-scale female reproductive stages, and validate the use of girths as a nonlethal whole-organism energetic assessment for fishes.
Epaulette sharks ( Hemiscyllium ocellatum ) inhabit shallow tropical habitats with elevated and fluctuating temperatures. Yet, according to global climate change projections, water temperatures in these habitats will rise beyond current cyclical variability, warranting further studies incorporating chronically elevated temperature exposure in this species. This study examined the differences in skeletal muscle morphological and metabolic properties in neonate epaulette sharks exposed to their current-day ambient (27 °C) or projected end-of-century (31 °C) habitat temperatures throughout embryonic and neonatal development. Metrics of skeletal muscle, such as muscle fiber size and density, nuclear density, and satellite cell density, were used to assess the relative contribution of hypertrophic and hyperplastic growth processes. Capillary density was measured as a proxy for peripheral oxygen supply to muscle tissue. At 31 °C, sharks hatched earlier, but were similar in body size 60 days post-hatch. Muscle fiber size, nuclear density, and capillary density were similar between temperature regimes. However, fiber density was lower, satellite cell density was higher, and fibers associated with satellite cells were smaller in sharks reared at 31 °C. These results suggest that elevated temperature may impair or slow satellite cell fusion to existing fibers and new fiber formation. To assess potential metabolic and developmental consequences of elevated temperatures, oxidative damage (2,4-DNPH, 8-OHdG, 4-HNE), protein degradation (Ubiquitin, LC3B, Hsp70), and muscle differentiation (Myf5, Myogenin) markers were measured. Protein carbonylation was higher at elevated temperatures, suggesting that warmer incubation temperatures at early life stages may result in oxidative damage accrual. However, protein degradation and muscle differentiation markers did not differ. These results suggest that projected end-of-century temperatures may alter muscle growth and metabolism in tropical shark species with potential consequences to shark growth and fitness.
Recent work in the Gulf of Maine multispecies recreational fishery has established responsible fishing practices that anglers can use to reduce bycatch and the discard mortality of three key groundfish species. However, anglers represent a diverse stakeholder group whose backgrounds and experiences may influence how they receive, support, and adopt responsible fishing practices that aim to sustain catch-and-release angling opportunities. We therefore surveyed Gulf of Maine recreational anglers who target groundfish, including Atlantic Cod Gadus morhua, Haddock Melanogrammus aeglefinus, and Cusk Brosme brosme, to assess whether differences among anglers influenced how likely anglers were to voluntarily adopt or consider adopting responsible fishing practices and which information channels they used to obtain such information. By broadly sampling Gulf of Maine recreational fishing license holders via an online survey, we collected responses from 306 respondents who targeted groundfish in some capacity; several topics, including fishing activity and experience, responsible fishing practices, information channels, and sociodemographics, were addressed in the survey. A latent class cluster analysis found that respondents who participate in this regional fishery can be broadly categorized into three distinct classes (Striped Bass [Morone saxatilis] Enthusiasts, All-rounders, and Offshore Groundfishers) from their primary fishing mode and target species. Despite the presence of these latent classes, class membership did not affect how likely respondents were to voluntarily adopt or consider adopting species-specific fishing practices from previous scientific investigations. However, class membership was observed to influence how respondents used information channels to receive angling information, with Offshore Groundfishers relying more often on captains and crew than the other classes. Therefore, to promote responsible fishing practices alongside regulations, we recommend that fishery managers use a mixed outreach program to effectively communicate and engage with this portion of the community until more directed studies can be conducted.
Owing to climate change, most notably the increasing frequency of marine heatwaves and long-term ocean warming, better elucidating the upper thermal limits of marine fishes is important for predicting the future of species and populations. The critical thermal maximum (CTmax), or the highest temperature a species can tolerate, is a physiological metric that is used to establish upper thermal limits. Among marine organisms, this metric is commonly assessed in bony fishes but less so in other taxonomic groups, such as elasmobranchs (subclass of sharks, rays and skates), where only thermal acclimation effects on CTmax have been assessed. Herein, we tested whether three life history stages, sex and body size affected CTmax in a tropical elasmobranch, the epaulette shark (Hemiscyllium ocellatum), collected from the reef flats surrounding Heron Island, Australia. Overall, we found no difference in CTmax between life history stages, sexes or across a range of body sizes. Findings from this research suggest that the energetically costly processes (i.e. growth, maturation and reproduction) associated with the life history stages occupying these tropical reef flats do not change overall acute thermal tolerance. However, it is important to note that neither embryos developing in ovo, neonates, nor females actively encapsulating egg cases were observed in or collected from the reef flats. Overall, our findings provide the first evidence in an elasmobranch that upper thermal tolerance is not impacted by life history stage or size. This information will help to improve our understanding of how anthropogenic climate change may (or may not) disproportionally affect particular life stages and, as such, where additional conservation and management actions may be required.
Biological rhythms that are mediated by exogenous factors, such as light and temperature, drive the physiology of organisms and affect processes ranging from cellular to population levels. For elasmobranchs (i.e. sharks, rays, and skates), studies documenting diel activity and movement patterns indicate that many species are crepuscular or nocturnal in nature. However, few studies have investigated the rhythmicity of elasmobranch physiology to understand the mechanisms underpinning these distinct patterns. Here, we assess diel patterns of metabolic rates in a small meso-predator, the epaulette shark (Hemiscyllium ocellatum), across ecologically relevant temperatures and upon acutely removing photoperiod cues. This species possibly demonstrates behavioral sleep during daytime hours, which is supported herein by low metabolic rates during the day and a 1.7-fold increase in metabolic rates at night. From spring to summer seasons, where average average water temperature temperatures for this species range 24.5 to 28.5 °C, time of day, and not temperature, had the strongest influence on metabolic rate. These results indicate that this species, and perhaps other similar species from tropical and coastal environments, may have physiological mechanisms in place to maintain metabolic rate on a seasonal time scale regardless of temperature fluctuations that are relevant to their native habitats.
Animal behavior varies in response to capture between/within species and fisheries, and its expression may contribute to incidental mortality when behaviors result in physiological ramifications that cannot be resolved. However, this relationship between capture behavior and animal health is poorly understood, and it remains a logistical challenge to evaluate behavior during capture. We describe an experimental technique that characterizes and quantifies capture behavior in hook-and-line fisheries. This technique includes (1) simultaneously monitoring the behavioral response to capture with accelerometers and cameras, (2) characterizing behavior from video footage and linking discrete behaviors to acceleration data, and (3) predicting behavior based solely on acceleration data using an ensemble of supervised classification methods. We captured oceanic whitetip sharks, Carcharhinus longimanus, with experimental (hook-and-line) gear to test these techniques (n = 38 capture events), with capture durations ranging from 4 to 68 min. In all, 145,589 tri-axial acceleration observations were collected across these events, including simultaneous video footage (six hours total) from 10 capture events. Three discrete capture behaviors were characterized: steady swimming, a high-energy response consisting of thrashing and burst swimming, and a loss of body orientation while hanging motionless from the gear. The latter two behaviors can lead to physiological stress if exhibited for prolonged periods. Our trained ensemble of supervised classification methods successfully predicted behaviors from acceleration data with up to 95.2% accuracy. This technique provides a better understanding of the behavioral response to hook-and-line capture and, if paired with health or fate assessments, can characterize the influence of behavior on mortality. Our technique also provides a method for predicting behavior based on acceleration data alone, which can be more feasible to collect across the spectrum of fishing conditions and practices within a fishery. Such information will assist in understanding how species respond to capture on hook-and-line gear and in the formulation of species- and fishery-specific strategies for mitigating mortality.
Environmental change and biodiversity loss are but two of the complex challenges facing conservation practitioners and policy makers. Relevant and robust scientific knowledge is critical for providing decision-makers with the actionable evidence needed to inform conservation decisions. In the Anthropocene, science that leads to meaningful improvements in biodiversity conservation, restoration and management is desperately needed. Conservation Physiology has emerged as a discipline that is well-positioned to identify the mechanisms underpinning population declines, predict responses to environmental change and test different in situ and ex situ conservation interventions for diverse taxa and ecosystems. Here we present a consensus list of 10 priority research themes. Within each theme we identify specific research questions (100 in total), answers to which will address conservation problems and should improve the management of biological resources. The themes frame a set of research questions related to the following: (i) adaptation and phenotypic plasticity; (ii) human-induced environmental change; (iii) human-wildlife interactions; (iv) invasive species; (v) methods, biomarkers and monitoring; (vi) policy, engagement and communication; (vii) pollution; (viii) restoration actions; (ix) threatened species; and (x) urban systems. The themes and questions will hopefully guide and inspire researchers while also helping to demonstrate to practitioners and policy makers the many ways in which physiology can help to support their decisions.
The Atlantic sea scallop Placopecten magellanicus dredge fishery is one of the most lucrative commercial fishing industries in the northeastern United States, and fish bycatch can comprise up to similar to 42% of the total catch. Benthic species, such as flatfish, are particularly susceptible to unintended capture in scallop dredge gear, and mitigating bycatch and associated mortality has been mandated a priority for fisheries management. Based on this management need, the present study evaluated the physical, physiological, and behavioral stress responses of Yellowtail Flounder Limanda ferruginea, Windowpane Scophthalmus aquosus, and Fourspot Flounder Paralichthys oblongus to capture in the scallop dredge fishery. More specifically, we used generalized additive models and linear regression models to assess the influence of various fishing practices, environmental conditions, and biological factors on injury condition, physiological parameters, and reflex indicators. Although these flatfish species appeared to be physically resilient to capture based on an observable injury assessment, dredge capture and handling factors proved stressful, with the degree of immediate mortality, physiological disturbances, and reflex impairment varying by species. While multiple factors influenced the degree of stress in these species, based on our results the reduction of tow duration and limiting air exposure/sorting duration would likely be the most effective strategies to mitigate the impact of scallop dredge fishing on these flatfish species.
Discard mortality studies are considered a primary research priority, particularly for species and fisheries where discard rates are high. Monkfish (the commercial name for Goosefish) Lophius americanus supports the most lucrative finfish fishery in New England, and it is also the second highest bycatch species by weight in the sea scallop dredge fishery. Despite its commercial importance, no data exist with respect to monkfish discard mortality estimates for any gear type. The goals of this study were to evaluate the discard mortality process for monkfish captured in sea scallop dredge gear, estimate mortality rate, and develop best handling/management practices to mitigate the impact of monkfish bycatch in the sea scallop dredge fishery. Discard mortality was estimated during a field study conducted between June and October 2017 on board sea scallop commercial fishing vessels on Georges Bank in the Northwest Atlantic. Pop-up satellite tags were affixed to 60 monkfish to track survival from 14 to 28 d postcapture. From these monitored individuals, high predation rates were observed (n = 18 out of 26 mortalities), and the bulk of mortalities (n = 21) occurred within the first 24 h of discarding. However, in light of having no clear method for disentangling capture-related and tag-induced predation, predation was noted exclusively as one or the other to account for uncertainty and provide an upper and lower bound of mortality. This approach suggested that the discard mortality rate was between 17.9% and 54.1% for monkfish discarded by scallop dredges and that elevated air temperatures (above thermal preferences) may contribute to increased mortality. Based on these results, it appears that monkfish discard mortality is lower than previous assumptions of 100%, and potential best-practice management suggestions moving forward may include minimizing fishing in areas of high monkfish abundance or scheduling rotating time/area closures during periods when air temperature exceeds monkfish thermal tolerance of 13 degrees C.
Inaccurate age determinations can have serious effects on age-structured stock assessments that are used to manage fish populations. A recent push toward using an age-based model for the northern stock of black sea bass (Centropristis striata) led to an increase in direct aging effort in the northeastern United States. Yet, no large-scale otolith age validation study for this stock exists. We examined the annual periodicity of otolith growth in this species through marginal increment analysis with otoliths of fish from 3 age groups (fish of ages 1-2, ages 3-4, and ages 5+) and from 2 regions, north and south of the Hudson Canyon. Additionally, we validated the assignment of the first annulus through modal length-frequency analysis of young-of-the-year fish. The marginal increment ratio differed between age groups throughout the year, supporting the separation of these samples for age validation purposes. Higher ratios were observed in black sea bass from the region south of the Hudson Canyon throughout most of the year; however, fish from north of the canyon appear to accrete more otolith material during winter. Annual growth increments were deposited once per year, in spring or early summer, for all fish. In addition, absolute age was validated for the first time for this stock.
Climate change is affecting thermal regimes globally, and organisms relying on their environment to regulate biological processes face unknown consequences. In ectotherms, temperature affects development rates, body condition, and performance. Embryonic stages may be the most vulnerable life history stages, especially for oviparous species already living at the warm edge of their distribution, as embryos cannot relocate during this developmental window. We reared 27 epaulette shark ( Hemiscyllium ocellatum ) embryos under average summer conditions (27 °C) or temperatures predicted for the middle and end of the twenty-first century with climate change (i.e., 29 and 31 °C) and tracked growth, development, and metabolic costs both in ovo and upon hatch. Rearing sharks at 31 °C impacted embryonic growth, yolk consumption, and metabolic rates. Upon hatch, 31 °C-reared sharks weighed significantly less than their 27 °C-reared counterparts and exhibited reduced metabolic performance. Many important growth and development traits in this species may peak after 27 °C and start to become negatively impacted nearing 31 °C. We hypothesize that 31 °C approximates the pejus temperature (i.e., temperatures at which performance of a trait begin to decline) for this species, which is alarming, given that this temperature range is well within ocean warming scenarios predicted for this species’ distribution over the next century.
Terminal tackle regulations can be a valuable tool for fisheries management, especially in multispecies fisheries where bycatch and discards are common issues. In the Gulf of Maine, recreational anglers frequently discard critically depleted Atlantic cod Gadus morhua L. as bycatch when targeting the abundant haddock Melanogrammus aeglefinus (L.) stock. The present study investigated species catch composition, catch rates and animal welfare across various terminal tackle setups, and aspects of capture and handling with the goal of reducing bycatch and discard mortality. Overall, 2558 cod and 4266 haddock were captured with six terminal tackle setups in the western Gulf of Maine from April to October 2018. Along with angler experience and capture depth, lure type primarily influenced species catch composition and catch-per-unit-effort; hook types additionally influenced hook-removal times and physical injuries to fish. Results indicate that using baited hooks can both promote haddock catch and reduce cod bycatch, with specific hook types promoting increased survival.
Information on elasmobranch mating behavior is limited. For batoids, observations of mating behavior in the wild are available only for a few species. We present video documentation of new cases of mating behavior for three species of myliobatiform rays. On July 20, 2013, a group of six cownose rays (Rhinoptera bonasus) were observed mating in shallow coastal waters off New Jersey. On August 19, 2014, two whitespotted eagle rays (Aetobatus narinari) were observed mating in Harrington Sound, Bermuda. In both cases, all stages of the mating sequence described in the literature were observed: 1) close following, 2) pre-copulatory biting, 3) copulation/insertion, 4) resting, and 5) separation. This is consistent with observations of mating behavior for whitespotted eagle rays and Javanese cownose rays (Rhinoptera javanica) in captivity. This is the first time a complete mating sequence has been documented in the wild for either species. Additionally, on May 18, 2015, a group of four bentfin devil rays (Mobula thurstoni) were observed engaging in pre-mating behaviors at the Archipelago of Saint Peter and Saint Paul, Brazil and is the first documented account of mating behavior for this species. In all three cases, we noted that the female was considerably darker in color than the males, which may be evidence of a visual pre-copulation cue, as seen in other marine fishes. The similarity of the behaviors presented here and those observed in other species (e.g., M. birostris, Hypanus americanus, and Taeniurops meyeni) suggests mating behavior may be highly conserved among batoids.
Applying physiological tools, knowledge and concepts to understand conservation problems (i.e. conservation physiology) has become common place and confers an ability to understand mechanistic processes, develop predictive models and identify cause-and-effect relationships. Conservation physiology is making contributions to conservation solutions; the number of 'success stories' is growing, but there remain unexplored opportunities for which conservation physiology shows immense promise and has the potential to contribute to major advances in protecting and restoring biodiversity. Here, we consider howconservation physiology has evolved with a focus on reframing the discipline to be more inclusive and integrative. Using a 'horizon scan', we further exploreways in which conservation physiology can be more relevant to pressing conservation issues of today (e.g. addressing the Sustainable Development Goals; delivering science to support the UN Decade on Ecosystem Restoration), as well as more forward-looking to inform emerging issues and policies for tomorrow. Our horizon scan provides evidence that, as the discipline of conservation physiology continues to mature, it provides a wealth of opportunities to promote integration, inclusivity and forward-thinking goals that contribute to achieving conservation gains. To advance environmenta lmanagement and ecosystem restoration, we need to ensure that the underlying science (such as that generated by conservation physiology) is relevant with accompanying messaging that is straightforward and accessible to end users.
Thorny skate (Amblyraja radiata) remain one of the most overfished species in the Gulf of Maine (GOM) despite being designated as a prohibited (zero-possession, mandatory release) species by the New England Fishery Management Council in 2003. To better understand the extent to which discard mortality (DM) occurring after incidental capture in the GOM groundfish bottom trawl fishery may be impeding recovery, 75 individuals (55-94 cm total length, TL) were tagged with pop-up satellite archival transmitting (PSAT) tags and monitored for up to 28 days following capture under representative commercial trawl fishing practices. Data recovered from 61 PSAT-tagged skate were analysed with a longitudinal survival analysis to estimate DM and identify influential capture-related variables. DM rate was a function of TL, with larger skates (>70 cm; DM = 16.5%) experiencing lower mortality than smaller conspecifics (55-70 cm; DM = 24.5%). From our results, we estimate annual thorny skate DM in the GOM groundfish bottom trawl fishery to be 79.2 +/- 0.2 mt, which accounts for <1% of the existing stock biomass in the GOM (8400 mt). This study confirms that thorny skate are relatively resilient to bottom trawl fishing practices in the GOM, and suggests that other sources of mortality may be impeding population recovery.
This study assessed the in vitro temporal changes that occur in blood pH and lactate concentrations for an elasmobranch species and a chelonian species, as well as blood gases (partial pressures of carbon dioxide [pCO(2)] and oxygen [pO(2)]) for a chelonian species, with a portable clinical point-of-care analyzer. Blood samples were collected from 10 cownose rays (Rhinoptera bonasus) and 10 red-eared sliders (Pseudemys scripta elegans), stored on ice, and serially analyzed at six time points up to 90 min postcollection. Results indicate that analysis should be conducted as soon as possible after blood collection for these species, with immediate analysis being preferred. However, if analysis must be delayed, syringes may be capped, placed on ice, and analyzed at a later time. Analysis within 90 min provided clinically acceptable results for pH and lactate in both species and for pCO(2) in red-eared sliders, whereas substantial artifactual increases of pO(2) were seen in red-eared sliders.