The effects of temperature and oxygen availability on aerobic performance in three coastal shark species; Squalus acanthias, Carcharhinus limbatus, and Carcharhinus leucas
Doctor of Philosophy (Ph.D.)
Degree Granting Department
Brad A. Seibel, Ph.D.
Christopher Stallings, Ph.D.
Cameron Ainsworth, Ph.D.
Jay Dean, Ph.D.
Dean Grubbs, Ph.D.
aerobic scope, hypoxia, oxygen supply, ram-ventilation, thermal sensitivity
Anthropogenically driven climate changes are altering marine habitats globally. Rising sea surface temperatures and coastal eutrophication, arising from global warming and coastal nutrient loading, have resulted in progressive ocean deoxygenation. This may restrict available habitat of marine organisms as studies suggest that the balance between metabolic oxygen demand and environmental supply plays an important role in limiting viable habitat and species fitness. As ectothermic predators, with temperature-dependent metabolism and high metabolic demands, coastal shark species may be susceptible to shifts in ocean temperature and oxygen. Such environmental changes may alter metabolic performance and ultimately success and survival within shark habitat. However, our understanding of species-specific physiological responses to environmental shifts in temperature and oxygen is lacking for the vast majority of shark species. This dissertation explores the effects of temperature and declining oxygen availability on energetic performance in three ecologically and economically valuable shark species of the US Atlantic and Gulf of Mexico coasts; the spiny dogfish shark, Squalus acanthias, the blacktip shark, Carcharhinus limbatus, and the bull shark, Carcharhinus leucas.
These species represent coastal “apex” and meso-predators found across temperate, tropical, and subtropical waters. Across their ranges, these highly migratory species likely experience steep oxygen and temperature gradients but differ in habitat and lifestyle. Squalus acanthias is a much slower, smaller, benthopelagic species found in waters 7-24˚C. These cold-temperate sharks spend much of the year in deep, offshore locations but routinely enter shallow coastal waters. Carcharhinus limbatus, and C. leucas are more active, large coastal species, considered tropical-subtropical in distribution known to occupy waters 20-34˚C and 20-37˚C respectively. Carcharhinus limbatus, and C. leucas use confined estuarine and riverine nursery habitats for their young where long-term residency in these shallow coastal habitats is important to species success and survival. In addition, C limbatus and C. leucas are obligate ram ventilators, thought to require forward motion to maintain oxygen supply, whereas S. acanthias have the ability to decrease activity and forcibly pump water over their gills while at rest (buccal pumping). Differences between species habitat, ecology, and activity level (metabolic demand) mean they likely exhibit varied environmental tolerances, responses to elevated temperature and hypoxia, and may display varied shifts in viable habitat with climate change. To better predict habitat suitability and species responses to climate change, we must first understand how the physiology that underpins animal behavior is fundamentally altered by changes in temperature and oxygen for each species.
Several environmentally-sensitive physiological performance metrics have been used to identify viable species habitat, based on the balance of organism energetic demands and environmental oxygen supply. As animals require oxygen to derive cellular energy for all life activities, the amount of oxygen available in a given environment may dictate an organism’s energetic potential. In addition, while temperature influences the rate of biochemical reactions in the body, it also causes elevated metabolic demands in ectothermic species. As temperatures rise, ectotherms require more oxygen to support elevated metabolic demands at high temperature. At a certain thermal or hypoxic threshold the balance of animal oxygen demand to ambient supply may fall below sustainable levels. Environments that do not confer enough energetic potential to support population energetic needs are considered non-viable species habitat. Increased presence of such environments within occupied species range has consequences for animal distribution and abundance, and the potential for metabolic tradeoffs in growth, reproduction, foraging, etc. My research aimed to establish the thermal and hypoxic sensitivity of metabolic demands and performance in marine sharks, quantify thermal and hypoxic limitation of aerobic energetic performance, and to test the species-specific utility of metabolic performance metrics such as aerobic scope and oxygen supply capacity as indicators of viable species habitat.
Aerobic scope, defined as an organism’s aerobic energetic potential, provides a measure of the energy available for sharks to perform all life activities within a given environment. This metric is derived from two components that can be directly measured in aquatic species: 1) maximum metabolic rate (MMR), the highest rate of organism energy use, vital for predator evasion and prey capture, and 2) resting or standard metabolic rate (SMR), i.e., the lowest energy required to maintain the body’s basal energetic needs while at rest. The difference between maximum and standard metabolic demand provides a measure of aerobic scope. This scope may be expressed in both absolute (absolute aerobic scope = MMR-SMR) and factorial terms (factorial aerobic scope = MMR/SMR), with each expression of aerobic scope providing distinct interpretations of species thermal optimality and or sublethal thermal limits. Factorial aerobic scope (FAS) is defined as the factorial change in aerobic energetic potential, or the factorial change in oxygen above what is needed at rest. This metric typically declines as temperatures rise and has been used to identify temperature and oxygen thresholds that limit viable habitat for species at the population level. At a limiting upper temperature, FAS reaches a minimum scope needed to support population energetic needs, and generally occurs between 2-5x what is needed to support basic resting metabolic demands of an individual.
Further, the temperature at which absolute aerobic scope (AAS) peaks, has been traditionally used to identify a species thermal “optimum” at which aerobic energetic potential is maximized and abundance and habitat use are expected to be highest the wild. Temperatures at which AAS declines significantly from its peak, are thought to represent sublethal limiting temperatures for the species, constraining wild distribution. A breakdown in the ability to supply oxygen to tissues (oxygen supply capacity) at high temperatures is thought to cause such decline in AAS by limiting maximum performance. As such, oxygen supply capacity, α, has been indicated as the primary driver of thermal tolerance in aquatic species, and represents another potential performance indicator of viable/evolved habitat.
Deficits in aerobic scope and oxygen supply capacity have been linked to shifts in organism habitat use, movement and migration, energetic tradeoffs in foraging, reproduction, growth and development. However, the aforementioned interpretations of thermal trends in metabolic performance and aerobic scope have not been tested mechanistically across a large number of aquatic species. In these studies, aerobic scope was evaluated as a predictive metric of “optimal” and limiting temperature for these three shark species. In addition, measured metabolic performance under declining ambient oxygen allowed for identification of critical oxygen limits for metabolic rates (critical oxygen partial pressure; Pc), and how aerobic scope is limited by environmental oxygen deficits in each species.
Within this dissertation, temperature-controlled intermittent respirometry was used to explore aerobic metabolic performance under two distinct metabolic challenges: environmental hypoxia and maximum aerobic exercise. Adult spiny dogfish sharks (TL=71-94.5cm) off the US Northeast Shelf (US NES) were tested at five experimental temperatures (10, 13, 17, 21, and 23˚C). Neonate/young-of-the-year (YOY) blacktip sharks (53-63 cm STL) and bull sharks (69-81cm STL) of the Eastern Gulf of Mexico were tested at 3-4 temperatures (22, 26, and 30 for bull sharks, 22, 26, 30 and 34°C for blacktips), within or bracketing species natural range.
My first study measured metabolic traits of the spiny dogfish shark, S. acanthias, across temperature and oxygen. The goal of this study was ultimately to assess the potential for rapidly rising temperature, and its interaction with oxygen, to influence viable habitat for members of a subpopulation of S. acanthias on the US NES. SMR for S. acanthias increased exponentially with temperature, from 10 to 23°C. MMR increased logistically with no decrement in maximum performance within measured thermal range. The α for S. acanthias followed the logistic trend in MMR in support of elevated metabolic demands across temperature, and with no decline in oxygen supply capacity within thermal range, oxygen supply appeared not to be the primary driver of thermal tolerance for this species. Behavioral observation revealed that sharks at rest began to lose equilibrium at 21°C, even when ambient oxygen exceeded levels that critically limit resting metabolic demands. Thus, internal systems other than physiological oxygen supply begin to fail for S. acanthias at 21°C. The peak in AAS ≥20.5°C, rather than indicating optimal temperature, marks the beginning of physiological failure in dogfish. Behavioral and metabolic results indicate that S. acanthias are likely living near their upper critical temperature (≈24°C) in the warmest seasons, reaching a FAS of 4.31 at 23˚C, within range of theoretical population thresholds (FAS=2-5). Declining ambient oxygen will additionally cause predictable limitation of maximum metabolic performance in S. acanthias, and cause limiting FAS thresholds to be reached at lower temperatures, further limiting viable habitat if oxygen is below air saturation. This study identified environmental thresholds for spiny dogfish that may be used to predict integrative constraints on suitable habitat in the face of climate change.
The purpose of my second study was to identify the effect of temperature on aerobic performance within the natural range of blacktip sharks (C. limbatus) and bull sharks (C. leucas) of the Eastern Gulf of Mexico. The results stipulate that routine metabolic demand (an estimate of minimum demands for ram ventilators inclusive of locomotion to support adequate ventilation) increased significantly with temperature in neonate/YOY of both species. This indicated that the oxygen needed to support lowest routine swimming in these species increases as temperatures rise. Blacktip and bull sharks demonstrated marked differences in aerobic performance. Specifically, blacktip sharks exhibited higher metabolic rates than bull sharks at all active levels and demonstrated no significant change in both MMR and α as temperatures rose. For blacktip sharks this may indicate an evolved need to maintain MMR across a large thermal range. Bull sharks showed significant increase in both MMR and α within the range of temperatures tested, with particular temperature sensitivity of maximum performance to cold temperatures. For bull sharks this may indicate a lack of need to maintain MMR across a large thermal range, that may be related to distinct ecological and physiological strategies of salinity use in this species. Maximum metabolic rates for both species in this study are also among the highest recorded for shark species to date. Differing thermal sensitivities for all metrics between species, lead to opposite thermal trends in aerobic scope between bull and blacktip sharks. Aerobic scope in blacktip sharks, was driven primarily by minimum routine metabolic rate, whereas for bull sharks, aerobic scope was driven by both maximum metabolic rate and to a lesser degree, minimum routine metabolic rate. Neither MMR, α, nor aerobic scope identified limiting thermal thresholds for these species within the experimental temperature range (22-30°C bull sharks; 22-34°C blacktip sharks), and as such, critical population thresholds for temperature in these species are likely to lie below the minimum factorial aerobic scope of ~1.4 found in this study. This research will be used as a basis for future studies to identify the bounds of thermal tolerance for these species and for comparison to historical distribution and habitat use to ground truth thermal realtionships.
Finally, my third study served to identify the effect of ambient oxygen availability and ventilation mode on aerobic performance in obligate ram ventilators. Obligate ram-ventilating species, such as bull and blacktip sharks, are thought to have diminished capacity to reduce activity and use active ventilation (buccal pumping) to support metabolic demands. Instead, support of oxygen delivery to respiring tissues is inherently tied to locomotion. The costs of locomotion are also inherently greater than metabolic costs at rest for shark species. Thus, high oxygen demands of continuous locomotion to support ram ventilation may lead these species to be particularly vulnerable to diminished oxygen availability during hypoxic events within their small nursery range. In this study, neonate/YOY blacktip sharks demonstrated no ability to sustainably use active ventilation (buccal pumping mechanisms) and rest under normoxic or hypoxic conditions. Bull sharks by contrast demonstrated continuous swimming as well as some resting behavior under normoxia and hypoxia, allowing for opportunistic measurement of demands and oxygen supply capacity across various modes of activity. Metabolic rate at rest for bull sharks was ~57% of minimum routine metabolic rate across temperature, and though resting reduced oxygen demands significantly, oxygen supply capacity was significantly diminished when bull shark activity was reduced. The oxygen supply capacity at rest was not enough to support energetic demands at rest, and for this reason, resting metabolism ultimately declined unsustainably after brief periods of rest in bull sharks. The use of buccal pumping (active ventilation) was not a sustainable or likely hypoxic coping strategy for either species, as a higher oxygen partial pressure was required to meet metabolic needs at rest, relative to swimming under hypoxia. Although a few individuals of each species increased swim speed as environmental oxygen declined, increased swim speed to improve ventilation volume was not universally observed. Though increases in swim speed may be used in an attempt to maximize ventilation under mild-moderate hypoxia, the critical oxygen level below which locomotion for ventilation and routine metabolic demands can no longer be supported provides a limit to this hypoxic ventilatory strategy. Although more data (both lab derived thresholds and field based thermal affinity) are needed to say with certainty where oxygen thresholds limiting population success and causing avoidance responses occur, a limiting oxygen partial pressure likely falls between ~8 and 12 kPa, between the critical oxygen limit for lowest locomotion supporting ram ventilation and the critical oxygen limit for routine swimming. As environmental hypoxia becomes more extensive within their natal habitat under climate change, we believe young bull sharks and blacktips will be vulnerable to habitat loss. More data are needed to identify current and phenotypically plastic limits to hypoxia for these species.
These studies represent some of the first physical measurements of their kind for these species, allowing us to quantify energetic needs and identify limits to aerobic performance across different environmental scenarios and species diversity. We have tested the application of several metabolic metrics as indicators of optimal or limiting habitats for these species and have applied new frameworks from which to interpret dynamics of metabolic performance, energetic scope, and hypoxic limits to activity. Through this work we have derived several physiological baselines from which these species may be further investigated, with results that help inform evolved species habitat suitability.
Scholar Commons Citation
Andres, Alyssa M., "The effects of temperature and oxygen availability on aerobic performance in three coastal shark species; Squalus acanthias, Carcharhinus limbatus, and Carcharhinus leucas" (2022). USF Tampa Graduate Theses and Dissertations.