Dynamic body acceleration as a proxy to predict the cost of locomotion in bottlenose dolphins

Estimates of the energetic costs of locomotion (COL) at different activity levels are necessary to answer fundamental eco-physiological questions and to understand the impacts of anthropogenic disturbance to marine mammals. We combined estimates of energetic costs derived from breath-by-breath respirometry with measurements of overall dynamic body acceleration (ODBA) from biologging tags to validate ODBA as a proxy for COL in trained common bottlenose dolphins (Tursiops truncatus). We measured resting metabolic rate (RMR); mean individual RMR was 0.71-1.42 times that of a similarly sized terrestrial mammal and agreed with past measurements which used breath-by-breath and flow-through respirometry. We also measured energy expenditure during submerged swim trials, at primarily moderate exercise levels. We subtracted RMR to obtain COL, and normalized COL by body size to incorporate individual swimming efficiencies. We found both mass-specific energy expenditure and mass-specific COL were linearly related with ODBA. Measurements of activity level and cost of transport (the energy required to move a given distance) improve understanding of the costs of locomotion in marine mammals. The strength of the correlation between ODBA and COL varied among individuals, but the overall relationship can be used at a broad scale to estimate the energetic costs of disturbance, daily locomotion costs to build energy budgets, and investigate the costs of diving in free-ranging animals where bio-logging data are available. We propose that a similar approach could be applied to other cetacean species.

Energetic costs of ectoparasite infection in Atlantic salmon

Parasites are widespread in nature where they affect energy budgets of hosts, and depending on the imposed pathogenic severity, this may reduce host fitness. However, the energetic costs of parasite infections are rarely quantified. In this study, we measured metabolic rates in recently seawater adapted Atlantic salmon (Salmo salar) infected with the ectoparasitic copepod Lepeophtheirus salmonis and used an aerobic scope framework to assess the potential ecological impact of this parasite-host interaction. The early chalimus stages of L. salmonis did not affect either standard or maximum metabolic rates. However, the later mobile pre-adult stages caused an increase in both standard and maximum metabolic rate yielding a preserved aerobic scope. Notably, standard metabolic rates were elevated by 26%, presumably caused by increased osmoregulatory burdens and costs of mobilizing immune responses. The positive impact on maximum metabolic rates was unexpected and suggests that fish are able to transiently overcompensate energy production to endure the burden of parasites and thus allow for continuation of normal activities. However, infected fish are known to suffer reduced growth, and this suggests that a trade-off exists in acquisition and assimilation of resources despite of an uncompromised aerobic scope. As such, when assessing impacts of environmental or biotic factors, we suggest that elevated routine costs may be a stronger predictor of reduced fitness than the available aerobic scope. Furthermore, studying effects on parasitized fish in an ecophysiological context deserves more attention, especially considering interacting effects of other stressors in the Anthropocene.

Mapping the Energetic Costs of Free-Swimming Gilthead Sea Bream (Sparus aurata), a Key Species in European Marine Aquaculture

Measurement of metabolic rates provides a valuable proxy for the energetic costs of different living activities. However, such measurements are not easy to perform in free-swimming fish. Therefore, mapping acceleration from accelerometer tags with oxygen consumption rates (MO2) is a promising method to counter these limitations and could represent a tool for remotely estimating MO2 in aquaculture environments. In this study, we monitored the swimming performance and MO2 of 79 gilthead sea bream (Sparus aurata; weight range, 219–971 g) during a critical swimming test. Among all the fish challenged, 27 were implanted with electromyography (EMG) electrodes, and 27 were implanted with accelerometer tags to monitor the activation pattern of the red/white muscles during swimming. Additionally, we correlated the acceleration recorded by the tag with the MO2. Overall, we found no significant differences in swimming performance, metabolic traits, and swimming efficiency between the tagged and untagged fish. The acceleration recorded by the tag was successfully correlated with MO2. Additionally, through EMG analyses, we determined the activities of the red and white muscles, which are indicative of the contributions of aerobic and anaerobic metabolisms until reaching critical swimming speed. By obtaining insights into both aerobic and anaerobic metabolisms, sensor mapping with physiological data may be useful for the purposes of aquaculture health/welfare remote monitoring of the gilthead sea bream, a key species in European marine aquaculture.

The damage-independent evolution of ageing by selective destruction

Ageing is currently believed to reflect the accumulation of molecular damage due to energetic costs of maintenance, as proposed in disposable soma theory (DST). Here we have used agent-based modelling to describe an alternative theory by which ageing could undergo positive selection independent of energetic costs. We suggest that the selective advantage of fast-growing mutants might necessitate a mechanism of counterselection we name selective destruction, which removes the faster growing cells from the tissue, preventing the threat of morbidity and mortality they pose. As a result, the survival advantage would shift to the slower cells, allowing them to spread, inducing ageing in the form of a metabolic slowdown. Selective destruction could therefore provide a proximal cause of ageing that is both consistent with the gene expression hallmarks of ageing, and independent of accumulating damage. If true, negligible senescence would acquire a new meaning of increased basal mortality.

Behaviour, temperature and terrain slope impact estimates of energy expenditure using oxygen and dynamic body acceleration

The energy used by animals is influenced by intrinsic (e.g. physiological) and extrinsic (e.g. environmental) factors. Accelerometers within biologging devices have proven useful for assessing energy expenditures and their behavioural context in free-ranging animals. However, certain assumptions are frequently made when acceleration is used as a proxy for energy expenditure, with factors, such as environmental variation (e.g. ambient temperature or slope of terrain), seldom accounted for. To determine the possible interactions between behaviour, energy expenditure and the environment (ambient temperature and terrain slope), the rate of oxygen consumption ($${\dot{\text{V}}\text{O}}_{2}$$ V ˙ O 2 ) was measured in pygmy goats (Capra hircus aegarus) using open-flow indirect calorimetry. The effect of temperature (9.7–31.5 °C) on resting energy expenditure was measured. The relationship between $${\dot{\text{V}}\text{O}}_{2}$$ V ˙ O 2 and dynamic body acceleration (DBA) was measured at different walking speeds (0.8–3.0 km h−1) and on different inclines (0, + 15°, − 15°). The daily behaviour of individuals was measured in two enclosures: enclosure A (level terrain during summer) and enclosure B (sloped terrain during winter) and per diem energy expenditures of behaviours estimated using behaviour, DBA, temperature, terrain slope and $${\dot{\text{V}}\text{O}}_{2}$$ V ˙ O 2 . During rest, energy expenditure increased below 22 °C and above 30.5 °C. $${\dot{\text{V}}\text{O}}_{2}$$ V ˙ O 2 (ml min−1) increased with DBA when walking on the level. Walking uphill (+ 15°) increased energetic costs three-fold, whereas walking downhill (− 15°) increased energetic costs by one third. Based on these results, although activity levels were higher in animals in enclosure A during summer, energy expenditure was found to be significantly higher in the sloped enclosure B in winter (means of enclosures A and B: 485.3 ± 103.6 kJ day−1 and 744.5 ± 132.4 kJ day−1). We show that it is essential to account for extrinsic factors when calculating animal energy budgets. Our estimates of the impacts of extrinsic factors should be applicable to other free ranging ungulates.

Subsurface swimming and stationary diving are metabolically cheap in adult Pacific walruses (Odobenus rosmarus divergens)

Walruses rely on sea-ice to efficiently forage and rest between diving bouts while maintaining proximity to prime foraging habitat. Recent declines in summer sea ice have resulted in walruses hauling out on land where they have to travel farther to access productive benthic habitat while potentially increasing energetic costs. Despite the need to better understand the impact of sea ice loss on energy expenditure, knowledge about metabolic demands of specific behaviours in walruses is scarce. In the present study, 3 adult female Pacific walruses (Odobenus rosmarus divergens) participated in flow-through respirometry trials to measure metabolic rates while floating inactive at the water surface during a minimum of 5 min, during a 180-second stationary dive, and while swimming horizontally underwater for ∼90 m. Metabolic rates during stationary dives (3.82±0.56 l O2 min−1) were lower than those measured at the water surface (4.64±1.04 l O2 min−1), which did not differ from rates measured during subsurface swimming (4.91±0.77 l O2 min−1). Thus, neither stationary diving nor subsurface swimming resulted in metabolic rates above those exhibited by walruses at the water surface. These results suggest that walruses minimize their energetic investment during underwater behaviours as reported for other marine mammals. Although environmental factors experienced by free-ranging walruses (e.g., winds or currents) likely affect metabolic rates, our results provide important information for understanding how behavioural changes affect energetic costs and can be used to improve bioenergetics models aimed at predicting the metabolic consequences of climate change on walruses.

Passing rail traffic reduces bat activity

Rail transport is expanding, with a global increase in infrastructure of up to one-third predicted by 2050. Greater reliance on rail is expected to benefit the environment at a planetary level, by mitigating transport-related carbon emissions. However, smaller-scale, more direct consequences for wildlife are unclear, as unlike roads, railway impacts on animal ecology are rarely studied. As a group, bats frequently interact with transport networks due to their broad distribution and landscape-scale movements. Additionally, their nocturnality, and use of echolocation mean bats are likely to be affected by light and noise emitted by trains. To investigate whether passing trains affect bat activity levels, we monitored the two most abundant UK species using ultrasonic detectors at 12 wooded rail-side sites in southern England. Activity fell by ≥ 30–50% each time a train passed, for at least two minutes. Consequently, activity was reduced for no less than one-fifth of the time at sites with median rail traffic, and two-thirds or more of the time at the busiest site. Such activity changes imply repeated evasive action and/or exclusion from otherwise favourable environments, with potential for corresponding opportunity or energetic costs. Hence, disturbance by passing trains may disadvantage bats in most rail-side habitats.

Leave or Stay: Simulating Motility and Fitness of Microorganisms in Dynamic Aquatic Ecosystems

Motility is a key adaptation factor in scarce marine environments inhabited by bacteria. The question of how a capacity for adaptive migrations influences the success of a microbial population in various conditions is a challenge addressed in this study. We employed the agent-based model of competition of motile and sedentary microbial populations in a confined aquatic environment supplied with a periodic batch nutrient source to assess the fitness of both. Such factors as nutrient concentration in a batch, batch period, mortality type and energetic costs of migration were considered to determine the conditions favouring different strategies: Nomad of a motile population and Settler of a sedentary one. The modelling results demonstrate that dynamic and nutrient-scarce environments favour motile populations, whereas nutrient-rich and stagnant environments promote sedentary microorganisms. Energetic costs of migration determine whether or not the Nomad strategy of the motile population is successful, though it also depends on such conditions as nutrient availability. Even without penalties for migration, under certain conditions, the sedentary Settler population dominates in the ecosystem. It is achieved by decreasing the local nutrient availability near the nutrient source, as motile populations relying on a local optimizing strategy tend to follow benign conditions and fail, enduring stress associated with crossing the valleys of suboptimal nutrient availability.

Heterothermy as a mechanism to offset energetic costs of environmental and homeostatic perturbations

Environmental and biotic pressures impose homeostatic costs on all organisms. The energetic costs of maintaining high body temperatures (Tb) render endotherms sensitive to pressures that increase foraging costs. In response, some mammals become more heterothermic to conserve energy. We measured Tb in banner-tailed kangaroo rats (Dipodomys spectabilis) to test and disentangle the effects of air temperature and moonlight (a proxy for predation risk) on thermoregulatory homeostasis. We further perturbed homeostasis in some animals with chronic corticosterone (CORT) via silastic implants. Heterothermy increased across summer, consistent with the predicted effect of lunar illumination (and predation), and in the direction opposite to the predicted effect of environmental temperatures. The effect of lunar illumination was also evident within nights as animals maintained low Tb when the moon was above the horizon. The pattern was accentuated in CORT-treated animals, suggesting they adopted an even further heightened risk-avoidance strategy that might impose reduced foraging and energy intake. Still, CORT-treatment did not affect body condition over the entire study, indicating kangaroo rats offset decreases in energy intake through energy savings associated with heterothermy. Environmental conditions receive the most attention in studies of thermoregulatory homeostasis, but we demonstrated here that biotic factors can be more important and should be considered in future studies.