Timothy D. Clark

Differences in Thermal Tolerance Among Sockeye Salmon Populations

Environmental conditions encountered during migration shape cardiorespiratory physiology in sockeye salmon. Climate change–induced increases in summer water temperature have been associated with elevated mortality of adult sockeye salmon (Oncorhynchus nerka) during river migration. We show that cardiorespiratory physiology varies at the population level among Fraser River sockeye salmon and relates to historical environmental conditions encountered while migrating. Fish from populations with more challenging migratory environments have greater aerobic scope, larger hearts, and better coronary supply. Furthermore, thermal optima for aerobic, cardiac, and heart rate scopes are consistent with the historic river temperature ranges for each population. This study suggests that physiological adaptation occurs at a very local scale, with population-specific thermal limits being set by physiological limitations in aerobic performance, possibly due to cardiac collapse at high temperatures.

Aerobic scope measurements of fishes in an era of climate change: respirometry, relevance and recommendations

Summary Measurements of aerobic scope [the difference between minimum and maximum oxygen consumption rate ( and , respectively)] are increasing in prevalence as a tool to address questions relating to fish ecology and the effects of climate change. However, there are underlying issues regarding the array of methods used to measure aerobic scope across studies and species. In an attempt to enhance quality control before the diversity of issues becomes too great to remedy, this paper outlines common techniques and pitfalls associated with measurements of , and aerobic scope across species and under different experimental conditions. Additionally, we provide a brief critique of the oxygen- and capacity-limited thermal tolerance (OCLTT) hypothesis, a concept that is intricately dependent on aerobic scope measurements and is spreading wildly throughout the literature despite little evidence for its general applicability. It is the intention of this paper to encourage transparency and accuracy in future studies that measure the aerobic metabolism of fishes, and to highlight the fundamental issues with assuming broad relevance of the OCLTT hypothesis.

Principles for the Conservation of Wild Living Resources

We describe broadly applicable principles for the conservation of wild living resources and mechanisms for their implementation. These principles were engendered from three starting points. First, a set of principles for the conservation of wild living resources (Holt and Talbot 1978) required reexamination and updating. Second, those principles lacked mechanisms for implementation and consequently were not as effective as they might have been. Third, all conservation problems have scientific, economic, and social aspects, and although the mix may vary from problem to problem, all three aspects must be included in problem solving. We illustrate the derivation of, and amplify the meaning of, the principles, and discuss mechanisms for their implementation. The principles are: Principle I. Maintenance of healthy populations of wild living resources in perpetuity is inconsistent with unlimited growth of human consumption of and demand for those resources. Principle II. The goal of conservation should be to secure present and future options by maintaining biological diversity at genetic, species, population, and ecosystem levels; as a general rule neither the resource nor other components of the ecosystem should be perturbed beyond natural boundaries of variation. Principle III. Assessment of the possible ecological and sociological effects of resource use should precede both proposed use and proposed restriction or expansion of ongoing use of a resource. Principle IV. Regulation of the use of living resources must be based on understanding the structure and dynamics of the ecosystem of which the resource is a part and must take into account the ecological and sociological influences that directly and indirectly affect resource use. Principle V. The full range of knowledge and skills from the natural and social sciences must be brought to bear on conservation problems. Principle VI. Effective conservation requires understanding and taking account of the motives, interests, and values of all users and stakeholders, but not by simply averaging their positions. Principle VII. Effective conservation requires communication that is interactive, reciprocal, and continuous. Mechanisms for implementation of the principles are discussed.

Biodiversity redistribution under climate change : Impacts on ecosystems and human well-being

Consequences of shifting species distributions Climate change is causing geographical redistribution of plant and animal species globally. These distributional shifts are leading to new ecosystems and ecological communities, changes that will affect human society. Pecl et al. review these current and future impacts and assess their implications for sustainable development goals. Science, this issue p. eaai9214 BACKGROUND The success of human societies depends intimately on the living components of natural and managed systems. Although the geographical range limits of species are dynamic and fluctuate over time, climate change is impelling a universal redistribution of life on Earth. For marine, freshwater, and terrestrial species alike, the first response to changing climate is often a shift in location, to stay within preferred environmental conditions. At the cooler extremes of their distributions, species are moving poleward, whereas range limits are contracting at the warmer range edge, where temperatures are no longer tolerable. On land, species are also moving to cooler, higher elevations; in the ocean, they are moving to colder water at greater depths. Because different species respond at different rates and to varying degrees, key interactions among species are often disrupted, and new interactions develop. These idiosyncrasies can result in novel biotic communities and rapid changes in ecosystem functioning, with pervasive and sometimes unexpected consequences that propagate through and affect both biological and human communities. ADVANCES At a time when the world is anticipating unprecedented increases in human population growth and demands, the ability of natural ecosystems to deliver ecosystem services is being challenged by the largest climate-driven global redistribution of species since the Last Glacial Maximum. We demonstrate the serious consequences of this species redistribution for economic development, livelihoods, food security, human health, and culture, and we document feedbacks on climate itself. As with other impacts of climate change, species range shifts will leave “winners” and “losers” in their wake, radically reshaping the pattern of human well-being between regions and different sectors and potentially leading to substantial conflict. The pervasive impacts of changes in species distribution transcend single systems or dimensions, with feedbacks and linkages between multiple interacting scales and through whole ecosystems, inclusive of humans. We argue that the negative effects of climate change cannot be adequately anticipated or prepared for unless species responses are explicitly included in decision-making and global strategic frameworks. OUTLOOK Despite mounting evidence for the pervasive and substantial impacts of a climate-driven redistribution of Earth’s species, current global goals, policies, and international agreements fail to account for these effects. With the predicted intensification of species movements and their diverse societal and environmental impacts, awareness of species “on the move” should be incorporated into local, regional, and global assessments as standard practice. This will raise hope that future targets—whether they be global sustainability goals, plans for regional biodiversity maintenance, or local fishing or forestry harvest strategies—can be achievable and that society is prepared for a world of universal ecological change. Human society has yet to appreciate the implications of unprecedented species redistribution for life on Earth, including for human lives. Even if greenhouse gas emissions stopped today, the responses required in human systems to adapt to the most serious effects of climate-driven species redistribution would be massive. Meeting these challenges requires governance that can anticipate and adapt to changing conditions, as well as minimize negative consequences. As the global climate changes, human well-being, ecosystem function, and even climate itself are increasingly affected by the shifting geography of life. Climate-driven changes in species distributions, or range shifts, affect human well-being both directly (for example, through emerging diseases and changes in food supply) and indirectly (by degrading ecosystem health). Some range shifts even create feedbacks (positive or negative) on the climate system, altering the pace of climate change. Distributions of Earth’s species are changing at accelerating rates, increasingly driven by human-mediated climate change. Such changes are already altering the composition of ecological communities, but beyond conservation of natural systems, how and why does this matter? We review evidence that climate-driven species redistribution at regional to global scales affects ecosystem functioning, human well-being, and the dynamics of climate change itself. Production of natural resources required for food security, patterns of disease transmission, and processes of carbon sequestration are all altered by changes in species distribution. Consideration of these effects of biodiversity redistribution is critical yet lacking in most mitigation and adaptation strategies, including the United Nation’s Sustainable Development Goals.

Circulatory limits to oxygen supply during an acute temperature increase in the Chinook salmon (Oncorhynchus tshawytscha)

This study was undertaken to provide a comprehensive set of data relevant to disclosing the physiological effects and possible oxygen transport limitations in the Chinook salmon (Oncorhynchus tshawytscha) during an acute temperature change. Fish were instrumented with a blood flow probe around the ventral aorta and catheters in the dorsal aorta and sinus venosus. Water temperature was progressively increased from 13 degrees C in steps of 4 degrees C up to 25 degrees C. Cardiac output increased from 29 to 56 ml.min(-1).kg(-1) between 13 and 25 degrees C through an increase in heart rate (58 to 105 beats/min). Systemic vascular resistance was reduced, causing a stable dorsal aortic blood pressure, yet central venous blood pressure increased significantly at 25 degrees C. Oxygen consumption rate increased from 3.4 to 8.7 mg.min(-1).kg(-1) during the temperature increase, although there were signs of anaerobic respiration at 25 degrees C in the form of increased blood lactate and decreased pH. Arterial oxygen partial pressure was maintained during the heat stress, although venous oxygen partial pressure (Pv(O(2))) and venous oxygen content were significantly reduced. Cardiac arrhythmias were prominent in three of the largest fish (>4 kg) at 25 degrees C. Given the switch to anaerobic metabolism and the observation of cardiac arrhythmias at 25 degrees C, we propose that the cascade of venous oxygen depletion results in a threshold value for Pv(O(2)) of around 1 kPa. At this point, the oxygen supply to systemic and cardiac tissues is compromised, such that the oxygen-deprived and acidotic myocardium becomes arrhythmic, and blood perfusion through the gills and to the tissues becomes compromised.

Aerobic scope does not predict the performance of a tropical eurythermal fish at elevated temperatures

Climate warming is predicted to negatively impact fish populations through impairment of oxygen transport systems when temperatures exceed those which are optimal for aerobic scope (AS). This concept of oxygen- and capacity-limited thermal tolerance (OCLTT) is rapidly gaining popularity within climate change research and has been applied to several fish species. Here, we evaluated the relevance of aerobic performance of juvenile barramundi (Lates calcarifer) in the context of thermal preference and tolerance by (1) measuring standard and maximum metabolic rates (SMR and MMR, respectively) and AS of fish acclimated to 29°C and acutely exposed to temperatures from 23 to 38°C, (2) allowing the fish to behaviourally select a preferred temperature between 29 and 38°C, and (3) quantifying alterations to AS after 5 weeks of acclimation to 29 and 38°C. SMR and MMR both increased continuously with temperature in acutely exposed fish, but the increase was greater for MMR such that AS was highest at 38°C, a temperature approaching the upper lethal limit (40–41°C). Despite 38°C eliciting maximum AS, when given the opportunity the fish selected a median temperature of 31.7±0.5°C and spent only 10±3% of their time at temperatures >36°C. Following acclimation to 38°C, AS measured at 38°C was decreased to the same level as 29°C-acclimated fish measured at 29°C, suggesting that AS may be dynamically modulated independent of temperature to accommodate the requirements of daily life. Together, these results reveal limited power of the OCLTT hypothesis in predicting optimal temperatures and effects of climate warming on juvenile barramundi.

Exceptional aerobic scope and cardiovascular performance of pink salmon ( Oncorhynchus gorbuscha ) may underlie resilience in a warming climate

SUMMARY Little is known of the physiological mechanisms underlying the effects of climate change on animals, yet it is clear that some species appear more resilient than others. As pink salmon (Oncorhynchus gorbuscha) in British Columbia, Canada, have flourished in the current era of climate warming in contrast to other Pacific salmonids in the same watershed, this study investigated whether the continuing success of pink salmon may be linked with exceptional cardiorespiratory adaptations and thermal tolerance of adult fish during their spawning migration. Sex-specific differences existed in minimum and maximum oxygen consumption rates ( and , respectively) across the temperature range of 8 to 28°C, reflected in a higher aerobic scope () for males. Nevertheless, the aerobic scope of both sexes was optimal at 21°C (Topt) and was elevated across the entire temperature range in comparison with other Pacific salmonids. As Topt for aerobic scope of this pink salmon population is higher than in other Pacific salmonids, and historic river temperature data reveal that this population rarely encounters temperatures exceeding Topt, these findings offer a physiological explanation for the continuing success of this species throughout the current climate-warming period. Despite this, declining cardiac output was evident above 17°C, and maximum attainable swimming speed was impaired above ∼23°C, suggesting negative implications under prolonged thermal exposure. While forecasted summer river temperatures over the next century are likely to negatively impact all Pacific salmonids, we suggest that the cardiorespiratory capacity of pink salmon may confer a selective advantage over other species.

Simultaneous biologging of heart rate and acceleration, and their relationships with energy expenditure in free-swimming sockeye salmon (Oncorhynchus nerka).

Monitoring the physiological status and behaviour of free-swimming fishes remains a challenging task, although great promise stems from techniques such as biologging and biotelemetry. Here, implanted data loggers were used to simultaneously measure heart rate (fH), visceral temperature, and a derivation of acceleration in two groups of wild adult sockeye salmon (Oncorhynchus nerka) held at two different water speeds (slow and fast). Calibration experiments performed with individual fish in a swim tunnel respirometer generated strong relationships between acceleration, fH, tail beat frequency and energy expenditure over a wide range of swimming velocities. The regression equations were then used to estimate the overall energy expenditure of the groups of fish held at different water speeds. As expected, fish held at faster water speeds exhibited greater fH and acceleration, and correspondingly a higher estimated energy expenditure than fish held at slower water speeds. These estimates were consistent with gross somatic energy density of fish at death, as determined using proximate analyses of a dorsal tissue sample. Heart rate alone and in combination with acceleration, rather than acceleration alone, provided the most accurate proxies for energy expenditure in these studies. Even so, acceleration provided useful information on the behaviour of fish and may itself prove to be a valuable proxy for energy expenditure under different environmental conditions, using a different derivation of the acceleration data, and/or with further calibration experiments. These results strengthen the possibility that biologging or biotelemetry of fH and acceleration may be usefully applied to migrating sockeye salmon to monitor physiology and behaviour, and to estimate energy use in the natural environment.

Use of portable blood physiology point-of-care devices for basic and applied research on vertebrates: a review

Portable blood physiology meters exist that enable researchers to measure various parameters in field settings rather than having to store and transport samples. Although there is need for more thorough calibrations of these devices, they have much promise for conservation physiology of vertebrates.

Physiological Benefits of Being Small in a Changing World: Responses of Coho Salmon (Oncorhynchus kisutch) to an Acute Thermal Challenge and a Simulated Capture Event

Evidence is building to suggest that both chronic and acute warm temperature exposure, as well as other anthropogenic perturbations, may select for small adult fish within a species. To shed light on this phenomenon, we investigated physiological and anatomical attributes associated with size-specific responses to an acute thermal challenge and a fisheries capture simulation (exercise+air exposure) in maturing male coho salmon (Oncorhynchus kisutch). Full-size females were included for a sex-specific comparison. A size-specific response in haematology to an acute thermal challenge (from 7 to 20°C at 3°C h−1) was apparent only for plasma potassium, whereby full-size males exhibited a significant increase in comparison with smaller males (‘jacks’). Full-size females exhibited an elevated blood stress response in comparison with full-size males. Metabolic recovery following exhaustive exercise at 7°C was size-specific, with jacks regaining resting levels of metabolism at 9.3±0.5 h post-exercise in comparison with 12.3±0.4 h for full-size fish of both sexes. Excess post-exercise oxygen consumption scaled with body mass in male fish with an exponent of b = 1.20±0.08. Jacks appeared to regain osmoregulatory homeostasis faster than full-size males, and they had higher ventilation rates at 1 h post-exercise. Peak metabolic rate during post-exercise recovery scaled with body mass with an exponent of b∼1, suggesting that the slower metabolic recovery in large fish was not due to limitations in diffusive or convective oxygen transport, but that large fish simply accumulated a greater ‘oxygen debt’ that took longer to pay back at the size-independent peak metabolic rate of ∼6 mg min−1 kg−1. Post-exercise recovery of plasma testosterone was faster in jacks compared with full-size males, suggesting less impairment of the maturation trajectory of smaller fish. Supporting previous studies, these findings suggest that environmental change and non-lethal fisheries interactions have the potential to select for small individuals within fish populations over time.