Journal of Experimental Biology最新文献

Muscle is the universal agent of animal movement, and limits to muscle performance are therefore an integral aspect of animal behaviour, ecology and evolution. A mechanical perspective on movement makes it amenable to analysis from first principles, and so brings the seeming certitude of simple physical laws to the challenging comparative study of complex biological systems. Early contributions on movement biomechanics considered muscle energy output to be limited by muscle work capacity, Wmax; triggered by seminal work in the late 1960s, it is now held broadly that a complete analysis of muscle energy output must also consider muscle power capacity, for no unit of work can be delivered in arbitrarily brief time. Here, we adopt a critical stance towards this paradigmatic notion of a power limit, and argue that the alternative constraint to muscle energy output is imposed instead by a characteristic kinetic energy capacity, Kmax, dictated by the maximum speed with which the actuating muscle can shorten. The two critical energies can now be directly compared, and define the physiological similarity index, Γ=Kmax/Wmax. It is the explanatory power of this comparison that lends weight to a shift in perspective from muscle power to kinetic energy capacity, as is argued through a series of illustrative examples. Γ emerges as an important dimensionless number in musculoskeletal dynamics, and sparks novel hypotheses on functional adaptations in musculoskeletal 'design' that depart from the parsimonious evolutionary null hypothesis of geometric similarity.

Regional heterothermy describes when body regions differ in temperature, which can have important ramifications for performance because most biological processes are temperature dependent. However, the relationship between regional heterothermy and environmental temperature is not well known, particularly for ectotherms. The relationship between environmental heterogeneity and regional heterothermy might also yield insight into how the latter is regulated. We examined the thermal dependence of regional heterothermy (between the head and the cloaca) in live ring-necked snakes (Diadophis punctatus) in both the lab and the field, as well as in one dead and preserved individual. We found that the magnitude of the head-cloaca difference declined with average environmental temperature, that the relationship between head temperature and ambient temperature differed from that of cloaca temperature and ambient temperature, and that the preserved snake specimen did not display a consistent head-cloaca temperature difference. Our results suggest that (1) cloacal and head temperatures are regulated differently, (2) the head-cloaca temperature difference is not merely due to differences in the material properties of the head and cloaca, and (3) this difference may arise from altered circulation and perhaps even endogenous heat-generating mechanisms. Our results also suggest that the thermal dependence of regional heterothermy likely has ramifications for organismal function.

Early-life experiences with signals used in communication are instrumental in shaping an animal's social interactions. In songbirds, which use vocalizations for guiding social interactions and mate choice, recent studies show that sensory effects on development occur earlier than previously expected, even in embryos and nestlings. Here, we explored the neural dynamics underlying experience-dependent song categorization in young birds prior to the traditionally studied sensitive period of vocal learning that begins around 3 weeks post-hatch. We raised zebra finches either with their biological parents, cross-fostered by Bengalese finches beginning at embryonic day 9, or with only the non-singing mother from 2 days post-hatch. Then, 1-5 days after fledging, we conducted behavioral experiments and extracellular recordings in the auditory forebrain to test responses to zebra finch and Bengalese finch songs. Auditory forebrain neurons in cross-fostered and isolated birds showed increases in firing rate and decreases in responsiveness and selectivity. In cross-fostered birds, decreases in responsiveness and selectivity relative to white noise were specific to conspecific song stimuli, which paralleled behavioral attentiveness to conspecific songs in those same birds. This study shows that auditory and social experience can already impact song 'type' processing in the brains of nestlings, and that brain changes at this age can portend the effects of natal experience in adults.

Honeybees encode in their waggle dances the vector (distance and direction) of an outbound flight to a food source or a new nest site. Optic flow has been identified as the major source of information in the distance estimation. Additional components of distance estimation were also identified, e.g. the sequence of experienced landmarks. Here, we address the question of whether bees also use the landscape memory developed during exploratory orientation flights to estimate distance. We took advantage of the fact that flights in a narrow tunnel lead to further distance measures as a result of higher optic flow. We found that this effect was lost when bees had explored the area in which the tunnel was located and when they had somewhat restricted visual access to the surrounding environment through the mesh on top of the tunnel. These data are interpreted in the context of other findings about the structure of navigational memory in bees that develops during exploratory orientation flights. In particular, the data suggest that bees embed distance measures into a representation of navigational space that stores previously experienced landscape features.

Diel fluctuations of oxygen levels characterize cyclic hypoxia and pose a significant challenge to wild fish populations. Although recent research has been conducted on the effects of hypoxia and reoxygenation, mechanisms by which fish acclimatize to cyclic hypoxia remain unclear, especially in hypoxia-sensitive species. We hypothesized that acclimation to cyclic hypoxia requires a downregulation of aerobic metabolic rate and an upregulation of mitochondrial respiratory capacities to mitigate constraints on aerobic metabolism and the elevated risk of oxidative stress upon reoxygenation. We exposed Arctic char (Salvelinus alpinus) to 10 days of cyclic hypoxia and measured their metabolic rate and mitochondrial physiology to determine how they cope with fluctuating oxygen concentrations. We measured oxygen consumption as a proxy of metabolic rate and observed that Arctic char defend their standard metabolic rate but decrease their routine metabolic rate during hypoxic phases, presumably through the repression of spontaneous swimming activities. At the mitochondrial level, acute cyclic hypoxia increases oxygen consumption without ADP (CI-LEAK) in the liver and heart. Respiration in the presence of ADP (OXPHOS) temporarily increases in the liver and decreases in the heart. Cytochrome c oxidase oxygen affinity also increases at day 3 in the liver. However, no change occurs in the brain, which is likely primarily preserved through preferential perfusion (albeit not measured in this study). Finally, in vivo measurements of reactive oxygen species revealed the absence of an oxidative burst in mitochondria in the cyclic hypoxia group. Our study shows that Arctic char acclimatize to cyclic hypoxia through organ-specific mitochondrial adjustments.

The global ocean is rapidly changing, posing a substantial threat to the viability of marine populations due to the co-occurrence of multiple drivers, such as ocean warming (OW) and ocean acidification (OA). To persist, marine species must undergo some combination of acclimation and adaptation in response to these changes. Understanding such responses is essential to measure and project the magnitude and direction of current and future vulnerabilities in marine ecosystems. Echinoderms have been recognised as a model in studies of OW-OA effects on marine biota. However, despite their global diversity, vulnerability and ecological importance in most marine habitats, brittle stars (ophiuroids) are poorly studied. A long-term mesocosm experiment was conducted on adult mottled brittle star (Ophionereis fasciata) as a case study to investigate the physiological response and trade-offs of marine organisms to ocean acidification, ocean warming and the combined effect of these two drivers. Long-term exposure of O. fasciata to high temperature and low pH affected survival, respiration and regeneration rates, growth rate, calcification/dissolution and righting response. Higher temperatures increased stress and respiration, and decreased regeneration and growth rates as well as survival. Conversely, changes in pH had more subtle or no effect, affecting only respiration and calcification. Our results indicate that exposure to a combination of high temperature and low pH produces complex responses for respiration, righting response and calcification. We address the knowledge gap of the impact of a changing ocean on ophiuroids in the context of echinoderm studies, proposing this class as an ideal alternative echinoderm for future research.

To decide whether to remain underground or to emerge from overwintering, fossorial ectotherms simultaneously process environmental, gravitational and circannual migratory cues. Here, we provide an experimental framework to study the behaviour of fossorial ectotherms during soil temperature inversion - a phenomenon that marks the transition between winter and spring - based on three non-mutually exclusive hypotheses (thermoregulation, negative geotaxis and migration restlessness). Using a vertical thermal gradient, we evaluated how temperature selection (Tsel), activity and vertical position selection differed under simulated soil temperature inversion (contrasting the active versus overwintering thermal gradients) in the spotted salamander (Ambystoma maculatum). Salamanders had different Tsel and activity levels between gradients, but selected similar heights regardless of thermal gradient orientation. Negative geotaxis may explain responses to changes in vertical thermal gradient orientation, with migratory restlessness contributing to differences in activity levels. Ultimately, our work should benefit those who aim to better understand the biology of fossorial ectotherms.

The work loop technique was developed to assess muscle performance during cyclical length changes with phasic activation, simulating the in vivo conditions of many muscles, particularly during locomotion. To estimate muscle function in vivo, the standard approach involves subjecting a muscle to length trajectories and activation timings derived from in vivo measurements, whilst simultaneously measuring force. However, the stimulation paradigm typically used, supramaximal, 'square-wave' stimulation, does not accurately reflect the graded intensity of activation observed in vivo. While the importance of the timing and duration of stimulation within the cycle on estimates of muscle performance has long been established, the importance of graded muscle activation has not been investigated. In this study, we investigated how the activation pattern affects muscle performance by comparing square-wave, supramaximal activation with a graded in vivo activation pattern. First, we used in vivo electromyography-derived activation patterns and fibre strains from the rabbit digastric muscle during mastication and replayed them in situ. Second, we used Hill-type musculoskeletal model-derived activation patterns and fibre strains in a trotting mouse, replayed ex vivo in the soleus (SOL) and extensor digitorum longus (EDL) muscles. In the rabbit digastric muscle, square-wave activation led to an 8-fold higher estimate of net power, compared with the in vivo graded activation pattern. Similarly, in the mouse SOL and EDL, supramaximal, square-wave activation resulted in significantly greater positive and negative muscle work. These findings highlight that realistic interpretations of in vivo muscle function rely upon more accurate representations of muscle activation intensity.

Escape jet propulsion swimming in cuttlefish (Sepia officinalis) is powered by the circular muscles surrounding the mantle cavity. This mode of locomotion is energetically costly compared with undulatory swimming. The energetic cost of swimming is determined by the mechanical power requirements and the efficiency with which chemical energy is transferred into useful mechanical work. One step in this energy transduction process is the transfer of energy from ATP hydrolysis into mechanical work by the muscles. Here, we determined the efficiency of this step, termed the contractile efficiency. Muscle preparations from the circular muscles of the mantle cavity were subjected to sinusoidal length changes at different cycle frequencies, and stimulated with a phase and duration that maximised initial net work. Changes in ATP, arginine phosphate and octopine content between control and exercised muscles were determined and used to calculate the energy released from ATP hydrolysis (Emet). The maximum contractile efficiency (the ratio of net work to Emet) was 0.37, occurring at the same cycle frequency at which mechanical power was maximal and that was used during jet propulsion swimming, suggesting that cuttlefish muscle is adapted to generate muscular power efficiently. The overall efficiency of cuttlefish jet propulsion swimming was estimated to be 0.17, which is broadly comparable to that measured during animal flight and human-powered pedalled locomotion, indicating the high energetic costs of jet propulsion swimming are not due to inefficient locomotion per se; instead, they result from the relatively high mechanical power requirements.

Division of labour (DOL) in eusocial insects plays an important role in colony fitness. Honeybees face a variety of stressors that compromise the homeostasis of the colony and reduce survival and reproduction. Considering the significance of DOL in colony homeostasis, it is important to understand whether and how DOL may be altered as a result of chronic stress. Therefore, we tested whether honeybee colonies shift DOL in response to high infestation with the parasitic mite Varroa destructor. For this, we monitored chronically stressed and presumably low-stress colonies from April till December 2022. During the experiment, we applied a cold shock to test whether a perturbation resulted in a larger alteration in DOL in chronically stressed colonies. We found that after cold shock, there was a lower proportion of nurses in the chronically stressed colonies. For foragers, we found higher activity post-cold shock in chronically stressed colonies, but no difference between treatments in nectar inflow, suggesting less efficient foragers. Furthermore, we found that there was an accelerated task switch in chronically stressed colonies after the cold shock. The large changes after the perturbation may indicate inefficient task allocation due to chronic stress. Our study contributes to the understanding of social resilience and chronic stress responses in eusocial animals.