Czechia

Small mammals are particularly vulnerable to increasing ambient heat loads and reduced food and water availability associated with climate change, given their high mass-specific metabolism, low thermal inertia, rapid water loss rate, and limited ability to store food and water. To better understand the mechanisms underlying this vulnerability, we implanted core body temperature and activity data loggers into meerkats (Suricata suricatta) and Cape ground squirrels (Xerus inauris), both of which are diurnal, and yellow mongooses (Cynictis penicillata), which exhibit some nocturnality, in the Kalahari of South Africa. We observed the behaviour of these habituated animals for one year while measuring black globe, air and burrow temperatures, solar radiation, wind, and rainfall. We also used infrared thermography to understand how surface body temperature relates to behaviour and core body temperature. Preliminary analyses indicate that animals avoided heat by retreating to shade and burrows, and responded to cold by shortening their active period and basking in the morning sun. These behavioural strategies may limit foraging time to replenish food and water. Our further analyses will assess the seasonal shifts in activity patterns and compare core body temperature patterns of all three species alongside their thermoregulatory behavioural strategies. We will also investigate the effects of reproductive behaviour and physiology (dispersal in males and pregnancy/lactation in females) on core body temperature. These findings will help us understand how small mammals in dryland environments respond to ongoing climate change and inform appropriate mitigation and conservation strategies.

SEB Conference 2024

The relationships between ambient heat load, behaviour and body temperature in small diurnal mammals in a dryland environment

environmental heat

small mammals

thermoregulation

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.

technical paper

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The mechanistic link between metabolic rate and foraging behaviour underpins several energy-based ecological theories, yet whether and how they interact remains unclear. Here we aimed to assess how modes of behaviour, in terms of cumulative space use, patch selection and time spent in an experimental resource patchy environment, are influenced by the foragers’ metabolic rate (SMR) and its main determinants i.e. body mass and temperature. We tested the individual behavioural patterns and metabolic rates of a model organism, the amphipod Gammarus insensibilis, across a range of body masses and temperatures. Our findings showed that body mass and temperature exert a major influence on foraging decisions and space use behaviour via their effects on metabolic rates. Individual cumulative space use was found to scale allometrically with body mass and exponentially with temperature, with patch giving-up time falling as body mass and temperature increased. Moreover, SMR had greater predictive power for behavioural patterns, explaining variation beyond that accounted for by body mass and temperature combined. Our results showed that cumulative space use scaled positively with mass-and-temperature-adjusted SMR (residual). Furthermore, the foraging decisions regarding patch choice and partitioning were strongly related to mass-and-temperature-adjusted SMR; individuals with higher mass-and-temperature-adjusted SMR initially preferred the most profitable patch and, as time progressed, abandoned the patch earlier compared to others. Our findings regarding the mechanistic relationship between behavioural patterns and metabolic rate across body mass and temperature shed light on higher-order energy-based ecological processes, with implications in the face of climate change.

Foraging decisions and space use behavior are linked to metabolic rate across temperatures

Animals on Earth are naturally exposed to environmental fluctuations, including changes in temperature, food availability and food quality. Their capacity to adapt to these environmental variations may be challenged by anthropogenic stressors, including global warming, extreme weather events, and changes in land use. The capacity of individuals to produce and use energy is an essential parameter in determining animals’ ability to cope with these environmental changes. In my talk, I will discuss how environmental stressors affect energy allocation in animals, exemplifying with own work on birds and fish, with the overarching goal to identify broad synergies and divergences in response to environmental change amongst endotherms and ectotherms. I will highlight the value of studying changes in energy metabolism at various stages of life and biological levels of organisation, to understand the mechanisms by which endotherms and ectotherms may maintain fitness in a changing world.

Similar challenges but different consequences: how climate change shapes metabolic strategies in endotherms and ectotherms

A paradox of avian long-distance migrations is that birds must greatly increase their body mass prior to departure, yet this is presumed to substantially increase their energy cost of flight, particularly given their tendency to fly relatively fast. However, our understanding of the interactive effects of speed and weight is limited on flight energy costs are based on a few constrained wind tunnel studies. The literature is missing experiments on free-ranging birds flying at similar speeds but with different body masses to test whether the additional energy costs of flying when heavier are very small as indicated by laboratory experiments, or are hyper-allometric as might be traditionally expected. We addressed this by undertaking a novel design of loading experiment on free-flying homing pigeons which utilised thin ventrally located weight and a heart rate data recorder. Our data show that when homing pigeons flying in a flock are loaded with ventral weight, both their heart rate and estimated energy expenditure barely rise. The net effect is that energy costs per unit time increase only slightly and per unit mass they decrease. We suggest that this is because homing pigeon flights are relatively fast, and consequently flight costs associated with increases in body parasite drag dominate over those of weight support, leading to an improvement in mass-specific flight economy. We propose that the small absolute aerodynamic penalty for carrying enlarged fuel stores and flight muscles during fast flight has helped to select for the evolution of long-distance migration.

Fat homing pigeons don't use more energy: an excellent animal model for investigating flight physiology in the wild

Birds are capable of incredible feats in the air, rapidly adapting flight to suit varying behavioural needs and environmental conditions. These feats are made possible through the interaction of biomechanical and sensory systems. One such system, mechanosensation, the ability to sense changes in aerodynamic forces caused by air flow, is thought to be critical for flight control. Notably in birds, vibration-based flow sensors are distributed throughout much of the wing surface; rather, they are localised at the base of the flight feathers. Therefore, it is flow-generated deformations of the passive and flexible flight feathers that are sensed by the flow sensors and not the airflow directly. The goal of this study is to understand how flow information is encoded by the feather aeroelastic response. Additionally, we aim to investigate how wing morphing behaviour can modify this structure-based signal processing. In a wind tunnel, we systematically altered the flow speed and direction acting on dried zebra finch (Taeniopygia guttata) wings in different morphs. By measuring and parametrising the shape of the frequency response under different flow conditions, we could then quantify how certain features of this vibration response can encode information on different flow characteristics. This study helps us understand the role wing structures play in flow sensing before any further neural signal processing and may inspire morphologically “smart” designs for distributed flow sensing in engineered structures.

Decoding aeroelastic response in flight feathers for flow sensing

Artificial light at night (ALAN) is a globally pervasive sensory pollutant that disrupts biological processes across taxa and at all levels of organisation, but its impact on colour-guided processes remains largely unexplored. This is especially concerning given the rapid and ongoing transition away from narrow-spectrum lighting and towards broad-spectrum technologies like white LEDs, which are rich in the short wavelengths of light to which many taxa are especially sensitive. Camouflage is particularly likely to be disrupted by broader ALAN spectra, due to changes in the conspicuousness of background matching prey altering prey recognition in visually guided predators. We simulated natural intensities of moonlight with and without ALAN, using both broad-spectrum ALAN and ALAN filtered to remove the characteristic short wavelength peak of white LEDs to test how exposure to these light treatments impacted predator-prey interactions between the intertidal crab Carcinus maenas and contrasting morphs of the colour-polymorphic snail Littorina obtusata. Exposure to broad-spectrum ALAN reduced overall predation by more than half and reversed the pattern of colour-based prey selection observed under control conditions. Exposure to filtered ALAN removed any significant difference in attack likelihood between colour morphs. Our results demonstrate that spectral composition is a crucial aspect of ALAN as a sensory pollutant, capable of instigating profound changes in predator-prey interactions that could drive changes in population demography and increase morphological homogeneity in species that depend on colour polymorphism for camouflage.

Now you see me, now you don't: artificial light at night alters predation on colour-polymorphic camouflaged prey

The evolution of increased thermal tolerance in aquatic ectotherms may affect genetically correlated traits and alter physiological performances. Here, we report the correlated responses of a range of life history, behavioural and physiological traits to seven generations of artificial selection for increased (Up-selected) or decreased (Down-selected) acute upper thermal tolerance limit (CTmax) in zebrafish (Danio rerio). Contrary to the prediction of a trade-off between warming and cooling tolerance, the thermal window increased in the Up-selected lines. No change was observed in the aerobic metabolic scope or in the thermal sensitivity of resting and maximum metabolic rates, thus contradicting the hypothesis that thermal tolerance limits are controlled by aerobic scope. We also found no difference in brain heat shock protein levels between the selected lines, contradicting the hypothesized role of heat shock protein expression in the evolution of acute warming tolerance. Finally, fecundity, growth and swimming speed did not change in the Up-selected lines, but tended to decrease in the Down-selected lines, suggesting that the evolution of lower thermal tolerance is accompanied by a decrease in individual quality. These results suggest that selection due to acute heating events can benefit tolerance to cold, making individuals more resilient to extreme temperature events.

Selection on warming tolerance alters physiology and life history traits in zebrafish

Coral-dwelling fish experience large daily fluctuations in oxygen, with hyperoxia occurring during the day and hypoxia building up at night. Nighttime hypoxia can be particularly severe between the branches of corals and intensifies in warmer temperatures due to the high respiring biomass of many shelter-seeking organisms. The damselfish, Dascyllus aruanus, is one of the species that seeks shelter within corals and must tolerate hypoxia on a nightly basis. Here we use a combination of field dissolved oxygen measurements, in situ underwater video recordings on the coral reef, and lab experiments to ask whether Dascyllus aruanus has evolved specific behavioural (e.g., changes in activity and sheltering) and physiological (e.g. changes in vision) adaptations to enhance performance under hypoxia. We compare these results to the nocturnal cardinalfish Ostorhinchus angustatus, which rarely experiences hypoxia, and predict it lacks hypoxia-related adaptations. Given the anticipated rise in severe hypoxia occurrences, understanding these adaptations is crucial for assessing the resilience of these species to a changing climate. By using a variety of methods, we aim to gain a new perspective on how oxygen shapes the behaviour and physiology of coral reef fish.

Behavioural and physiological responses of coral reef fish to progressive hypoxia

Nuclear Pore Complexes (NPCs) are large macromolecular assemblies embedded into the nuclear envelope (NE). Their main function is to mediate the selective nucleocytoplasmic transport of macromolecules, although they are involved in other processes such as chromatin organization, and DNA repair. NPCs are organized into subcomplexes composed of repetitions of about 30 highly conserved nucleoporins (NUPs). The NUP107–160 complex is in the outer ring and is conserved between distantly related eukaryotes such as yeast and mammals. Here, we are going to focus on two Arabidopsis mutants deficient for this subcomplex: nup160 and nup96, also known as suppressor of auxin resistance1 (sar1) and sar3, respectively. NUP160 and NUP96 are critical for the nucleocytoplasmic transport of mRNAs and play important functions in auxin signalling, plant growth, and flowering time regulation, as well as in immune defence and cold stress tolerance. In the context of our global study about the possible role of NPCs during meiosis, we decided to explore the potential function of NUP160 and NUP96 during this cell division because the corresponding mutants show reduced fertility. The results of our study have demonstrated that meiosis is altered in a percentage of the meiocytes from these mutants, which would explain the reduction in the number of seeds. Our observations have revealed that the alteration of the NUP107-160 complex causes problems related to chromatin instability with abnormalities associated with condensation and fragmentation. The possible origins of these problems will be discussed.

The connection between structural nucleoporins and meiosis: when the chromatin collapses.

Paramutation represents a clear exception to the principles of inheritance established by Gregor Mendel in the 19th century. It involves the transfer of repressive epigenetic marks from a silent to an active allele and thereby violates Mendel's first law of independent allele segregation. By violating Mendel's first law of independent allele segregation, paramutation results from the transfer of repressive epigenetic marks from silent to active homologous alleles. It is best known from conspicuous pigmentation phenotypes in maize but the Paramutation phenomena was also reported across diverse plant and animal species. Paramutation-like events are common in tomato hybrids suggesting that paramutation may be less exceptional and rather a frequently co-occurring process during cross-hybridisation.



Here we use the classic example of paramutation in tomato – sulfurea (sulf), an understudied chlorosis phenotype associated with transgenerationally dependent allele segregation patterns – to dissect the epigenetic- and transgenerational mechanisms underlying paramutation in tomato plants. Our results show that the DNA- and histone-methyl transferases CMT3 and KYP are required for the maintenance of paramutation and that there is a change in chromatin architecture associated with the silent epiallele. We further demonstrate that in tomato the developmental and transgenerational maintenance of paramutation might be independent of sRNAs, which were previously suggested to explain the trans-communication between homologues as well as the maintenance of silent paramutated states across mitotic and meiotic divisions in maize. Together, our data significantly extends the current understanding of the paramutation model in plants by integrating existing concepts into a revised framework of non-Mendelian heredity.

Defying Mendel's laws: sulfurea paramutation unveils new principles of epigenetic inheritance in tomato.

Plants in the natural environment experience continuous dynamic changes in light intensity. We have limited understanding on how plants adapt to such variable conditions. Here, we exposed Arabidopsis thaliana plants to naturally fluctuating light regimes alongside traditional square light regimes such as those often found in control environment growth chambers. The physiological response was highly consistent across experiments, indicating the involvement of an epigenetic mechanism, leading us to investigated differences in DNA methylation. Our results identified a large number of alterations in DNA methylation patterns between fluctuating light acclimated plants, and square light acclimated plants, demonstrating natural fluctuations in light impacts the plant epigenetic mechanisms. Most importantly, there are more differences in DNA methylation patterns between different light pattern regimes than between different light intensities. These differences in DNA methylation were accompanied by significant changes in gene expression, some of which correlated with altered DNA methylation. Interestingly, several transposable elements which displayed differential methylation were found to be differentially expressed between light regimes. Our data suggests DNA methylation plays a role in acclimation to natural light which may directly regulate gene expression and impact transposable element activation.

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