Renato Filogonio, Sandy E Saunders, Michael Gray, Jose A Viteri, Joseph M Santin
Many animals undergo prolonged dormancy periods to survive cold or dry environments. While humans and most laboratory-based mammals experience a loss of neuromuscular function during inactivity, hibernators possess physiological mechanisms to mitigate this loss. The American bullfrog provides an extreme model of this phenomenon, as brainstem circuits that generate breathing are completely inactive during underwater hibernation, during which motoneurons employ various types of synaptic plasticity to ensure adequate respiratory motor output in the spring. In addition to synapses, voltage-gated ion channels may undergo plasticity to boost neuronal output. Therefore, we hypothesized that motoneuron excitability would also be enhanced after hibernation via alterations in voltage-gated ion channels. We used whole-cell patch clamp electrophysiology to measure membrane excitability and activities of several voltage-gated channels (K+, Ca2+, Na+) from motoneurons that innervate muscles of the buccal pump (hypoglossal) and glottal dilator (vagal). Surprisingly, compared to controls, overwintered hypoglossal motoneurons displayed multiple indices of reduced excitability (hyperpolarized resting membrane potential, lower firing rates, greater lag to first spike). Mechanistically, this occurred via enhanced voltage-gated K+ and reduced Ca2+ channel activity. In contrast, vagal motoneurons excitability was unaltered, but exhibited altered ion channel profiles which seemed to stabilize neuronal output, involving either reduced Ca2+ or K+ currents. Therefore, different motoneurons of the same neuromuscular behavior respond differently to overwintering by altering the function of voltage-gated channels. We suggest divergent responses may reflect different energetic demands of these neurons and/or their specific contribution to breathing and other orofacial behaviors.
{"title":"Plasticity in voltage-gated ion channels following overwintering in respiratory motoneurons of American bullfrogs.","authors":"Renato Filogonio, Sandy E Saunders, Michael Gray, Jose A Viteri, Joseph M Santin","doi":"10.1242/jeb.249687","DOIUrl":"https://doi.org/10.1242/jeb.249687","url":null,"abstract":"<p><p>Many animals undergo prolonged dormancy periods to survive cold or dry environments. While humans and most laboratory-based mammals experience a loss of neuromuscular function during inactivity, hibernators possess physiological mechanisms to mitigate this loss. The American bullfrog provides an extreme model of this phenomenon, as brainstem circuits that generate breathing are completely inactive during underwater hibernation, during which motoneurons employ various types of synaptic plasticity to ensure adequate respiratory motor output in the spring. In addition to synapses, voltage-gated ion channels may undergo plasticity to boost neuronal output. Therefore, we hypothesized that motoneuron excitability would also be enhanced after hibernation via alterations in voltage-gated ion channels. We used whole-cell patch clamp electrophysiology to measure membrane excitability and activities of several voltage-gated channels (K+, Ca2+, Na+) from motoneurons that innervate muscles of the buccal pump (hypoglossal) and glottal dilator (vagal). Surprisingly, compared to controls, overwintered hypoglossal motoneurons displayed multiple indices of reduced excitability (hyperpolarized resting membrane potential, lower firing rates, greater lag to first spike). Mechanistically, this occurred via enhanced voltage-gated K+ and reduced Ca2+ channel activity. In contrast, vagal motoneurons excitability was unaltered, but exhibited altered ion channel profiles which seemed to stabilize neuronal output, involving either reduced Ca2+ or K+ currents. Therefore, different motoneurons of the same neuromuscular behavior respond differently to overwintering by altering the function of voltage-gated channels. We suggest divergent responses may reflect different energetic demands of these neurons and/or their specific contribution to breathing and other orofacial behaviors.</p>","PeriodicalId":15786,"journal":{"name":"Journal of Experimental Biology","volume":" ","pages":""},"PeriodicalIF":2.8,"publicationDate":"2025-02-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143441178","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Michael Meece, Shubham Rathore, Diego Zagazeta, Elke K Buschbeck
It has previously been shown that near-infrared light can positively affect the physiology of damaged tissue. This is likely mediated by the modulation of metabolic activity via cytochrome c oxidase (COX), the rate of ATP production, and generation of reactive oxygen species. It has been suggested that this process can be influenced by light, with different wavelengths potentially having different efficacy. The impact of these effects on retinal health is not yet well understood. To answer this question, we first induced photoreceptor damage in the eyes of white mutant D. melanogaster through prolonged exposure to bright light. We then investigated the recovery of retinal health following exposure to different wavelengths of near-infrared light (670, 750, 810, 850, and 950 nm) over the course of 10 days. Retinal health was assessed through electroretinograms and fluorescent imaging of live photoreceptors. We found that all treatments except for 950 nm light facilitated the recovery of the electroretinogram response in previously light-damaged flies - though efficacy varied across treatments. All near-infrared exposed groups showed at least some improvement in retinal organization and auto-fluorescence compared to an untreated recovery control. We also showed that our results do not stem from a fly specific artifact relating to opsin photoconversion. Finally, we made use of a bioassay to show enhanced ATP levels in light treatments. This study represents a much-needed direct comparison of the effect of a multitude of different wavelengths and contributes to an emerging body of literature that highlights the promise of phototherapy.
此前已有研究表明,近红外线能对受损组织的生理产生积极影响。这可能是通过细胞色素 c 氧化酶 (COX)、ATP 生成速度和活性氧生成来调节新陈代谢活动。有人认为,这一过程会受到光线的影响,不同波长的光线可能具有不同的功效。这些影响对视网膜健康的影响尚不十分清楚。为了回答这个问题,我们首先通过长时间暴露在强光下诱导白色突变体黑腹蝇眼睛的感光器受损。然后,我们研究了视网膜健康在暴露于不同波长的近红外线(670、750、810、850 和 950 nm)10 天后的恢复情况。视网膜健康状况通过视网膜电图和活体光感受器荧光成像进行评估。我们发现,除了 950 纳米波长的光以外,其他所有处理方法都有助于先前受光损伤的苍蝇恢复视网膜电图反应,但不同处理方法的效果各不相同。与未经处理的恢复对照组相比,所有暴露于近红外光的组在视网膜组织和自身荧光方面都至少有一些改善。我们的研究还表明,我们的结果并非源于蝇类特有的与视蛋白光电转换有关的人工现象。最后,我们利用一种生物测定方法显示了在光照处理中 ATP 水平的提高。这项研究直接比较了多种不同波长的光照效果,是一项亟需的研究,同时也为新出现的强调光疗前景的文献做出了贡献。
{"title":"Assessing recovery of Drosophila melanogaster photoreceptors with different wavelengths of red and infrared light.","authors":"Michael Meece, Shubham Rathore, Diego Zagazeta, Elke K Buschbeck","doi":"10.1242/jeb.250043","DOIUrl":"https://doi.org/10.1242/jeb.250043","url":null,"abstract":"<p><p>It has previously been shown that near-infrared light can positively affect the physiology of damaged tissue. This is likely mediated by the modulation of metabolic activity via cytochrome c oxidase (COX), the rate of ATP production, and generation of reactive oxygen species. It has been suggested that this process can be influenced by light, with different wavelengths potentially having different efficacy. The impact of these effects on retinal health is not yet well understood. To answer this question, we first induced photoreceptor damage in the eyes of white mutant D. melanogaster through prolonged exposure to bright light. We then investigated the recovery of retinal health following exposure to different wavelengths of near-infrared light (670, 750, 810, 850, and 950 nm) over the course of 10 days. Retinal health was assessed through electroretinograms and fluorescent imaging of live photoreceptors. We found that all treatments except for 950 nm light facilitated the recovery of the electroretinogram response in previously light-damaged flies - though efficacy varied across treatments. All near-infrared exposed groups showed at least some improvement in retinal organization and auto-fluorescence compared to an untreated recovery control. We also showed that our results do not stem from a fly specific artifact relating to opsin photoconversion. Finally, we made use of a bioassay to show enhanced ATP levels in light treatments. This study represents a much-needed direct comparison of the effect of a multitude of different wavelengths and contributes to an emerging body of literature that highlights the promise of phototherapy.</p>","PeriodicalId":15786,"journal":{"name":"Journal of Experimental Biology","volume":" ","pages":""},"PeriodicalIF":2.8,"publicationDate":"2025-02-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143433279","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Understanding how muscles use energy is essential for elucidating the role of skeletal muscle in animal locomotion. Yet, experimental measures of in vivo muscle energetics are challenging to obtain, so physiologically-based muscle models are often used to estimate energy use. These predictions of individual muscle energy expenditure are not often compared to indirect whole-body measures of energetic cost. Here, we examined and illustrated the capability of physiologically-based muscle models to predict in vivo measures of energy use, which rely on fundamental relationships between muscle mechanical state and energy consumption. To improve model predictions and ensure a physiological basis for model parameters, we refined our model to include data from isolated muscle experiments and account for inefficiencies in ATP recovery processes. Simulations were performed to capture three different experimental protocols, which involved varying contraction frequency, duty cycle, and muscle fascicle length. Our results demonstrated the ability of the model to capture the dependence of energetic cost on mechanical state across contractile conditions, but tended to under predict the magnitude of energetic cost. Our analysis revealed that the model was most sensitive to the force-velocity parameters and the data informing the energetic parameters when predicting in vivo energetic rates. This work highlights it is the mechanics of skeletal muscle contraction that govern muscle energy use, although the precise physiological parameters for human muscle likely require detailed investigation.
{"title":"Using physiologically-based models to predict in vivo skeletal muscle energetics.","authors":"Ryan N Konno, Glen A Lichtwark, Taylor J M Dick","doi":"10.1242/jeb.249966","DOIUrl":"https://doi.org/10.1242/jeb.249966","url":null,"abstract":"<p><p>Understanding how muscles use energy is essential for elucidating the role of skeletal muscle in animal locomotion. Yet, experimental measures of in vivo muscle energetics are challenging to obtain, so physiologically-based muscle models are often used to estimate energy use. These predictions of individual muscle energy expenditure are not often compared to indirect whole-body measures of energetic cost. Here, we examined and illustrated the capability of physiologically-based muscle models to predict in vivo measures of energy use, which rely on fundamental relationships between muscle mechanical state and energy consumption. To improve model predictions and ensure a physiological basis for model parameters, we refined our model to include data from isolated muscle experiments and account for inefficiencies in ATP recovery processes. Simulations were performed to capture three different experimental protocols, which involved varying contraction frequency, duty cycle, and muscle fascicle length. Our results demonstrated the ability of the model to capture the dependence of energetic cost on mechanical state across contractile conditions, but tended to under predict the magnitude of energetic cost. Our analysis revealed that the model was most sensitive to the force-velocity parameters and the data informing the energetic parameters when predicting in vivo energetic rates. This work highlights it is the mechanics of skeletal muscle contraction that govern muscle energy use, although the precise physiological parameters for human muscle likely require detailed investigation.</p>","PeriodicalId":15786,"journal":{"name":"Journal of Experimental Biology","volume":" ","pages":""},"PeriodicalIF":2.8,"publicationDate":"2025-02-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143441164","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Mathieu Lutier, Fabrice Pernet, Vincent Vanaa, Carole Di Poi, Jérémy Le Luyer
Ocean acidification occurs at a rate unprecedented for millions of years, forcing sessile organisms, such as oysters, to respond in the short term by relying on their phenotypic plasticity. Phenotypic plasticity has limits, tipping points, beyond which species will have to adapt or disappear. These limits could be related to the adaptation of species to different habitat variabilities. Here we expose juvenile pearl oysters, Pinctada margaritifera, to a broad range of pH and determine the response at the gross physiological, lipidome and transcriptome levels. Thus, we identify its high tolerance with low tipping points at pH 7.3-6.8 below which most physiological parameters are impacted. We then compare the transcriptomic reaction norms of the tropical subtidal P. margaritifera, with those of an intertidal temperate oyster, Crassostrea gigas, reusing data from a previous study. Despite showing similar tipping points with C. gigas, P. margaritifera exhibits strong mortalities and depletion of energy reserves below the tipping points, which is not the case for C. gigas. This divergence relies mainly on the induction of metabolic depression, an adaptation to intertidal habitats in C. gigas, but not in P. margaritifera. Our method makes it possible to detect divergences in phenotypic plasticity, probably linked to the species' specific life-history strategies related to different habitats, which will determine the survival of species to ongoing global changes. Such an approach is particularly relevant for studying the physiology of species in a world where physiological tipping points will be increasingly exceeded.
{"title":"Transcriptomic reaction norms highlight metabolic depression as a divergence in phenotypic plasticity between oyster species under ocean acidification.","authors":"Mathieu Lutier, Fabrice Pernet, Vincent Vanaa, Carole Di Poi, Jérémy Le Luyer","doi":"10.1242/jeb.249458","DOIUrl":"https://doi.org/10.1242/jeb.249458","url":null,"abstract":"<p><p>Ocean acidification occurs at a rate unprecedented for millions of years, forcing sessile organisms, such as oysters, to respond in the short term by relying on their phenotypic plasticity. Phenotypic plasticity has limits, tipping points, beyond which species will have to adapt or disappear. These limits could be related to the adaptation of species to different habitat variabilities. Here we expose juvenile pearl oysters, Pinctada margaritifera, to a broad range of pH and determine the response at the gross physiological, lipidome and transcriptome levels. Thus, we identify its high tolerance with low tipping points at pH 7.3-6.8 below which most physiological parameters are impacted. We then compare the transcriptomic reaction norms of the tropical subtidal P. margaritifera, with those of an intertidal temperate oyster, Crassostrea gigas, reusing data from a previous study. Despite showing similar tipping points with C. gigas, P. margaritifera exhibits strong mortalities and depletion of energy reserves below the tipping points, which is not the case for C. gigas. This divergence relies mainly on the induction of metabolic depression, an adaptation to intertidal habitats in C. gigas, but not in P. margaritifera. Our method makes it possible to detect divergences in phenotypic plasticity, probably linked to the species' specific life-history strategies related to different habitats, which will determine the survival of species to ongoing global changes. Such an approach is particularly relevant for studying the physiology of species in a world where physiological tipping points will be increasingly exceeded.</p>","PeriodicalId":15786,"journal":{"name":"Journal of Experimental Biology","volume":" ","pages":""},"PeriodicalIF":2.8,"publicationDate":"2025-02-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143433280","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-02-15Epub Date: 2025-02-21DOI: 10.1242/jeb.250344
Kathryn Knight
{"title":"Announcing the 2024 Journal of Experimental Biology Outstanding Paper Prize shortlist and winner.","authors":"Kathryn Knight","doi":"10.1242/jeb.250344","DOIUrl":"https://doi.org/10.1242/jeb.250344","url":null,"abstract":"","PeriodicalId":15786,"journal":{"name":"Journal of Experimental Biology","volume":"228 4","pages":""},"PeriodicalIF":2.8,"publicationDate":"2025-02-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143468084","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-02-15Epub Date: 2025-02-19DOI: 10.1242/jeb.249308
Tessa S Blanchard, Madison L Earhart, Nicholas Strowbridge, Patricia M Schulte
Cross-protection occurs when exposure to one stressor confers heightened tolerance against a different stressor. Alternatively, exposure to one stressor could result in reduced tolerance against other stressors. Although cross-protection has been documented in a wide range of taxa at juvenile and adult life stages, whether early developmental exposure to a stressor confers cross-protection or reduced tolerance to other stressors later in life through developmental plasticity remains largely unexplored. In this study, we examined whether altered temperature during embryonic development results in developmental plasticity in upper thermal tolerance or hypoxia tolerance using a small topminnow, Fundulus heteroclitus, and examined potential underlying molecular mechanisms. We incubated embryos at one of two ecologically relevant temperatures (20°C or 26°C) until hatch. Once hatched, fish were raised at a common temperature of 20°C for 1 year, and tolerance was assessed in both juveniles (6 months) and early adults (1 year). Developmental temperature had no significant effect on thermal tolerance (CTmax) in juvenile fish, or on the transcript abundance of thermal tolerance-related genes (constitutive heat shock proteins, hsc70, hsp90b). In contrast, reduced developmental temperature decreased hypoxia tolerance but increased transcript levels of the hypoxia inducible factor hif1α in juvenile fish but the effects were less evident in older fish. Overall, we found no indication of developmental plasticity for thermal tolerance, but there was evidence of negative impacts of lower developmental temperature on hypoxia tolerance in juveniles associated with changes in gene expression, providing evidence of developmental plasticity across stressors and levels of organization.
{"title":"Exposure to sub-optimal temperature during early development decreases hypoxia tolerance in juvenile Fundulus heteroclitus.","authors":"Tessa S Blanchard, Madison L Earhart, Nicholas Strowbridge, Patricia M Schulte","doi":"10.1242/jeb.249308","DOIUrl":"10.1242/jeb.249308","url":null,"abstract":"<p><p>Cross-protection occurs when exposure to one stressor confers heightened tolerance against a different stressor. Alternatively, exposure to one stressor could result in reduced tolerance against other stressors. Although cross-protection has been documented in a wide range of taxa at juvenile and adult life stages, whether early developmental exposure to a stressor confers cross-protection or reduced tolerance to other stressors later in life through developmental plasticity remains largely unexplored. In this study, we examined whether altered temperature during embryonic development results in developmental plasticity in upper thermal tolerance or hypoxia tolerance using a small topminnow, Fundulus heteroclitus, and examined potential underlying molecular mechanisms. We incubated embryos at one of two ecologically relevant temperatures (20°C or 26°C) until hatch. Once hatched, fish were raised at a common temperature of 20°C for 1 year, and tolerance was assessed in both juveniles (6 months) and early adults (1 year). Developmental temperature had no significant effect on thermal tolerance (CTmax) in juvenile fish, or on the transcript abundance of thermal tolerance-related genes (constitutive heat shock proteins, hsc70, hsp90b). In contrast, reduced developmental temperature decreased hypoxia tolerance but increased transcript levels of the hypoxia inducible factor hif1α in juvenile fish but the effects were less evident in older fish. Overall, we found no indication of developmental plasticity for thermal tolerance, but there was evidence of negative impacts of lower developmental temperature on hypoxia tolerance in juveniles associated with changes in gene expression, providing evidence of developmental plasticity across stressors and levels of organization.</p>","PeriodicalId":15786,"journal":{"name":"Journal of Experimental Biology","volume":" ","pages":""},"PeriodicalIF":2.8,"publicationDate":"2025-02-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143006516","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-02-15Epub Date: 2025-02-20DOI: 10.1242/jeb.249585
Andrew A Biewener, Alan M Wilson
Scientific fields evolve a culture and vocabulary that create a group identity but may result in reduced understanding by people in apparently adjacent but different fields. Here, a series of articles written by scientists active in biomechanics, energetics and ecology relevant to locomotion forms the basis of researchers striving to bridge those divides and providing a common language and perspective.
{"title":"Integrating biomechanics, energetics and ecology perspectives in locomotion.","authors":"Andrew A Biewener, Alan M Wilson","doi":"10.1242/jeb.249585","DOIUrl":"https://doi.org/10.1242/jeb.249585","url":null,"abstract":"<p><p>Scientific fields evolve a culture and vocabulary that create a group identity but may result in reduced understanding by people in apparently adjacent but different fields. Here, a series of articles written by scientists active in biomechanics, energetics and ecology relevant to locomotion forms the basis of researchers striving to bridge those divides and providing a common language and perspective.</p>","PeriodicalId":15786,"journal":{"name":"Journal of Experimental Biology","volume":"228 Suppl_1","pages":""},"PeriodicalIF":2.8,"publicationDate":"2025-02-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143458151","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-02-15Epub Date: 2025-02-20DOI: 10.1242/jeb.248022
Glen A Lichtwark, Luke N Jessup, Ryan N Konno, Cristian D Riveros-Matthey, Taylor J M Dick
In this Review, we explore the state of the art of biomechanical models for estimating energy consumption during terrestrial locomotion. We consider different mechanical models that provide a solid framework to understand movement energetics from the perspective of force and work requirements. Whilst such models are highly informative, they lack specificity for predicting absolute metabolic rates across a range of species or variations in movement patterns. Muscles consume energy when they activate to generate tension, as well as when they shorten to generate positive work. Phenomenological muscle models incorporating steady-state parameters have been developed and are able to reproduce how muscle fibre energy consumption changes under different contractile conditions; however, such models are difficult to validate when scaled up to whole muscle. This is, in part, owing to limited availability of data that relate muscle dynamics to energetic rates during contraction of large mammalian muscles. Furthermore, factors including the compliance of tendinous tissue, dynamic shape changes and motor unit recruitment can alter the dynamics of muscle contractile tissue and potentially improve muscle efficiency under some locomotion conditions. Despite the many challenges, energetic cost estimates derived from musculoskeletal models that simulate muscle function required to generate movement have been shown to reasonably predict changes in human metabolic rates under different movement conditions. However, accurate predictions of absolute metabolic rate are still elusive. We suggest that conceptual models may be adapted based on our understanding of muscle energetics to better predict the variance in movement energetics both within and between terrestrial species.
{"title":"Integrating muscle energetics into biomechanical models to understand variance in the cost of movement.","authors":"Glen A Lichtwark, Luke N Jessup, Ryan N Konno, Cristian D Riveros-Matthey, Taylor J M Dick","doi":"10.1242/jeb.248022","DOIUrl":"https://doi.org/10.1242/jeb.248022","url":null,"abstract":"<p><p>In this Review, we explore the state of the art of biomechanical models for estimating energy consumption during terrestrial locomotion. We consider different mechanical models that provide a solid framework to understand movement energetics from the perspective of force and work requirements. Whilst such models are highly informative, they lack specificity for predicting absolute metabolic rates across a range of species or variations in movement patterns. Muscles consume energy when they activate to generate tension, as well as when they shorten to generate positive work. Phenomenological muscle models incorporating steady-state parameters have been developed and are able to reproduce how muscle fibre energy consumption changes under different contractile conditions; however, such models are difficult to validate when scaled up to whole muscle. This is, in part, owing to limited availability of data that relate muscle dynamics to energetic rates during contraction of large mammalian muscles. Furthermore, factors including the compliance of tendinous tissue, dynamic shape changes and motor unit recruitment can alter the dynamics of muscle contractile tissue and potentially improve muscle efficiency under some locomotion conditions. Despite the many challenges, energetic cost estimates derived from musculoskeletal models that simulate muscle function required to generate movement have been shown to reasonably predict changes in human metabolic rates under different movement conditions. However, accurate predictions of absolute metabolic rate are still elusive. We suggest that conceptual models may be adapted based on our understanding of muscle energetics to better predict the variance in movement energetics both within and between terrestrial species.</p>","PeriodicalId":15786,"journal":{"name":"Journal of Experimental Biology","volume":"228 Suppl_1","pages":""},"PeriodicalIF":2.8,"publicationDate":"2025-02-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143458166","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-02-15Epub Date: 2025-02-21DOI: 10.1242/jeb.249539
Kandace R Griffin, Christopher M Holbrook, Daniel P Zielinski, Christopher L Cahill, C Michael Wagner
Efficient navigation is crucial for the reproductive success of many migratory species, often driven by competing pressures to conserve energy and reduce predation risk. Little is known about how non-homing species achieve this balance. We show that sea lamprey (Petromyzon marinus), an ancient extant vertebrate, uses persistent patterns in hydro-geomorphology to quickly and efficiently navigate through complex ecosystems. Hydrodynamic flow models coupled with bathymetric mapping and fine-scale acoustic telemetry revealed movement paths that tracked thalweg scour channels, which are often the deepest and fastest-flowing sections of a river. These paths allow rapid and efficient upstream migration and suggest the existence of a bathymetric highway system. Near-substrate swimming along this path resulted in a median of 5.8% energy savings while also promoting improved safety from nocturnally active predators. We hypothesize sea lampreys use hydrostatic pressure-guided rheotaxis to achieve this navigation. It is likely this tactic relies on sensory information from the animal's primitive lateral line and perhaps the inner ear. Insights from this study can be used to redesign conservation practices to achieve improved control where the animal is invasive and improved fish passage within its native range.
{"title":"Not all who meander are lost: migrating sea lamprey follow river thalwegs to facilitate safe and efficient passage upstream.","authors":"Kandace R Griffin, Christopher M Holbrook, Daniel P Zielinski, Christopher L Cahill, C Michael Wagner","doi":"10.1242/jeb.249539","DOIUrl":"10.1242/jeb.249539","url":null,"abstract":"<p><p>Efficient navigation is crucial for the reproductive success of many migratory species, often driven by competing pressures to conserve energy and reduce predation risk. Little is known about how non-homing species achieve this balance. We show that sea lamprey (Petromyzon marinus), an ancient extant vertebrate, uses persistent patterns in hydro-geomorphology to quickly and efficiently navigate through complex ecosystems. Hydrodynamic flow models coupled with bathymetric mapping and fine-scale acoustic telemetry revealed movement paths that tracked thalweg scour channels, which are often the deepest and fastest-flowing sections of a river. These paths allow rapid and efficient upstream migration and suggest the existence of a bathymetric highway system. Near-substrate swimming along this path resulted in a median of 5.8% energy savings while also promoting improved safety from nocturnally active predators. We hypothesize sea lampreys use hydrostatic pressure-guided rheotaxis to achieve this navigation. It is likely this tactic relies on sensory information from the animal's primitive lateral line and perhaps the inner ear. Insights from this study can be used to redesign conservation practices to achieve improved control where the animal is invasive and improved fish passage within its native range.</p>","PeriodicalId":15786,"journal":{"name":"Journal of Experimental Biology","volume":" ","pages":""},"PeriodicalIF":2.8,"publicationDate":"2025-02-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11883278/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143047028","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-02-15Epub Date: 2025-02-20DOI: 10.1242/jeb.248011
James C Liao
Most of our understanding of fish locomotion has focused on elementary behaviors such as steady swimming and escape responses in simple environments. As the field matures, increasing attention is being paid to transient and unsteady behaviors that characterize more complex interactions with the environment. This Commentary advocates for an ecologically relevant approach to lab studies. Specific examples have brought new understanding to the energetic consequences of fish swimming, such as (1) station holding around bluff bodies, which departs drastically from steady swimming in almost all aspects of kinematics, muscle activity and energetics, and (2) transient behaviors such as acceleration and feeding, which are critical to survival but often neglected because of challenges in measuring costs. Beyond the lab, a far richer diversity of behaviors is available when fish are given enough space and time to move. Mesocosm studies are poised to reveal new insights into fish swimming that are inaccessible in laboratory settings. Next-generation biologgers that incorporate neural recordings will usher in a new era for understanding biomechanics in the wild and open the door for a more mechanistic understanding of how changing environments affect animal movement. These advances promise to allow insights into animal locomotion in ways that will mutually complement and accelerate laboratory and field studies in the years to come.
{"title":"Towards the yin and yang of fish locomotion: linking energetics, ecology and mechanics through field and lab approaches.","authors":"James C Liao","doi":"10.1242/jeb.248011","DOIUrl":"https://doi.org/10.1242/jeb.248011","url":null,"abstract":"<p><p>Most of our understanding of fish locomotion has focused on elementary behaviors such as steady swimming and escape responses in simple environments. As the field matures, increasing attention is being paid to transient and unsteady behaviors that characterize more complex interactions with the environment. This Commentary advocates for an ecologically relevant approach to lab studies. Specific examples have brought new understanding to the energetic consequences of fish swimming, such as (1) station holding around bluff bodies, which departs drastically from steady swimming in almost all aspects of kinematics, muscle activity and energetics, and (2) transient behaviors such as acceleration and feeding, which are critical to survival but often neglected because of challenges in measuring costs. Beyond the lab, a far richer diversity of behaviors is available when fish are given enough space and time to move. Mesocosm studies are poised to reveal new insights into fish swimming that are inaccessible in laboratory settings. Next-generation biologgers that incorporate neural recordings will usher in a new era for understanding biomechanics in the wild and open the door for a more mechanistic understanding of how changing environments affect animal movement. These advances promise to allow insights into animal locomotion in ways that will mutually complement and accelerate laboratory and field studies in the years to come.</p>","PeriodicalId":15786,"journal":{"name":"Journal of Experimental Biology","volume":"228 Suppl_1","pages":""},"PeriodicalIF":2.8,"publicationDate":"2025-02-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143458188","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}