Aerobic scope protection reduces ectotherm growth under warming

1. Temperature has a dramatic effect on the physiology of ectothermic animals, impacting most of their biology. When temperatures increase above optimal for an animal, their growth gradually decreases. The main mechanism behind this growth rate reduction is unknown. 2. Here, we suggest the 'aerobic scope protection' hypothesis as a mechanistic explanation for the reduction in growth. 3. After a meal, metabolic rate, and hence oxygen consumption rate, transiently increase in a process called specific dynamic action (SDA). At warmer temperatures, the SDA response usually becomes temporally compressed, leading to a higher peak oxygen consumption rate. This peak in oxygen consumption rate risks taking up much of the animal's aerobic scope (the difference between resting and maximum rates of oxygen consumption), which would leave little residual aerobic scope for other aerobic functions. 4. We propose that water-breathing ectothermic animals will protect their postprandial residual aerobic scope by reducing meal sizes in order to regulate the peak SDA response during times of warming, leading to reductions in growth. 5. This hypothesis is consistent with the published literature on fishes, and we provide predictions that can be tested.Peer reviewe

Metabolic rate and rates of protein turnover in food-deprived cuttlefish, Sepia officinalis (Linnaeus 1758)

To determine the metabolic response to food deprivation, cuttlefish (Sepia officinalis) juveniles were either fed, fasted (3 to 5 days food deprivation), or starved (12 days food deprivation). Fasting resulted in a decrease in triglyceride levels in the digestive gland, and after 12 days, these lipid reserves were essentially depleted. Oxygen consumption was decreased to 53% and NH4 excretion to 36% of the fed group following 3-5 days of food deprivation. Oxygen consumption remained low in the starved group, but NH4 excretion returned to the level recorded for fed animals during starvation. The fractional rate of protein synthesis of fasting animals decreased to 25% in both mantle and gill compared with fed animals and remained low in the mantle with the onset of starvation. In gill, however, protein synthesis rate increased to a level that was 45% of the fed group during starvation. In mantle, starvation led to an increase in cathepsin A-, B-, H-, and L-like enzyme activity and a 2.3-fold increase in polyubiquitin mRNA that suggested an increase in ubiquitin-proteasome activity. In gill, there was a transient increase in the polyubiquitin transcript levels in the transition from fed through fasted to the starved state and cathepsin A-, B-, H-, and L-like activity was lower in starved compared with fed animals. The response in gill appears more complex, as they better maintain rates of protein synthesis and show no evidence of enhanced protein breakdown through recognized catabolic processes

Oxygen- and capacity-limited thermal tolerance: blurring ecology and physiology

No abstract available

Enzymatic capacities of metabolic fuel use in cuttlefish (Sepia officinalis) and responses to food deprivation: insight into the metabolic organization and starvation survival strategy of cephalopods

Food limitation is a common challenge for animals. Cephalopods are sensitive to starvation because of high metabolic rates and growth rates related to their "live fast, die young" life history. We investigated how enzymatic capacities of key metabolic pathways are modulated during starvation in the common cuttlefish (Sepia officinalis) to gain insight into the metabolic organization of cephalopods and their strategies for coping with food limitation. In particular, lipids have traditionally been considered unimportant fuels in cephalopods, yet, puzzlingly, many species (including cuttlefish) mobilize the lipid stores in their digestive gland during starvation. Using a comprehensive multi-tissue assay of enzymatic capacities for energy metabolism, we show that, during long-term starvation (12 days), glycolytic capacity for glucose use is decreased in cuttlefish tissues, while capacities for use of lipid-based fuels (fatty acids and ketone bodies) and amino acid fuels are retained or increased. Specifically, the capacity to use the ketone body acetoacetate as fuel is widespread across tissues and gill has a previously unrecognized capacity for fatty acid catabolism, albeit at low rates. The capacity for de novo glucose synthesis (gluconeogenesis), important for glucose homeostasis, likely is restricted to the digestive gland, contrary to previous reports of widespread gluconeogenesis among cephalopod tissues. Short-term starvation (3-5 days) had few effects on enzymatic capacities. Similar to vertebrates, lipid-based fuels, putatively mobilized from fat stores in the digestive gland, appear to be important energy sources for cephalopods, especially during starvation when glycolytic capacity is decreased perhaps to conserve available glucose

Hypoxia tolerance in fishes : cardiorespiratory performance and metabolism

Cardiac failure occurs in most vertebrates including humans following even short hypoxia exposure due to an inability to match cardiac energy demand to the limited energy supply. In contrast, hypoxia-tolerant ectothermic vertebrates show the remarkable ability to maintain cardiac energy balance and stable cardiac function during prolonged exposure to severe hypoxia (cardiac hypoxia tolerance, CHT). I investigated how CHT is achieved and its relationship to whole-animal hypoxia tolerance using measurements at multiple physiological levels in two study models: 1) tilapia, a hypoxia-tolerant teleost, and 2) a two-species comparison of elasmobranchs with different hypoxia tolerance. I tested the hypothesis that CHT depends upon the depression of cardiac power output (PO) (i.e., cardiac energy demand) to a level lower than the cardiac maximum glycolytic potential (MGP). All species showed a hypoxic PO depression via bradycardia and my work generally supports this hypothesis. However, in tilapia, hypoxic PO depression is not necessarily required to maintain cardiac energy balance, contrary to previous suggestions, because of an exceptionally high MGP. Thus, in certain species, PO depression may primarily benefit CHT by minimizing fuel use and waste production. I also tested the hypothesis that greater hypoxia tolerance is associated with enhanced hypoxic O₂ supply and consequently enhanced cardiovascular function (i.e., less PO depression and improved cardiac energy balance). My work on elasmobranchs supported this hypothesis and also suggested a role for strategic cardiac O₂ supply via O₂ sparing resulting from metabolic rate depression (MRD) in non-essential tissues. Finally, my work on elasmobranchs showed that critical oxygen tension (Pcrit) predicts hypoxic blood O₂ transport, supporting the use of Pcrit as an indicator of hypoxia tolerance. Next, I tested the hypothesis that hypoxic PO depression is associated with the depression of whole-animal O₂ consumption rate below Pcrit. I found that this occurred in all species, suggesting that modulation of peripheral demand for blood flow (e.g., via MRD) may influence CHT. Finally, my work on in vivo and in situ cardiac responses in tilapia provided little evidence for the hypothesis that hypoxic modulation of aerobic energy production pathways, including provision of aerobic fuels (specifically, fatty acids), contributes to CHT.Science, Faculty ofZoology, Department ofGraduat

Ecological significance of thermal tolerance and performance in fishes: new insights from integrating field and laboratory approaches

No abstract available

Hepatosomatic index & liver lipid composition of chondrichthyan fishes (compiled literature data) - Treberg & Speers-Roesch (2016) Does the physiology of chondrichthyan fishes constrain their distribution in the deep-sea? Journal of Experimental Biology

Supplementary compiled literature data (Excel format) for: Jason R. Treberg and Ben Speers-Roesch (2016) Does the physiology of chondrichthyan fishes constrain their distribution in the deep-sea? <i>Journal of Experimental Biology. </i>doi:10.1242/jeb.12810

Using Fatty-Acid Profile Analysis as an Ecologic Indicator in the Management of Tourist Impacts on Marine Wildlife: A Case of Stingray-Feeding in the Caribbean

Feeding marine wildlife as a tourism experience has become a popular means by which to attract both people and wildlife, although management efforts are still in their infancy. “Stingray City Sandbar” in the Cayman Islands, where visitors can hand feed free-ranging Southern Stingrays (Dasyatis americana), is a world-famous attraction currently undergoing visitor and wildlife management. One plan is to decrease the amount of nonnatural food provided by tourists with the intention of decreasing stingray habituation to the artificial food source and promoting stingray health. However, the effectiveness of this action is uncertain given that neither the extent of squid composition in the stingray diet nor the degree of nutrient similarity between the fed and natural diets is unknown. We used fatty acid (FA) profile analysis to address these questions by assessing the serum nonesterified FA composition of fed and unfed stingrays around the island and compared them with FA profiles of (1) the provisioned food source (squid) and (2) other warm- and cold-water elasmobranchs (sharks and rays). Our results indicated that fed stingrays were distinct. The FA profiles of the fed stingray population were expressly different from those of the unfed populations and showed a remarkable similarity to the FA composition of squid, suggesting that squid is the main food source. The tropical fed stingrays also exhibited essential FA ratios, specific to both species and habitat, comparable with those of elasmobranchs and squid from cold-water environs, implying that the provisioned food does not provide a similar nutritional lipid composition to that eaten in the wild. Our results suggest that FA profiles are a valuable indicator for the management and monitoring of fed Southern Stingrays because they can be used to assess differences in diet composition and provide an index of nutritional similarity. Our findings are currently being used by Caymanian stakeholders in designing practical management actions for their wildlife attraction