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Metabolic rate represents an organism’s cost of living, as it sets its demands for food and oxygen from the environment. Yet, within species, an approximately 2-fold variation in metabolic rate exists among comparable individuals, so that one individual can have twice the metabolic rate of another of the same age, size, and sex. In addition to this variation in metabolic rate at a given size, variation also exists among individuals in how steeply metabolic rate changes (scales) with body size, but the causes and consequences of individual variation in metabolic rate and its scaling relationship with body size are poorly understood. Using examples from my work on fish, I will here discuss how and why there is variation in metabolic rate and its scaling, and what it means for our understanding of the physiology, ecology, and life-history of animals.

SEB Conference 2024

Animal President Medallist Talk - Dr. Tommy Norin

Metabolic rate is closely related to body size (body mass), but when mass increases, metabolic rate usually increases less. This allometric scaling relationship between metabolic rate and body mass is fundamental to biology and widely applied, but also one of the most debated concepts in integrative and comparative physiology, ecology, and evolutionary biology.

Several theories and hypotheses have been put forward to explain why and how metabolic rate scales with body mass, and why there appears to be variation in how steep this scaling relationship is among different taxa and physiological or ecological conditions (e.g. 'surface area', 'cell size', 'fractal distribution network', ‘dynamic energy budget’, and ‘metabolic-level boundaries’ theories or hypotheses). However, the lack of consensus on these important topics is a major barrier to our understanding of the pace at which organisms of different sizes and species expend energy and need to consume resources such as food and oxygen from the environment. It also limits our ability to predict how metabolic rate and body size (co)evolves, and how climate change affects metabolic demands and body sizes, as metabolic scaling exponents are used to model how these key organismal traits are affected by changing temperature and oxygen levels. The importance of metabolic scaling is clear, yet it remains one of the most controversial concepts in biology.

The overall aim of this satellite meeting is to bring together researchers working with metabolic scaling, to: (1) bring the field up to speed on state-of-the-art knowledge and research on metabolic scaling; (2) help understand how the vastly different views and opinions on metabolic scaling can persist despite more than a century of research (e.g. scaling in proportion to surface area or not, universal ¾-power scaling or not, governed by ecological vs. physical or geometric factors); and (3) identify and help streamline specific areas of research on metabolic scaling that will be particularly important for our further understanding of why and how metabolic rate scales with body size.

The meeting is being organised as part of the Animal Section of the SEB and will therefore have a focus on metabolic scaling of animals, but work on other organisms is welcome where this can provide insight into metabolic scaling in general.

Why and how does metabolic rate scale with body size?

The overall aim of this satellite meeting is to bring together researchers working with metabolic scaling, to: bring the field up to speed on state-of-the-art knowledge and research on metabolic scaling; help understand how the vastly different views and opinions on metabolic scaling can persist despite more than a century of research (e.g. scaling in proportion to surface area or not, universal ¾-power scaling or not, governed by ecological vs. physical or geometric factors); and identify and help streamline specific areas of research on metabolic scaling that will be particularly important for our further understanding of why and how metabolic rate scales with body size.

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Increasing drought frequency and duration pose a significant threat to fish species in dryland river systems. As ectotherms, thermal and hypoxia tolerances directly determine the capacity of fish species to persist in these environments during low flow periods when water temperatures are high and waterbodies become stratified. Managing the ecological function of dryland river refugia requires an understanding of how chronically elevated temperatures and hypoxia affect fish physiological performance, and their capacity to compensate performance in response. We studied the effects of chronic high temperature (30oC) or chronic hypoxia (50% air saturation) on two species of freshwater fish, golden perch Macquaria ambigua, and Murray cod, Maccullochella peelii. In both species, cross tolerance resulted in improved hypoxia and thermal tolerance limits following acclimation to either chronic hypoxia or high temperature. Physiological plasticity of the heart also resulted following acclimation to hypoxic waters in golden perch, increasing in size to support an elevated oxygen transport capacity. In Murray cod, body size significantly affected thermal and hypoxia responses. Small M. peelii were significantly less hypoxia tolerant than larger individuals, while larger fish were significantly less thermally tolerant than smaller fish. Our data suggests that acclimation to elevated temperature or elevated hypoxia can improve both hypoxia and thermal tolerance limits in some fish species, but that responses man differ across size classes. This information will be critical in developing habitat suitability models to inform policy decisions that serve to balance competing demands on freshwater resources in dryland rivers.

Between a hot place and hypoxia: Physiological responses of fish to high temperature and hypoxia in dryland river systems

Coastal and estuary ecosystems are increasingly subjected to compound events, where multiple extreme events such as marine heatwaves (MHW) and hypoxia occur simultaneously. Given the fundamental role of temperature and oxygen in biological processes, the combined alteration of these parameters is often expected to have non-linear effects on organisms. However, the potential for an extreme temperature event to elicit a different response than gradual warming when combined with hypoxia remains understudied. Therefore, we examined the within-generational response to simultaneous hypoxia and MHW, and the transgenerational plastic responses during the recovery phase of the foundational marine copepod species, Acartia tonsa. In more detail, we measured survival, egg production rates, metabolic rates and upper thermal limits on mature males and females (F1) following a five-day exposure to the isolated and combined effects of hypoxia and a MHW, and on their offspring (F2) placed back in a control condition for their whole development, once they reached adulthood. Surprisingly, we observed only synergistic effects for F1 males’ upper thermal limits and no strong carry-over effects in the recovering F2 coming from the parental combined condition. However, MHW had a dominant effect on the physiology of A. tonsa, decreasing survival, increasing metabolic rates and causing strong carry-over effects on F2 individuals’ survival. These results indicate that potential cross-protection mechanisms between the two stressors were at play, enabling copepods to face the deletarious effects of MHW when exposed simultaneously to hypoxia. This supports the importance of looking at the impact of compound events on marine organisms.

Two extreme events are better than one? Physiological responses following simultaneous exposure to hypoxia and marine heatwave in Acartia tonsa 

Florida Bay’s shallow seagrass beds experience daily diurnal fluctuations in environmental oxygen, leading to hypoxic episodes (PO2 < 2 mg∙L-1, 4.6 kPa) that have increased in recent decades. To survive, the native Gulf toadfish can employ a suite of adaptive cardiorespiratory and metabolic adjustments. Previous work has demonstrated that toadfish reduce heart rate (HF) and increase ventilatory amplitude during moderate hypoxia (PO2 ~2-4 kPa for 20 min). Toadfish also have a regulation index of 0.5, suggesting that they use strategies other than maintaining oxygen consumption to tolerate hypoxia. The objective of this study was to characterize the acute response of Gulf toadfish to severe hypoxia (< 2 kPa). We hypothesized that Gulf toadfish would respond to severe hypoxia by reducing energy expenditure while switching to anaerobic metabolism. Cannulated adult toadfish (0.062 kg ± 0.003; n=29) were exposed to either control conditions (normoxia for 4 h) or hypoxia (PO2 ~ 0.44 kPa for 3 h followed by 1 h recovery). Cardiovascular and ventilatory parameters were monitored and blood samples were taken from both groups at t = 0, 1.5, and 4 h, and analyzed for pH, glucose, lactate, and other endpoints. Hypoxia-exposed fish experienced a ~72% decrease in HF and a ~25% decrease in VF during hypoxia exposure. Moreover, plasma glucose concentrations increased 5-fold, and plasma lactate concentrations increased 10-fold while pH decreased by 2.7% during hypoxia exposure. Our findings support our hypothesis that toadfish survive hypoxia by reducing energy expenditure and switching to anaerobic metabolism.

The key mechanisms associated with the survival of Gulf toadfish, Opsanus beta, when in severe hypoxia

Migratory flight is an intensive exercise that requires birds to maintain high aerobic capacities for many hours or days. Maintaining oxygen supply to flight muscles is therefore important during migration, especially since tracking studies have shown that songbirds will ascend to altitudes of 6,000 m during migratory flight where oxygen is less readily available (hypoxia). Whether there are adaptations or seasonal plasticity along the oxygen cascade and hypoxic chemoreflex that allow songbirds to fly at such high altitudes during the migratory season is unknown. Research during my postdoc has shown that migratory songbirds exhibit seasonal plasticity along the oxygen cascade which enhance oxygen uptake and movement to the flight muscle during migration. This includes changes in breathing pattern, haemoglobin-oxygen binding affinity, and muscle fiber size and phenotype. We have also shown that the magnitude of seasonal plasticity may be dictated by migratory distance and/or whether the songbird species is migratory or resident. Additionally, in yellow-rumped warblers there appears to be a blunted hypoxic chemoreflex in response to flight at high altitude (~3,000 m above sea level). Measurements of adrenaline concentration increased with flight, but were not significantly higher when flight was conducted at high altitude. Together, these findings show that songbirds exhibit seasonal plasticity along the oxygen cascade which would be important for maintain oxygen movement to the flight muscle during high altitude flight.

Seasonal flexibility along the oxygen cascade allows for high-altitude flights in migratory songbirds

Heatwaves and hypoxic events are major stressors for marine fishes in an era of global change. We investigated impacts of these extreme events on growth and indicators of metabolism in the three genetically distinct populations of European seabass, Atlantic (AT), West and East-Mediterranean (WM, EM). Fish were reared in common garden in three seasonal thermal regimes that reflect their natural environments (eAT 10.2-18.4°C; eWM 12.5-23.0°C; eEM 16.7-28.0°C) and, at peak summer temperature, subsamples were weighed, measured and exposed in triplicate for 10 days to a heatwave (+4°C), hypoxia (50% saturation), heatwave+hypoxia, or control. At the end of the events, weight and length were measured, and blood samples were collected to measure plasma indicators of energy and hydromineral homeostasis (glucose, lactate, triglycerides, protein, calcium, chloride, sodium, osmotic pressure). By comparison to the control, in eAT warming from 18.4 to 22.4°C stimulated feeding and growth, an effect abolished by hypoxia and hypoxia+heatwave. In eWM, there was little effect of heatwave or hypoxia on growth, but heatwave+hypoxia caused some inhibition. In eEM, all the extreme events caused loss of appetite and weight loss. Despite evolving in different thermal environments, the three populations did not differ in the effects of the extreme events on growth, plasma indicators are being analysed. The results demonstrate that heatwaves can be beneficial for growth in cold environments, that seabass are resilient to moderate hypoxia even when in combination to a heatwave, but extreme events clearly have negative effects in warmer environments.

Impacts of heatwaves and hypoxia on three European seabass Dicentrarchus labrax populations reared in three seasonal thermal regimes

Confidence and competence in skills pertaining to data manipulation, analysis, interpretation, and presentation are increasingly sort and valued across numerous sectors but improving these competencies in students can be challenging. There is a disconnect between the steps taken to understand and analyse data and then present findings in a professional setting and students frequently struggle with this. In response to this, I have created fresh resources, introduced new teaching tools, modified assessment strategy and reinforced key concepts in data literacy across the curriculum with an aim of improving student engagement and attainment in the data sciences. This process, as with many advances in improving pedagogical practice, has largely been ad hoc and evidence for initial success and impact began as observational and qualitative. However, long-term cohort wide data sets can come into effect with consistent use of assessment and marking strategy. Here, I show how different evidence can be used to measure impact of pedagogical practice to students and then how this evidence can be applied to guide course curriculums, and more broadly, influence best practice beyond the institution.

Scholarship in data literacy; establishing evidence of pedagogical efficacy and measuring impact and influence within and beyond the institution.

The process of joining compatible plants that then continue to grow together, also known as plant grafting, offers a platform for manipulating agronomically relevant traits spanning both favourable and undesirable traits. In this study, we investigated the changes in crop productivity between eggplant and tomato heterografts using a comprehensive approach that integrates phenotypic, physiologic, and genomic data. We observed that a rootstock can affect the physiology and horticultural trait of the scion. Through genomic analysis and an innovative mapping approach, we identified potential mobile RNA molecules associated to the alteration observed. Our study highlights how grafting could be a valuable tool as an alternative perspective to investigating the molecular basis of phenotypic traits, thereby laying the groundwork for further investigations aimed at optimizing crop yield.

Mobile RNAs and their potential role in grafting-induced traits in Solanaceous heterografts

Understanding crop yield requires navigating the intricate interaction between genotype and environments (GxE), which presents challenges for accurate predictions due to the plant's plastic responses. To study the environmental impacts on grain yield, we addressed two questions: Q1) Do environmental factors affect the consistency (R2trait) of trait performance? Q2) Can physiological relationships between traits across field environments be represented by simulation (APSIM-wheat)? To explore the GxE effect on trait performance of yield (R2yield), we utilise a multi-environment trials (MET) dataset featuring 220 genotypes and 45 environments over three years, five locations and three managements. The management includes combinations of two treatments: total nitrogen fertiliser application (high-HN: 220 kg N ha-1, low-LN: 110 kg N ha-1) and fungicide application (with-WF, without-NF). Resulting three managements are HN_WF, HN_NF and LN_NF. R2trait is calculated using standardised major axis (SMA) regression between two environments grouped by three environmental factors: management, location and year. Trait-trait Pearson correlation (r) was calculated between nine traits in both field and simulation dataset. Our results reveal: 1) significance differences in R2yield between all environmental factors, notably with HN_WF reducing R2yield comparing to HN_NF, indicating varying genotypic responses to fungicide. 2) simulation results confirm a trade-off between grain number and grain protein, but highlight discrepancies in dry matter allocation to grain yield and straw dry matter at maturity between fields and simulation. These insights underscore the indispensable role of understanding environmental influences on trait performance for precise phenotype prediction and crop modelling.

Unravelling yield consistency in winter wheat (Triticum aestivum L.): insights from multi-environment trials and crop simulation

In West Africa, cereals production per capita is declining due to the fast growth in population outpacing the increase in food production. Moreover, models predict that global changes will reduce cereals yield in this region. Improve crop productivity and resilience is therefore a major challenge. Pearl millet is a key cereal for food security in sub-Saharan Africa, mostly grown in areas with limited agronomic potential characterized by low rainfall and low-fertility soils. 
Root traits represent potential new targets for breeding pearl millet varieties more adapted to future climate scenarios. The aim of this work was to characterize the main water stress pattern faced by pearl millet in West Africa and to identify root traits that contribute to tolerance to this stress. 
Crop modelling revealed that vegetative drought stress is a major constraint in the Sahel. Subsequently, a panel of 160 newly re-sequenced inbred lines was grown under irrigated and vegetative drought stress over two years in field conditions in Senegal and was phenotyped for root anatomical traits, as well as yield components traits. We observed a large diversity of response to drought stress for root traits and yield stress tolerance indexes. We found that some root vasculature traits were associated with tolerance to vegetative drought stress. Further physiological studies suggest a link between metaxylem traits and transpiration efficiency and suggest an overall strategy to deal with vegetative stress. QTLs controlling these traits were identified by association genetics. Our results could provide new avenues to improve drought tolerance in pearl millet.


Targeting root traits to improve tolerance to vegetative drought episodes in pearl millet (Pennisetum glaucum L.) 

Reproductive senescence is increasingly reported to occur in vertebrate populations in the wild but how the onset and rate of reproductive senescence vary in response to environmental fluctuations remains poorly understood. Taking benefit on a long-term detailed individual monitoring of reproductive performance of known-aged females for over 35 years in a forest roe deer population in western France, we first provide firm evidence that both pregnancy rates and litter size display senescence, with different age at onset and different rate of senescence. Then, we show that cohort quality markedly influences reproductive senescence patterns. Moreover, condition-dependence of reproductive performance differs both across female ages and among cohorts of different quality.

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