Oxygen availability and body mass modulate ectotherm responses to ocean warming.

In an ocean that is rapidly warming and losing oxygen, accurate forecasting of species' responses must consider how this environmental change affects fundamental aspects of their physiology. Here, we develop an absolute metabolic index (ΦA) that quantifies how ocean temperature, dissolved oxygen and organismal mass interact to constrain the total oxygen budget an organism can use to fuel sustainable levels of aerobic metabolism. We calibrate species-specific parameters of ΦA with physiological measurements for red abalone (Haliotis rufescens) and purple urchin (Strongylocentrotus purpuratus). ΦA models highlight that the temperature where oxygen supply is greatest shifts cooler when water loses oxygen or organisms grow larger, providing a mechanistic explanation for observed thermal preference patterns. Viable habitat forecasts are disproportionally deleterious for red abalone, revealing how species-specific physiologies modulate the intensity of a common climate signal, captured in the newly developed ΦA framework.

Ocean warming favours a northern Argyrosomus species over its southern congener, whereas preliminary metabolic evidence suggests that hybridization may promote their adaptation.

Anthropogenic-induced climate change is having profound impacts on aquatic ecosystems, and the resilience of fish populations will be determined by their response to these impacts. The northern Namibian coast is an ocean warming hotspot, with temperatures rising faster than the global average. The rapid warming in Namibia has had considerable impacts on marine fauna, such as the southern extension of the distribution of Argyrosomus coronus from southern Angola into northern Namibian waters, where it now overlaps and hybridizes with the closely related Namibian species, A. inodorus. Understanding how these species (and their hybrids) perform at current and future temperatures is vital to optimize adaptive management for Argyrosomus species. Intermittent flow-through respirometry was used to quantify standard and maximum metabolic rates for Argyrosomus individuals across a range of temperatures. The modelled aerobic scope (AS) of A. inodorus was notably higher at cooler temperatures (12, 15, 18 and 21°C) compared with that of A. coronus, whereas the AS was similar at 24°C. Although only five hybrids were detected and three modelled, their AS was in the upper bounds of the models at 15, 18 and 24°C. These findings suggest that the warming conditions in northern Namibia may increasingly favour A. coronus and promote the poleward movement of the leading edge of their southern distribution. In contrast, the poor aerobic performance of both species at cold temperatures (12°C) suggests that the cold water associated with the permanent Lüderitz Upwelling Cell in the south may constrain both species to central Namibia. This is most concerning for A. inodorus because it may be subjected to a considerable coastal squeeze.

Breathless through Time: Oxygen and Animals across Earth's History.

AbstractOxygen levels in the atmosphere and ocean have changed dramatically over Earth history, with major impacts on marine life. Because the early part of Earth's history lacked both atmospheric oxygen and animals, a persistent co-evolutionary narrative has developed linking oxygen change with changes in animal diversity. Although it was long believed that oxygen rose to essentially modern levels around the Cambrian period, a more muted increase is now believed likely. Thus, if oxygen increase facilitated the Cambrian explosion, it did so by crossing critical ecological thresholds at low O2. Atmospheric oxygen likely remained at low or moderate levels through the early Paleozoic era, and this likely contributed to high metazoan extinction rates until oxygen finally rose to modern levels in the later Paleozoic. After this point, ocean deoxygenation (and marine mass extinctions) is increasingly linked to large igneous province eruptions-massive volcanic carbon inputs to the Earth system that caused global warming, ocean acidification, and oxygen loss. Although the timescales of these ancient events limit their utility as exact analogs for modern anthropogenic global change, the clear message from the geologic record is that large and rapid CO2 injections into the Earth system consistently cause the same deadly trio of stressors that are observed today. The next frontier in understanding the impact of oxygen changes (or, more broadly, temperature-dependent hypoxia) in deep time requires approaches from ecophysiology that will help conservation biologists better calibrate the response of the biosphere at large taxonomic, spatial, and temporal scales.

Integrative Approaches to Understanding Organismal Responses to Aquatic Deoxygenation.

AbstractOxygen bioavailability is declining in aquatic systems worldwide as a result of climate change and other anthropogenic stressors. For aquatic organisms, the consequences are poorly known but are likely to reflect both direct effects of declining oxygen bioavailability and interactions between oxygen and other stressors, including two-warming and acidification-that have received substantial attention in recent decades and that typically accompany oxygen changes. Drawing on the collected papers in this symposium volume ("An Oxygen Perspective on Climate Change"), we outline the causes and consequences of declining oxygen bioavailability. First, we discuss the scope of natural and predicted anthropogenic changes in aquatic oxygen levels. Although modern organisms are the result of long evolutionary histories during which they were exposed to natural oxygen regimes, anthropogenic change is now exposing them to more extreme conditions and novel combinations of low oxygen with other stressors. Second, we identify behavioral and physiological mechanisms that underlie the interactive effects of oxygen with other stressors, and we assess the range of potential organismal responses to oxygen limitation that occur across levels of biological organization and over multiple timescales. We argue that metabolism and energetics provide a powerful and unifying framework for understanding organism-oxygen interactions. Third, we conclude by outlining a set of approaches for maximizing the effectiveness of future work, including focusing on long-term experiments using biologically realistic variation in experimental factors and taking truly cross-disciplinary and integrative approaches to understanding and predicting future effects.

Thermal tolerance, safety margins and vulnerability of coastal species: Projected impact of climate change induced cold water variability in a temperate African region.

Anthropogenic induced climate change is predicted to increase the thermal variability in coastal waters, which can have strong physiological effects on individuals and populations of marine ectotherms. The magnitude and direction of these thermal effects varies depending on species, life stage, biogeography, habitat and season. This study aimed to compare the thermal tolerance of a range of juvenile fish and adult macro-invertebrates from intertidal and estuarine habitats in a warm-temperate, thermally variable region on the south-east coast of South Africa. Seasonal variability in thermal tolerance was compared between species, taxonomic groups, biogeographical distribution and habitat affinity and related to existing and projected water temperature data to gauge the local vulnerability of each species. Critical thermal maximum (CTmax), critical thermal minimum (CTmin), thermal breadths and scopes, and the thermal safety margins of each species were quantified. The greatest differences in thermal tolerance patterns were based on taxonomy, with macro-invertebrates having broader thermal tolerance compared to fish, with the exception of the Cape sea urchin, in both summer and winter. Relatively narrow lower breadths in tolerance and safety margin values for transient juvenile sub-tropical and temperate fish species from the intertidal rocky low-shore habitat were observed in both summer and winter. This indicates that these fish species and the Cape sea urchin may be more vulnerable to projected increases in cold temperature (upwelling in summer) than warm temperature variability in this warm-temperate region if they are unable to seek thermal habitat refuge.

The use of internal heart rate loggers in determining cardiac breakpoints of fish.

As marine environments are influenced by global warming there is a need to thoroughly understand the relationship between physiological limits and temperature in fish. One quick screening method of a physiological thermal tipping point is the temperature at which maximum heart rate (ƒHmax) can no longer scale predictably with warming and is referred to as the Arrhenius break temperature (TAB). The use of this method has been successful for freshwater fish by using external electrodes to detect an electrocardiogram (ECG), however, the properties of this equipment pose challenges in salt water when evaluating marine fish. To overcome these challenges, this study aimed to explore the potential use of implantable heart rate loggers to quantify the TAB of Chrysoblephus laticeps, a marine Sparid, following the ECG method protocols where ƒHmax is monitored over an acute warming event and the TAB is subsequently identified using a piece-wise linear regression model. Of the nine experimental fish, only five (56%) returned accurate ƒHmax data. The TAB of successful trials was identified each time and ranged from 18.09 to 20.10 °C. This study therefore provides evidence that implantable heart rate loggers can estimate TAB of fish which can be applied to many marine species.

Implantation, orientation and validation of a commercially produced heart-rate logger for use in a perciform teleost fish.

Quantifying how the heart rate of ectothermic organisms responds to environmental conditions (e.g. water temperature) is important information to quantify their sensitivity to environmental change. Heart rate studies have typically been conducted in lab environments where fish are confined. However, commercially available implantable heart rate biologgers provide the opportunity to study free-swimming fish. Our study aimed to determine the applicability of an implantable device, typically used on fusiform-shaped fish (e.g. salmonids), for a perciform fish where morphology and anatomy prevent ventral incisions normally used on fusiform-shaped fish. We found that ventrolateral incisions allowed placement near the heart, but efficacy of the loggers was sensitive to their orientation and the positioning of the electrodes. Electrocardiogram detection, signal strength and subsequent heart rate readings were strongly influenced by logger orientation with a significant effect on the quality and quantity of heart rate recordings. We provide details on the surgical procedures and orientation to guide future heart rate biologger studies on perciform-shaped fish.

Different drivers, common mechanism; the distribution of a reef fish is restricted by local-scale oxygen and temperature constraints on aerobic metabolism.

The distributions of ectothermic marine organisms are limited to temperature ranges and oxygen conditions that support aerobic respiration, quantified within the metabolic index (ϕ) as the ratio of oxygen supply to metabolic oxygen demand. However, the utility of ϕ at local scales and across heterogenous environments is unknown; yet, these scales are often where actionable management decisions are made. Here, we test if ϕ can delimit the entire distribution of marine organisms when calibrated across an appropriate temperature range and at local scales (~10 km) using the endemic reef fish, Chrysoblephus laticeps, which is found in the highly heterogenous temperature and oxygen environment along the South African coastal zone, as a model species. In laboratory experiments, we find a bidirectional (at 12°C) hypoxia tolerance response across the temperature range tested (8 to 24°C), permitting a piecewise calibration of ϕ. We then project this calibrated ϕ model through temperature and oxygen data from a high spatial resolution (11 to 13 km) ocean model for the periods 2005 to 2009 and 2095 to 2099 to quantify various magnitudes of ϕ across space and time paired with complementary C. laticeps occurrence points. Using random forest species distribution models, we quantify a critical ϕ value of 2.78 below which C. laticeps cannot persist and predict current and future distributions of C. laticeps in line with already observed distribution shifts of other South African marine species. Overall, we find that C. laticeps' distribution is limited by increasing temperatures towards its warm edge but by low oxygen availability towards its cool edge, which is captured within ϕ at fine scales and across heterogenous oxygen and temperature combinations. Our results support the application of ϕ for generating local- and regional-scale predictions of climate change effects on organisms that can inform local conservation management decisions.

Exploitation may influence the climate resilience of fish populations through removing high performance metabolic phenotypes.

Physiological rates and processes underpin the relationships between ectothermic organisms, such as fish, and their environment. The response and persistence of fish populations in an increasingly variable ocean is dependent on the distribution and diversity of physiological phenotypes. Growing evidence suggests that fisheries exploitation can selectively target certain physiological and behavioural phenotypes, which may shift exploited populations to altered physiological states. Here we test if commercial fisheries have the potential to do this in a "natural laboratory" along the South African coast. We compare metabolic traits of exploited and protected populations of the fish species, Chrysoblephus laticeps, which is a major component of the South African hook and line fishery. We find that high-performance aerobic scope phenotypes are reduced in the fished population. The most likely mechanism for this finding is a positive relationship between aerobic scope and capture vulnerability in passive-gear fisheries. Our results further highlight the selective nature of capture-fisheries and suggest that exploitation has the capacity to alter climate responses of fish populations on a physiological level. Our finding also implicates how Marine Protected Areas, through harbouring individuals with a greater diversity of physiological traits, may provide greater fish response diversity to environmental variability.