Ecological and evolutionary consequences of metabolic rate plasticity in response to environmental change

Basal or standard metabolic rate reflects the minimum amount of energy required to maintain body processes, while the maximum metabolic rate sets the ceiling for aerobic work. There is typically up to three-fold intraspecific variation in both minimal and maximal rates of metabolism, even after controlling for size, sex and age; these differences are consistent over time within a given context, but both minimal and maximal metabolic rates are plastic and can vary in response to changing environments. Here we explore the causes of intraspecific and phenotypic variation at the organ, tissue and mitochondrial levels. We highlight the growing evidence that individuals differ predictably in the flexibility of their metabolic rates and in the extent to which they can suppress minimal metabolism when food is limiting but increase the capacity for aerobic metabolism when a high work rate is beneficial. It is unclear why this intraspecific variation in metabolic flexibility persists—possibly because of trade-offs with the flexibility of other traits—but it has consequences for the ability of populations to respond to a changing world. It is clear that metabolic rates are targets of selection, but more research is needed on the fitness consequences of rates of metabolism and their plasticity at different life stages, especially in natural conditions

Metabolic costs of feeding predictively alter the spatial distribution of individuals in fish schools

Group living is ubiquitous among animals [1, 2], but the exact benefits of group living experienced by individual groupmates is related to their spatial location within the overall group [3, 4, 5]. Individual variation in behavioral traits and nutritional state is known to affect interactions between individuals and their social group [6, 7], but physiological mechanisms underpinning collective animal behavior remain largely unexplored [8]. Here, we show that while fish at the front of moving groups are most successful at capturing food items, these individuals then show a systematic, post-feeding movement toward the rear of groups. Using observations of fish feeding in groups coupled with estimates of metabolic rate in fish consuming different meal sizes, we demonstrate that the magnitude of this shift in spatial position is directly related to the aerobic metabolic scope remaining after accounting for energetic costs of digestion. While previous work has shown that hungry individuals occupy anterior positions in moving groups [9, 10], our results show that the metabolic demand of food processing reduces the aerobic capacity available for locomotion in individuals that eat most, thus preventing them from maintaining leading positions. This basic trade-off between feeding and locomotor capacity could fundamentally dictate the spatial position of individuals within groups, perhaps obviating the role of individual traits in determining spatial preferences over shorter timescales (e.g., hours to days). This may be a general constraint for individuals within animal collectives, representing a key, yet overlooked, mediator of group functioning that could affect leadership, social information transfer, and group decision making

Hypoxia alters vulnerability to capture and the potential for trait-based selection in a scaled-down trawl fishery

No abstract available

Exploring key issues of aerobic scope interpretation in ectotherms: absolute versus factorial

Aerobic scope represents an animal’s capacity to increase its aerobic metabolic rate above maintenance levels (i.e. the difference between standard (SMR) and maximum (MMR) metabolic rates). Aerobic scope data can be presented in absolute or factorial terms (AAS or FAS, respectively). However, the robustness of these calculations to noise or variability in measures of metabolic rate can influence subsequent interpretations of patterns in the data. We explored this issue using simple models and we compared the predictions from these models to experimental data from the literature. First, we investigated the robustness of aerobic scope calculations as a function of varying SMR when MMR is fixed, and vice versa. While FAS is unexpectedly robust to variability in SMR, even in species with low aerobic scopes, AAS is less sensitive to variation in SMR than is FAS. However, where variation in MMR is the main concern, FAS is more robust than AAS. Our findings highlight the equal importance of minimising variability in MMR, rather than just the variability in SMR, to obtain robust aerobic scope estimates. Second, we analysed metabolic rate accounting for locomotor speed and body mass for swimming fish. The interactions among these factors in relation to AAS and FAS are complex and the appropriate metric is dependent on the specific eco-physiological context of the research question. We conclude with qualified recommendations for using and interpreting AAS and FAS

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

Adaptive effects of parental and developmental environments on offspring survival, growth and phenotype

1. Phenotypic adjustments to environmental variation are particularly relevant to cope with putative environmental mismatches often imposed by natal dispersal. 2. We used an intergenerational cross-transplant field-based experiment to evaluate the morphological and physiological effects of parental and postsettlement water flow environments on the orange-fin anemonefish Amphiprion chrysopterus through ontogeny (at pre- and postsettlement stages). 3. Offspring born from parents under high water flow had an 18% higher caudal fin aspect ratio (a compound measure of shape) at the presettlement stage, 10% slower growth after settlement, and 55% lower survival after settlement compared to offspring from low water flow parents. At the presettlement stage, caudal fin length was determined by parental caudal fin length. At the postsettlement stage, fish survived equally well with similar phenotypes in both high and low developmental flow environments. However, results suggest potential developmental phenotypic plasticity in caudal fin length, which increases more under low water flow during development. After settlement, growth was the only morphological or physiological trait that was associated with parental water flow, which was lower from parents under high flow, as was survival. 4. These results give important insights into the parental contribution, both genetic and nongenetic, in determining early offspring phenotype and subsequent growth and survival. Our results also suggest that offspring may possess flexibility to cope with a wide range of local environments including those different from their parents. Overall, the findings of this study show the fitness consequences of living in different environments and the likely trade-offs between parental and offspring fitness in a wild population

Physiological and behavioural effects of anemone bleaching on symbiont anemonefish in the wild

1. Climate change causes extreme heat waves that have induced worldwide mass coral bleaching. The impacts of temperature‐induced bleaching events on the loss of algal endosymbionts in both corals and anemones are well documented. However, the cascading impacts of bleaching on animals that live in association with corals and anemones are understudied. 2. We performed a field‐based experiment to investigate how host anemone bleaching affected the metabolic rate, growth, behaviour and survival of wild juvenile orange‐fin anemonefish Amphiprion chrysopterus over 1, 2 and (for survival) 9 months. 3. We found that the standard metabolic rate of anemonefish residing in bleached anemones decreased over time but was unaffected in fish from healthy anemones. Despite the reduced metabolic cost, the growth rate of fish from bleached anemones was significantly lower compared to fish from healthy anemones, suggesting that animals residing in bleached hosts are at an energetic disadvantage. This was corroborated by our finding that fish from bleached anemones spent more time out of their anemones, suggestive of a greater need to forage in the water column. However, fish from bleached anemones were overall less active and used less space around the anemone, resulting in a negative correlation between space use and survival after 4 weeks. 4. Our results provide insight into the physiological and behavioural effects of host bleaching on juvenile fish in the wild, and highlight how relatively short‐term thermal anomalies can have long‐lasting impacts beyond the bleached anemones or corals themselves

Guidelines for reporting methods to estimate metabolic rates by aquatic intermittent-flow respirometry

Interest in the measurement of metabolic rates is growing rapidly, because of the importance of metabolism in advancing our understanding of organismal physiology, behaviour, evolution and responses to environmental change. The study of metabolism in aquatic animals is undergoing an especially pronounced expansion, with more researchers utilising intermittent-flow respirometry as a research tool than ever before. Aquatic respirometry measures the rate of oxygen uptake as a proxy for metabolic rate, and the intermittent-flow technique has numerous strengths for use with aquatic animals, allowing metabolic rate to be repeatedly estimated on individual animals over several hours or days and during exposure to various conditions or stimuli. There are, however, no published guidelines for the reporting of methodological details when using this method. Here, we provide the first guidelines for reporting intermittent-flow respirometry methods, in the form of a checklist of criteria that we consider to be the minimum required for the interpretation, evaluation and replication of experiments using intermittent-flow respirometry. Furthermore, using a survey of the existing literature, we show that there has been incomplete and inconsistent reporting of methods for intermittent-flow respirometry over the past few decades. Use of the provided checklist of required criteria by researchers when publishing their work should increase consistency of the reporting of methods for studies that use intermittent-flow respirometry. With the steep increase in studies using intermittent-flow respirometry, now is the ideal time to standardise reporting of methods, so that - in the future - data can be properly assessed by other scientists and conservationists

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

No abstract available

Solving the conundrum of intra-specific variation in metabolic rate: A multidisciplinary conceptual and methodological toolkit

Researchers from diverse disciplines, including organismal and cellular physiology, sports science, human nutrition, evolution and ecology, have sought to understand the causes and consequences of the surprising variation in metabolic rate found among and within individual animals of the same species. Research in this area has been hampered by differences in approach, terminology and methodology, and the context in which measurements are made. Recent advances provide important opportunities to identify and address the key questions in the field. By bringing together researchers from different areas of biology and biomedicine, we describe and evaluate these developments and the insights they could yield, highlighting the need for more standardisation across disciplines. We conclude with a list of important questions that can now be addressed by developing a common conceptual and methodological toolkit for studies on metabolic variation in animals