Pub Date : 2024-10-01Epub Date: 2024-10-04DOI: 10.1242/jeb.247887
Luis L Kuchenmüller, Elizabeth C Hoots, Timothy D Clark
Increasing evidence shows that larger fish are more vulnerable to acute warming than smaller individuals of the same species. This size-dependency of thermal tolerance has been ascribed to differences in aerobic performance, largely owing to a decline in oxygen supply relative to demand. To shed light on these ideas, we examined metabolic allometry in 130 rainbow trout ranging from 12 to 358 g under control conditions (17°C) and in response to acute heating (to 25°C), with and without supplemental oxygen (100% versus 150% air saturation). Under normoxia, high temperature caused an average 17% reduction in aerobic scope compared with 17°C. Aerobic performance disproportionally deteriorated in bigger fish as the scaling exponent (b) for aerobic scope declined from b=0.87 at 17°C to b=0.74 at 25°C. Hyperoxia increased maximum metabolic rate and aerobic scope at both temperatures and disproportionally benefited larger fish at 25°C as the scaling exponent for aerobic scope was reestablished to the same level as at 17°C (b=0.86). This suggests that hyperoxia may provide metabolic refuge for larger individuals, allowing them to sustain aerobic activities when facing acute warming. Notably, the elevated aerobic capacity afforded by hyperoxia did not appear to improve thermal resilience, as mortality in 25°C hyperoxia (13.8%, n=4) was similar to that in normoxia (12.1%, n=4), although we caution that this topic warrants more targeted research. We highlight the need for mechanistic investigations of the oxygen transport system to determine the consequences of differential metabolic scaling across temperature in a climate warming context.
{"title":"Hyperoxia disproportionally benefits the aerobic performance of large fish at elevated temperature.","authors":"Luis L Kuchenmüller, Elizabeth C Hoots, Timothy D Clark","doi":"10.1242/jeb.247887","DOIUrl":"10.1242/jeb.247887","url":null,"abstract":"<p><p>Increasing evidence shows that larger fish are more vulnerable to acute warming than smaller individuals of the same species. This size-dependency of thermal tolerance has been ascribed to differences in aerobic performance, largely owing to a decline in oxygen supply relative to demand. To shed light on these ideas, we examined metabolic allometry in 130 rainbow trout ranging from 12 to 358 g under control conditions (17°C) and in response to acute heating (to 25°C), with and without supplemental oxygen (100% versus 150% air saturation). Under normoxia, high temperature caused an average 17% reduction in aerobic scope compared with 17°C. Aerobic performance disproportionally deteriorated in bigger fish as the scaling exponent (b) for aerobic scope declined from b=0.87 at 17°C to b=0.74 at 25°C. Hyperoxia increased maximum metabolic rate and aerobic scope at both temperatures and disproportionally benefited larger fish at 25°C as the scaling exponent for aerobic scope was reestablished to the same level as at 17°C (b=0.86). This suggests that hyperoxia may provide metabolic refuge for larger individuals, allowing them to sustain aerobic activities when facing acute warming. Notably, the elevated aerobic capacity afforded by hyperoxia did not appear to improve thermal resilience, as mortality in 25°C hyperoxia (13.8%, n=4) was similar to that in normoxia (12.1%, n=4), although we caution that this topic warrants more targeted research. We highlight the need for mechanistic investigations of the oxygen transport system to determine the consequences of differential metabolic scaling across temperature in a climate warming context.</p>","PeriodicalId":15786,"journal":{"name":"Journal of Experimental Biology","volume":null,"pages":null},"PeriodicalIF":2.8,"publicationDate":"2024-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142132928","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 : 2024-10-01Epub Date: 2024-10-10DOI: 10.1242/jeb.247665
Elizabeth Atchoi, Mindaugas Mitkus, Biana Machado, Valter Medeiros, Sofia Garcia, Manuela Juliano, Joël Bried, Airam Rodríguez
Seabirds, and particularly fledglings of burrow-nesting species, are greatly impacted by light pollution. During their inaugural flights from colony to sea, fledglings become grounded after encountering artificial light. Such groundings, or fallout events, affect many fledglings each year, causing mass mortality events. To mitigate this light-induced mortality, rescue programmes have been implemented for decades at many locations worldwide. Despite the notoriety of fallouts and their conservation implications, the contributing behavioural and biological factors remain mostly unknown. How the mechanisms of light attraction and light avoidance interact and how they manifest in different groups (e.g. age, personality, populations) or light pollution levels remain open questions. We tested behavioural choices of Cory's shearwater Calonectris borealis fledglings, rescued after being grounded in urban areas, and choices of breeding adults for contrasting light sources. Fledglings and adults were exposed to one of three treatments in an experimental Y-maze set-up: white light versus no light, blue versus red light, and a control with no light on each arm of the Y-maze. Both age groups clearly chose the no-light arms and the red light arm. This choice for longer wavelengths and darker environments, along with slower responses by fledglings, suggests that close range artificial light causes disorientation in seabirds. Our study helps to clarify the behavioural components of fallouts and provides further evidence on the disruptive effects of nocturnal artificial light on sensitive species like Procellariiformes.
海鸟,尤其是穴巢物种的雏鸟,受到光污染的严重影响。雏鸟在从栖息地飞向海洋的初始飞行中,遇到人造光后会搁浅。这种搁浅或坠落事件每年都会影响许多雏鸟,造成大量死亡。为了减少这种光照导致的死亡,几十年来,全球许多地方都实施了救援计划。尽管坠落事件及其对自然保护的影响声名狼藉,但其行为和生物因素仍大多不为人知。光吸引和光规避机制是如何相互作用的,它们在不同的群体(如年龄、个性、种群)或光污染水平中又是如何表现的,这些都是悬而未决的问题。我们测试了在城市地区搁浅后被救起的科里氏剪嘴鸥(Calonectris borealis)雏鸟的行为选择,以及繁殖期成鸟对对比光源的选择。雏鸟和成鸟在实验性 Y 形迷宫中接受三种处理中的一种:白光与无光、蓝光与红光,以及 Y 形迷宫两臂无光的对照组。两个年龄组的孩子都明显选择了无光臂和红光臂。雏鸟对波长较长和较暗环境的选择以及较慢的反应速度表明,近距离的人造光似乎会导致海鸟迷失方向。我们的研究有助于澄清落羽的行为成分,并进一步证明夜间人造光对鳞翅目等敏感物种的干扰作用。
{"title":"Do seabirds dream of artificial lights? Understanding light preferences of Procellariiformes.","authors":"Elizabeth Atchoi, Mindaugas Mitkus, Biana Machado, Valter Medeiros, Sofia Garcia, Manuela Juliano, Joël Bried, Airam Rodríguez","doi":"10.1242/jeb.247665","DOIUrl":"10.1242/jeb.247665","url":null,"abstract":"<p><p>Seabirds, and particularly fledglings of burrow-nesting species, are greatly impacted by light pollution. During their inaugural flights from colony to sea, fledglings become grounded after encountering artificial light. Such groundings, or fallout events, affect many fledglings each year, causing mass mortality events. To mitigate this light-induced mortality, rescue programmes have been implemented for decades at many locations worldwide. Despite the notoriety of fallouts and their conservation implications, the contributing behavioural and biological factors remain mostly unknown. How the mechanisms of light attraction and light avoidance interact and how they manifest in different groups (e.g. age, personality, populations) or light pollution levels remain open questions. We tested behavioural choices of Cory's shearwater Calonectris borealis fledglings, rescued after being grounded in urban areas, and choices of breeding adults for contrasting light sources. Fledglings and adults were exposed to one of three treatments in an experimental Y-maze set-up: white light versus no light, blue versus red light, and a control with no light on each arm of the Y-maze. Both age groups clearly chose the no-light arms and the red light arm. This choice for longer wavelengths and darker environments, along with slower responses by fledglings, suggests that close range artificial light causes disorientation in seabirds. Our study helps to clarify the behavioural components of fallouts and provides further evidence on the disruptive effects of nocturnal artificial light on sensitive species like Procellariiformes.</p>","PeriodicalId":15786,"journal":{"name":"Journal of Experimental Biology","volume":null,"pages":null},"PeriodicalIF":2.8,"publicationDate":"2024-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142347998","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 : 2024-10-01Epub Date: 2024-10-10DOI: 10.1242/jeb.248187
Abel Mebrahtu, Ian C Smith, Shuyue Liu, Ziad Abusara, Timothy R Leonard, Venus Joumaa, Walter Herzog
Cross-sectional area (CSA) is a fundamental variable in characterizing muscle mechanical properties. Typically, the CSA of a single muscle fibre is assessed by measuring either one or two diameters, and assuming the cross-section is either circular or elliptical in shape. However, fibre cross-sections have irregular shapes. The accuracy and precision of CSAs determined using circular and elliptical shape assumptions are unclear for mammalian skinned muscle fibres. Second harmonic generation imaging of skinned rabbit soleus fibres revealed that the circular assumption overstated real CSA by 5.3±25.9% whereas the elliptical assumption overstated real CSA by 2.8±6.9%. A preferred rotational alignment can bias the circular assumption, as real CSA was overstated by 22.1±24.8% when using the larger fibre diameter and understated by 11.4±13% when using the smaller fibre diameter. With 73% lower variable error and reduced bias, the elliptical assumption is superior to the circular assumption when assessing the CSA of skinned mammalian fibres.
{"title":"Reconsidering assumptions in the analysis of muscle fibre cross-sectional area.","authors":"Abel Mebrahtu, Ian C Smith, Shuyue Liu, Ziad Abusara, Timothy R Leonard, Venus Joumaa, Walter Herzog","doi":"10.1242/jeb.248187","DOIUrl":"10.1242/jeb.248187","url":null,"abstract":"<p><p>Cross-sectional area (CSA) is a fundamental variable in characterizing muscle mechanical properties. Typically, the CSA of a single muscle fibre is assessed by measuring either one or two diameters, and assuming the cross-section is either circular or elliptical in shape. However, fibre cross-sections have irregular shapes. The accuracy and precision of CSAs determined using circular and elliptical shape assumptions are unclear for mammalian skinned muscle fibres. Second harmonic generation imaging of skinned rabbit soleus fibres revealed that the circular assumption overstated real CSA by 5.3±25.9% whereas the elliptical assumption overstated real CSA by 2.8±6.9%. A preferred rotational alignment can bias the circular assumption, as real CSA was overstated by 22.1±24.8% when using the larger fibre diameter and understated by 11.4±13% when using the smaller fibre diameter. With 73% lower variable error and reduced bias, the elliptical assumption is superior to the circular assumption when assessing the CSA of skinned mammalian fibres.</p>","PeriodicalId":15786,"journal":{"name":"Journal of Experimental Biology","volume":null,"pages":null},"PeriodicalIF":2.8,"publicationDate":"2024-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142348005","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}
van Oordt Francis, Jaime Silva, Allison Patterson, Kyle H Elliott
Daily energy expenditure (DEE) is the result of decisions on how to allocate time among activities (resting, commuting, and foraging) and the energy costs of those activities. Dynamic body acceleration (DBA), which measures acceleration associated with movement, can be used to estimate DEE. Previous studies of DBA-DEE correlations in birds occurred on species foraging below their thermoneutral zone, potentially decoupling the DBA-DEE relationship. We used doubly-labelled water (DLW) to validate the use of DBA on plunge-diving seabirds, Peruvian boobies (Sula variegata), foraging in waters above their thermoneutral zone (>19 °C). Mass-specific DEEDLW in boobies was 1.12 kJ/d/g, and higher in males than in females. DBA alone provided the best fitting model to estimate mass-specific DEEDLW compared to models partitioned per activity and time-budget models. Nonetheless, the model parametrizing activity at and away of their onshore breeding colony was the most parsimonious model (r=0.6). This r value, although high, is lower than all other avian studies, implying that temperature is not the main cause of DBA-DEE decoupling in birds. Time at the colony (∼80% of the day) was the largest contributor to DEE as it was the most time-consuming activity and involved nest defense. However, foraging was the most power-consuming activity (4.6 times higher activity-specific metabolic rate than resting at the colony), and commuting-flight was higher than in other gliding seabirds. In short, DBA alone can act as a proxy for DEE, opening avenues to measure the conservation energetics of this seabird in the rapidly-changing Peruvian Humboldt Current System.
每日能量消耗(DEE)是决定如何在各种活动(休息、通勤和觅食)之间分配时间以及这些活动的能量成本的结果。动态身体加速度(DBA)可用于估算与运动相关的加速度。以前对鸟类的 DBA 与 DEE 相关性的研究是针对在热中性区以下觅食的物种进行的,这可能会使 DBA 与 DEE 的关系脱钩。我们在秘鲁鲣鸟(Sula variegata)身上使用了双标记水(DLW)来验证 DBA 的使用,秘鲁鲣鸟在高于其中温带(>19 °C)的水域中觅食。鲣鸟的体重特异性 DEEDLW 为 1.12 kJ/d/g,雄鸟高于雌鸟。与按活动划分的模型和时间预算模型相比,单独的DBA模型是估算质量特异性DEEDLW的最佳拟合模型。尽管如此,将陆上繁殖地和远离繁殖地的活动参数化的模型是最拟合的模型(r=0.6)。这个r值虽然很高,但低于所有其他鸟类研究,这意味着温度不是鸟类DBA-DEE脱钩的主要原因。在鸟群中的时间(占一天的 80%)对 DEE 的贡献最大,因为这是最耗时的活动,而且涉及巢的防御。然而,觅食是最耗能的活动(活动特定代谢率比在巢穴休息时高4.6倍),通勤飞行比其他滑翔海鸟高。总之,DBA本身可以作为DEE的替代物,为测量这种海鸟在瞬息万变的秘鲁洪堡洋流系统中的保护能量开辟了途径。
{"title":"Plunge-diving into dynamic body acceleration and energy expenditure in the Peruvian booby.","authors":"van Oordt Francis, Jaime Silva, Allison Patterson, Kyle H Elliott","doi":"10.1242/jeb.249555","DOIUrl":"https://doi.org/10.1242/jeb.249555","url":null,"abstract":"<p><p>Daily energy expenditure (DEE) is the result of decisions on how to allocate time among activities (resting, commuting, and foraging) and the energy costs of those activities. Dynamic body acceleration (DBA), which measures acceleration associated with movement, can be used to estimate DEE. Previous studies of DBA-DEE correlations in birds occurred on species foraging below their thermoneutral zone, potentially decoupling the DBA-DEE relationship. We used doubly-labelled water (DLW) to validate the use of DBA on plunge-diving seabirds, Peruvian boobies (Sula variegata), foraging in waters above their thermoneutral zone (>19 °C). Mass-specific DEEDLW in boobies was 1.12 kJ/d/g, and higher in males than in females. DBA alone provided the best fitting model to estimate mass-specific DEEDLW compared to models partitioned per activity and time-budget models. Nonetheless, the model parametrizing activity at and away of their onshore breeding colony was the most parsimonious model (r=0.6). This r value, although high, is lower than all other avian studies, implying that temperature is not the main cause of DBA-DEE decoupling in birds. Time at the colony (∼80% of the day) was the largest contributor to DEE as it was the most time-consuming activity and involved nest defense. However, foraging was the most power-consuming activity (4.6 times higher activity-specific metabolic rate than resting at the colony), and commuting-flight was higher than in other gliding seabirds. In short, DBA alone can act as a proxy for DEE, opening avenues to measure the conservation energetics of this seabird in the rapidly-changing Peruvian Humboldt Current System.</p>","PeriodicalId":15786,"journal":{"name":"Journal of Experimental Biology","volume":null,"pages":null},"PeriodicalIF":2.8,"publicationDate":"2024-09-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142348003","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 : 2024-09-15Epub Date: 2024-09-24DOI: 10.1242/jeb.247793
Pauline N C Chanel, Nigel C Bennett, Maria K Oosthuizen
Highveld mole-rats (Cryptomys hottentotus pretoriae) are social rodents that inhabit networks of subterranean tunnels. In their natural environment, they are rarely exposed to light, and consequently their visual systems have regressed over evolutionary time. However, in the laboratory they display nocturnal activity, suggesting that they are sensitive to changes in ambient illumination. We examined the robustness of the Highveld mole-rat circadian system by assessing its locomotor activity under decreasing light intensities. Mole-rats were subjected to seven consecutive light cycles commencing with a control cycle (overhead fluorescent lighting at 150 lx), followed by decreasing LED lighting (500, 300, 100, 10 and 1 lx) on a 12 h light:12 h dark (L:D) photoperiod and finally a constant darkness (DD) cycle. Mole-rats displayed nocturnal activity under the whole range of experimental lighting conditions, with a distinct spike in activity at the end of the dark phase in all cycles. The mole-rats were least active during the control cycle under fluorescent light, locomotor activity increased steadily with decreasing LED light intensities, and the highest activity was exhibited when the light was completely removed. In constant darkness, mole-rats displayed free-running rhythms with periods (τ) ranging from 23.77 to 24.38 h, but was overall very close to 24 h at 24.07 h. Our findings confirm that the Highveld mole-rat has a higher threshold for light compared with aboveground dwelling rodents, which is congruent with previous neurological findings, and has implications for behavioural rhythms.
{"title":"Light sensitivity of the circadian system in the social Highveld mole-rat Cryptomys hottentotus pretoriae.","authors":"Pauline N C Chanel, Nigel C Bennett, Maria K Oosthuizen","doi":"10.1242/jeb.247793","DOIUrl":"10.1242/jeb.247793","url":null,"abstract":"<p><p>Highveld mole-rats (Cryptomys hottentotus pretoriae) are social rodents that inhabit networks of subterranean tunnels. In their natural environment, they are rarely exposed to light, and consequently their visual systems have regressed over evolutionary time. However, in the laboratory they display nocturnal activity, suggesting that they are sensitive to changes in ambient illumination. We examined the robustness of the Highveld mole-rat circadian system by assessing its locomotor activity under decreasing light intensities. Mole-rats were subjected to seven consecutive light cycles commencing with a control cycle (overhead fluorescent lighting at 150 lx), followed by decreasing LED lighting (500, 300, 100, 10 and 1 lx) on a 12 h light:12 h dark (L:D) photoperiod and finally a constant darkness (DD) cycle. Mole-rats displayed nocturnal activity under the whole range of experimental lighting conditions, with a distinct spike in activity at the end of the dark phase in all cycles. The mole-rats were least active during the control cycle under fluorescent light, locomotor activity increased steadily with decreasing LED light intensities, and the highest activity was exhibited when the light was completely removed. In constant darkness, mole-rats displayed free-running rhythms with periods (τ) ranging from 23.77 to 24.38 h, but was overall very close to 24 h at 24.07 h. Our findings confirm that the Highveld mole-rat has a higher threshold for light compared with aboveground dwelling rodents, which is congruent with previous neurological findings, and has implications for behavioural rhythms.</p>","PeriodicalId":15786,"journal":{"name":"Journal of Experimental Biology","volume":null,"pages":null},"PeriodicalIF":2.8,"publicationDate":"2024-09-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11449439/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142107967","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 : 2024-09-15Epub Date: 2024-09-19DOI: 10.1242/jeb.249238
Roger W P Kissane, Karl T Bates, Michael J Fagan, Linjie Wang, Peter J Watson, Graham N Askew
Muscle spindle abundance is highly variable in vertebrates, but the functional determinants of this variation are unclear. Recent work has shown that human leg muscles with the lowest abundance of muscle spindles primarily function to lengthen and absorb energy, while muscles with a greater spindle abundance perform active-stretch-shorten cycles with no net work, suggesting that muscle spindle abundance may be underpinned by muscle function. Compared with other mammalian muscles, the digastric muscle contains the lowest abundance of muscle spindles and, therefore, might be expected to generate substantial negative work. However, it is widely hypothesised that as a jaw-opener (anatomically) the digastric muscle would primarily function to depress the jaw, and consequently do positive work. Through a combination of X-ray reconstruction of moving morphology (XROMM), electromyography and fluoromicrometry, we characterised the 3D kinematics of the jaw and digastric muscle during feeding in rabbits. Subsequently, the work loop technique was used to simulate in vivo muscle behaviour in situ, enabling muscle force to be quantified in relation to muscle strain and hence determine the muscle's function during mastication. When functioning on either the working or balancing side, the digastric muscle generates a large amount of positive work during jaw opening, and a large amount of negative work during jaw closing, on average producing a relatively small amount of net negative work. Our data therefore further support the hypothesis that muscle spindle abundance is linked to muscle function; specifically, muscles that absorb a relatively large amount of negative work have a low spindle abundance.
脊椎动物的肌肉纺锤体丰度变化很大,但这种变化的功能决定因素尚不清楚。最近的研究表明,肌肉纺锤体丰度最低的人类腿部肌肉的主要功能是拉长和吸收能量,而肌肉纺锤体丰度较高的肌肉则执行主动-拉伸-缩短循环,不做净功,这表明肌肉纺锤体丰度可能是肌肉功能的基础。与其他哺乳动物的肌肉相比,腹肌含有的肌束最少,因此可能会产生大量负功。然而,人们普遍认为,作为下颌开启器(解剖学上),地肌的主要功能是压低下颌,从而产生正功。通过 X 射线运动形态重建(XROMM)、肌电图和荧光显微测定法的组合,我们描述了兔子进食时下颌和地腹肌的三维运动学特征。随后,我们利用工作环技术在原位模拟了体内肌肉的行为,从而能够量化肌肉力量与肌肉应变的关系,进而确定肌肉在咀嚼时的功能。在工作侧或平衡侧工作时,颌间肌在下颌张开时产生大量正功,在下颌闭合时产生大量负功,平均产生的净负功相对较小。因此,我们的数据进一步支持了肌肉纺锤体丰度与肌肉功能相关的假设;具体来说,吸收相对大量负功的肌肉纺锤体丰度较低。
{"title":"The functional role of the rabbit digastric muscle during mastication.","authors":"Roger W P Kissane, Karl T Bates, Michael J Fagan, Linjie Wang, Peter J Watson, Graham N Askew","doi":"10.1242/jeb.249238","DOIUrl":"10.1242/jeb.249238","url":null,"abstract":"<p><p>Muscle spindle abundance is highly variable in vertebrates, but the functional determinants of this variation are unclear. Recent work has shown that human leg muscles with the lowest abundance of muscle spindles primarily function to lengthen and absorb energy, while muscles with a greater spindle abundance perform active-stretch-shorten cycles with no net work, suggesting that muscle spindle abundance may be underpinned by muscle function. Compared with other mammalian muscles, the digastric muscle contains the lowest abundance of muscle spindles and, therefore, might be expected to generate substantial negative work. However, it is widely hypothesised that as a jaw-opener (anatomically) the digastric muscle would primarily function to depress the jaw, and consequently do positive work. Through a combination of X-ray reconstruction of moving morphology (XROMM), electromyography and fluoromicrometry, we characterised the 3D kinematics of the jaw and digastric muscle during feeding in rabbits. Subsequently, the work loop technique was used to simulate in vivo muscle behaviour in situ, enabling muscle force to be quantified in relation to muscle strain and hence determine the muscle's function during mastication. When functioning on either the working or balancing side, the digastric muscle generates a large amount of positive work during jaw opening, and a large amount of negative work during jaw closing, on average producing a relatively small amount of net negative work. Our data therefore further support the hypothesis that muscle spindle abundance is linked to muscle function; specifically, muscles that absorb a relatively large amount of negative work have a low spindle abundance.</p>","PeriodicalId":15786,"journal":{"name":"Journal of Experimental Biology","volume":null,"pages":null},"PeriodicalIF":2.8,"publicationDate":"2024-09-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11449450/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142288922","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 : 2024-09-15Epub Date: 2024-09-20DOI: 10.1242/jeb.246824
Jorge Ayala-Berdon, Kevin I Medina-Bello
Torpor is an adaptive strategy allowing heterothermic animals to cope with energy limitations. In birds and mammals, intrinsic and extrinsic factors, such as body mass and ambient temperature, are the main variables influencing torpor use. A theoretical model of the relationship between metabolic rate during torpor and ambient temperature has been proposed. Nevertheless, no empirical attempts have been made to assess the model predictions under different climates. Using open-flow respirometry, we evaluated the ambient temperature at which bats entered torpor and when torpid metabolic rate reached its minimum, the reduction in metabolic rate below basal values, and minimum torpid metabolic rate in 11 bat species of the family Vespertilionidae with different body mass from warm and cold climates. We included data on the minimum torpid metabolic rate of five species we retrieved from the literature. We tested the effects using mixed-effect phylogenetic models. All models showed a significant interaction between body mass and climate. Smaller bats went into torpor and reached minimum torpid metabolic rates at warmer temperatures, showed a higher reduction in the metabolic rate below basal values, and presented lower torpid metabolic rates than larger ones. The slopes of the models were different for bats from different climates. These results are likely explained by differences in body mass and the metabolic rate of bats, which may favor larger bats expressing torpor in colder sites and smaller bats in the warmer ones. Further studies to assess torpor use in bats from different climates are proposed.
{"title":"Torpor energetics are related to the interaction between body mass and climate in bats of the family Vespertilionidae.","authors":"Jorge Ayala-Berdon, Kevin I Medina-Bello","doi":"10.1242/jeb.246824","DOIUrl":"10.1242/jeb.246824","url":null,"abstract":"<p><p>Torpor is an adaptive strategy allowing heterothermic animals to cope with energy limitations. In birds and mammals, intrinsic and extrinsic factors, such as body mass and ambient temperature, are the main variables influencing torpor use. A theoretical model of the relationship between metabolic rate during torpor and ambient temperature has been proposed. Nevertheless, no empirical attempts have been made to assess the model predictions under different climates. Using open-flow respirometry, we evaluated the ambient temperature at which bats entered torpor and when torpid metabolic rate reached its minimum, the reduction in metabolic rate below basal values, and minimum torpid metabolic rate in 11 bat species of the family Vespertilionidae with different body mass from warm and cold climates. We included data on the minimum torpid metabolic rate of five species we retrieved from the literature. We tested the effects using mixed-effect phylogenetic models. All models showed a significant interaction between body mass and climate. Smaller bats went into torpor and reached minimum torpid metabolic rates at warmer temperatures, showed a higher reduction in the metabolic rate below basal values, and presented lower torpid metabolic rates than larger ones. The slopes of the models were different for bats from different climates. These results are likely explained by differences in body mass and the metabolic rate of bats, which may favor larger bats expressing torpor in colder sites and smaller bats in the warmer ones. Further studies to assess torpor use in bats from different climates are proposed.</p>","PeriodicalId":15786,"journal":{"name":"Journal of Experimental Biology","volume":null,"pages":null},"PeriodicalIF":2.8,"publicationDate":"2024-09-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142107971","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 : 2024-09-15Epub Date: 2024-09-30DOI: 10.1242/jeb.247413
Grégoire Boulinguez-Ambroise, Doug M Boyer, Noah T Dunham, Gabriel S Yapuncich, Madison Bradley-Cronkwright, Angel Zeininger, Daniel Schmitt, Jesse W Young
Jumping is a crucial behavior in fitness-critical activities including locomotion, resource acquisition, courtship displays and predator avoidance. In primates, paleontological evidence suggests selection for enhanced jumping ability during their early evolution. However, our interpretation of the fossil record remains limited, as no studies have explicitly linked levels of jumping performance with interspecific skeletal variation. We used force platform analyses to generate biomechanical data on maximal jumping performance in three genera of callitrichine monkeys falling along a continuum of jumping propensity: Callimico (relatively high propensity jumper), Saguinus (intermediate jumping propensity) and Callithrix (relatively low propensity jumper). Individuals performed vertical jumps to perches of increasing height within a custom-built tower. We coupled performance data with high-resolution micro-CT data quantifying bony features thought to reflect jumping ability. Levels of maximal performance between species - e.g. maximal take-off velocity of the center of mass (CoM) - parallel established gradients of jumping propensity. Both biomechanical analysis of jumping performance determinants (e.g. CoM displacement, maximal force production and peak mechanical power during push-off) and multivariate analyses of bony hindlimb morphology highlight different mechanical strategies among taxa. For instance, Callimico, which has relatively long hindlimbs, followed a strategy of fully extending of the limbs to maximize CoM displacement - rather than force production - during push-off. In contrast, relatively shorter-limbed Callithrix depended mostly on relatively high push-off forces. Overall, these results suggest that leaping performance is at least partially associated with correlated anatomical and behavioral adaptations, suggesting the possibility of improving inferences about performance in the fossil record.
{"title":"Biomechanical and morphological determinants of maximal jumping performance in callitrichine monkeys.","authors":"Grégoire Boulinguez-Ambroise, Doug M Boyer, Noah T Dunham, Gabriel S Yapuncich, Madison Bradley-Cronkwright, Angel Zeininger, Daniel Schmitt, Jesse W Young","doi":"10.1242/jeb.247413","DOIUrl":"10.1242/jeb.247413","url":null,"abstract":"<p><p>Jumping is a crucial behavior in fitness-critical activities including locomotion, resource acquisition, courtship displays and predator avoidance. In primates, paleontological evidence suggests selection for enhanced jumping ability during their early evolution. However, our interpretation of the fossil record remains limited, as no studies have explicitly linked levels of jumping performance with interspecific skeletal variation. We used force platform analyses to generate biomechanical data on maximal jumping performance in three genera of callitrichine monkeys falling along a continuum of jumping propensity: Callimico (relatively high propensity jumper), Saguinus (intermediate jumping propensity) and Callithrix (relatively low propensity jumper). Individuals performed vertical jumps to perches of increasing height within a custom-built tower. We coupled performance data with high-resolution micro-CT data quantifying bony features thought to reflect jumping ability. Levels of maximal performance between species - e.g. maximal take-off velocity of the center of mass (CoM) - parallel established gradients of jumping propensity. Both biomechanical analysis of jumping performance determinants (e.g. CoM displacement, maximal force production and peak mechanical power during push-off) and multivariate analyses of bony hindlimb morphology highlight different mechanical strategies among taxa. For instance, Callimico, which has relatively long hindlimbs, followed a strategy of fully extending of the limbs to maximize CoM displacement - rather than force production - during push-off. In contrast, relatively shorter-limbed Callithrix depended mostly on relatively high push-off forces. Overall, these results suggest that leaping performance is at least partially associated with correlated anatomical and behavioral adaptations, suggesting the possibility of improving inferences about performance in the fossil record.</p>","PeriodicalId":15786,"journal":{"name":"Journal of Experimental Biology","volume":null,"pages":null},"PeriodicalIF":2.8,"publicationDate":"2024-09-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142108025","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 : 2024-09-15Epub Date: 2024-09-25DOI: 10.1242/jeb.247431
Melinda G Conners, Jonathan A Green, Richard A Phillips, Rachael A Orben, Chen Cui, Petar M Djurić, Eleanor Heywood, Alexei L Vyssotski, Lesley H Thorne
Estimates of movement costs are essential for understanding energetic and life-history trade-offs. Although overall dynamic body acceleration (ODBA) derived from accelerometer data is widely used as a proxy for energy expenditure (EE) in free-ranging animals, its utility has not been tested in species that predominately use body rotations or exploit environmental energy for movement. We tested a suite of sensor-derived movement metrics as proxies for EE in two species of albatrosses, which routinely use dynamic soaring to extract energy from the wind to reduce movement costs. Birds were fitted with a combined heart-rate, accelerometer, magnetometer and GPS logger, and relationships between movement metrics and heart rate-derived V̇O2, an indirect measure of EE, were analyzed during different flight and activity modes. When birds were exclusively soaring, a metric derived from angular velocity on the yaw axis provided a useful proxy of EE. Thus, body rotations involved in dynamic soaring have clear energetic costs, albeit considerably lower than those of the muscle contractions required for flapping flight. We found that ODBA was not a useful proxy for EE in albatrosses when birds were exclusively soaring. As albatrosses spend much of their foraging trips soaring, ODBA alone was a poor predictor of EE in albatrosses. Despite the lower percentage of time flapping, the number of flaps was a useful metric when comparing EE across foraging trips. Our findings highlight that alternative metrics, beyond ODBA, may be required to estimate energy expenditure from inertial sensors in animals whose movements involve extensive body rotations.
运动成本的估计对于了解能量和生命史权衡至关重要。虽然从加速度计数据中得出的整体动态身体加速度(ODBA)被广泛用作自由活动动物能量消耗(EE)的替代指标,但其效用尚未在主要使用身体旋转或利用环境能量进行运动的物种中进行过测试。我们在两种信天翁中测试了一套传感器衍生的运动指标作为 EE 的替代指标,这两种信天翁通常使用动态翱翔从风中获取能量以降低运动成本。鸟类安装了心率、加速度计、磁力计和全球定位系统综合记录器,在不同的飞行和活动模式下分析了运动指标与心率衍生 VO2(EE 的间接测量指标)之间的关系。当鸟类完全处于翱翔状态时,由偏航轴角速度得出的指标可有效替代 EE。因此,动态翱翔中的身体旋转有明显的能量成本,尽管比拍打飞行所需的肌肉收缩低得多。我们发现,当信天翁只进行翱翔时,ODBA并不能有效地替代EE。由于信天翁觅食的大部分时间都在翱翔,因此仅凭ODBA不能很好地预测信天翁的EE。尽管信天翁拍打的时间比例较低,但在比较不同觅食行程的EE时,拍打次数是一个有用的指标。我们的研究结果突出表明,对于那些在运动中需要大量身体旋转的动物,可能需要ODBA以外的其他指标来估算惯性传感器的能量消耗。
{"title":"Dynamic soaring decouples dynamic body acceleration and energetics in albatrosses.","authors":"Melinda G Conners, Jonathan A Green, Richard A Phillips, Rachael A Orben, Chen Cui, Petar M Djurić, Eleanor Heywood, Alexei L Vyssotski, Lesley H Thorne","doi":"10.1242/jeb.247431","DOIUrl":"10.1242/jeb.247431","url":null,"abstract":"<p><p>Estimates of movement costs are essential for understanding energetic and life-history trade-offs. Although overall dynamic body acceleration (ODBA) derived from accelerometer data is widely used as a proxy for energy expenditure (EE) in free-ranging animals, its utility has not been tested in species that predominately use body rotations or exploit environmental energy for movement. We tested a suite of sensor-derived movement metrics as proxies for EE in two species of albatrosses, which routinely use dynamic soaring to extract energy from the wind to reduce movement costs. Birds were fitted with a combined heart-rate, accelerometer, magnetometer and GPS logger, and relationships between movement metrics and heart rate-derived V̇O2, an indirect measure of EE, were analyzed during different flight and activity modes. When birds were exclusively soaring, a metric derived from angular velocity on the yaw axis provided a useful proxy of EE. Thus, body rotations involved in dynamic soaring have clear energetic costs, albeit considerably lower than those of the muscle contractions required for flapping flight. We found that ODBA was not a useful proxy for EE in albatrosses when birds were exclusively soaring. As albatrosses spend much of their foraging trips soaring, ODBA alone was a poor predictor of EE in albatrosses. Despite the lower percentage of time flapping, the number of flaps was a useful metric when comparing EE across foraging trips. Our findings highlight that alternative metrics, beyond ODBA, may be required to estimate energy expenditure from inertial sensors in animals whose movements involve extensive body rotations.</p>","PeriodicalId":15786,"journal":{"name":"Journal of Experimental Biology","volume":null,"pages":null},"PeriodicalIF":2.8,"publicationDate":"2024-09-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142154292","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 : 2024-09-15Epub Date: 2024-09-25DOI: 10.1242/jeb.247503
Soonyoung Kim, Krishna N Badhiwala, Guillaume Duret, Jacob T Robinson
Understanding how internal states such as satiety are connected to animal behavior is a fundamental question in neuroscience. Hydra vulgaris, a freshwater cnidarian with only 12 neuronal cell types, serves as a tractable model system for studying state-dependent behaviors. We found that starved hydras consistently move towards light, while fed hydras do not. By modeling this behavior as a set of three sequences of head orientation, jump distance and jump rate, we demonstrate that the satiety state only affects the rate of the animal jumping to a new position, while the orientation and jump distance are unaffected. These findings yield insights into how internal states in a simple organism, Hydra, affect specific elements of a behavior, and offer general principles for studying the relationship between state-dependent behaviors and their underlying molecular mechanisms.
{"title":"Phototaxis is a satiety-dependent behavioral sequence in Hydra vulgaris.","authors":"Soonyoung Kim, Krishna N Badhiwala, Guillaume Duret, Jacob T Robinson","doi":"10.1242/jeb.247503","DOIUrl":"10.1242/jeb.247503","url":null,"abstract":"<p><p>Understanding how internal states such as satiety are connected to animal behavior is a fundamental question in neuroscience. Hydra vulgaris, a freshwater cnidarian with only 12 neuronal cell types, serves as a tractable model system for studying state-dependent behaviors. We found that starved hydras consistently move towards light, while fed hydras do not. By modeling this behavior as a set of three sequences of head orientation, jump distance and jump rate, we demonstrate that the satiety state only affects the rate of the animal jumping to a new position, while the orientation and jump distance are unaffected. These findings yield insights into how internal states in a simple organism, Hydra, affect specific elements of a behavior, and offer general principles for studying the relationship between state-dependent behaviors and their underlying molecular mechanisms.</p>","PeriodicalId":15786,"journal":{"name":"Journal of Experimental Biology","volume":null,"pages":null},"PeriodicalIF":2.8,"publicationDate":"2024-09-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11449437/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142000080","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}