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Variation of body condition and plasma energy substrates with life stage, sex, and season in wild-sampled nurse sharks Ginglymostoma cirratum
Abstract
Reported here are the relationships among morphological (i.e., body condition) and biochemical (i.e., plasma concentrations of triglycerides, cholesterol, free fatty acids, and ketone bodies and ketone body ratios) parameters related to energy storage and use, as well as the variation of such parameters, for 107 free-ranging nurse sharks Ginglymostoma cirratum sampled off South Florida. Immature G. cirratum exhibited a higher variance in body condition, plasma free fatty acid concentrations and ketone body ratios compared to adults. Mature female G. cirratum had significantly higher body condition than mature males, driven by a seasonal increase in mature female body condition during the wet season. Mature male G. cirratum showed a decrease in the ketone body β-hydroxybutyric acid during the dry season. Taken together, this study provides a baseline assessment of body condition and internal physiological state for a data-poor marine species and demonstrates significant ontogenetic, sexual and seasonal variation in G. cirratum energetic state. As concluded by other studies of energy metabolism in free-ranging sharks, this research highlights the importance of considering intraspecific patterns and sampling context for inferring the drivers of variation.
... As concentrações de TAG durante a estação chuvosa pode indicar um aumento na condição corpórea (e.g., Gallagher et al., 2014bHammerschlag et al., 2018) talvez relacionado à reprodução da espécie que ocorre neste período (abrilsetembro, Afonso et al., 2016;. Em um estudo comparando substratos energéticos entre as estações chuvosa e seca para o G. cirratum no sul da Florida não encontrou diferença estatística no TAG entre as duas estações, mas encontrou a condição corpórea era superior em fêmeas durante a estação chuvosa (Moorhead et al., 2021). ...
... Isso porque a GLU é liberada dos estoques de glicogênio no fígado durante o exercício, pelas catecolaminas (e.g., epinefrina e norepinefrina; DeRoos e DeRoos, 1978), e poderia explicar as elevadas concentrações em espécies com maior demanda energética. Além disso, maiores concentrações de GLU foram encontradas durante a estação chuvosa nos tubarões G. cuvier e G. cirratum, estação correspondente ao período reprodutivo de ambas as espécies (Afonso et al., 2016;Rangel et al., em revisão), quando é esperado que os tubarões tenham maior atividade muscular (Valls et al., 2016;Moorhead et al., 2021;. ...
... To test this hypothesis, we used plasma fatty acid profile as short- Moorhead et al. 2021). We therefore expected to find increased circulating n3 and n6 PUFAs in adults during the spermatogenesis phase, coincident with increased testosterone levels (i.e. ...
Dada a elevada diversidade nas estratégias de história de vida, os elasmobrânquios (tubarões e raias) tornam-se interessantes modelos para o estudo de relações entre a fisiologia e interações ecológicas no ambiente marinho. Embora os esforços para a conservação dos elasmobrânquios, que é atualmente o segundo grupo de vertebrados mais ameaçado do planeta, tenha estimulado um aumento no número de estudos sobre os padrões ecológicos e impactos antrópicos, pouco ainda se sabe sobre sua fisiologia. Assim, nesta tese de doutorado foram investigadas as variações fisiológicas sazonais e espaciais associadas ao estágio de vida e comportamento de tubarões de diferentes histórias de vida, utilizando múltiplas ferramentas não-letais para fornecer uma melhor compreensão dos padrões energéticos e reprodutivos, além de uma base fisiológica que ajude a prever os efeitos de distúrbios ambientais nos tubarões. O capítulo 1 aborda as variações inter- e intraespecíficas na ecologia nutricional de tubarões de diferentes estratégias de história de vida em um sistema insular oceânico protegido, o Arquipélago de Fernando de Noronha. Foram abordados também as variações nos padrões de dieta e condição nutricional e metabólica relacionados à reprodução de fêmeas de tubarões-tigre Galeocerdo cuvier (capítulo 2) e machos de tubarões-lixa Ginglymostoma cirratum e tubarões-galha-preta Carcharhinus limbatus (capítulo 3). Os capítulos 4, 5 e 6 abordam os efeitos da vida urbana na condição nutricional e padrões alimentares de tubarões com diferentes estilos de vida, o tubarão-lixa, o tubarão-galha-preta e o tubarão-tigre, respectivamente. Os resultados mostraram que a influência da urbanização na qualidade da dieta dos tubarões parece ser mais pronunciada em espécies sedentárias, como o tubarão-lixa, quando comparado com espécies mais ativas. Por fim, o capítulo 7 trouxe uma abordagem inédita na pesquisa de tubarões, combinando múltiplos marcadores fisiológicos com informações obtidas através de ultrassonografia e da telemetria acústica passiva para entender relações entre os aspectos fisiológicos e comportamentais de tubarões-tigre expostos ao turismo de alimentação. Os resultados demonstraram que o estágio de vida, a regulação endócrina e a condição nutricional influenciam e/ou são influenciadas pelo tempo que os tubarões passam interagindo com o turismo de alimentação. Em conjunto, os resultados mostraram que os biomarcadores nutricionais, reprodutivos e metabólicos utilizados nesta tese fornecem uma poderosa ferramenta para descrever padrões ecológicos complexos dos tubarões, especialmente quando combinados com outras tecnologias para rastreamento da movimentação e identificação do estágio reprodutivo dos tubarões.
... limbatus), blacktip reef (C. melanopterus), nurse (Ginglymostoma cirratum), tiger (Galeocerdo cuvier) and white sharks (Carcharodon carcharias) (Gallagher et al., 2014;Merly et al., 2019;Moorhead et al., 2021;Weideli et al., 2019). However, to date, no comparison between this metric and Fulton's condition factor has been conducted for a species across all life-history stages. ...
Body condition is an important proxy for 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 intra-specifically, 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 sixteen captive epaulette sharks across one 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 (R2 = 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 non-lethal whole-organism energetic assessment for fishes. This article is protected by copyright. All rights reserved.
... They may also enable more widespread data collection, including repeated samples from the same individuals, providing more comprehensive and long-term measures of energy composition and being increasingly used assessments of species of conservation interest (Brosset et al., 2015;Schloesser and Fabrizio, 2016;Whiterod, 2010). Another potential non-lethal indicator of recent consumption and energetic/ nutritional state in fishes is blood plasma sampling for analysis of fatty acids and ketone bodies, with some recent successful applications (e.g., Eldøy et al., 2021;Moorhead et al., 2021). ...
Energy is a fundamental currency of life that can be quantified in organisms to understand how environmental conditions and anthropogenic stressors affect individuals, scaling up to populations and entire ecosystems. Bioenergetics studies have been conducted extensively on fishes, with an historical focus on lab-based experiments relevant to fisheries and aquaculture; however, recent methodological and technological advances are enabling more widespread applications in ecology and conservation including in situ measurement of various aspects of fish bioenergetics in aquatic ecosystems. Much of the utility of bioenergetics is based on a generalized mass-balance equation that describes energy allocation, and there are numerous advanced modeling techniques available to quantify how various environmental and intrinsic biological factors influence fish energetics, as well as relevant endpoints such as growth and reproduction. In this chapter, we discuss (1) key components of fish bioenergetics, (2) available measurement techniques, (3) common modeling techniques, and (4) case studies that highlight some key applications to date. We conclude by discussing current limitations and future research directions in this field. Bioenergetics is an increasingly powerful approach to build mechanistic connections between environmental conditions, stressors, and fish populations that is especially valuable for predicting the responses of fishes to rapidly changing conditions in the Anthropocene.
... For some taxa, elevated concentrations may reflect individuals of better nutritional condition, as is typically seen in sharks (e.g., Gallagher et al. 2017) and teleost fishes (Eldøy et al. 2021). For example, strong relationships between TAG, morphometric body condition, and reproductive status were observed in tiger sharks (Galeocerdo cuvier, Gallagher et al. 2014;Hammerschlag et al. 2018), while several plasma lipids were found to respond to life-history stage, sex, and season in several species of coastal shark (Gallagher et al. 2017;Moorhead et al. 2021). Conversely, elevated plasma lipid concentrations indicate poorer nutritional condition in animals like mammals or birds that exhibit tissue catabolism during energetically demanding events like migration (Jenni-Eiermann and Jenni 1994) or fasting (Kaduce and Folk 2002). ...
Understanding how intraspecific variation in the use of prey resources impacts energy metabolism has strong implications for predicting long-term fitness such as reproductive success and survival and is critical for predicting population-to-community level responses to environmental change. Here we examine the energetic consequences of variable prey resource use in a widely distributed marine carnivore, juvenile sand tiger sharks (Carcharias taurus). We used carbon and nitrogen isotope analysis to identify three primary prey resource pools – demersal omnivores, pelagic forage, and benthic detritivores and estimated the proportional assimilation of each resource using Bayesian mixing models. We then quantified how the utilization of these resource pools impacted the concentrations of six plasma lipids and how this varied by ontogeny. Sharks exhibited variable reliance on two of three predominant prey resource pools: demersal omnivores and pelagic forage. Resource use variation was a strong predictor of energetic condition, whereby individuals more reliant upon pelagic forage exhibited higher blood plasma concentrations of very low-density lipoproteins, cholesterol, and triglycerides. These findings underscore how intraspecific resource use variation may impact the energy metabolism of animals, and more broadly, that natural and anthropogenically-driven fluctuations in prey resources could have longer term energetic consequences.
... Such a pattern may indicate a greater importance of triglycerides for females during this period due to vitellogenesis that takes place prior to embryo development and requires great hepatic energy reserve mobilization. Similar concentrations of both cholesterol and ketone bodies in adults of both sexes have also been reported in Atlantic nurse sharks (Ginglymostoma cirratum) (Moorhead et al., 2021), and similar concentrations of total cholesterol in the serum of adult males and females were also reported for small-spotted catsharks (Scyliorhinus canicula) (Valls et al., 2016). In contrast, 3-β-hydroxybutyrate concentrations were higher in male S. canicula, attributed to higher physical activity compared to females. ...
Elasmobranchs have a very distinct metabolism, and many aspects related to the energetic dynamics of these animals remain poorly investigated. The reproductive period is particularly vulnerable for viviparous species, as part of the energy reserves of the parental biomass is reallocated for gamete production and embryo development. In this context, this study aimed to characterize parental metabolite provisioning to the offspring (both sperm and developing embryos) of the Brazilian Guitarfish, Pseudobatos horkelii, through glucose, β-hydroxybutyrate, triglycerides, and total cholesterol determinations in the uterine liquid (UL) and serum of pregnant females and in the seminal fluid (SF) and serum of males during the copulation period. No significant difference was observed for the analyzed markers between the UL and SF. Except for triglycerides, higher in female serum samples, all other energy markers were present at similar concentrations in the serum of both females and males. When comparing female UL and serum, significant differences were observed for triglycerides and total cholesterol. No differences were observed between SF and serum in males. The results indicate that all markers are being made available to offspring, possibly complementary to the yolk in the case of maternal liquid, and as an additional source for sperm mobilization required during egg fertilization in the case of the paternal fluid. Correlations between the markers in the parental matrices were also noted, compatible with the metabolic pathways activated during energy mobilization in vertebrates. Moreover, distinct marker predominance patterns were also noted for both UL and SF. Energy mobilization characterization directed to offspring through parental fluids aids in unraveling metabolic dynamics during the reproduction stage while also providing support for stress physiology studies to evaluate the indirect effects of parental allostatic overload in both sperm and developing embryos. Finally, energy mobilization assessments of parental fluids may also help elucidate how internal fertilization and viviparity evolved in this very distinct taxonomic group.
... Although we used a non-lethal approach that has been successful used in ecophysiological studies with sharks (e.g. Moorhead et al., 2021;Rangel et al., 2021aRangel et al., , 2021bShiffman et al., 2019), our study has some limitations. This includes the fact that we do not know the spatial or temporal movement patterns of blacktip sharks in the study area, i.e. their residency patterns in South Florida remain unknown. ...
The synergistic effects of coastal urbanization have dramatically impacted biological communities. Yet, few studies have investigated how urbanization can influence the diet quality and trophic ecology of coastal sharks. In a preliminary study, we examined for spatial variation in the nutritional ecology of a highly active marine predator, the blacktip sharks (Carcharhinus limbatus) exposed to regional differences in coastal urbanization in southeast Florida. We used medium-term nutritional indicators (i.e., body condition; whole blood stable isotopes [δ¹⁵N and δ¹³C]) and short-term dietary markers (i.e., plasma fatty acid profiles) to test the hypothesis that the nutritional ecology of marine predators would differ in areas exposed to increased urbanization. Our initial results showed that blacktip sharks sampled in high urbanized area (hereafter, ‘urban sharks’) exhibited relatively higher body condition, blood δ¹⁵N levels, and percentages of saturated fatty acids compared to sharks sampled in low urbanized area (hereafter ‘non-urban sharks’). Collectively, these results suggest a possible positive alteration in the amount of food consumed by sharks and/or in the caloric value of their prey. We also found lower percentages of bacterial markers and higher values of dinoflagellate markers in urban sharks. Compared to more resident species evaluated in the region, we did not detect a reduction in diet quality (in terms of essential fatty acids) in this highly active species exposed to urbanization. Therefore, it is possible that the lifestyle and feeding behavior have an influence on the quality of food consumed by urban sharks, and maybe the impacts of urbanization are more pronounced in resident, sedentary and benthic species.
... It remains difficult to separate potential seasonal changes from changes in body condition. Although plasma testosterone was significantly higher in June, body condition again cannot be ruled out as contributors to the difference, especially as cholesterol is the primary component of steroid hormone synthesis and also has previously been correlated with body condition in elasmobranchs [45]. Conversely, further research will determine whether season has any effect on southern stingray ejaculates. ...
This study investigated the reproductive biology and sperm cryopreservation of ex situ southern stingrays (Hypanus americanus) by semen collection and characterization and the develop- ment and validation of an enzyme-linked immunoassay for plasma total testosterone. Semen was collected in March and June using a manual massage technique, and the ejaculates were assessed for volume, pH, osmolarity, motility, status (0–5 scale: 0 = no forward progression, 5 = rapid linear progression) and total sperm count. Semen was extended in Hank’s elasmobranch ringer solution containing 10% DMSO, 10% glycerol or 5% glycerol with 5% N-methylformamide and cryopre- served using a conventional freezing method (~−50 ◦C/min) or a modified slow freezing method (~−3 ◦C/min). Body condition was scored from 1–5 and was noted to be low in March (1.93 ± 0.07) due to feeding practices and increased by June (2.93 ± 0.05) after dietary corrections were made. A concomitant increase (p < 0.05) in plasma total testosterone concentration and sperm motility was noted between March (8.0 ± 7.2 ng/mL, 5.71 ± 2.77%) and June (97.3 ± 11.3 ng/mL, 51.4 ± 14.3%). Samples cryopreserved using a modified slow freeze method (~−3 ◦C/min) had higher post-thaw motility and plasma membrane integrity than conventionally cryopreserved samples. Data indicate that southern stingray sperm morphometrics adheres to those of other elasmobranch species and that a slow cooling rate may be an avenue of research to improve southern stingray sperm survival during cryopreservation.
The well-being of fish used in aquaculture is of great interest. Oxygen and temperature are the main factors affecting the welfare of the crucian carp (carassius); however, there are few studies on the combined effects of these on the species. Therefore, this study investigated the impact of different temperatures (18 °C, 24 °C, 30 °C) and oxygen concentrations (2.1 mgL ⁻¹ , 5.4 mgL ⁻¹ , 9.3 mgL ⁻¹ ) on serum antibacterial activity, antioxidant activity, hematological parameters and growth performance of the crucian carp. The results showed that there were greater antibacterial properties under conditions of hypoxia at 18 °C (L18) and hyperoxia at 24 °C (H24). The activities of catalase, glutathione peroxidase and total superoxide dismutase were the highest at 24 °C under hypoxia and hyperoxia. In addition, the contents of glucose and total protein first increased and then decreased with the change of temperature; triglycerides were the lowest at 30 °C. The blood parameters of the carp were within a normal range at 24 °C; however, the growth rate was at its lowest under hypoxia treatment at 30 °C (L30). This study showed that high temperature impairs the antibacterial ability, antioxidant capacity and growth performance of the crucian carp, and high oxygen levels can alleviate these adverse reactions. This research provides a theoretical basis for subsequent aquaculture studies.
Elasmobranch fishes (sharks, skates and rays) are some of the most morphologically and behaviourally diverse vertebrate species on the planet, demonstrating a wide repertoire of feeding strategies. The nurse shark (Ginglymostoma cirratum) is a large, widely distributed shark species which is commonly observed on tropical reefs worldwide; yet it remains vastly understudied relative to other large species. To advance our understanding of nurse shark behaviour and ecology, we used opportunistic video observations gathered throughout the islands of Turks and Caicos from September 2020 – April 2021. We made 233 observations from 78 camera deployments and identified five behaviours, four of which were attributed to foraging. Stationary feeding behaviour was most observed and was strongly influenced by habitat type with a greater number of observations occurring on sand banks relative to reefs. Unique to this study was the first empirical description of novel pectoral positioning behaviour, by which individuals can position their body relative to a food-source through mobilization of the pectoral fins. We discuss these findings in relation to mechanical processes and kinematics, and the implications of expanding our knowledge of the functional role nurse sharks play in the transfer of energy across tropical seascapes.
Despite its consequences for ecological processes and population dynamics, intra-specific variability is frequently overlooked in animal movement studies. Consequently, the necessary resolution to reveal drivers of individual movement decisions is often lost as animal movement data are aggregated to infer average or population patterns. Thus, an empirical understanding of why a given movement pattern occurs remains patchy for many taxa, especially in marine systems. Nonetheless, movement is often rationalized as being driven by basic life history requirements, such as acquiring energy (feeding), reproduction, predator-avoidance, and remaining in suitable environmental conditions. However, these life history requirements are central to every individual within a species and thus do not sufficiently account for the high intra-specific variability in movement behavior and hence fail to fully explain the occurrence of multiple movement strategies within a species. Animal movement appears highly context dependent as, for example, within the same location, the behavior of both resident and migratory individuals is driven by life history requirements, such as feeding or reproduction , however different movement strategies are utilized to fulfill them. A systematic taxa-wide approach that, instead of averaging population patterns, incorporates and utilizes intra-specific variability to enable predictions as to which movement patterns can be expected under a certain context, is needed. Here, we use intra-specific variability in elasmobranchs as a case study to introduce a stepwise approach for studying animal movement drivers that is based on a context-dependence framework. We examine relevant literature to illustrate how this context-focused approach can aid in reliably identifying drivers of a specific movement pattern. Ultimately, incorporating behavioral variability in the study of movement drivers can assist in making predictions about behavioral responses to environmental change, overcoming tagging biases, and establishing more efficient conservation measures.
Serum proteins found in the blood have been used as diagnostic markers in both human and animal medicine. Evaluating proteins in the blood of sharks may be a valuable way to assess shark health. The purpose of this study was to perform serum protein electrophoresis from non-lethal blood samples of wild sharks and establish baseline values for six species off South Florida: blacknose (Carcharhinus acronotus), blacktip (Carcharhinus limbatus), bull (Carcharhinus leucas), lemon (Negaprion brevirostris), sandbar (Carcharhinus plumbeus), and tiger shark (Galeocerdo cuvier). Two hundred and fifty-one serum samples were collected between 2015-2018 along with sex determination and morphometric measurements. Agarose gel analysis was performed using mammalian protein fraction delimits albumin, alpha 1-globulins, alpha 2-globulins, beta globulins, and gamma globulins alternatively defined as fractions 1-5. Reference electrophoretic profiles were established for each species, revealing the dominance of protein fractions 3 and 4. The fraction 3:4 ratio was determined for each shark and reference intervals for total solids, protein fractions, and fraction 3:4 ratio are reported for each species. There were no significant differences in total solids or protein fractions between males and females of any species. In both blacktip sharks and bull sharks, total solids was positively correlated with body size, but not in the other species evaluated. In blacknose sharks, the fraction 3:4 ratio was positively correlated with body condition. Results suggest that there may be differences in total solids values across dry and wet seasons for some species. Newly established reference intervals can now be utilized in future research to evaluate the health of captive sharks and to investigate the health status of individuals in the wild as well as relate health measures to environmental conditions.
Energetic condition is one of the most important factors that influence fitness and reproductive performance in vertebrates. Yet, we lack evidence on how energetic states change in response to reproduction in large marine vertebrates. In the present study, we used a non-lethal approach to assess relationships among reproductive stage, circulating steroid hormones (testosterone and relative corticosteroid levels), plasma fatty acids, and the ketone body β-hydroxybutyrate in male sharks of two species with divergent ecologies, the benthic nurse shark (Ginglymostoma cirratum) and the epipelagic blacktip shark (Carcharhinus limbatus). We found higher relative corticosteroid levels in adult nurse sharks during the pre-mating period and in blacktip sharks during the mating period. Higher levels of β-hydroxybutyrate were found in adult nurse sharks during the mating period, but concentrations of this ketone body did not significantly vary across reproductive stages in blacktip sharks. We also detected reduced percentages of essential fatty acids during the mating period of both nurse and blacktip sharks. Taken together, our findings suggest that nurse and blacktip sharks differ in their energetic strategy to support reproduction, however, they likely rely on physiologically important fatty acids during mating, to support spermatogenesis.
The indirect effect of predators on prey behavior, recruitment, and spatial relationships continues to attract considerable attention. However, top predators like sharks or large, mobile teleosts, which can have substantial top–down effects in ecosystems, are often difficult to study due to their large size and mobility. This has created a knowledge gap in understanding how they affect their prey through nonconsumptive effects. Here, we investigated how different functional groups of predators affected potential prey fish populations across various habitats within Biscayne Bay, FL. Using baited remote underwater videos (BRUVs), we quantified predator abundance and activity as a rough proxy for predation risk and analyzed key prey behaviors across coral reef, sea fan, seagrass, and sandy habitats. Both predator abundance and prey arrival times to the bait were strongly influenced by habitat type, with open homogenous habitats receiving faster arrival times by prey. Other prey behaviors, such as residency and risk‐associated behaviors, were potentially driven by predator interaction. Our data suggest that small predators across functional groups do not have large controlling effects on prey behavior or stress responses over short temporal scales; however, habitats where predators are more unpredictable in their occurrence (i.e., open areas) may trigger risk‐associated behaviors such as avoidance and vigilance. Our data shed new light on the importance of habitat and context for understanding how marine predators may influence prey behaviors in marine ecosystems. Assessing behavioral risk effects of marine predators on mobile prey species across varying habitats in Biscayne Bay, FL. Providing new insights into the role marine predators play in influencing prey behavior in a variety of contexts.
A strength of physiological ecology is its incorporation of aspects of both species’ ecology and physiology; this holistic approach is needed to address current and future anthropogenic stressors affecting elasmobranch fishes that range from overexploitation to the effects of climate change. For example, physiology is one of several key determinants of an organism’s ecological niche (along with evolutionary constraints and ecological interactions). The fundamental role of physiology in niche determination led to the development of the field of physiological ecology. This approach considers physiological mechanisms in the context of the environment to understand mechanistic variations that beget ecological trends. Physiological ecology, as an integrative discipline, has recently experienced a resurgence with respect to conservation applications, largely in conjunction with technological advances that extended physiological work from the lab into the natural world. This is of critical importance for species such as elasmobranchs (sharks, skates and rays), which are an especially understudied and threatened group of vertebrates. In 2017, at the American Elasmobranch Society meeting in Austin, Texas, the symposium entitled `Applications of Physiological Ecology in Elasmobranch Research’ provided a platform for researchers to showcase work in which ecological questions were examined through a physiological lens. Here, we highlight the research presented at this symposium, which emphasized the strength of linking physiological tools with ecological questions. We also demonstrate the applicability of using physiological ecology research as a method to approach conservation issues, and advocate for a more available framework whereby results are more easily accessible for their implementation into management practices.
Some shark populations face declines owing to targeted capture and by-catch in longline fisheries. Exercise intensity during longline capture and physiological status may be associated, which could inform management strategies aimed at reducing the impacts of longline capture on sharks. The purpose of this study was to characterize relationships between exercise intensity and physiological status of longline-captured nurse sharks (Ginglymostoma cirratum) and Caribbean reef sharks (Carcharhinus perezi). Exercise intensity of longline-captured sharks was quantified with digital cameras and accelerometers, which was paired with blood-based physiological metrics from samples obtained immediately post-capture. Exercise intensity was associated with physiological status following longline capture. For nurse sharks, blood pH increased with capture duration and the proportion of time exhibiting low-intensity exercise. Nurse sharks also had higher blood glucose and plasma potassium concentrations at higher sea surface temperatures. Associations between exercise intensity and physiological status for Caribbean reef sharks were equivocal; capture duration had a positive relation with blood lactate concentrations and a negative relationship with plasma chloride concentrations. Because Caribbean reef sharks did not appear able to influence blood pH through exercise intensity, this species was considered more vulnerable to physiological impairment. While both species appear quite resilient to longline capture, it remains to be determined if exercise intensity during capture is a useful tool for predicting mortality or tertiary sub-lethal consequences. Fisheries management should consider exercise during capture for sharks when developing techniques to avoid by-catch or reduce physiological stress associated with capture.
Nurse sharks have not previously been known to migrate. Nurse sharks of the Dry Tortugas (DRTO) mating population have a highly predictable periodic residency cycle, returning to the Dry Tortugas Courtship and Mating Ground (DTCMG) annually (males) or bi- to triennially (females) during the June/July mating season. For 23 years we have followed the movements of 76 recaptured adults of a total of 115 tagged adults. Telemetry detections of 40 females tagged with acoustic transmitters show that most tagged and presumably post-partum females are continuously present in the DRTO in the fall, winter and early spring following the June mating season but these females depart in late March to early May. Detections reveal these females avoid the DTCMG completely during the next mating season, returning from late summer to fall. Telemetry records of nine of 17 adult males that co-habited with these females in the DTCMG depart DRTO waters every July. Both sexes may overwinter in the DRTO. Between 2011 and 2016 three males and five females with transmitters were detected to move up the west coast of Florida outside of the mating season as far north as the waters off Tampa Bay (335 km). Six others were only detected in the lower Florida Keys (292 km). Nine sharks returned to DRTO; one returned six times. Some overwintered and some resumed courtship in June, demonstrating both resident and migratory contingents within their population, partial migration and an ability to navigate with high spatial and temporal precision.
Evaluating how predators metabolize energy is increasingly useful for conservation physiology, as it can provide information on their current nutritional condition. However, obtaining metabolic information from mobile marine predators is inherently challenging owing to their relative rarity, cryptic nature and often wide-ranging underwater movements. Here, we investigate aspects of energy metabolism in four free-ranging shark species (n = 281; blacktip, bull, nurse, and tiger) by measuring three metabolic parameters [plasma triglycerides (TAG), free fatty acids (FFA) and cholesterol (CHOL)] via non-lethal biopsy sampling. Plasma TAG, FFA and total CHOL concentrations (in millimoles per litre) varied inter-specifically and with season, year, and shark length varied within a species. The TAG were highest in the plasma of less active species (nurse and tiger sharks), whereas FFA were highest among species with relatively high energetic demands (blacktip and bull sharks), and CHOL concentrations were highest in bull sharks. Although temporal patterns in all metabolites were varied among species, there appeared to be peaks in the spring and summer, with ratios of TAG/CHOL (a proxy for condition) in all species displaying a notable peak in summer. These results provide baseline information of energy metabolism in large sharks and are an important step in understanding how the metabolic parameters can be assessed through non-lethal sampling in the future. In particular, this study emphasizes the importance of accounting for intra-specific and temporal variability in sampling designs seeking to monitor the nutritional condition and metabolic responses of shark populations. Cite as: Gallagher AJ, Skubel RA, Pethybridge HR, Hammerschlag N (2017) Energy metabolism in mobile, wild-sampled sharks inferred by plasma lipids. Conserv Physiol 5(1): cox002; doi:10.1093/conphys/cox002.
Hybridization can influence a range of characteristics and outcomes for an organism; however, relatively little is known about evolutionary consequences on nutritional performance. Information on hybrid nutritional performance would provide an understanding of how hybrids interact with their environment and insights into mechanisms affecting survival. Our goal was to test for relationships between hybridization and nutritional performance in invasive bigheaded carps (Hypophthalmichthys nobilis), silver carp (Hypophthalmichthys molitrix), and their hybrids in the Marseilles reach of the Illinois River, Illinois, USA. Silver carp showed better nutritional performance relative to bighead carp. Early generation bighead and silver carp hybrid groups were intermediate to both parental lines, thereby, reducing their nutritional performance, and advanced generation bighead and silver carp groups were nutritionally more similar to their respective parental species. Differences in gill raker morphology and feeding habits among bigheaded carps and their hybrids are plausible mechanisms explaining observed nutritional performance patterns. In addition to providing unique insights about how hybridization influences the nutritional performance of wild organisms relative to parentals, our findings may have management implications for bigheaded carps if interbreeding persists over time and reduced nutritional performance is further manifested by continued hybridization.
Land use changes within watersheds can have large effects on stream ecosystems, but the mechanistic basis of those effects remains poorly understood. While changes to population size presumably reflect underlying variation in organismal health and condition, such individual-level metrics are rarely evaluated in the context of ecosystem disturbance. To address this deficiency, we combined physiological sampling with geographic information systems to quantify the effects of land use on physiological indicators of health in largemouth bass. More specifically, we first quantified blood metrics relating to nutrition, oxidative stress, and the glucocorticoid stress response from largemouth bass residing in eight watersheds. We then used Akaike's information criterion to define relationships between these blood metrics and land cover, including forests, agricultural areas, urban areas, and wetlands. The proportion of forest cover in a watershed was the best predictor of blood metrics representing recent feeding and resistance to oxidative stress, whereas the proportion of wetlands was the best predictor of glucocorticoid function; however, further investigation is needed, as the explanatory power of the models was relatively low. Patterns in energy reserves were not influenced by any land use practices. Interestingly, anthropogenic land use categories, such as urban and agricultural areas, were not the best predictor for any blood metrics. Together, our results indicate that fish health is most related to natural features of a landscape rather than anthropogenic land uses. Furthermore, these findings suggest that physiological methods could supplement traditional population and community assessments to develop a more comprehensive understanding of ecosystem interactions and improve stream management.
Animal condition typically reflects the accumulation of energy stores (e.g. fatty acids), which can influence an individual's decision to undertake challenging life-history events, such as migration and reproduction. Accordingly, researchers often use measures of animal body size and/or weight as an index of condition. However, values of condition, such as fatty acid levels, may not always reflect the physiological state of animals accurately. While the relationships between condition indi-ces and energy stores have been explored in some species (e.g. birds), they have yet to be examined in top predatory fishes, which often undertake extensive and energetically expensive migrations. We used an apex predatory shark (Galeocerdo cuvier, the tiger shark) as a model species to evaluate the relationship between triglycerides (energy metabolite) and a metric of overall body condition. We captured, blood sampled, measured and released 28 sharks (size range 125–303 cm pre-caudal length). In the laboratory, we assayed each plasma sample for triglyceride values. We detected a positive and significant relationship between condition and triglyceride values (P < 0.02). This result may have conservation implica-tions if the largest and highest-condition sharks are exploited in fisheries, because these individuals are likely to have the highest potential for successful reproduction. Our results suggest that researchers may use either plasma triglyceride val-ues or an appropriate measure of body condition for assessing health in large sharks. Cite as: Gallagher AJ, Wagner DN, Irschick DJ, Hammerschlag N (2014) Body condition predicts energy stores in apex predatory sharks. Conserv Physiol 2: doi:10.1093/conphys/cou022.
Reef fish assemblage structure was assessed in 2006–2007 (“recent” period) in Biscayne National Park, Florida, USA, and compared with data collected from 1977 to 1981 (“historical” period) from the same location. Substantial differences were observed in reef fish assemblage structure between periods. Sixty-four percent of species were observed less frequently in the recent period. Mean species richness per survey declined at all sites, with declines ranging from 9% to 27%. Declines of fishery-targeted species were also observed and were consistent with but not greater than those observed for the reef fish assemblage as a whole. The observed declines appeared to be assemblage-wide, as a majority of species within all trophic guilds examined (spongivores, planktivores, herbivores, omnivores, invertivores, generalist carnivores, and piscivores) declined in frequency of occurrence between periods, with declines ranging from 55% of species for piscivores to 75% for omnivores. Mean number of species per survey declined for all guilds but herbivores, and ranged from a 14% decline for piscivores to 67% for planktivores. The declines observed in the present study are conceptually consistent with, but more extensive than, those recently documented for the Caribbean region as a whole and with those expected in coral reef systems that are heavily utilized by humans.
We quantified nutritional and stress parameters (alkaline phosphatase, cholesterol, protein, triglycerides, cortisol, and glu-cose) in invasive silver carp (Hypophthalmichthys molitrix) inhabiting four large rivers throughout three distinct time periods in the Midwestern USA. Examining the basic biology and ecology of an invasive species is crucial to gain an understanding of the interaction between an organism and its environment. Analysis of the physiological condition of wild-caught silver carp across broad spatial and temporal scales is essential because stress and nutritional parameters can link individuals to their habitats and vary among populations across environments. During each time period, we collected blood samples from indi-vidual silver carp in the Illinois River and portions of the Mississippi, Ohio, and Wabash rivers in Illinois. We tested for relation-ships between silver carp nutrition and stress across rivers, reaches within rivers, and time periods. Principal component analyses separated physiological parameters into a stress component (cortisol and glucose) and two nutritional components representative of short-term feeding (alkaline phosphatase, protein, and triglycerides) and body energy reserves (cholesterol and protein). Akaike's information criterion suggested that time period had the greatest influence on stress. Stress levels were consistent in all four rivers, and declined across time periods. Akaike's information criterion also suggested that interactions of time period and river had the greatest influence on short-term feeding and body energy reserves. There was no specific pattern across time periods within each river, nor was there a pattern across rivers. Our results provide a better understanding of nutritional and stress conditions in invasive silver carp across a broad landscape and temporal scale, with implications for managing and predicting the spread of this species.
Rapid land use transformations due to extensive agricultural and urban development in south Florida (USA) threaten water resources such as Biscayne Bay, an oligotrophic estuary draining the Miami metropolitan complex and South Dade Agricultural Area. Biscayne Bay is sensitive to nutrient inputs and this study evaluated watershed land use-water quality relationships from 1995 to 2004. Using eight monitoring sites, three spatial extents were considered: sub-basins, canal buffers, and site buffers. Selected sites represented agricultural, urban, and mixed land use classes. Disturbance indicators (landscape metrics; Landscape Development Intensity (LDI) index; percent imperviousness), nutrient loads (nitrate/nitrite-nitrogen (NO(x)-N); total ammonia nitrogen (NH(3)-N); total phosphorus (TP)), and multivariate regression models were used to determine land use factors influencing water quality variability. The sub-basin regression model was the best predictor of annual NO(x)-N loads in the watershed. Both LDI and largest patch index variables were included in this model, indicating that the relative distribution of dominant land use classes influences NOx-N loads. There were no significant regression models for total inorganic nitrogen (NO(x)-N plus NH(3)-N) loads. Total phosphorus loads were more closely related to disturbance indicators at a smaller spatial extent (1000 m canal buffer), which is a function of watershed nutrient transport processes. The relative proportion of directly connected impervious areas (DCIA) was not identified as a significant land use variable for regression models. Positive correlations between LDI and DCIA values suggested both indicators provided similar information regarding the intensity of human disturbance. However, the LDI index incorporates anthropogenic intensity associated with a broad range of land uses while DCIA primarily reflects the impact of watershed urbanization. Watershed managers can use the LDI index with landscape metrics that evaluate spatial patterns to link land use development to water quality parameters. (C) 2010 Elsevier Ltd. All rights reserved.
Biscayne Bay is a shallow subtropical lagoon on Florida's southeastern coast that is bordered to the west by the mainland and to the east by barrier islands and keys. Fish assemblages inhabiting two types of mangrove-lined shoreline that encompass the Bay were examined using a visual 'belt-transect' census method over four consecutive seasons. Several significant differences were evident between shoreline habitats in terms of fish species composition, taxonomic richness and taxon-specific densities; seasonal changes and fish size-structure differences were few. The mangrove shorelines along the mainland (ML) consistently harbored less fish taxa than those on the leeward side of the islands and keys (LK), but harbored higher densities of several euryhaline forms (i.e., killifishes and livebearers). Densities of fishes that are typically associated with coral reef habitats (i.e., snappers and grunts) tended to be higher within LK vs ML mangrove shorelines, but there were exceptions (e.g., great barracuda, Sphyraena barracuda). For five fish species, length-frequency distributions were compared between the Bay's mangrove shorelines and nearby coral reef habitats. These data comparisons lent partial support to an ontogenetic 'mangrove-to-reef' migration model for only two of the five species examined. Results suggest that these shoreline habitats play varying ontogenetic and trophic roles, depending on location, season and fish species. Biscayne Bay's mangrove shoreline fish assemblages appear to reflect: (1) proximity of the mangroves that they occupy to offshore reef habitats; (2) salinity regime along the shoreline; and (3) water depths within the mangrove forest interior. The fish assemblage information collected here may serve as a 'baseline' in future assessments of fishing impacts or the effects of other anthropogenic changes to Biscayne Bay and its watershed.
This research examines the foraging energetics and diving behavior of the Australian sea lion, Neophoca cinerea. We examine whether the foraging ecology of the Australian sea lion is typical for an animal that has evolved to exploit benthic habitats. Such a strategy is in marked contrast to those utilized by some seabirds and other pinnipeds that feed in the midwater, where travel and search components of the time at sea become more important. Onshore and at-sea field metabolic rates (FMR) were measured using doubly labeled water in lactating sea lions at Kangaroo Island, South Australia. during the winter of 1988 (early lactation, breeding season 1) and the summer of 1990 (early lactation, breeding season 2). Dive behavior was also measured with dataloggers during these seasons, as well as in the summer of 1991 (late lactation, breeding season 2). The foraging behavior of Neophoca cinerea indicated that it works hard to exploit benthic habitats in the waters around its breeding site. Sea lions maximized time spent at or near the benthos, with 61% of each dive and 35% of their time at sea being spent at the deepest 20% of the dives. The dive pattern was characterized by almost continuous diving when at sea, with 57.9% of their time at sea spent at depths greater than or equal to6 m. and dive rates of 10.7 dives/h. Mean surface intervals (1.0-1.9 min) accounted for only 42% of mean dive durations (2.2-4.1 min). Mean dive depths ranged from 41.5 m to 83.1 m, with maximum dives ranging from 60 m to 105 m. The energetic costs of this strategy are high when compared with those of other otariids: the mean at-sea FMR was 7.05 +/- 0.99 W/kg. We report seasonal variability in foraging energetics and dive behavior that is likely to be sensitive to regional oceanography, the maintenance costs of female sea lions and their offspring, and the distribution and behavior of their prey. Further, we note that Australian sea lions are functionally adapted to benefit from benthic foraging strategies because their larger size and insulating blubber convey an advantage over the generally smaller sympatric fur seals that would have a decrease in air/fur insulation with compression at deeper depths and would experience greater water infiltration of the fur with longer dives.
The nurse shark is an extremely abundant shallow water species in Florida and the Caribbean, yet its biology is poorly known. Moreover, there is a great deal of misinformation about it in the literature. The maximum size and weight attained by the nurse shark have often been exaggerated. None of the specimens measured in this study exceeded 265cm TL and 114.5kg, and none of the specimens actually measured by other researchers exceeded 280cm. Females reach maturity at a length of 223–231cm, or at 86% of their maximum size. Males reach maturity between 214 and 214.6cm in length or at about 83% of their maximum size. Mating primarily occurs from mid-June to early July. The embryos are enclosed in sturdy egg capsules for the first 12–14 weeks of gestation. In a gravid female, the embryos are at different stages of development during the first four months of gestation. Embryos are lecithotrophic and there is no evidence of any supplemental mode of embryonic nourishment. Embryos measure 28–30.5cm at birth. The gestation period is estimated at about five to six months. Brood sizes are large, ranging from 21 to 50 young, with a median of 34 young. The reproductive cycle of the nurse shark consists of a five to six-month gestation period and a two-year ovarian cycle. Thus, the reproductive cycle is biennial and a female produces a brood every two years. The nurse shark is an opportunistic predator that consumes a wide range of small fishes, primarily grunts (Haemulidae).
Although South Florida coral reefs are frequently considered to be confined to the Florida Keys, a complex of relict early
Holocene shelf-edge and mid-shelf reefs as well as limestone ridges extends along the continental coast of Southeast Florida
(Fig. 5.1) from offshore south Miami (N25°34') northward to offshore West Palm Beach (N26°43'). This extends the distance
spanned overall by reefs in SE Florida by 125 km (Fig. 5.2). The nomenclature proposed by Moyer et al. (2003) and Banks et
al. (2007) identifying these structures as ridge complex and inner, middle, and outer reef will be used herein. The reefs
are arranged linearly and parallel to the trend of the shoreline. They are separated by sandy sedimentary deposits of varying
thicknesses that overly erosional hardground surfaces (Duane and Meisburger 1969a, b; Raymond 1972; Shinn et al. 1977; Banks
et al. 2007). The reefs themselves are presently not framebuilding but are colonized by a rich tropical fauna otherwise characteristic
of the West Atlantic/Caribbean reef systems.
The inflow of fresh water into coastal lagoons is a key factor influencing the structure and function of these ecosystems. Biscayne Bay, a coastal lagoon adjacent to the city of Miami, is located downstream of the Everglades ecosystem where the extensive water management system now in place has modified the historical hydrology, replacing groundwater and overland flows with pulsed releases from canals. In areas where canals discharge directly into littoral habitats, an environment with low-mean salinity and high-salinity variability is created. In this study, we characterize the salinity patterns of nearshore habitats (<500 m from shore) and document patterns of seasonal abundance and distribution of submerged aquatic vegetation (SAV) to evaluate the impacts of water management practices. Seagrasses were the principal component of the SAV community during the 2005 dry season (mean cover = 25.5%), while macroalgae dominated during the wet season (mean cover = 33.4%). The distribution and abundance of SAV were directly related to the tolerance of each taxon to salinity patterns. Seagrass species with high tolerance to low and variable salinity such as Halodule
wrightii and Ruppia maritima were found only in canal-influenced areas and increased in abundance and spatial distribution in the wet season when freshwater inflow is highest. The dominance of rhizophytic macroalgae during the wet season was determined by the appearance and high abundance of Chara, a taxon commonly associated with freshwater environments. Thalassia testudinum, the most abundant seagrass species, was found throughout the study region, but decreased in abundance in the canal-influenced areas during the wet season when lower, more variable salinity resulted in lowered productivity. The data presented here showed a significant relationship between salinity patterns and the seasonal abundance and distribution of SAV. These findings support the use of SAV as appropriate indicators of changes in water quality resulting from future restoration projects associated with the Everglades Restoration Plan, which will once again modify the delivery of fresh water into littoral habitats with unknown ecological consequences.
There are conflicting reports over whether albumin is present in the Chondrichthyes. In addition, it is unknown whether given
their low levels of extrahepatic β-oxidation, there is actually a need for a plasma FFA transport system. We examined the plasma of several Chondrichthyan species,
including representatives of both the Holocephali and the Neoselachii using a combination of agarose gel electrophoresis,
[14C]palmitic acid binding, SDS-PAGE, and Oil Red O staining following cellulose acetate electrophoresis. None of the eight species
examined had a major acidic palmitate-binding protein with the characteristics of albumin and they all lacked proteins with
the mass of albumin, 66kDa. Palmitate was bound to specific plasma proteins in all elasmobranch species examined and these
palmitate-binding proteins resembled lipoproteins based on their diffuse and variable mobilities and Oil Red O staining. These
lipoproteins are potentially LDL and VLDL based on their migration positions. Albumin appears to be absent from Chondrichthyan
plasma and lipoproteins bind LCFA in its absence.
Measuring fish condition has become a standard practice in the management of fishes, both at the individual and population level. The comparative application of several condition indices to sharks, however, has not yet received a rigorous evaluation. Data for a total of 2120 dusky sharks Carcharhinus obscurus (Lesueur, 1818), ranging in size from newborns (≤79 cm precaudal length [PCL]) to mature adults (≥210 cm PCL), were used to calculate seasonal trends in condition and to facilitate index comparisons. Four commonly used condition measures were selected, including a somatic measure, hepatosomatic index (HSI), and 3 morphometric measures, condition factor (CF), relative condition (Kn) and residual condition (RrPCL). The effect of month was significant for most condition analyses by size class, sex and reproductive state. HSI was found to be the most sensitive index and rapid indicator of condition, but its appropriate use requires the disaggregation of data by clearly defined life stages and reproductive states. The relatively large liver size of neonates and the relatively small liver size of pregnant and postpartum females may otherwise bias interpretations of seasonal variations in condition. HSI was also affected by increasing size of the animal, which confounds inter-size-class comparisons and may require the further division of life-stage data into additional size classes. The results of the 3 morphometric measures were comparable but were not correlated with HSI. CF, Kn and Rr PCL lagged behind HSI, were unable to differentiate between neonate and juvenile animals and were insensitive to short-term variations. The effect of increasing size did not affect calculated CF and RrPCL, but Kn demonstrated a negative correlation. The fact that large predators may consume large volumes of food in a single feeding event was identified as a possible complicating factor in interpreting condition indices.
In recent decades, large pelagic and coastal shark populations have declined dramatically with increased fishing; however, the status of sharks in other systems such as coral reefs remains largely unassessed despite a long history of exploitation. Here we explore the contemporary distribution and sighting frequency of sharks on reefs in the greater-Caribbean and assess the possible role of human pressures on observed patterns.
We analyzed 76,340 underwater surveys carried out by trained volunteer divers between 1993 and 2008. Surveys were grouped within one km2 cells, which allowed us to determine the contemporary geographical distribution and sighting frequency of sharks. Sighting frequency was calculated as the ratio of surveys with sharks to the total number of surveys in each cell. We compared sighting frequency to the number of people in the cell vicinity and used population viability analyses to assess the effects of exploitation on population trends. Sharks, with the exception of nurse sharks occurred mainly in areas with very low human population or strong fishing regulations and marine conservation. Population viability analysis suggests that exploitation alone could explain the large-scale absence; however, this pattern is likely to be exacerbated by additional anthropogenic stressors, such as pollution and habitat degradation, that also correlate with human population.
Human pressures in coastal zones have lead to the broad-scale absence of sharks on reefs in the greater-Caribbean. Preventing further loss of sharks requires urgent management measures to curb fishing mortality and to mitigate other anthropogenic stressors to protect sites where sharks still exist. The fact that sharks still occur in some densely populated areas where strong fishing regulations are in place indicates the possibility of success and encourages the implementation of conservation measures.
Serum protein electrophoresis (EPH) is used to assess relative
concentrations of blood proteins in clinical and biological studies.
Serum EPH fractions have been determined for elasmobranchs using
mammalian albumin, alpha 1-, alpha 2-, beta-, and gamma-globulin
fractions, and have been deemed fractions 1 through 5, respectively.
However, serum EPH fraction concentration reference intervals
(RIs) have not been widely established for different elasmobranch
species. In this study, RIs for fractions 1 through 5 were determined
from 45 wild-caught Nurse Sharks Ginglymostoma cirratum (27
females and 23 males) in South Florida. Serum samples were isolated
from whole blood following caudal venipuncture. Body condition was
also measured in the field to assess the relative health of the individuals
sampled. There was no relationship between body condition and
serum EPH fraction concentrations. In addition, there was no difference
in body condition or serum EPH fraction concentrations
between females and males. Total solids and total protein values
were significantly different (P < 0.001). Nurse Shark serum EPH
fraction 1 was found within the mammalian albumin migrating band
distance and was negligible. Fraction 2 showed no peak in the mammalian
alpha 1-globulin range. A thin, medium peak in the mammalian
alpha 2-globulin range represented fraction 3. In the
mammalian beta-globulin range, fraction 4 consisted of the majority
of protein observed. It was represented by a smooth, broad peak. A
short, medium broad peak in the mammalian gamma-globulin range
represented fraction 5. The Nurse Shark serum EPH fraction RIs
provided in this study may be utilized to clinically evaluate the health
of Nurse Sharks in captivity and in the wild, and to compare the
health of their populations around the world experiencin
Meyer et al (2019) recently proposed that the nutritional condition of white sharks is unaffected by cage diving tourism. This conclusion was reached after analysing changes in the fatty acid profile of muscle samples collected from sharks that had spent more time around cage diving and contrasting them to sharks relatively unexposed to these activities. Here we want to caution on the interpretation of these results which do not fully take into consideration the way energy metabolism functions in elasmobranchs. We provide some alternative metabolic targets which could be retrieved from the field and would be more relevant to estimate the potential population consequences of tourism disturbances on white sharks.
Silver carp (Hypophthalmichthys molitrix) are invasive to North America, and their range has expanded within the Mississippi River Basin, seemingly unchecked, since their introduction in the late 1970s, with the exception of the upper reaches of the Illinois River. With the imminent threat of their movement into the Great Lakes, the goal of the present study was to assess whether differences in the physiological status between silver carp at the leading edge of their invasion front and core population sites could explain their lack of expansion upstream toward Lake Michigan over the past decade. A transcriptomic approach using RNA sequencing and analysis of plasma variables were used to quantify differences among fish at the leading edge and two downstream core population sites. Leading-edge fish exhibited upregulation of genes associated with xenobiotic defense (e.g., ATP-binding cassette C1 [abcc1], abcc2, abcc6), decreased cell integrity (i.e., macroautophagy and apoptosis; autophagy-related protein 9A [atg9a], caspase 3b [casp3b]), and cholesterol metabolism (e.g., abca1, apolipoprotein A1 [apoa1], sterol O-acyltransferase [soat1]) and downregulation of genes associated with DNA repair (e.g., tumor suppressor p53-binding protein 1 [tp53bp1]) compared to core population sites. Transcriptomic profiles of leading-edge fish were consistent with fish inhabiting a polluted environment and suggest that poorer water quality conditions upstream of the leading edge may represent a non-permanent barrier to silver carp range expansion. The present study provides potential molecular targets for monitoring the physiological status of silver carp over time and in response to future improvements in water quality upstream of their leading edge.
To fuel the high energetic demands of reproduction, vertebrates employ different tactics of resource use. Large sharks exhibit long gestation periods and have relatively few well-developed young, which likely incurs high energetic costs. However, information on the relationship between the reproductive and energetic states for most shark species is lacking. In the present study, we used a noninvasive approach to assess relationships among reproductive stage, plasma triglyceride levels, body condition, and circulating reproductive hormones in free-ranging female tiger sharks (Galeocerdo cuvier). A total of 57 sharks were sampled (19 immature, 15 mature/nongravid, and 23 gravid). Circulating plasma triglycerides did not significantly differ among female tiger sharks of different reproductive stages, but body condition values were significantly higher for mature/nongravid sharks (1.29±0.23) compared with gravid (1.15±0.08) and immature (1.13±0.07) sharks. For gravid and mature/nongravid sharks, no significant correlations existed among values of reproductive hormones, plasma triglycerides, and body condition. However, for immature sharks, estradiol values were negatively correlated with body condition values. Additionally, progesterone levels were positively correlated with testosterone levels in immature females. Our results suggest that this large generalist predator may not necessarily be easily characterized as a pure capital breeder, as has been previously hypothesized for ectotherms, but may rely on a mix of energy stores and opportunistic feeding to support reproduction. We present several hypotheses to explain these patterns and discuss our results in terms of energetic reproductive strategies.
In both commercial and recreational fisheries, sharks are captured and released alive to comply with regulations or due to low economic value or voluntary conservation ethic. As a result, understanding the physiological and behavioural responses of sharks to capture stress is important for determining subsequent effects of fisheries interactions on a species-specific basis, as well as for identifying factors that influence mortality. Here, we employed a suite of conventional blood physiology endpoints (glucose, lactate, and haematocrit) integrated with assessments of reflex impairment on blacktip (Carcharhinus limbatus), great hammerhead (Sphyrna mokarran), nurse (Ginglymostoma cirratum) and sand-bar sharks (Carcharhinus plumbeus) captured via experimental drumline gear. We documented a wide range of species-specific differences in all parameters assessed, with nurse sharks consistently having the lowest relative levels of physiological disturbance and reflex impairment; and with great hammerheads exhibiting the highest level of physiological disturbance and reflex impairment, suggesting higher vulnerability to fishing. In general, increases in lactate were positively associated with hook time and correlated with reflex impairment assessment. Moreover, reflex indices showed significant impairment with hook time, with the "jaw" reflex emerging as the most potential predictor of disturbance. Our study results connect previously reported species-specific at-vessel and post-release mortality rates to their physiological disturbance and reflex impairment.
The response to capture is important in fisheries because it can reveal potential threats to species beyond fishing mortalities resulting from direct harvest. To date, the vast majority of studies assessing shark stress responses have used physiology or biotelemetry to look at sensitivity after capture, leaving a gap in our understanding of the behaviours of sharks during capture. We examined the behavioural responses of sharks to capture by attaching accelerometers to fishing gear and measuring the immediate and prolonged forces they exerted while on the line. We recorded acceleration vectors and derived the rate of intense fighting behaviours of 23 individual sharks comprising three species. Results suggest that blacktip sharks (Carcharhinus limbatus) exhibited intense bouts of fighting behaviour at the onset of hooking, while nurse (Ginglymostoma cirratum) and tiger sharks (Galeocerdo cuvier) displayed more subdued acceleration values during capture. We also obtained plasma lactate from a subset of ind...
This work was supported in part by grants from the Scientific Research Fund of the Ministry of Education and a Grant-in-Aid for Cancer Research from the Ministry of Health and Welfare, Japan.
Marine predators, such as elasmobranchs, exhibit variations in nutritional conditions related to both reproductive traits and food availability in the marine environment throughout the year. The main objective of this study was to examine changes in several blood physiological parameters in a demersal shark, the small-spotted catshark (Scyliorhinus canicula), in the wild in relation to season, sex and maturity stage. For this purpose, 108 individuals at different developmental stages were captured and released alive in the western Mediterranean. Blood was obtained from caudal vessels and plasma lipid fractions (total cholesterol, triglycerides and phospho-lipids) and a ketone body (3-β-hydroxybutyrate) were measured. During summer, plasma triglyceride and phos-pholipid levels were lower in adults than in juveniles (mainly in females, probably related to breeding season and laying eggs). Plasma cholesterol levels also showed higher values in summer, indicating higher physical activities during summer and revealing that lipid fractions are more related to reproduction than to nutrition. Plasma 3-β-hydroxybutyrate variations showed a different pattern. No differences were found between sex or maturity stage during summer, although the highest values in adult and juvenile males during winter indicates higher physical activity of males. This study, uses an innovative methodology to establish a correlation between lipid fractions and ketone bodies from the blood of wild individuals and changes in sexual and nutritional status. This method was conducted without damage to the target species and provides new information on the physiology of this abundant elasmobranch in the Mediterranean Sea.
It is thought that the elasmobranch corticosteroid hormone 1α-hydroxycorticosterone (1α-B) functions as both a glucocorticoid (GC) and mineralocorticoid (MC). Classical antinatriuretic MC activities would run counter to the osmoregulatory strategy of euryhaline elasmobranchs acclimating to fresh water (FW). Therefore we hypothesize that FW acclimation will be accompanied by a decrease in plasma corticosteroids in these animals. However, events that activate the "fight-or-flight" response could mask changes associated with acclimation to lower salinities. To better define the MC role of corticosteroids in elasmobranchs, we designed a transfer system that allows the acclimation of Atlantic stingrays (Dasyatis sabina) from seawater (SW) to FW over 12h while minimizing other extraneous stressors. Blood and interrenal glands were sampled from one group of stingrays 24h after FW transfer, while another group was sampled two weeks after FW transfer. Two other groups served as mock-transfer controls in that they were treated and sampled in the same way, but remained in SW for the entire period. Plasma corticosteroids, osmolality, chloride, and urea were significantly lower in FW-acclimated stingrays (compared to mock-transfer stingrays) 24h after FW transfer. This pattern remained after two weeks in FW, with the exception that plasma corticosteroids returned to pre-acclimation levels. There were no significant differences between experimental groups in interrenal levels of mRNAs encoding key steroidogenic proteins (steroidogenic acute regulatory protein and cholesterol side chain cleavage enzyme). Temporally decreased corticosteroid levels during FW acclimation are consistent with the unique strategy of euryhaline elasmobranchs, whereby lower plasma osmolality is maintained in FW vs. SW environments to reduce hydromineral gradients.
Copyright © 2015. Published by Elsevier Inc.
The effectiveness of several non-lethal techniques as indicators of total lipid content in smallmouth bass Micropterus dolomieu, walleye Sander vitreus and channel catfish Ictalurus punctatus was investigated. The techniques included (1) the Fulton and relative condition factors, (2) relative mass, (3) plasma indicators of nutritional status (alkaline phosphatase, calcium, cholesterol, protein, triglycerides and glucose) and (4) readings from a hand-held, microwave energy meter. Although simple linear regression analysis showed that lipid content was significantly correlated with several predictor variables in each species, the r2 values for the relations ranged from 0·17 to 0·50 and no single approach was consistent for all species. Only one model, between energy-meter readings and lipid content in I. punctatus, had an r2 value (0·83) high enough to justify using it as a predictive tool. Results indicate that no single variable was an accurate and reliable indicator of whole body lipid content in these fishes, except the energy meter for I. punctatus.
A simple metric (span condition analysis; SCA) is presented for quantifying the condition of sharks based on four measurements of body girth relative to body length. Data on 104 live sharks from four species that vary in body form, behaviour and habitat use (Carcharhinus leucas, Carcharhinus limbatus, Ginglymostoma cirratum and Galeocerdo cuvier) are given. Condition shows similar levels of variability among individuals within each species. Carcharhinus leucas showed a positive relationship between condition and body size, whereas the other three species showed no relationship. There was little evidence for strong differences in condition between males and females, although more male sharks are needed for some species (e.g. G. cuvier) to verify this finding. SCA is potentially viable for other large marine or terrestrial animals that are captured live and then released.
Elasmobranch reproductive behavior has been inferred from freshly caught specimens, laboratory examinations of reproductive structures and function, or determined from direct observations of captive or free swimming wild animals. Several general behaviors have been described including seasonal sexual segregation, courtship and copulation. Courtship behavior was inferred for many species from the presence of scars and tooth cuts on the female's body, and noted in more detail from underwater observations. Copulation has been directly observed in captive settings for several species of elasmobranchs in large aquaria, and in the wild for three species of urolophids and for Triaenodon obesus and Ginglymostoma cirratum. A detailed ‘case history’ of nurse shark reproductive behavior is presented that may be used as a template for future work on shark reproductive behavior of other species. Our studies, using diver identifiable tags and in situ behavioral observations, provide unprecedented information on social structure and mating behavior in this species. Since 1993, 115 G. cirratum, 45 adults and 70 juveniles have been tagged in the Dry Tortugas, Florida. Observations show that adult males visit the study site every year with three males dominant. Individual adult females visit the study area to mate in alternate years. Polygyny and polyandry are common. Future research on reproductive behavior of elasmobranchs should address questions on male access to females, sexual selection and dominance hierarchies.
The liver is an essential metabolic organ, and its metabolic function is controlled by insulin and other metabolic hormones. Glucose is converted into pyruvate through glycolysis in the cytoplasm, and pyruvate is subsequently oxidized in the mitochondria to generate ATP through the TCA cycle and oxidative phosphorylation. In the fed state, glycolytic products are used to synthesize fatty acids through de novo lipogenesis. Long-chain fatty acids are incorporated into triacylglycerol, phospholipids, and/or cholesterol esters in hepatocytes. These complex lipids are stored in lipid droplets and membrane structures, or secreted into the circulation as very low-density lipoprotein particles. In the fasted state, the liver secretes glucose through both glycogenolysis and gluconeogenesis. During pronged fasting, hepatic gluconeogenesis is the primary source for endogenous glucose production. Fasting also promotes lipolysis in adipose tissue, resulting in release of nonesterified fatty acids which are converted into ketone bodies in hepatic mitochondria though β-oxidation and ketogenesis. Ketone bodies provide a metabolic fuel for extrahepatic tissues. Liver energy metabolism is tightly regulated by neuronal and hormonal signals. The sympathetic system stimulates, whereas the parasympathetic system suppresses, hepatic gluconeogenesis. Insulin stimulates glycolysis and lipogenesis but suppresses gluconeogenesis, and glucagon counteracts insulin action. Numerous transcription factors and coactivators, including CREB, FOXO1, ChREBP, SREBP, PGC-1α, and CRTC2, control the expression of the enzymes which catalyze key steps of metabolic pathways, thus controlling liver energy metabolism. Aberrant energy metabolism in the liver promotes insulin resistance, diabetes, and nonalcoholic fatty liver diseases. © 2014 American Physiological Society. Compr Physiol 4:177-197, 2014.
This study was carried out to establish biochemical parameters with potential diagnostic value to assess the nutritional status of healthy seabass. For that purpose, triplicate groups of seabass juveniles were submitted to different feeding protocols: fed for 14 days; fed for 7 days followed by 7 days of fasting or fasted for 14 days. At the end of the trial, body, liver and viscera were randomly sampled for proximate composition analysis. Blood was also collected and the following plasma parameters were analyzed by standard clinical methods: glucose; cholesterol; triglycerides; protein; inorganic phosphorus; calcium; magnesium; alkaline phosphatase (ALP); aspartate aminotransferase; lactate dehydrogenase; creatine phosphokinase and lipase. No major effect of feed deprivation on body composition, visceral index, perivisceral and hepatic lipid content were observed, whereas hepatosomatic index and hepatic glycogen were reduced. Previous feeding conditions strongly influenced the plasma parameters in seabass. Comparatively to the fed group, plasma glucose, cholesterol and calcium levels were reduced after 2 weeks of fasting while plasma triglycerides, protein, inorganic phosphorus and ALP attained minimum levels after 1 week of fasting. Overall, enzymatic activity parameters showed higher variability than biochemistry parameters. In conclusion, during short-term starvation (<14 days) hepatic energy depots were extensively mobilized while perivisceral and body lipids reserves were preserved. Among measured parameters, plasma protein, triglycerides, inorganic phosphorus and ALP seem to have potential as predicative diagnostic tools to assess the nutritional status of seabass and may be useful to monitor feeding practices in aquaculture. Further studies are, however, required to extend results of this study to other fish size classes.
Elasmobranchs are of metabolic interest for several reasons, including their primitive evolutionary position, their osmotic strategy and their low incidence of neoplasia. Some aspects of the metabolism of elasmobranch fishes are unique when compared with those of the other vertebrates. Although many features of their metabolism can be attributed to their primitive evolutionary position (e.g., fewer isoforms of enzymes and other proteins), some unique features appear to be related to the unusual solute system (urea and methylamines) used by elasmobranchs. The solute system exerts widespread effects, which has an impact on the metabolism of lipids, ketone bodies and amino acids and the structure of proteins and membranes. Effects of urea on the transport of lipid may influence aspects of lipid metabolism, reducing extrahepatic lipid catabolism via effects on nonesterified fatty acid transport and enhancing a need for reliance on ketone bodies. Amino acid metabolism of elasmobranchs is also heavily influenced by the need for continuous synthesis of urea with glutamine as the nitrogen donor. These effects, in turn, may play a role in their low incidence of cancer. Specifically, the reduced availability of glutamine (an important nutrient for rapidly growing cells) coupled with the low levels of nonesterified fatty acids in the blood reduces the availability of molecules essential for tumor growth. This metabolic design may thus provide marine elasmobranchs with a “systemic” resistance to cancer.
1. Juvenile freshwater stingrays of the family Potamotrygonidae are unable to survive in salinities in excess of 20.6‰ when gradually acclimated.2. No differences were observed in blood pH or hematological parameters when fish adapted to a salinity of 14.5‰ were compared with freshwater controls.3. Significant increases were found in serum sodium (21%), chloride (21%), calcium (48%), and magnesium (51%). Increases in total CO2 (16%), potassium (21%), and inorganic phosphorus (35%) were not significant on account of high variance. Serum osmolarity increased 69%.4. There was no apparent effect of salinity on serum total cholesterol, organically bound phosphorus, or total carbohydrates. Glucose contributed only 25% of the latter.5. Serum urea was low (1.1 mM/1) as previously reported, and the trend to increase in a saline environment was not osmotically significant.6. Freshwater stingrays are unique among elasmobranchs in possessing significant amounts of a protein with the electrophoretic mobility of human ...
This study examined whether simple indicators of condition in individual Atlantic cod (Gadus morhua) are related to biochemical composition and energy content for the whole range of conditions potentially observed in natural populations. The energy content of muscle was largely associated with its protein content, while liver energy content mainly consisted of lipids. Accurate predictions of muscle and liver energy content can also be made from the measurement of their water content. Relationships between energy content, water content, and simple measures such as condition factor and hepatosomatic index provide a fast and accurate assessment of seasonal changes in total available energy reserves in cod. These indices could advantageously be used to monitor the status and recovery of cod stocks and to ensure improved management of that resource.
We used factor analysis to examine the correlation structure of six multivariate blood chemistry data sets for migrating hatchery and wild juvenile chinook salmon (Oncorhynchus tshawytscha). Fish were sampled (19982002) from juvenile fish bypass systems at dams or (one data set) from fish transport barges on the Snake and Columbia rivers. Analyses were performed to determine which blood chemistry analytes covaried, to facilitate interpretation of the data sets, and to provide insight into controlling physiological mechanisms. Four underlying factors were derived from the analyses: (i) a nutritional factor composed of total protein, cholesterol, calcium, and alkaline phosphatase, (ii) a tissue damage factor composed of the enzymes alanine aminotransferase, aspartate aminotransferase, and creatine kinase, (iii) a lipid metabolism factor composed of triacylglycerol lipase and triglycerides, and (iv) a stress factor composed of cortisol, glucose, Na+, and Cl. Although causal mechanisms cannot be directly inferred from our analyses, findings of published research provide tenable causal mechanisms for the observed structure. The consistency of the correlation structure among data sets suggests that composite (latent) variables may be more reliable indicators of some physiological responses than changes in individual variables.
Sharks are top predators in many marine ecosystems. Despite recent concerns over declines in shark populations, studies of shark communities in coastal habitats are limited. We used drumlines and longlines to determine shark community composition and habitat affinities in the Florida Keys, USA. Community composition varied among habitats. Catch rates of smaller sharks were highest in protected shallow waters, while large sharks were more abundant in deep channels. Overall probabilities of catching large sharks on drumlines did not vary with water temperature, while catches of small sharks on longlines increased with increasing water temperature. Individual species differed in their responsiveness to variation in water temperatures and habitat. Bait type affected catch rates of some species, suggesting that fishing methods should be considered explicitly in studies describing shark communities or temporal trends in abundance. Catch rates of large-bodied sharks were higher in a remote and protected location compared with similar habitats near inhabited Keys. Also, historical accounts of a shark fishery in the Study area during the 1920s suggest substantial declines in large shark abundance and shifts in community composition. By implication, ecosystem impacts of changes in the large shark community may be dramatic and likely occurred before adequate baselines were established.
Although off-channel habitats in the estuaries of large rivers impart many benefits to fish that rear within them, it is less clear how these habitats benefit migrating anadromous species that utilize these habitats for short periods of time. We evaluated the physiological correlates (nutritional condition, growth, and smoltification) of habitat utilization (main-channel vs. off-channel) by juvenile Chinook salmon Oncorhynchus tshawytscha during emigration. Fish from the off-channel had higher condition factor scores and relative weights than fish from the main-channel throughout the study period. Plasma triglyceride and protein concentrations were significantly different between habitat types and across the sampling period, suggesting that fish utilizing the off-channel habitats were compensating for energy losses associated with emigration as compared to main-channel fish. Growth potential (RNA to DNA ratio) did not vary by habitat or sampling period, presumably due to short residency time. There were no differences in osmoregulatory capacity (gill Na(+), K(+)-ATPase activity) based on habitat type. Our results indicate that short-term off-channel habitat use may mitigate for energy declines incurred during migration, but likely does not impart significant gains in energy stores or growth.
A study was carried out on the serum levels of cholesterol [total (TC) and that associated with high-density lipoproteins (HDLC)] and triglyceride (TG) in 127 specimens of Scyliorhinus canicula. The values obtained were correlated with sex, size, liver weight and reproductive stage. Results showed that male dogfish have higher levels of TC and HDLC, and lower TG than female. In adult males, TC increased and HDLC decreased with both size and spermatogenesis. Females carrying capsulated eggs showed a noticeable increase in TG together with a decrease of the HDLC levels, which were apparently not related with size.
Paired, serial blood samples were collected for a minimum of 6 hr to a maximum of 15 days from cannulae chronically placed in the internal carotid artery (A) to the brain and the anterior cardinal sinus (V) from the brain of the spiny dogfish shark (Squalus acanthias). Previously fed animals were fasted for either 3 to 8 days (short-fasted) or 20 to 29 days (long-fasted) before the surgery to implant the cannulae and during the subsequent sampling periods. Plasma β-hydroxybutyrate, acetoacetate, glucose, lactate, and alanine levels were measured by standard enzymatic procedures. The internal carotid artery plasma β-hydroxybutyrate and acetoacetate levels were in the approximate ratio of 4 to 6:1, were greater in the long-fasted than in the short-fasted animals, and both ketones increased throughout the observation periods. In contrast, plasma lactate and alanine levels declined by postoperative day 2 to levels that, like glucose, remained relatively stable and were characteristic of the individual animal. The A-V metabolite differences between the short- and long-fasted animals were not significantly different and the data from the two groups of animals were combined for purpose of analysis. β-Hydroxybutyrate was extracted from the plasma by the brain during both the surgery and recovery period (⩽ 2 days) and the “normal” under the observational conditions period (> 2 days). The small negative A-V differences in acetoacetate during both periods, and in glucose during the > 2 day period, were not statistically significant. There were no evident A-V differences in plasma alanine. Lactate was released by the brain during both the ⩽ 2 days and > 2 day periods. The uptake of β-hydroxybutyrate and the release of lactate indicate that the spiny dogfish brain used both β-hydroxybutyrate and glucose during the observation periods. The data suggest that the plasma was the immediate source of β-hydroxybutyrate, but, as proposed by previous authors, the proximate glucose source may have been provided by the mobilization of endogenous brain glycogen stores. © 1994 Wiley-Liss, Inc.
The seasonal variation in lipid class composition (triacylglycerols, free fatty acids, cholesterols and polar lipids) was described for juvenile Atlantic salmon sampled at 12 occasions over an 18-month period in the Norwegian River Alta (70 degrees N). Lipid class composition was determined for pooled samples of groups of fish sorted by cohort and condition factor. Mass-specific lipid content ranged from 2.3% and 8.1% of fresh mass, and mass-specific triacylglycerol content between 0.16% and 5.6% of fresh mass. Total lipid content decreased by 34-57% during the winter period, before increasing by 155-176% between May and July. A large proportion of the variation in total lipid content was due to variation in triacylglycerol content (r(2) = 0.95), except for variations at low total lipids levels when triacylglycerols were absent. The temporal variation in polar lipid content was, although to a lesser degree, related to total lipid content (r(2) = 0.62), indicating that the fish also utilised polar lipids as an energy source during periods of starvation. Analyses of 39 individual parr collected in May showed a large individual variation in lipid class composition in the most critical period of the year. It is concluded that information on variation in lipid class composition may give more precise and detailed information of energy status during critical periods, although total lipid content will in most cases give a fair description of the energy status of the fish.
Predators can play important roles in structuring their communities through top-down effects on the distribution and abundance of their prey. Sharks are top predators in many marine communities, yet few studies have quantified those factors influencing their distribution and hunting behaviour. Here, we use location data from 340 predatory interactions between white sharks Carcharodon carcharias (Linnaeus), and Cape fur seals Arctocephalus pusillus pusillus (Schreber), data on associated environmental factors, and spatial analysis, including a novel application of geographic profiling – a tool originally developed to analyse serial crime – to investigate spatial patterns of shark attack and search behaviour at Seal Island in False Bay, South Africa. We found that spatial patterns of shark predation at this site are nonrandom. Sharks appear to possess a well-defined search base or anchor point, located 100 m seaward of the seal's primary island entry–exit point. This location is not where chances of intercepting seals are greatest and we propose it may represent a balance among prey detection, capture rates, and competition. Smaller sharks exhibit more dispersed prey search patterns and have lower predatory success rates than larger conspecifics, suggesting possible refinement of hunting strategy with experience or competitive exclusion of smaller sharks from the most profitable hunting locations. As many of the features of this system will be common to other instances of foraging, our conclusions and approach employed may have implications and applications for understanding how large predators hunt and for studying other predator–prey systems.
Dogfish sharks are opportunistic predators, eating large meals at irregular intervals. Here we present a synthesis of data from several previous studies on responses in plasma metabolites after natural feeding and during prolonged fasting (up to 56 days), together with new data on changes in plasma concentrations of amino acids and non-esterified fatty acids. Post-prandial and long-term fasting responses were compared to control sharks fasted for 7 days, a typical inter-meal interval. A feeding frenzy was created in which dogfish were allowed to feed naturally on dead teleosts at two consumed ration levels, 2.6% and 5.5% of body weight. Most responses were more pronounced at the higher ration level. These included increases in urea and TMAO concentrations at 20 h, followed by stability through to 56 days of fasting. Ammonia levels were low and exhibited little short-term response to feeding, but declined to very low values during the extended fast. Glucose and β-hydroxybutyrate both fell after feeding, the latter to a greater and more prolonged extent (up to 60 h), whereas acetoacetate did not change. During prolonged fasting, glucose concentrations were well regulated, but β-hydroxybutyrate increased to 2–3-fold control levels. Total plasma amino acid concentrations increased in a biphasic fashion, with peaks at 6–20 h, and 48–60 h after the meal, followed by homeostasis during the extended fast. Essential and non-essential amino acids generally followed this same pattern, though some exhibited different trends after feeding: taurine, β-alanine, and glycine (decreases or stability), alanine and glutamine (modest prolonged increases), and threonine, serine, asparagine, and valine (much larger short-term increases). Plasma non-esterified fatty acid concentrations declined markedly through 48 h after the 2.6% meal. These data are interpreted in light of companion studies showing elevations in aerobic metabolic rate, urea production, rectal gland function, metabolic base excretion, and activation of ornithine–urea cycle and aerobic enzymes after the meal, and muscle N-depletion but maintenance of osmolality and urea production during long-term fasting.
The endocrine underpinnings of the stress response in fish have been the subject of intense research for well over 50years. Much of the research has focussed on teleost fish and so the endocrine mechanisms for cortisol production, transport and action at the target site have received significant attention. However, corticosteroidogenesis in elasmobranchs is exceptional on a number of levels. Unlike teleost fish the interrenal tissue is anatomically distinct from both renal and chromaffin (catecholamine producing) tissue; further the final product, 1α-hydroxycorticosterone (1α-OH-B), is unique to chondrichthyans where the carbon atom at position 1 of corticosterone has a hydroxyl group attached in the α orientation. The homologous nature of interrenal tissue in elasmobranchs presents an obvious advantage in the study of corticosteroidogenesis, however, the unique chemical nature of 1α-OH-B has presented distinct disadvantages as it has proven to be difficult to synthesise, and therefore studies examining the mineralocorticoid and glucocorticoid actions of this steroid are limited. Over the last decade molecular techniques have provided significant insight in the involvement of corticosteroiogenic enzymes in the elasmobranch interrenal in addition to the evolution of corticosteroid receptors. Given the number of excellent reviews focussing on the role of cortisol in the stress response of teleost fish, this short review aims to synthesise the endocrine basis for the synthesis, release, and action, of the enigmatic 1α-OH-B in elasmobranch fish.
The unusual energy metabolism of elasmobranchs is characterized by limited or absent fatty acid oxidation in cardiac and skeletal muscle and a great reliance on ketone bodies and amino acids as oxidative fuels in these tissues. Other extrahepatic tissues in elasmobranchs rely on ketone bodies and amino acids for aerobic energy production but, unlike muscle, also appear to possess a significant capacity to oxidize fatty acids. This organization of energy metabolism is reflected by relatively low plasma levels of non-esterified fatty acids (NEFA) and by plasma levels of the ketone body ss-hydroxybutyrate that are as high as those seen in fasted mammals. The preference for ketone body oxidation rather than fatty acid oxidation in muscle of elasmobranchs under routine conditions is opposite to the situation in teleosts and mammals. Carbohydrates appear to be utilized as a fuel source in elasmobranchs, similar to other vertebrates. Amino acid- and lipid-fueled ketogenesis in the liver, the lipid storage site in elasmobranchs, sustains the demand for ketone bodies as oxidative fuels. The liver also appears to export NEFA and serves a buoyancy role. The regulation of energy metabolism in elasmobranchs and the effects of environmental factors remain poorly understood. The metabolic organization of elasmobranchs was likely present in the common ancestor of the Chondrichthyes ca. 400million years ago and, speculatively, it may reflect the ancestral metabolism of jawed vertebrates. We assess hypotheses for the evolution of the unusual energy metabolism of elasmobranchs and propose that the need to synthesize urea has influenced the utilization of ketone bodies and amino acids as oxidative fuels.
Changes in the free NAD+/NADH ratio and the energy charge (ATP + 1/2 ADP/ATP + ADP + AMP) of the liver were compared with the ratio of acetoacetate to beta-hydroxybutyrate of arterial blood in rabbits subjected to ligation of the common bile duct. Both the acetoacetate/beta-hydroxybutyrate ratio of the liver, which reflects mitochondrial free NAD+/NADH ratio, and the heptic energy charge decreased in accordance with the decrease of mitochondrial phosphorylative activity after the ligation. The decrease in the acetoacetate/beta-hydroxybutyrate ratio of the liver was attributed to a restricted mitochondrial reoxidation of NADH due to an inhibition of oxidative phosphorylation. Moreover, changes in the ratio of acetoacetate to beta-hydroxybutyrate in arterial blood were positively correlated with those of the liver (r = 0.695, P less than 0.01) and the hepatic energy charge (r = 0.844, P less than 0.01). It is suggested that the ratio of acetoacetate to beta-hydroxybutyrate in blood can reflect the energy charge of the liver in jaundiced rabbits.