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A Comparison of Reproductive and Energetic States in a Marine Apex Predator (the Tiger Shark, Galeocerdo cuvier )
Abstract
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.
... Além disso, é possível que as elevadas concentrações de TAG encontradas em G. cirratum seja impulsionado por um aumento sazonal durante a estação chuvosa. 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). ...
... et al. 2005) and mating strategies, with polyandry and polygyny, as well as sperm storage and multiple paternity being commonly reported(Pratt and Carrier, 2005). Despite their importance for reproductive performance, energetic investment are rarely considered in studies of shark reproduction (e.g.Dudley and Cliff 1993;Hammerschlag et al. 2018;. Furthermore, there are no published studies investigating the nutritional quality and dietary patterns of free-living male sharks across life-stages.In male sharks, energetic investments in reproduction is mainly associated with spermatogenesis, copulation, male-male competition, and where necessary, migration to access mates (e.g. ...
... Although studies investigating the role of glucocorticoids in sharks are lacking, these hormones are known to play an important role in regulating the acquisition and mobilization of resources in many vertebrates, and is expected to be higher during energetically expensive life history stages, such as reproduction (e.g.Romero 2002;Crespi et al. 2013;Romero and Wingfield 2016). As such, measuring hormones integrated with nutritional indicators can offer a great opportunity to non-lethally examine patterns of energy regulation across reproductive stages (e.g.Hammerschlag et al. 2018). ...
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.
... For example, free-circulating plasma lipid concentrations, such as triglycerides (TAGs), cholesterol (CHOL), free fatty acids (FFAs), and associated lipoprotein fractions (Kaduce and Folk 2002;Gallagher et al. 2014Gallagher et al. , 2017 can provide an effective, non-lethal assessment of energetic condition. Such evaluations have been applied to fishes (Gallagher et al. 2017;Hammerschlag et al. 2018), marine mammals (Kaduce and Folk 2002;Whiteman et al. 2013), and birds (Jenni-Eiermann and Jenni 1994). ...
... 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). ...
... suggest that juvenile sharks undergo periods of fasting and/ or starvation, which was found to drive higher TAG concentrations in larger vertebrates such as polar bears (Kaduce and Folk 2002). Second, though lipid metabolite concentrations have been linked to reproductive status in sharks (Hammerschlag et al. 2018;Rangel et al. 2021), all of the individuals sampled in this study were juveniles, suggesting that reproductive status was unlikely to impact the energetic condition of individuals. Finally, there are a growing number of studies that have validated the use of plasma lipid concentrations as a proxy for condition in sharks (Gallagher et al. 2014(Gallagher et al. , 2017Hammerschlag et al. 2018) and teleosts (Ballantyne 1997;Norton et al. 2001;Congleton and Wagner 2006;Eldøy et al. 2021, see Table 1). ...
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.
... Lawson et al., 2018). Nevertheless, variability in reproductive costs provides insights into the potential for species to respond to stressors (Hammerschlag et al., 2018). Estimating reproductive costs can inform changes in reproductive rates or numbers of breeding adults. ...
... Ectotherms are mostly capital breeders, while endotherms are generally income breeders (Jönsson, 1997;Houston et al., 2006). This is because capital breeding is energetically more efficient in ectotherms due to low costs of storage, maintenance and mobilisation of energy reserves, although some species depart from this strategy due to factors such as resource availability (Houston et al., 2006;Hammerschlag et al., 2018). Use of a capital breeding strategy is common in elasmobranchs (e.g. ...
... Use of a capital breeding strategy is common in elasmobranchs (e.g. Pierce et al., 2009;Lteif et al., 2016;Corsso et al., 2018), but there is also evidence of income breeding strategies (Castro, 2009;Cotton et al., 2011) and species that exhibit both (Hammerschlag et al., 2018). The relative energy requirements for capital or income breeding strategies may be important for continued reproductive success in species that experience changing environments (Hammerschlag et al., 2018). ...
This study investigated the measurements of energy density and bioenergetic modelling for a pelagic ray, Mobula eregoodoo, to estimate its relative allocation to various bodily processes and especially reproduction. The data revealed M. eregoodoo uses up to 21.0% and 2.5% of its annual energy budget on growth and reproduction, respectively. During pregnancy, females depleted energy reserves in the liver, which, along with their biennial reproductive cycle, aligns with general theory that ectotherms are capital breeders and thus build energy reserves before reproduction. Nonetheless, the reduction in energy reserves did not account for all reproductive costs, and therefore, gravid females supplement reproductive costs through energy derived from the diet, according to an income‐breeding strategy. These characteristics imply that M. eregoodoo exhibits some flexibility in fuelling reproduction depending on energy availability throughout the reproductive cycle, which may be prevalent in other elasmobranchs. The data represent the first estimates of both the metabolic costs of gestation in elasmobranchs and the relative cost of reproduction in rays. Energy costs and plasticity associated with highly variable reproductive strategies in elasmobranchs may influence long‐term population viability under a rapidly changing environment.
... Although studies have investigated the trophic roles and relationships among predators (e.g. Hussey et al. 2015, Shipley et al. 2019, our understanding of how diet and energy intake is influenced by life stage, and the consequences of foraging variation on the nutritional status of the predator, remains limited (Wai et al. 2012, Dicken et al. 2017, Hammerschlag et al. 2018. ...
... Rangel, N. Hammerschlag, J. Sulikowski, R. Mo reira unpubl. data), and a coincident elevation in body condition and plasma triglycerides (Hammerschlag et al. 2018). These findings suggest that nongravid females may increase food intake and allocation of energy stored. ...
... If tiger sharks relied only on energy stored for reproduction, we would have expected to find high percentages of SFAs in gravid females, as SFAs tend to be catabolized for energy and PUFAs are normally conserved (Tocher 2003), but this was not the case. Consistent with our hypotheses, our data suggest that gravid females likely require dietary n3 and n6 HUFAs, corroborating a previous hypothesis of a mixed capital−income breeding strategy for tiger sharks, in which females forage during gestation (Hammerschlag et al. 2018). Future research should investigate the diet preferences and fatty acid profiles of potential prey items across all life stages of female tiger sharks to confirm our findings (Fig. 1). ...
Knowledge of the nutritional requirements of apex predators is key for determining ecological interactions. However, an understanding of how diet is influenced by reproduction, and the consequences of foraging variation on the nutritional status of a predator, is limited. Here, we used short-term dietary markers (plasma and whole-blood fatty acids) integrated with reproductive hormones (17β-estradiol and testosterone) and ultrasonography as a non-lethal approach to investigate the effect of life stage on nutritional status and trophic dynamics of female tiger sharks Galeocerdo cuvier. Despite their generalist feeding behavior, female tiger sharks fed on different food sources and/or modulated their fatty acid metabolism depending on the reproductive context. This suggests some adjustment in their nutritional requirements associated with changes in their reproductive state. Plasma and whole-blood fatty acids indicated distinct dietary sources across life stages, with a high dependence on coastal/benthic food resources during juvenile life stages, and on pelagic/oceanic and reef-associated food resources during adult life stages. Higher percentages of highly unsaturated omega-3 fatty acids found in females during their reproductive cycles suggest the dependency on these fatty acids as a source of metabolic energy during reproduction. A high percentage of arachidonic acid (ARA) found in plasma of gravid females suggests the possibility of a selective diet of ARA-rich prey species and/or selective mobilization of ARA from stored energy during gestation. Based on our findings, we propose a conceptual model of expected changes in nutritional and trophic markers across life stages of female tiger sharks.
... Developed by Irschick and Hammerschlag (2014), span condition analysis is based on various measures of shark girth along the dorsal surface relative to their length. This method can be readily integrated with nonlethal blood sampling of various energetic biochemical parameters for a more holistic assessment of energetic state (Gallagher et al., 2014;Hammerschlag et al., 2018). ...
... However, the sample was more similar to plasma than serum as it was extracted from unclotted blood, thereby retaining clotting proteins that are not present in serum (Issaq et al., 2007). other elasmobranchs (e.g., Gallagher et al., 2014Gallagher et al., , 2017aHammerschlag et al., 2018;Lyons, 2018), as well as teleost fish (e.g., Hanson et al., 2012;Jeffery et al., 2019;King et al., 2016;Liss et al., 2013Liss et al., , 2016. TAG, CHOL and FFA assays were assayed in triplicate, while ketone body assays were assayed in duplicate. ...
... Accordingly, the positive relationship found here between body condition and KB ratio in immature G. cirratum may suggest that body condition, measured via span condition analysis, is a good indicator of energetic state during this life stage. The lack of such a relationship in mature G. cirratum may imply that morphological body condition parameters may only reflect an organism's energy reserves during certain life stages or reproductive states (Hammerschlag et al., 2018;Hussey et al., 2009;Mesa & Rose, 2015;Naesje et al., 2006;Sardenne et al., 2016). Future research should continue to explore plasma KB ratio as an indicator of energetic state in elasmobranchs and its relationships with other parameters related to elasmobranch condition (e.g., HSI). ...
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.
... (2018) also investigated tiger shark body condition (SCA) and plasma triglyceride concentrations, exploring how these metrics varied with reproductive state and reproductive hormones. While this study did not detect the same significant, positive correlation between SCA and plasma triglycerides identified by Gallagher et al. (2014b), results did reveal some variation in the metrics with reproductive state and reproductive hormones: body condition varied significantly between reproductive states, but plasma triglyceride concentrations did not, and plasma estradiol in immature sharks was significantly positively correlated with plasma triglycerides and significantly negatively correlated with body condition (Hammerschlag et al. 2018). As heightened estradiol is considered an indicator of vitellogenin production, it was hypothesized that these correlations could be related to sexual maturation (Hammerschlag et al. 2018). ...
... While this study did not detect the same significant, positive correlation between SCA and plasma triglycerides identified by Gallagher et al. (2014b), results did reveal some variation in the metrics with reproductive state and reproductive hormones: body condition varied significantly between reproductive states, but plasma triglyceride concentrations did not, and plasma estradiol in immature sharks was significantly positively correlated with plasma triglycerides and significantly negatively correlated with body condition (Hammerschlag et al. 2018). As heightened estradiol is considered an indicator of vitellogenin production, it was hypothesized that these correlations could be related to sexual maturation (Hammerschlag et al. 2018). Garcia-Garrido et al. (1990) assessed the blood serum metabolites of smallspotted catsharks (Scyliorhinus canicula), revealing ontogenetic and sexual variation in serum concentrations of cholesterol and triglycerides, thought to be related to gametogenesis. ...
... This discrepancy may be due to the inclusion of immature sharks in the present study; both Irschick and Hammerschlag (2014) and Gallagher et al. (2017) excluded small juveniles (< 100 cm TL) from their analyses, focusing on subadult and adult sharks. Though significant differences in mean metric values between immature and mature sharks were not detected in the present study, maturity state is known to influence both body condition and plasma metabolite concentrations in a number of shark species (Garcia-Garrido et al. 1990;Hussey et al. 2009;Valls et al. 2016;Hammerschlag et al. 2018). Disparities between the results of the present study and the aforementioned prior studies could also be related to differences between study locations. ...
The way an animal utilizes and stores energy directly affects its ability to perform essential life functions (e.g. foraging, migration, reproduction), with implications for its health and fitness; therefore, individual variation in energy storage and metabolism within a population leads to intra-population variation in individual fitness and survival. Consequently, understanding the factors that contribute to variation in energy storage and metabolism within a population can aid in identifying factors that influence that population’s fitness. Compared to other taxa, there has been relatively little research to investigate the factors that govern variation in elasmobranch energy use and storage, particularly in wild populations. Furthermore, there has been almost no research conducted to explore how urbanization, a growing threat to marine ecosystems and organisms, affects elasmobranch energy storage and metabolism and, ultimately, their health and fitness. To address this knowledge gap, morphological (i.e. body condition) and biochemical (i.e. plasma cholesterol, free fatty acid, triglyceride, and ketone body concentrations) metrics related to energy storage and utilization were measured for 118 wild-sampled south Florida nurse sharks (Ginglymostoma cirratum). Statistical analyses were performed to identify any correlations between metrics and explore ontogenetic, sexual, seasonal, and spatial variation in body condition and plasma metabolite concentrations within the population. Results demonstrated that several metrics can be significantly linearly correlated with one another, but these relationships are highly dependent on nurse shark life stage and sex. The mean plasma metabolite concentrations for immature, mature female, and mature male nurse sharks was not significantly different; however, mature female nurse sharks had significantly higher body condition than mature male sharks. Further analysis revealed that this difference is driven by seasonal variation in mature female body condition, likely related to the accumulation of energy stores prior to reproduction. Significant seasonal variation also occurred in plasma concentrations of β-hydroxybutyric acid for mature male nurse sharks, possibly related to energetically exhausting mating activity during the wet season. Significant spatial variation occurred in the plasma concentrations of both triglycerides and free fatty acids for immature nurse sharks. Immature nurse sharks sampled within the more urbanized Metropolitan zone had higher mean triglyceride concentrations, and lower mean free fatty acid concentrations, than their conspecifics sampled within the relatively more natural National Park zone; this may imply that nurse sharks in the Metropolitan zone are feeding more, or more frequently, than nurse sharks in the National Park zone. The results of this thesis contribute to the growing knowledge base on energy storage and metabolism in wild-sampled elasmobranchs, as well as provide the first exploration of variation in elasmobranch body condition and plasma metabolites relative to urbanization, an anthropogenic threat with the capacity to influence elasmobranch fitness and survival.
... Our study involved adult male sharks and given that sex-based differences may influence reproductive decisionsoften shaped by energetic costs associated with physiological maintenance, growth and survival, which includes immune responses (Hammerschlag et al., 2018) this aspect requires further discussion. There are few studies on how sex affects the immune response in fishes (Campbell et al., 2021). ...
... et al., 2018); these involve specific immune hypothalamicpituitary-gonadal axis interactions and limiting demands are placed on the immune system (Campbell et al., 2021). However, comparable information on the relationship between the reproductive and energetic states of many shark species is lacking (Hammerschlag et al., 2018). Researchers should consider oviparous species such as small-spotted catsharks (Coolen et al., 2008) and viviparous shark species since the energetic investment in reproduction may differ. ...
Marine heatwaves (MHW) have recently been proposed as more relevant in driving population changes than the continuous increase in average temperatures associated with climate change. The causal processes underpinning MHW effects in sharks are unclear but may be linked to changes in fitness caused by physiological trade-offs that influence the immune response. Considering the scarcity of data about the immune response of sharks under anomalous warming events, the present study analyzed several fitness indices and characterized the immune response (in the blood, epigonal organ, liver, spleen, and intestine) of temperate adult small-spotted catsharks (Scyliorhinus canicula) after a 30-day exposure to a Category II MHW. The results indicated that adult small-spotted catsharks have developed coping strategies for the MHW. Specifically, among the 35 parameters investigated, only the gonad-to-body ratio (GBR) and plasma glucose showed significant increases. In contrast, igm and tumor necrosis factor receptor (tnfr) gene expression in blood cells, tnfr in the epigonal organ, and the number of monocytes significantly decreased. Although a decline in immune function in small-spotted catsharks was revealed following the MHW exposure, energy mobilization restored homeostasis and indicated a shift in energy allocation towards reproduction. Group resilience may be due to the variable tolerance of individuals, the phenotypic plasticity of cellular immunity, thermal imprinting, and/or metabolic capacity of the individuals.
... Until recently, many elasmobranch studies have been conducted post-mortem, but it has been recognized that non-lethal sampling should replace these methods [11]. Semen collection, hormone analysis and ultrasound examinations on live specimens are becoming more prevalent for investigating the reproductive biology of elasmobranch species, including the southern stingray [7,12,13]. In addition, ultrasonography can be a useful tool in assessing body condition, an indicator of reproductive function in elasmobranch species [12]. ...
... Semen collection, hormone analysis and ultrasound examinations on live specimens are becoming more prevalent for investigating the reproductive biology of elasmobranch species, including the southern stingray [7,12,13]. In addition, ultrasonography can be a useful tool in assessing body condition, an indicator of reproductive function in elasmobranch species [12]. As liver size is a classic measure of body condition in elasmobranchs [13], researchers can use ultrasound as a non-invasive technique to establish body condition [14]. ...
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.
... Despite their importance for reproductive performance, energetic investments are rarely considered in studies of shark reproduction (e.g. Dudley and Cliff 1993;Hammerschlag et al. 2018;Rangel et al. 2021a). Furthermore, there are no published studies investigating the nutritional quality and dietary patterns of free-living male sharks across life-stages. ...
... As such, measuring hormones integrated with nutritional indicators can offer a great opportunity to non-lethally examine patterns of energy regulation across reproductive stages (e.g. Hammerschlag et al. 2018). Nutritional quality is one of the most important factors that influence reproductive performance in vertebrates, including those related to gamete quality (both eggs and sperm), fecundity, and offspring survival (Izquierdo et al. 2001;Wathes et al. 2007;Bobe and Labbé 2010). ...
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 female from August 2021 (ID 00543) that was not pregnant had similar levels of E 2 and P 4 as the pregnant female sampled in July 2022 (ID 00521). This has been observed in other species such as tiger sharks (Galeocerdo cuvier; Sulikowski et al., 2016;Hammerschlag et al., 2018) where hormone concentrations were found to be of similar levels between females in different reproductive stages. The low levels of E 2 concentrations exhibited by the pregnant female in this study (ID 00521) is consistent with the completion of ovulation (Awruch, 2013). ...
Effective management and conservation of threatened species biodiversity requires knowledge of reproductive biology, such as cyclicity, mode, and age at maturity. We combined reproductive endocrinology and in-situ ultrasonography to examine reproductive characteristics of female Caribbean reef sharks Carcharhinus perezi, a widely distributed, threatened marine predator which remains largely understudied throughout its range. Unique to this study was the opportunity to conduct longitudinal assessments of two individuals, recaptured across multiple seasons during sampling in The Bahamas. Within-individual, paired hormone analyses and in-situ ultrasounds of female sharks that were confirmed as either pregnant, non-pregnant, or reproductively active, suggest a biennial reproductive cycle for Carcharhinus perezi. This unique opportunity to assess the reproductive biology of the same individuals over time underscore the importance of repeated sampling for elucidating population reproductive cyclicity of highly mobile sharks in the wild.
... Of all these non-lethal methods, reproductive endocrinology, which measures the concentrations of hormones that act as either triggers or regulators of all aspects of reproduction, may be the most accurate and reliable to assess the reproductive biology and ecology in male and female elasmobranchs (29). The use of male and female steroid hormones to study reproduction has been on the rise in elasmobranchs under captive or semi-captive conditions (30-32), in wild individuals but using reproductive organ dissections from dead animals to validate plasma-based results (33)(34)(35)(36), or in the wild using completely non-lethal methods with the release of sharks at sea after blood sampling and using other complementary methods to validate plasma-based results of maturity (28,37,38). ...
Introduction: Overexploitation of sharks and the destruction of their habitat has led to severe population declines and the need for conservation and management actions. Effective conservation management requires knowledge of the size at which a shark matures and an understanding of their breeding season, fundamental information to maintain appropriate population levels.
Methods: Here we used reproductive endocrinology, estrogen and androgen steroids, in combination with rare direct observations of mating, visual monitoring of reproductive status such as gestation and mating scars, as well as parentage analysis, to assess reproductive biology in male and female Chondrichthyans from the wild.
Results and discussion: Lengths at sexual maturity of female and male blacktip reef sharks corresponded closely with plasma 17β-estradiol, testosterone and 11-ketotestosterone measures respectively, but we found considerable variation in androgen levels for mature males. Size at sexual maturity of male and female blacktip reef shark deduced from direct or indirect evidence (mating scars or parentage assignment respectively, corresponded closely with plasma 17β-estradiol, testosterone and 11-ketotestosterone measures respectively, but we found considerable variation in androgen levels for mature males. Females attained sexual maturity from around 121 to 123 cm and males from 104 to 111 cm. The mating season extends from September to February but female 17β-estradiol levels are elevated 1 month prior to mating. Endocrinology has brought additional important information to the reproductive biology and ecology of blacktip reef sharks.
... observed sexual dimorphism in anterior body scaling appears broadly consistent with existing literature regarding the spatial ecology of bull sharks, where selection would likely favour greater streamlining and drag reduction in adult males as a result of their increased dispersal potential relative to females and juveniles (Devloo-Delva et al., 2023),whereas this selective pressure may be comparatively weaker in adult females. Additionally, females may require greater energy stores than males due to the physiological and bioenergetic consequences of pregnancy(Hammerschlag et al., 2018). ...
Recent studies have uncovered mosaic patterns of allometric and isometric growth underlying ontogenetic shifts in the body form of elasmobranch species (shark and rays). It is thought that shifts in trophic and spatial ecology through ontogeny drive these morphological changes; however, additional hypotheses relating to developmental constraints have also been posed. The bull shark (Carcharhinus leucas) is a large-bodied coastal shark that exhibits strong ontogenetic shifts in trophic and spatial ecology. In this study, we utilise a large data set covering a large number of morphological structures to reveal ontogenetic shifts in the body form of C. leucas, stratifying analyses by sex and size classes to provide fine-scale, more ecomorpho-logically relevant results. Our results indicate shifts in functional demands across the body through ontogeny, driven by selective pressures relating to trophic and spatial ecology driving the evolution of allometry. We also find significant differences in scaling trends between life stages, and between the sexes, highlighting the importance of utilising large, diverse datasets that can be stratified in this way to improve our understanding of elasmobranch morphological evolution. Ultimately, we discuss the implications of these results for existing ecomorphological hypotheses regarding the evolution of specific morphological structures, and pose novel hypotheses where relevant.
... However, despite the wide range of strategies in this taxon, there is very limited research on Blank the various costs of these modes (Lawson et al., 2019(Lawson et al., , 2022. Our primary knowledge stems from bomb calorimetry of embryos and reproductive tissues (e.g., Lawson et al., 2022), assessing the relationship between hepatosomatic and gonadal somatic indices (HSI and GSI, respectively) that reflect energy storage and usage in relation to reproduction (e.g., Awruch et al., 2008;Hoffmayer et al., 2006), and measurements of circulating energetic blood markers in reproducing individuals (e.g., Hammerschlag et al., 2018;Rangel et al., 2021ab). However, these costs likely do not easily highlight temporal changes in reproductive energetic effort, which needs to be measured in the whole organism over time (Van Dyke and Beaupre 2011). ...
... Most of what is known about shark reproduction comes from post-mortem examinations (Whitney et al. 2004, Pratt et al. 2005) and the study of captive animals (Pratt & Carrier 2001), although a growing number of recent studies have presented data on shark reproductive ecology in situ using non-lethal approaches (e.g. Sulikowski et al. 2016, Hammerschlag et al. 2018. Circulating concentrations of the gonadal steroid hormone testosterone (T), for example, are often used to indicate reproductive stage and correlate well with seasonal spermatogenesis and copulation in male sharks. ...
Oceanic whitetip sharks Carcharhinus longimanus aggregate at Columbus Point, Cat Island, The Bahamas, in at least April and May. We show that signs of putative mating activity (i.e. bite wounds) on mature females, which dominate the aggregation, are exceedingly rare at that time, but may be more common in July. Male plasma testosterone concentrations also suggest that spermatogenesis occurs in April and May and copulation is underway or has just ended by July. We support these preliminary data with direct observations of putative precopulatory behavior made at Columbus Point in July 2019. Using 25 min of video footage from the event, we identify common shark mating behaviors such as echelon or parallel swimming, following, shielding, nosing, and biting. We also describe the ‘circle-back’, a newly observed behavior where the male orients to the trail of the female, possibly to investigate olfactory cues. Based on these 3 parallel lines of evidence, we hypothesize that mating could occur in the eastern Bahamas as early as May, but is probably concentrated in midsummer (i.e. July), and that Columbus Point, Cat Island, may be a mating habitat for the oceanic whitetip shark.
... In their reproductive cycle, tiger sharks exhibit long gestation periods (12-16 months), producing relatively large broods (3-70) of large-sized offspring (∼ 75 cm in total length; Whitney and Crow 2007; Castro 2011). It has been suggested that females reproduce every 2 (i.e., biennial cycle (Castro 2009)) or 3 years (i.e., triennial cycle (Whitney and Crow 2007)), and they seem to use a mixed capital-income breeding strategy, relying on a mix of energy stores and recently acquired resources to support reproduction (Hammerschlag et al. 2018;Rangel et al. 2021). ...
Although many shark species display predictable and seasonal aggregations related to breeding activities, few studies have reported direct evidence of reproductive interactions of large sharks. In this context, the present study reports the first evidence of mating scars in female tiger sharks Galeocerdo cuvier at the Fernando de Noronha Archipelago (FEN), an oceanic remote insular system in the South Atlantic Ocean. Results from the records of seven wounded females suggest that mating activity may occur between February and August. These females measured between 267 and 372 cm in total length, which is aligned with previous studies reporting size at sexual maturity for Atlantic tiger sharks. Although some females exhibited healed wounds, three of them had fresh, open wounds. One of the females also had a swollen and red cloaca. We also report the first presumably gravid female tiger shark for the region. Although sporadic, the observations herein reported indicate the importance of FEN for tiger shark reproduction in western equatorial Atlantic waters. This finding is especially relevant as FEN has been identified as an important genetic hotspot for tiger sharks, with the largest global genetic diversity for the species.
... Hematology is a very useful tool to perform physiological assessment of health status in fish, given the ease of collection and analysis of the samples, the little impact it generates on the life quality of the individuals, and its complementarity with other evaluation and diagnosis routine practices (Walsh and Luer, 2004;Semeniuk et al., 2009;Oliveira et al., 2012Oliveira et al., , 2015. Analysis of blood constants has been used in fish as stress and disease indicators, for diets analysis, to establish individual and population variations (Adams et al., 2003;Semeniuk et al., 2009;Jerome et al., 2018), as well as to characterize metabolic and adaptive physiological strategies related to environmental variations (Gallagher et al., 2014;Oliveira et al., 2016a,b;Hammerschlag et al., 2018;Lambert et al., 2018). Similarly, studies on qualitative and quantitative characteristics of leukocytes may indicate particularities of the immune system of a given species or population (Tavares-Dias and Moraes, 2007;Sueiro et al., 2019). ...
Hematological and blood biochemical reference information is important to establish physiological status of freshwater stingray populations and improve care and management protocols in artificial environments. Here, we used a commercial freshwater stingray with high mortality rates in the market (Potamotrygon magdalenae), as an example to understand how artificial environments and handling protocols influence physiological status of captive freshwater stingrays. To this purpose, blood from five adult males and six adult females was collected to perform complete blood counts and blood chemistry analyses. All sampled animals showed good body condition with no differences between sexes. Differences between sexes were only found for the differential count of lymphocytes. Red blood results were consistent with previously studied potamotrygonids while white blood results showed higher values of leukocytes, thrombocytes, heterophils and lymphocytes in P. magdalenae compared to other Potamotrygonids. All types of leukocytes described for elasmobranchs were found except neutrophils and basophils. Blood metabolites showed an influence of ex situ diet in total protein, triglycerides and cholesterol. Glucose results were consistent while urea showed lower levels than those recorded for other freshwater stingrays. These results highlight the importance of physical, physiological and health analysis in freshwater stingrays as a part of welfare assessment to improve monitoring protocols and survival rates in public or private aquaria.
... Aines et al., 2018;Dicken et al., 2017). Recent studies showed that despite being an opportunistic forager, their dietary patterns, nutritional and metabolic condition are life stage-dependent, suggesting female tiger shark can adjust their nutritional and metabolic requirement during reproduction (Hammerschlag et al., 2018;Rangel et al., 2021b). ...
How varying levels of human activity, such as proximity and size of the nearest market (i.e., market gravity), influence the nutritional ecology and physiological condition of highly migratory marine predators is poorly understood. In the present study, we used a non-lethal approach to compare the concentration of metabolic hormones (i.e. corticosteroids and thyroid hormones) and plasma fatty acids between juvenile female tiger sharks (Galeocerdo cuvier) sampled in two areas of the subtropical north Atlantic, which differed markedly in their levels of coastal urbanization, Florida and the Bahamas (high versus low, respectively). We hypothesized that juvenile female tiger sharks sampled in water surrounding high coastal urbanization (Florida), would exhibit evidence of lower prey quality and higher energetic demands as compared to individuals sampled in relatively less urbanized areas of Northern Bahamas. Results revealed that relative corticosteroid levels (a proxy for energy mobilization) were higher in juvenile female tiger sharks sampled in Florida; however, no differences were found in concentrations of thyroid hormones (proxies of energetic adjustments) between the two locations. We found higher percentages of omega-3 polyunsaturated fatty acids (indicative of high prey quality) in juvenile tiger sharks from Florida, whereas higher percentages of bacterial markers (often indicative of domestic sewage effluent) were detected in the individuals sampled in the Bahamas. Taken together, these findings do not suggest that the differences in nutritional quality and metabolic condition found between the two sampling locations can be fully attributed to foraging in areas exposed to differing levels of urbanization. We speculate that these patterns may be due to the highly migratory nature and generalist feeding strategy of this species, even at the juvenile life stage, as well as proximity of sampling locations from shore.
... Reproductive strategies, however, differ markedly between cheloniids, and the mobulids and carcharhinids. Whereas mobulids and carcharhinids are live-bearing, producing on average 1-5 pups per breeding event (Wetherbee et al., 1997;Ward-Paige et al., 2010;Marshall et al., 2011;Whitney et al., 2012), characteristic of slow life histories [Stearns, 1992; but note that, e.g., the tiger shark Galeocerdo cuvier can produce up to 80 pups per breeding event (Hammerschlag et al., 2018)], cheloniids can lay hundreds of eggs within one nesting season (Heppell et al., 1996a,b;Miller, 1997;Broderick et al., 2003), characteristic of fast life histories (Stearns, 1992). These large differences in reproductive strategy lead to large differences in juvenile mortality rates, which are relatively low for mobulids and carcharhinids, characteristic of slow life histories [Stearns, 1992; but note again that juvenile mortality is high in the tiger shark (Ward-Paige et al., 2010)], and very high for cheloniids (Heppell et al., 1996a,b;Miller, 1997;Broderick et al., 2003), characteristic of fast life histories (Stearns, 1992). ...
Understanding why different life history strategies respond differently to changes in environmental variability is necessary to be able to predict eco-evolutionary population responses to change. Marine megafauna display unusual combinations of life history traits. For example, rays, sharks and turtles are all long-lived, characteristic of slow life histories. However, turtles also have very high reproduction rates and juvenile mortality, characteristic of fast life histories. Sharks and rays, in contrast, produce a few live-born young, which have low mortality rates, characteristic of slow life histories. This raises the question if marine megafaunal responses to environmental variability follow conventional life history patterns, including the pattern that fast life histories are more sensitive to environmental autocorrelation than slow life histories. To answer this question, we used a functional trait approach to quantify for different species of mobulid rays, cheloniid sea turtles and carcharhinid sharks – all inhabitants or visitors of (human-dominated) coastalscapes – how their life history, average size and log stochastic population growth rate, log(λs), respond to changes in environmental autocorrelation and in the frequency of favorable environmental conditions. The faster life histories were more sensitive to temporal frequency of favourable environmental conditions, but both faster and slower life histories were equally sensitive, although of opposite sign, to environmental autocorrelation. These patterns are atypical, likely following from the unusual life history traits that the megafauna display, as responses were linked to variation in mortality, growth and reproduction rates. Our findings signify the importance of understanding how life history traits and population responses to environmental change are linked. Such understanding is a basis for accurate predictions of marine megafauna population responses to environmental perturbations like (over)fishing, and to shifts in the autocorrelation of environmental variables, ultimately contributing toward bending the curve on marine biodiversity loss.
... This behavior may thus present a different prey base 11 , or ambient concentrations of metals in the water column (i.e., if the primary pathway of metal accumulation is through the gills). As sharks reach sexual maturity, energetic requirements associated with reproduction may increase overall daily energy budgets 44 , requiring individuals to consume a greater biomass of potentially higher trophic position prey items. Although we were unable to definitively test this hypothesis within the confines of this study, ecogeochemical tracer techniques such as stable isotope and fatty acid analyses may provide insight into whether resource-use shifts are in fact occurring between size classes. ...
Over the last century anthropogenic activities have rapidly increased the influx of metals and metalloids entering the marine environment, which can bioaccumulate and biomagnify in marine top consumers. This may elicit sublethal effects on target organisms and have broad implications for human seafood consumers. We provide the first assessment of metal (Cd, Pb, Cr, Mn, Co, Cu, Zn, As, Ag, and THg) and metalloid (As) concentrations in the muscle tissue of coastal sharks from The Bahamas. A total of 36 individual sharks from six species were evaluated, spanning two regions/study areas, with a focus on the Caribbean reef shark (Carcharhinus perezi), and to a lesser extent the tiger shark (Galeocerdo cuvier), due their high relative abundance and ecological significance throughout coastal Bahamian and regional ecosystems. Caribbean reef sharks exhibited some of the highest metal concentrations compared to five other species, and peaks in the concentrations of Pb, Cr, Cu, Zn, and Ag were observed as individuals reached sexual maturity. Observations were attributed to foraging on larger, more piscivorous prey, high longevity, as well a potential slowing rate of growth. We observed correlations between some metals, which are challenging to interpret but may be attributed to trophic level and ambient metal conditions. Our results provide the first account of metal concentrations in Bahamian sharks, suggesting individuals exhibit high concentrations which may potentially cause sublethal effects. Finally, these findings underscore the potential toxicity of shark meat and have significant implications for human consumers.
... Elevated δ 15 N can also inaccurately represent the trophic interactions of neonate and young-of-the-year individuals (McMeans et al. 2009;Olin et al. 2018). Additionally, many species also undergo long distance migrations for breeding, which can lead to depletions in body reserves through heightened catabolic activity that cause enrichment in 15 N, particularly for animals that limit foraging activity during these migrations (Fleming et al. 2018;Hammerschlag et al. 2018). Similar to addressing the potential effects of ontogenetic niche shifts, assessing the ecological and life history characteristics of a study species prior to sampling will greatly enhance abilities to interpret stable isotope data after analysis, and sampling should be conducted for each sex across different reproductive stages to determine the potential impacts of the issues discussed. ...
The development of the isotopic niche, an n-dimensional hypervolume (with n being the number of isotopes) occupied by a population in delta-space, has revolutionized the study of animal interactions in wild populations. While the isotopic niche offers a useful means to understand interactions at many ecological resolutions (e.g., individual, population, community, ecosystem), a variety of intrinsic and extrinsic factors drive isotopic variability and influence the ultimate geometry of observed niche dimensions. Here, we provide an updated synthesis to guide the application of bulk stable isotope ratios to study ecological niches. We summarize progress in the application of bulk stable isotope ratios for evaluating niches to synthesize a formal definition of the isotopic niche. We identify six broad categories to describe drivers of isotopic variance introduced by the animal, its environment, and the researcher, and provide recommendations to account for such variations before, during, and after sample collection and data analyses. Our synthesis illustrates the considerations that should be made before employing the isotopic niche to describe trophic ecology, and guidance for the use and interpretation of isotopic niche dynamics in future studies.
... In addition to consumptive effects, predation risk can induce plastic and/or genetic alterations in prey traits, including changes in prey behavior [29], morphology [30], life history [31], and physiology [32]. Such risk effects can also initiate trophic cascades [33,34]. ...
Arguments for the need to conserve aquatic predator (AP) populations often focus on the ecological and socioeconomic roles they play. Here, we summarize the diverse ecosystem functions and services connected to APs, including regulating food webs, cycling nutrients, engineering habitats, transmitting diseases/parasites, mediating ecological invasions, affecting climate, supporting fisheries, generating tourism, and providing bioinspiration. In some cases, human-driven declines and increases in AP populations have altered these ecosystem functions and services. We present a social ecological framework for supporting adaptive management decisions involving APs in response to social and environmental change. We also identify outstanding questions to guide future research on the ecological functions and ecosystem services of APs in a changing world.
Nitrogen isotope (δ15N) analysis of bulk tissues and individual amino acids (AA) can be used to assess how consumers maintain nitrogen balance with broad implications for predicting individual fitness. For elasmobranchs, a ureotelic taxa thought to be constantly nitrogen limited, the isotopic effects associated with nitrogen-demanding events such as prolonged gestation remain unknown. Given the linkages between nitrogen isotope variation and consumer nitrogen balance, we used AA δ15N analysis of muscle and liver tissue collected from female bonnethead sharks (Sphyrna tiburo, n = 16) and their embryos (n = 14) to explore how nitrogen balance may vary across gestation. Gestational stage was a strong predictor of bulk tissue and AA δ15N values in pregnant shark tissues; decreasing as individuals neared parturition. This trend was observed in trophic (e.g., Glx, Ala, Val), source (e.g., Lys), and physiological (e.g., Gly) AAs. Several potential mechanisms may explain these results including nitrogen conservation, scavenging, and bacterially mediated breakdown of urea to free ammonia that is used to synthesize AAs. We observed contrasting patterns of isotopic discrimination in embryo tissues, which generally became enriched in 15N throughout development. This was attributed to greater excretion of nitrogenous waste in more developed embryos, and the role of physiologically sensitive AAs (i.e., Gly and Ser) to molecular processes such as nucleotide synthesis. These findings underscore how AA isotopes can quantify shifts in nitrogen balance, providing unequivocal evidence for the role of physiological condition in driving δ15N variation in both bulk tissues and individual AAs.
Given climate change threats to ecosystems, it is critical to understand the responses of species to warming. This is especially important in the case of apex predators since they exhibit relatively high extinction risk, and changes to their distribution could impact predator–prey interactions that can initiate trophic cascades. Here we used a combined analysis of animal tracking, remotely sensed environmental data, habitat modeling, and capture data to evaluate the effects of climate variability and change on the distributional range and migratory phenology of an ectothermic apex predator, the tiger shark (Galeocerdo cuvier). Tiger sharks satellite tracked in the western North Atlantic between 2010 and 2019 revealed significant annual variability in the geographic extent and timing of their migrations to northern latitudes from ocean warming. Specifically, tiger shark migrations have extended farther poleward and arrival times to northern latitudes have occurred earlier in the year during periods with anomalously high sea-surface temperatures. A complementary analysis of nearly 40 years of tiger shark captures in the region revealed decadal-scale changes in the distribution and timing of shark captures in parallel with long-term ocean warming. Specifically, areas of highest catch densities have progressively increased poleward and catches have occurred earlier in the year off the North American shelf. During periods of anomalously high sea-surface temperatures, movements of tracked sharks shifted beyond spatial management zones that had been affording them protection from commercial fishing and bycatch. Taken together, these study results have implications for fisheries management, human–wildlife conflict, and ecosystem functioning.
Intraspecific variability in life-history patterns is well documented in elasmobranchs, and defining regionally specific parameters is essential for proper management and sustainability of species. Studies on the reproductive biology of finetooth sharks (Carcharhinus isodon) have noted a potential disparity in periodicity within North American waters. To better define regional variability, the current study collected 1490 finetooth sharks (831 female, 659 male) from the northern Gulf of Mexico. The size-at-maturity was determined to be 995- and 961-mm fork length for females and males respectively. In males, the peak gonadosomatic index (GSI) in March and presence of semen in the seminal vesicles in April suggested spermatogenesis occurs from March to April. In females, ovulation occurred from May to June, with a peak GSI occurring in May and maximum vitellogenic follicle diameter occurring in May and June. Gestation was found to be 11–12 months, with parturition occurring in May and June and a mean brood size was 3.8±0.1 embryos. Of the 50 females examined during the ovulatory period, 32 exhibited annual and 18 exhibited biennial reproductive periodicity. The results from this study will be impactful, because regionally distinct reproductive parameters can now be considered for future assessments.
Physiological adaptations have evolved to help sharks face rapid periods of feast. Tiger sharks are generalist apex predators that rely on a high-lipid/protein diet. To achieve a satisfactory nutritional condition, proper lipid absorption and hepatic storage are needed. Bile secretion in sharks is low and sporadic but increases during short periods of fasting. The present study describes a physiological impairment caused by bile accumulation in juvenile tiger sharks, possibly due to prolonged fasting. These evidences suggest that, even though sharks have adaptations that prevent them from dying from starvation, alarming physiological alterations might occur. Future studies are needed to assess how such a condition can affect wild populations, as well as possible sublethal consequences that could impact their long-term survival.
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.
Elasmobranch fishes (sharks, skates, and rays) are particularly susceptible to anthropogenic threats, making a thorough understanding of their life history characteristics essential for proper management. Historically, elasmobranch reproductive data have been collected by lethal sampling, an approach that is problematic for threatened and endangered species. However, recent studies have demonstrated that non-lethal approaches can be as effective as lethal ones for assessment of the reproductive status of an animal. For example, plasma has been used to examine concentrations of steroid hormones. Additionally, skeletal muscle tissue, which can be obtained non-lethally and with minimal stress, can also be used to quantify concentrations of steroid hormones. Skeletal muscle progesterone, testosterone, and estradiol concentrations were determined to be statistically significant indicators of reproductive status in the oviparous Leucoraja erinacea, the yolk-dependent viviparous Squalus acanthias, and the yolk-sac placental viviparous Rhizoprionodon terraenovae. The results of the present study demonstrate that steroid hormones present in non-lethally harvested skeletal muscle tissue can be used as reliable indicators of reproductive status in elasmobranchs.
How are tiger shark embryos nourished to large size without a placental connection? Tiger sharks belong to the family Carcharhinidae, and all carcharhinid sharks are placental with the exception of the tiger shark. The aim of this study was to test the hypothesis that tiger shark embryos are nourished to large size by imbibing a clear uterine fluid found in their egg cases. Based on weights of fertilized eggs and of term embryos, the tiger shark is a matrotrophic species, and its embryos appear to reach gains of 2119% in wet weight and 1092% in dry weight during gestation. By measuring the total energy content of the fluid in the egg case by chemical oxygen demand (COD), the authors demonstrate that clear liquid in the tiger shark egg case is an energy-rich embryotrophe that nourishes the embryos to large size. We suggest that the process be termed ‘embryotrophy'. The process appears to be an adaptation for producing large broods of large embryos in a species lacking a placental connection.
Advancing our knowledge of the reproductive biology and mating systems of freeranging sharks is inherently challenging. The large size and mobility of the specimens are just a few of the problems that make such studies complicated, and in some respects, impractical. The tiger shark Galeocerdo cuvier is a large, roving, apex predator found in many oceans throughout the world. Although their nomadic nature is primarily linked to large-scale migrations, these sharks can also display site fidelity. One site where this is known to occur is at Tiger Beach, Bahamas. Unique to the waters of this area is the consistent sighting of large females. While the sex-specific use of the area remains unknown, the shallow, warm environment could represent a critical habitat for reproductive events. To investigate the reproductive biology of tiger sharks at Tiger Beach, 65 individuals were opportunistically sampled between 2011 and 2014. Reproductive status of captured females (n = 59) was assessed with ultrasonography and by measuring circulating sex steroid hormones (progesterone, testosterone and estradiol). Our results indicate that Tiger Beach is a high-use site for female tiger sharks of mixed life stages. The results also suggest that Tiger Beach may function as a refuge habitat, allowing females to reach maturity free from male mating harassment, as well as functioning as a gestation ground where gravid females can benefit from year-round calm warm waters, which may reduce the gestation period and accelerate embryo development.
Identification of the importance of habitats that are frequently used by any species is essential to a complete understanding of the species' biology and to incorporate their ecological role into conservation and management programmes. In this con-text, the present study investigated whether Tasmanian coastal waters have any reproductive relevance for the broadnose sevengill shark (Notorynchus cepedianus). Although this species is a large coast-associated apex predator in these areas, there is a complete gap in understanding the role that these coastal systems could play in its reproduction. Reproductive hormones were used as a non-lethal method to address the reproductive biology of this species. Females seemed to have at least a bi-annual reproductive cycle, being pregnant for ~1 year and spending at least 1 year non-pregnant, with the ovulatory cycle separated from gestation. Mature females were found to be ovulating, in the initial stages of pregnancy, resting or starting a new vitellogenic cycle. Notorynchus cepedianus did not use these coastal habitats for mating or as a pupping ground. Although the mating season was distinguished between September to April, only 22% of males showed mating scars during the peak of the mating period and no near-term pregnant females were observed. Thus, despite these coastal waters being an important foraging ground for this species, these areas did not have any reproductive relevance. In consequence, future management and conservation planning programmes need to identify whether there are other areas in Tasmania that play a critical role for reproductive purposes in this species. Finally, although previous studies have linked reproductive hormones with external examination of the gonads to validate the use of steroids as a non-lethal tool to address reproduction, the present study used this methodology without killing any animals. This has important implications for conservation programmes of threatened and endangered species worldwide where the methodology cannot be validated. Cite as: Awruch CA, Jones SM, García Asorey M, Barnett A (2014) Non-lethal assessment of the reproductive status of broadnose sevengill sharks (Notorynchus cepedianus) to determine the significance of habitat use in coastal areas. Conserv Physiol 2: doi:10.1093/conphys/cou013.
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.
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.
This study analyses the sexual activity and segregation of sand tiger sharks, Carcharias taurus, from Anegada Bay (Argentina). Reproduction-linked movements along the South American Atlantic coast were inferred from data from several SW Atlantic localities. Male sand tigers (n=162) matured at 193 cm total length (LT). Females (n=77) matured between 218 and 235 cm LT. These figures are similar to those from other populations, although size-at-maturity of males was slightly different from South African and Australian populations. In females, the size of ovarian follicles was positively correlated with gonadosomatic index and negatively correlated with hepatosomatic index, while the liver was significantly larger than in males. Sand tiger sharks were present in Anegada Bay from December to April. Males were significantly more abundant than females (2:1). Significant differences in reproductive condition through time were observed in males. During January and February males had seminal vesicles full of spermatozeugmata but by March and April the vesicles were empty. As the proportion of males with a lighter colouration peaked from January to March, it is very likely that mating takes place during January and February. The skewed sex-ratio during the mating season indicates a possible strong competition for mates among males, as observed in captivity. Males, females and some juveniles occur in Argentinean and Uruguayan waters, where mating takes place. Pregnant females occur in subtropical waters of southern Brazil, where they give birth. Given that pregnant and non-pregnant females occur at the same time in different zones, we suggest that the female reproductive cycle is biennial. Striking differences among migratory patterns of sand tiger sharks from the SW and NW Atlantic and South Africa were observed. © 2002 International Council for the Exploration of the Sea. Published by Elsevier Science Ltd. All rights reserved.
Little is known about the long-term movement patterns of most marine apex predators. A network of acoustic receivers was used to quantify the long-term movements of transmitter-equipped tiger sharks Galeocerdo cuvier Peron & Lesueur, 1822 in the Main Hawaiian Islands. Tiger sharks were wide-ranging, swam between islands and patrolled up to 109 km of contiguous coastline. Visits to specific acoustic receiver sites were typically brief (mean duration 3.3 min), unpredictable and interspersed by absences of weeks, months or years. This pattern may be an optimal foraging strategy for capturing risk-averse prey. Tiger sharks may have to move on soon after arriving in an area because the element of surprise is quickly lost and potential prey become wary and difficult to catch. Juvenile tiger sharks were significantly wider-ranging and less frequently detected than mature females. Juveniles may be avoiding predation by larger individuals, or exploring to find suitable home ranges. Tiger sharks may also switch movement patterns and foraging strategies to take advantage of different prey types, restricting their movements to exploit seasonally abundant and naive prey. Further empirical studies are required to directly link movement patterns with foraging.
Many species undertake long-distance annual migrations between foraging and reproductive areas. Such migrants depend on the efficient packaging, storage and utilization of energy to succeed. A diverse assemblage of organisms accomplishes this through the use of lipid reserves; yet, it remains unclear whether the migrations of elasmobranchs, which include the largest gill breathers on Earth, depend on such a mechanism. We examine depth records from pop-up satellite archival tags to discern changes in buoyancy as a proxy for energy storage in Eastern Pacific white sharks, and assess whether lipid depletion fuels long-distance (approx. 4000 km) migrations. We develop new algorithms to assess body condition, buoyancy and drift rate during drift dives and validate the techniques using a captive white shark. In the wild, we document a consistent increase in drift rate over the course of all migrations, indicating a decrease in buoyancy caused by the depletion of lipid reserves. These results comprise, to our knowledge, the first assessment of energy storage and budgeting in migrating sharks. The methods provide a basis for further insights into using electronic tags to reveal the energetic strategies of a wide range of elasmobranchs.
1. There has been considerable debate over the past decade with respect to wildlife provisioning, especially resultant behavioural changes that may impact the ecological function of an apex predator. The controversy is exemplified by the shark diving industry, where major criticisms based on inference, anecdote and opinion stem from concerns of potential behaviourally mediated ecosystem effects because of ecotourism provisioning (aka‘chumming’ or feeding).
2. There is a general lack of empirical evidence to refute or support associated claims. The few studies that have investigated the behavioural impacts of shark provisioning ecotourism have generated conflicting conclusions, where the confidence in such results may suffer from a narrow spatial and temporal focus given the highly mobile nature of these predators. There is need for studies that examine the potential behavioural consequences of provisioning over ecologically relevant spatial and temporal scales.
3. To advance this debate, we conducted the first satellite telemetry study and movement analysis to explicitly examine the long-range migrations and habitat utilization of tiger sharks (Galeocerdo cuvier) originating in the Bahamas and Florida, two areas that differ significantly with regards to the presence/absence of provisioning ecotourism.
4. Satellite telemetry data rejected the behaviourally mediated effects of provisioning ecotourism at large spatial and temporal scales. In contrast, to the restricted activity space and movement that were hypothesized, geolocation data evidenced previously unknown long-distance migrations and habitat use for both tiger shark populations closely associated with areas of high biological productivity in the Gulf Stream and subtropical western Atlantic Ocean. We speculate that these areas are likely critically important for G. cuvier feeding forays and parturition.
5. We concluded that, in the light of potential conservation and public awareness benefits of ecotourism provisioning, this practice should not be dismissed out of hand by managers. Given the pressing need for improved understanding of the functional ecology of apex predators relative to human disturbance, empirical studies of different species sensitivities to disturbance should be used to guide best-practice ecotourism policies that maximize conservation goals.
Energy storage is an important component of life-history variation. Some organisms ("income breeders") fuel reproductive expenditure by simultaneous feeding, whereas others ("capital breeders") fuel reproduction from energy gained earlier, and stored prior to use. Most published discussions of this topic have focused primarily on endothermic animals (birds and mammals), and have interpreted the costs and benefits of these alternative breeding tactics in the context of endothermy. The far more diverse array of ectothermic animals has received less attention in this respect. Many features associated with ectothermy preadapt organisms to store energy for long periods prior to use (i.e. to rely on "capital" rather than "income"). For example, birds and mammals experience high costs (in terms of mobility and thermoregulatory efficiency) if they store large body reserves. By contrast, the energetic and demographic costs associated with storage, maintenance, and utilisation of body reserves are low in many ectotherms. Thus, capital breeding (which may also be more efficient energetically in many situations) is extremely common in these low energy systems. Ectotherms comprise the most extreme examples of capital breeders, with a strong tendency towards semelparity where the capital of reserves is massively invested into a single reproductive event. Overall, theoretical and empirical studies of the evolution of capital versus income breeding as alternative strategies of resource use should take account of the important role played by alternative thermoregulatory and metabolic systems. The acquisition of endothermy in avian and mammalian lineages has involved a massive shift towards reliance on "income breeding", and the full spectrum of life-history variation in this respect cannot be appreciated without detailed examination of ectothermic organisms.
Abstract Fatty acid (FA) analysis is a tool for dietary investigation that complements traditional stomach content analyses. Controlled feeding experiments were used to determine the extent to which the FA composition of diet is reflected in the liver and muscle tissue of the Port Jackson shark Heterodontus portusjacksoni. Over 10 wk, two groups of sharks were fed prawns or squid, which have distinct FA profiles. The percentage of total FA was significantly different for shark liver and muscle tissue when comparing controls with prawn- and squid-fed sharks. Compared with experimentally fed sharks, control shark muscle and liver had higher levels of 18:1n-9 and 20:2n-9. When comparing prawn- and squid-fed sharks, only liver tissue showed a significant difference in FA profiles. The livers of prawn-fed sharks were comparatively higher in 18:1n-7, 22:5n-3, 20:0, and 18:1n-9, while the squid-fed sharks had higher levels of 16:0 and 22:6n-3. These FAs in shark liver tissue were all reflective of higher amounts in their respective dietary items, demonstrating the conservative transfer of FA from diet to liver tissue. This study shows that liver and muscle FA profiles can be used as indicators of dietary change through the comparison of controls and fed sharks. The timescale of this study may not have been sufficient for capturing the integration of FA into muscle tissue because only liver FA profiles were useful to distinguish between sharks fed different diets. These findings have important implications for sampling design where FA profiles are used to infer dietary preferences.
▪ Abstract The functional causes of life history trade-offs have been a topic of interest to evolutionary biologists for over six decades. Our review of life history trade-offs discusses conceptual issues associated with physiological aspects of trade-offs, and it describes recent advances on this topic. We focus on studies of four model systems: wing polymorphic insects, Drosophila, lizards, and birds. The most significant recent advances have been: (a) incorporation of genetics in physiological studies of trade-offs, (b) integration of investigations of nutrient input with nutrient allocation, (c) development of more sophisticated models of resource acquisition and allocation, (d) a shift to more integrated, multidisciplinary studies of intraspecific trade-offs, and (e) the first detailed investigations of the endocrine regulation of life history trade-offs.
The tiger shark (Galeocerdo cuvier) is the largest shark in the family Carcharhinidae and the only carcharhinid with aplacental viviparous (ovoviviparous) reproduction.
Despite its size and prevalence, many details of tiger shark reproductive biology are unknown. Size at maturity and litter
size have been reported by several authors, but a lack of large numbers of pregnant females has made it difficult to determine
gestation period, seasonality, and timing of the female reproductive cycle. Here we analyze data from shark control program
fishing and incidental catches in Hawaii (n=318) to construct the most complete picture of tiger shark reproduction to date. Males reached maturity at approximately
292cm total length (TL) based on clasper calcification, whereas females matured between 330 and 345cm TL based on oviducal
gland and uterus widths. Litter sizes ranged from 3 to 57 with a mean of 32.6 embryos per litter. Data from 23 litters from
various months of the year indicate that tiger sharks are usually 80–90cm TL at birth, and that the gestation period is 15–16
months. Mating scars were observed in January–February and sperm is presumably stored for 4–5months until ovulation takes
place in May–July. Gestation begins in June–July and pups are born in September–October of the following year. Our data suggest
that female tiger sharks in Hawaii give birth only once every three years. This could have major implications for conservation
and management of this species, as it suggests that tiger shark fecundity is 33% lower than previously thought. This could
greatly reduce the ability of this species to rebound from fishing pressure.
Energy storage is an important component of life-history variation. A distinction is recognized between species that provision offspring using energy gained concurrently (income breeders) and those that provision offspring using energy stores accumulated at an earlier time (capital breeders). Although this distinction has been recognized for some time, surprisingly little attention has been paid to the general adaptive value of the 2 strategies. Here, we present a simple, general framework for modeling female reproductive strategies. We show that our framework can be applicable either to annual breeders that aim to maximize the energy delivered to their offspring before independence, or to species with shorter reproductive cycles that aim to maximize reproductive rate, given that their offspring must build up a given level of reserves before independence. For both scenarios, we show that the costs of accumulating capital can lead to pure income breeding, pure capital breeding, or a mixture of the 2 strategies. Our model allows the effects of a variety of parameters to be assessed. Length of gestation, offspring metabolism, efficiency of energy transfer from mother to offspring, and the relative rates of energy gain by females with and without offspring are all important factors. The cost associated with accumulated capital is a particularly critical determinant of the strategy adopted. More detailed approaches to specific systems may provide a greater understanding of the factors promoting different maternal strategies for offspring provisioning. Copyright 2007.
During reproduction, male vertebrates may exhibit a continuum of interactions between sex and adrenal steroids during stressful events, the outcome of which may be important in either reducing or promoting male reproductive success. We studied adult male green turtles (Chelonia mydas) to examine if they altered plasma corticosterone (CORT) and androgen levels in response to a standardized capture/restraint stressor as potential mechanisms to maintain reproductive activity during stressful events. At the population level, we found that migrant breeding males had a significantly smaller CORT response to the capture/restraint stressor compared to nonbreeding males and that this decreased response coincided with the generally poorer body condition of migrant breeders. In contrast, plasma androgen levels decreased significantly in response to the capture/restraint stressor in migrant breeding males, but not in nonbreeding and pre-migrant breeding males. For individual migrant breeding males, the magnitude of their CORT and androgen responses to the capture/restraint stressor was highly correlated with their body condition and body length, respectively. Our results demonstrate that male green turtles exhibit complex interactions in their endocrine responses to a capture/restraint stressor and that variation in these interactions is associated with differences in males' reproductive, energetic, and physical state. We hypothesize that interplay between physical status and plasma hormone responses to stressors could have important consequences for male green turtle reproduction.
During avian egg production, oestrogen mediates marked increases in hepatic lipid production and changes in the diameter of assembled very-low density lipoprotein (VLDL). A nearly complete shift from generic VLDL ( approximately 70 nm in diameter), which transports lipids to peripheral tissues, to yolk-targeted VLDL (VLDLy) ( approximately 30 nm), which supplies the yolk with energy-rich lipid, has been observed in the plasma of laying domestic fowl. We validated an established dynamic laser scattering technique for a passerine songbird Taeniopygia guttata, the zebra finch, to characterize the dynamics of VLDL particle diameter distribution in relation to egg production. We predicted that non-gallinaceous avian species that have not been selected for maximum egg production would exhibit less dramatic shifts in lipid metabolism during egg production. As predicted, there was considerable overlap between the VLDL particle diameter distributions of laying and non-laying zebra finches. But unexpectedly, non-laying zebra finches had VLDL diameter distributions that peaked at small particles and had relatively few large VLDL particles. As a result, laying zebra finches, in comparison, had diameter distributions that were shifted towards larger VLDL particles. Nevertheless, laying zebra finches, like laying chickens, had larger proportions of particles within proposed VLDLy particle diameter ranges than non-laying zebra finches (e.g. sVLDLy: 50% vs 37%). Furthermore, zebra finches and chickens had similar modal (29.7 nm in both species) and median (32.7 nm vs 29.6 nm) VLDL particle diameters during egg production. Therefore, although zebra finches and chickens exhibited opposing directional shifts in VLDL particle diameter distribution during egg production, the modifications to VLDL particle structure in both species resulted in the realization of a common goal, i.e. to produce and maintain a large proportion of small VLDL particles of specific diameters that are capable of being incorporated into newly forming egg yolks.
For organisms with complex life cycles, variation among individuals in traits associated with survival in one life-history stage can strongly affect the performance in subsequent stages with important repercussions on population dynamics. To identify which individual attributes are the most influential in determining patterns of survival in a cohort of reef fish, we compared the characteristics of Pomacentrus amboinensis surviving early juvenile stages on the reef with those of the cohort from which they originated. Individuals were collected at hatching, the end of the planktonic phase, and two, three, four, six and eight weeks post-settlement. Information stored in the otoliths of individual fish revealed strong carry-over effects of larval condition at hatching on juvenile survival, weeks after settlement (i.e. smaller-is-better). Among the traits examined, planktonic growth history was, by far, the most influential and long-lasting trait associated with juvenile persistence in reef habitats. However, otolith increments suggested that larval growth rate may not be maintained during early juvenile life, when selective mortality swiftly reverses its direction. These changes in selective pressure may mediate growth-mortality trade-offs between predation and starvation risks during early juvenile life. Ontogenetic changes in the shape of selectivity may be a mechanism maintaining phenotypic variation in growth rate and size within a population.
A major challenge in biology is understanding how organisms partition limited resources among physiological processes. For example, offspring production and self-maintenance are important for fitness and survival, yet these critical processes often compete for resources. While physiological trade-offs between reproduction and immune function have been documented, their regulation remains unclear. Most current evidence suggests that physiological changes during specific reproductive states directly suppress various components of the immune system; however, some studies have not found this clear relationship. We performed two experiments in female tree lizards (Urosaurus ornatus) that demonstrate the presence of trade-offs between the reproductive and immune systems under controlled laboratory conditions. These results also support the hypothesis that these trade-offs are a facultative response to resource availability and are not obligatory responses to physiological changes during reproduction. We found that (1) experimentally increasing reproductive investment under limited resources resulted in suppressed immune function and (2) experimentally limiting resources resulted in immunosuppression but only during resource costly reproductive activities. There seems to be a critical balance of resources that is maintained between multiple processes, and changes in the balance between energy intake and output can have major consequences for immune function.
Knowledge of the diel spatial ecology of wild animals is of great interest to ecologists and relevant to resource management and conservation. Sharks are generally considered to be more active during nocturnal periods than during the day; however, few studies have empirically evaluated diel variation in shark habitat use and how anthropogenic disturbances may influence these patterns. In the western central Atlantic Ocean, tiger sharks (Galeocerdo cuvier) are highly abundant in the shallow waters of the Little Bahama Bank, Bahamas. Within the northwest edge of the Bank, there is an area nicknamed “Tiger Beach,” where tiger sharks are provisioned year-round at spatially discrete ecotourism dive sites spanning ~ 1.5 km². In this study, we used an array of acoustic receivers encircling an area of 102.4 km² to evaluate for potential differences in diel spatial habitat use patterns for 42 tagged tiger sharks at Tiger Beach and the surrounding area. Using tracking data from 24 June 2014 to 13 May 2015, we evaluated spatial and diel patterns of shark activity space, centers of activity, residency and the daily proportion of sharks detected within the array. Sharks were detected during both day and night with no significant diel differences in habitat use metrics across the array, although spatial differences in residency existed. Four sharks accounted for 53.8% of residency data throughout the tracking period, with the majority of sharks primarily entering and exiting the array, except during summer months when the most of the tagged tiger sharks were absent from the array. We also found limited empirical support for hypothesized effects of provisioning tourism on tiger shark habitat use. However, additional research at finer, individual scales, may be needed to better resolve the potential influence of provisioning on tiger sharks at Tiger Beach.
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.
The functional causes of life history trade-offs have been a topic of interest to evolutionary biologists for over six decades. Our review of life history trade-offs discusses conceptual issues associated with physiological aspects of trade-offs, and it describes recent advances on this topic. We focus on studies of four model systems: wing polymorphic insects, Drosophila, lizards, and birds. The most significant recent advances have been: (a) incorporation of genetics in physiological studies of trade-offs, (b) integration of investigations of nutrient input with nutrient allocation, (c) development of more sophisticated models of resource acquisition and allocation, (d) a shift to more integrated, multidisciplinary studies of intraspecific trade-offs, and (e) the first detailed investigations of the endocrine regulation of life history trade-offs.
Body form can change across ontogeny, and can influence how animals of different sizes move and feed. Scaling data on live apex predatory sharks are rare and, therefore, we examined patterns of scaling in ontogenetic series of four sympatric shark species exhibiting a range of sizes, ecologies and life histories (tiger, bull, blacktip, and nurse shark). We evaluated 13 linear morphological variables and two areas (caudal and dorsal) that could influence both animal condition and locomotor performance. These measurements included dimensions of the dorsal, pectoral, and caudal fins, as well as several dimensions of body circumference, and of the head. For all four species, the body axis (eye-to-eye, lateral span, frontal span, proximal span) scaled close to isometry (expected slope of 1.0). The two largest sharks (tiger and bull sharks) also showed significant negative allometry for elements of the caudal fin. We found significant negative allometry in the lengths of the upper lobe of the caudal fin (caudal fin 1) and the overall height of the caudal fin (caudal fin 2) in tiger and bull sharks, with slopes ranging from about 0.60 to 0.73. Further, tiger sharks showed negative allometry in caudal fin area. These results suggest that in terms of overall body dimensions, small sharks are roughly geometrically similar to large sharks, at least within the species we examined. However, juvenile tiger (and to a lesser extent bull sharks) are notable in having proportionately larger caudal fins compared to adult sharks. As the caudal fin contributes to generating thrust during forward locomotion, this scaling implies differences among adult and juvenile sharks in locomotor ability. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, ●●, ●●–●●.
An aspect of life history that has seen increasing attention in recent years is that of strategies for financing the costs of offspring production. These strategies are often described by a continuum ranging from capital breeding, in which costs are met purely from endogenous reserves, to income breeding, in which costs are met purely from concurrent intake. A variety of factors that might drive strategies toward a given point on the capital-income continuum has been reviewed, and assessed using analytical models. However, aspects of food supply, including seasonality and unpredictability, have often been cited as important drivers of capital and income breeding, but are difficult to assess using analytical models. Consequently, we used dynamic programming to assess the role of the food supply in shaping offspring provisioning strategies. Our model is parameterized for a pinniped (one taxon remarkable for the range of offspring-provisioning strategies that it illustrates). We show that increased food availability, increased seasonality, and, to a lesser extent, increased unpredictability can all favor the emergence of capital breeding. In terms of the conversion of energy into offspring growth, the shorter periods of care associated with capital breeding are considerably more energetically efficient than income breeding, because shorter periods of care are associated with a higher ratio of energy put into offspring growth to energy spent on parent and offspring maintenance metabolism. Moreover, no clear costs are currently associated with capital accumulation in pinnipeds. This contrasts with general assumptions about endotherms, which suggest that income breeding will usually be preferred. Our model emphasizes the role of seasonally high abundances of food in enabling mothers to pursue an energetically efficient capital-breeding strategy. We discuss the importance of offspring development for dictating strategies for financing offspring production.
Animals are often faced with complex movement decisions, particularly those that involve long-distance dispersal. Partial migrations, ubiquitous among all groups of vertebrates, are a form of long-distance movement that occurs when only some of the animals in a population migrate. The decision to migrate or to be a resident can be dependent on many factors, but these factors are rarely quantified in fishes, particularly top predators, even though partial migrations may have important implications for ecosystem dynamics and conservation. We utilized passive acoustic telemetry, with a Brownian bridge movement model and generalized additive mixed models, to explore the factors regulating partial migration in a large marine predator, the tiger shark, throughout the Hawaiian Islands. Although sharks tended to utilize a particular "core" island, they also demonstrated inter-island movements, particularly mature females that would swim from the northwestern Hawaiian Islands to the main Hawaiian Islands (MHI). Immigration to another island was a function of season, sea surface temperature (SST), and chlorophyll a concentration. Our results predict that 25% of mature females moved from remote French Frigate Shoals atoll to the MHI during late summer/early fall, potentially to give birth. Females with core home ranges within the MHI showed limited movements to the NWHI, and immigration to an island was better explained by SST and chlorophyll a concentration, suggesting a foraging function. Dispersal patterns in tiger sharks are complex but can be considered a mix of skipped-breeding partial migration by mature females and individual-based inter-island movements potentially linked to foraging. Therefore, sharks appear to use a conditional strategy based on fixed intrinsic and flexible extrinsic states. The application of Brownian bridge movement models to electronic presence/absence data provides a new technique for assessing the influence of habitat and environmental conditions on patterns of movement for fish populations.
Top oceanic predators, especially large predatory sharks (TOPS), appear to be experiencing varying degrees of population declines. Life history data (e.g. diet, reproductive status, age and growth, mortality) are critical for developing effective conservation strategies for TOPS. Presently, lethal sampling remains the most effective and accurate means of gathering these data. To meet such challenges, many scientists have utilized specimens obtained from recreational and commercial fisheries, but have needed to supplement those data with fishery-independent sampling. However, there is growing public and scientific debate as to whether lethal sampling of TOPS is justified for obtaining conservation data. Here we describe the development and use of non-lethal alternatives for collecting data on (1) trophodynamics; (2) maturity state and fecundity; and (3) growth and mortality rates necessary to enact conservation measures for threatened or even data-deficient TOPS.
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.
The influence of a lower condition on reproductive investment, somatic energy losses, and postspawning condition of Atlantic cod (Gadus morhua) was examined under the hypothesis that females, in response to lower available energy reserves, would reduce reproductive investment in order to limit somatic energy losses. Laboratory experiments revealed that female cod with high prespawning condition factors ended reproduction in better condition than females with low prespawning condition factors. Fecundity and total egg dry weight were significantly lower in poor-condition females. The loss in somatic mass and energy in these poor-condition females was nevertheless higher, in relative terms, than the losses experienced by females in good condition. Consequently, energy reserves invested in reproduction by poor-condition females increase their risk of mortality. In the northern Gulf of St. Lawrence during the early 1990s, reproductive females had lower fecundities and were in worse prespawning and postspawning condition. The condition of spent females suggested a greater impact of changes in environmental conditions on adult than on immature cod. Reproductive potential and possibly recruitment may have suffered from that situation and could have contributed to the failure of that stock to recover despite the moratorium on commercial fishing.
In order to compensate for the resource demands of reproduction, organisms usually increase the amount of total food resources available. This may be achieved by different tactics of resource use that also include foraging decisions. Two such general tactics are discussed in this paper under the concepts of capital and income breeding. These are defined mainly from the temporal distribution of resource acquisition relative to resource use. A capital breeder acquires its resources in advance and store them endogenously or exogenously until they are needed to supply aspects of offspring production. An income breeder, on the other hand, adjusts its food intake concurrently with breeding, without reliance on stores. In a perfectly predictable environment without limited resources, income breeding is the best option since capital breeders may have to pay a number of energetic and demographic costs for their stored resources. However, under unpredictable food conditions, food/time limitations, and risky fora
Low internal energy reserves at the beginning of the breeding season may impose physiological constraints on an animal's reproductive investment and may alter the optimal trade‐off between investment in reproduction and somatic condition.
Here we examine how the energetic condition of female Mountain Pine Beetles ( Dendroctonus ponderosae ) affects their reproductive investment. We starved beetles to simulate the decrease in energy that accompanies dispersal and tested whether starved beetles had decreased egg number and decreased egg size, or both. We further distinguished whether changes are due to physiological constraints or shifts in allocation between reproduction and somatic condition.
We found that starved beetles produced smaller eggs than non‐starved beetles, but females were able to partially offset the energetic deficit by feeding at their breeding habitat. Starvation did not decrease the number of eggs beetles produced.
The number and size of eggs produced depended on whether females allocated energy to reproduction or to somatic condition. However, this life‐history allocation decision was independent of the amount of energy beetles had at the beginning of reproduction.
Our results demonstrate the importance of assessing reproductive investment in the context of other life‐history trade‐offs. Specifically, since egg size in Mountain Pine Beetles was highly dependent on both the amount of energy remaining after dispersal and whether energy was allocated to reproduction or somatic maintenance, we expect both of these trade‐offs to be under strong selection.
Roscoe DW, Hinch SG, Cooke SJ, Patterson DA. Behaviour and thermal experience of adult sockeye salmon migrating through stratified lakes near spawning grounds: the roles of reproductive and energetic states. Ecology of Freshwater Fish 2010: 19: 51–62. © 2009 John Wiley & Sons A/S
Abstract – Little is known about physiological factors underlying thermal behaviour in Pacific salmon ( Oncorhynchus spp.). We implanted acoustic transmitters and temperature loggers into migrating adult sockeye salmon ( Oncorhynchus nerka ) and nonlethally assessed their reproductive hormone levels and energetic states immediately prior to their passing through natal lakes en route to spawning grounds. We tested the hypothesis that energetic and reproductive status influence thermoregulatory and other in‐lake behaviours. More reproductively advanced females with lower levels of energy transited through cooler temperatures compared to less mature females with high levels of energy, possibly to reduce metabolic energy expenditure and delay final maturation. Transit temperatures of males were not related to physiological variables. Salmon travelled on average 13.6 km·day ⁻¹ through two lakes, and often circled or held for more than 1 day before moving upstream, but these behaviours were generally not related to physiological variables.
The winter skate, Leucoraja ocellata (Mitchill, 1815) is a large oviparous skate that is endemic to inshore waters of the western North Atlantic. The reproductive cycle of this species was characterized in monthly samples taken off the coast of New Hampshire, USA (4215N; 7025W), at depths of 9–107m from November 2000 to October 2001. Plasma concentrations of the sex steroids testosterone (T), 17-estradiol (E2), and progesterone (P4) were determined by radioimmunoassay in mature male and female skates. Changes in ovary weight, shell gland weight, and follicle size for 66 female skates were compared to patterns of all three steroid hormones. Beginning in January, ovary weight, shell gland weight, average diameter of the largest follicle, and plasma E2 increased steadily, culminating in a transient peak in July. This peak was followed by a steady decline in plasma E2 concentrations, which returned to the lowest values in December. Although T concentrations fluctuated throughout the year, a low concentration in July coincided with a peak in E2. Skates sampled in September, October, and November had the highest P4 concentrations, coinciding with the period of egg-case production. For males (n=64), annual cycles of T and E2 were compared to stages of spermatogenic development. Testosterone concentrations displayed two peaks, one in December/January and the other in July, which were associated with maximum spermatocyst concentration, while E2 peaks in February, June, and October coincided with maximum spermatocyte concentration. Along with our observations that some reproductive individuals were present throughout the year, these findings suggest that the winter skate has a partially defined reproductive cycle.
Relationships between body storage (estimated as fat content and residuals of body mass regressed against body length) and
offspring investment [brood mass, brood size (number of embryos per brood) and embryo mass] were examined within and among
populations of the amphipod Gammarus minus in ten cold springs in central Pennsylvania, USA. Two major hypotheses and six corollary hypotheses were tested. Total reproductive
investment (brood mass and brood size) was usually strongly positively correlated with maternal body length and body storage
both within and among populations. These positive associations between reproductive and somatic investments are expected if
individual variation in resource acquisition exceeds that of resource allocation. That is, individuals or populations that
are able to acquire more resources should also be able to allocate more resources to both reproduction and somatic reserves
than those acquiring fewer resources. This hypothesis is consistent with evidence showing that individual differences in body
storage in G. minus and other amphipods are related to differences in resource acquisition. Positive associations between reproductive and somatic
investments do not mean that energy costs of reproduction do not exist in G. minus. Evidence for reproductive energy costs included the lower body-fat contents of brooding versus nonbrooding females and the
relatively low body mass per length of females who had just deposited eggs in their brood pouch. Unlike brood mass and brood
size, individual embryo mass was usually unrelated to maternal body length and body storage. This pattern is largely consistent
with optimal offspring investment theory, which predicts that offspring size should be insensitive to variation in parental
resource status. However, in contrast to theory, embryo mass increased in winter when brooding females were significantly
”fatter”, presumably due to the availability of autumn-shed leaf food. This seasonal change in offspring size may be a maternally
mediated effect of increased resource availability, though other explanations are possible. Overall, this study suggests that
”fatter” female amphipods are fitter than ”thinner” ones, though both the costs and benefits of increased body storage and
brood size require investigation to substantiate this claim. This study also suggests that effects of individual variation
in resource acquisition on life-history patterns deserve more theoretical and empirical attention by ecologists than they
have received. It should be recognized that positive and/or nonsignificant correlations between life-history traits are just
as interesting and important as are the negative correlations predicted by many theoretical models.
The habitat use and movements of the round stingray Urobatis halleri were compared between shallow restored and natural habitats of the Anaheim Bay Estuary (CA, U.S.A.) in relation to water temperature. Restored habitat remained significantly warmer than natural habitat from spring through to autumn. Strong sexual segregation occurred in the restored habitat with mature female U. halleri forming large unisex aggregations in summer, during months of peak seasonal water temperatures, and males only present during spring. Most mature females collected from restored habitat during months of high abundance were determined to be pregnant using non-invasive field ultrasonography. Tagged females typically spent <14 days in the restored habitat, using the habitat less as seasonal water temperatures decreased. Females tended to emigrate from the estuary by mid-August, coinciding with the time of year for parturition. The elevated water temperatures of the restored habitat may confer an energetic cost to male U. halleri, but females (particularly pregnant females) may derive a thermal reproductive benefit by using warm, shallow habitats for short periods of time during months of peak water temperatures. These findings have management implications for the design of coastal habitat restoration projects and marine protected areas that incorporate thermal environments preferred by aggregating female elasmobranchs.
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 rate of reproduction, age at maturity and longevity vary widely among species. Most of this life-history variation falls on a slow-fast continuum, with low reproductive rate, slow development and long life span at one end and the opposite traits at the other end. The absence of alternative combinations of these variables implies constraint on the diversification of life histories, but the nature of this constraint remains elusive. Here, we argue that individual and adaptive responses to different environments are limited by physiological mechanisms. Although energy and materials allocations are important results of physiological tradeoffs, endocrine control mechanisms can produce incompatible physiological states that restrict life histories to a single dominant axis of variation. To approach the problem of life-history variation properly, studies should integrate behavior and physiology within the environmental and demographic contexts of selection.
1.1. The contents of cholesterol and free fatty acids (FFA) in blood plasma were examined in 22 species of marine fishes caught in the Skagerrak and representing various groups of fishes (Cyclostomi, Holocephali, Elasmobranchii and Teleostei).2.2. The cholesterol level in most fishes, except elasmobranchs, was 2–6 times higher than that of higher vertebrates. In the majority of examined fish species 65–75% of the plasma cholesterol was in esterified form.3.3. A seasonal variation in plasma cholesterol, probably associated with spawning, was found in the teleosts Gadus virens and Gadus morrhua.4.4. The plasma FFA level, which showed great interspecies variation, seemed to be dependent both on storage sites of lipid reserves and on the activity of the fish species.5.5. Various factors affecting the blood plasma levels of cholesterol and FFA in fish are reviewed.
Job number added acc. to DOCREP assignment
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.
The authors develop models predicting adaptive responses for both foraging speed and proportion of time active when individual growth rate and mortality risk are functions of these variables. Using the criterion that animals should minimize the ratio of mortality to growth rates, it is shown that, when both growth and mortality rates are linear with activity levels, the latter should be either maximal or minimal depending on resource level. If growth rate is a decelerating function of activity, then speed or time active should decrease with increases in resources, handling time, or the effect of activity on mortality rate. If mortality rate unrelated to activity increases, then activity rate also should increase. Predictions are developed for cases in which time horizon is critical using a dynamic programming framework. The general patterns of predicted activity responses are similar to the time-invariant analytical solutions, but foraging speed is reduced relative to the analytical solutions when time remaining is long or when accumulated reserves are high. This effect is ameliorated when accumulated reserves (size) increase resource capture efficiency or reduce mortality risk. If resources decline with time (eg because of competition) optimal foraging speeds are also higher than predicted by the analytical solutions. -from Authors
Conventional classification of reproductive modes in female elasmobranchs fails to account for the diversity in ovarian dynamics that operate during oviparous and viviparous cycles. Delineating this diversity is crucial for understanding the endocrine regulation of the manifold physiological mechanisms utilized to retain and protect eggs and developing embryos, to fuel embryogenesis, and to manage the intrauterine milieu. Oocyte development and follicular steroidogenesis overlap with egg retention and pregnancy in some species, whereas in others the follicular phase of the cycle is temporally separated from the gravid period. A luteal phase predominates the post-ovulatory period in viviparous species. In oviparous species, the luteal phase overlaps with the follicular cycle. This heterogeneity in ovulatory cycles suggests that the endocrine system evolved a transmutable system for regulating steroidogenesis and the control of the reproductive events. The reproductive biology and endocrinology of the oviparous little skate and lecithotrophic viviparous spiny dogfish are reviewed in order to derive a working hypothesis that explains the complex nature of endocrine patterns observed in species utilizing disparate reproductive modes. An understanding of the adaptations in ovarian dynamics to particular ovulatory cycles is key to developing theories about the evolution of reproductive strategies in female elasmobranchs. J. Exp. Zool. 284:557-574, 1999.
Koalas are generally considered to be limited by their ability to acquire energy from their diet of Eucalyptus foliage and have the lowest mass-specific peak lactational energy output measured in any mammal to date. This study considered the energetics and sources of energy utilised for reproduction in free-ranging female koalas. Energy requirements and foliage intake were greater in both lactating and non-lactating females in winter than summer, presumably due to demands of thermoregulation. Koalas met the peak energy requirements of lactation primarily by a 36% increase in their intake of foliage. Metabolic energy expenditure (field metabolic rate, 1778 kJ.day(-1) for a 6.25-kg female at the time of peak lactation) was not elevated during lactation. This was due to compensation for part of their lactational demands by reduction of another, non-reproductive, component of their energy budget. The observed energetic compensation was probably due primarily to substitution of the waste heat from the metabolic costs of milk production and increased heat increment of feeding for thermoregulatory energy expenditure. There may also have been energetic compensation by reduction of some aspect of maintenance metabolism. Such energetic compensation, together with the strategy of spreading lactation over a long period, minimises the magnitude of lactational energy demands on koalas, and thus the increase in daily food intake required during lactation. As the nutritional requirements of females at peak lactation are the highest of any members of the population, low reproductive requirements effectively increase the types and amount of habitat able to support koala populations.
Enhanced antioxidant status in polar fishes may occur due to high dissolved oxygen levels and membranes rich in peroxidation-sensitive polyunsaturated fatty acids. To evaluate the importance of antioxidant enzymes in polar fishes, activities of catalase (CAT), superoxide dismutase (SOD), and glutathione reductase (GR), as well as the aerobic enzyme cytochrome c oxidase (CCO), were measured at 6 degrees C and 1 degrees C in livers of confamilial Arctic and temperate teleosts: the Arctic fourhorn sculpin Triglopsis quadricornis (Cottidae) and saddled eelpout Lycodes mucosus (Zoarcidae) vs. the temperate longhorn sculpin (Myoxocephalus octodecimspinosus) (Cottidae) and ocean pout (Zoarces americanus) (Zoarcidae), respectively. At both assay temperatures, CAT activities were substantially lower in both Arctic species, SOD was similar in the cottids but lower in the Arctic zoarcid, and GR was similar in temperate and Arctic fishes. Activities at respective habitat temperatures were always significantly lower in the Arctic fishes. The lower antioxidant enzyme activities in the Arctic fishes cannot be attributed to lower aerobic status because CCO activity was similar or higher in the Arctic fishes; significant negative relationships were found between CCO and CAT and GR (but not SOD) when all species were combined, indicating that a higher apparent aerobic status does not necessarily coincide with higher antioxidant enzyme activities. Antioxidant enzyme activities may not be enhanced as part of cold adaptation in Arctic fishes, at least in the liver.
Mammals that live in seasonal environments may adjust their reproductive cycles to cope with fluctuations in food availability. Because lemurs in Madagascar experience highly seasonal variation in food availability, we examined the effects of fluctuating food availability on body condition and reproduction in one of the larger living species, Verreaux's sifaka (Propithecus verreauxi verreauxi), in the Kirindy Forest of western Madagascar. Seven years of demographic data were combined with an intensive study of 25 individuals over the course of 18 months. In contrast to other populations of Verreaux's sifaka, females were found to have greater body mass than males. Both male and female sifaka exhibited significant losses of body mass and fat during the dry season. Females were more likely to give birth and successfully wean an infant when they had higher body mass during the mating season. They mated during the periods of high and declining food availability, gave birth during the lean season, and then timed mid/late lactation with the period of increasing food availability. Thus, we conclude that sifaka follow the "classic" reproductive strategy (sensu van Schaik and van Noordwijk [Journal of Zoology (London) 206:533-549, 1985]).
A review of elasmobranch reproductive behavior with a case study on the nurse shark, Ginglymostoma cirratum. Pp. 157-188 in The behavior and sensory biology of elasmobranch fishes: an anthology in memory of Donald Richard Nelson
- H L Pratt
- J C Jr
- Carrier
Pratt H.L., Jr., and J.C. Carrier. 2001. A review of elasmobranch reproductive behavior with a case study on the nurse
shark, Ginglymostoma cirratum. Pp. 157-188 in The behavior
and sensory biology of elasmobranch fishes: an anthology in
memory of Donald Richard Nelson. Springer, Dordrecht.
Endocrine control of the female reproductive tract
- I Callard
- J George
- T Koob
Activities of antioxidant enzymes and cytochrome c oxidase in liver of Arctic Life-History Stages and Energy States in Tiger Sharks 941
- B Speers-Roesch
- J S Ballantyne
Speers-Roesch B. and J.S. Ballantyne. 2006. Activities of antioxidant enzymes and cytochrome c oxidase in liver of Arctic
Life-History Stages and Energy States in Tiger Sharks 941