Journal of Experimental Biology最新文献

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.

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.

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.

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.

A long-standing problem in the study of avian flight is determining how biomechanics and physiology are associated with behaviour, ecological interactions and evolution. In some avian clades, flight mechanisms are strongly linked to ecology. Hummingbirds, for example, exhibit traits that support both hovering flight and nectar foraging. In most avian clades, however, features such as wing shape are highly variable among taxa without clear relationships to biomechanics, energetics or ecology. In this Commentary, we discuss challenges to understanding associations between phenotype and performance in avian flight. A potential pitfall in studies that attempt to link trait specialization with performance is that the most relevant traits and environments are not being considered. Additionally, a large number of studies of the mechanisms of avian flight are highly phenomenological. Although observations are essential for hypothesis development, we argue that for our discipline to make progress, we will need much more integration of the observational phase with developing crucial tests of competing hypotheses. Direct comparison of alternative hypotheses can be accomplished through analytical frameworks as well as through experimentation.

The most recent and largest radiation of marine filter feeders are edentulous baleen whales (Mysticeti) that use keratinized racks of fringed and matted baleen to filter zooplankton (e.g. krill) or small schooling fish (e.g. anchovies, sardines). Rorqual whales (Balaeopteridae) exhibit the greatest size range among mysticetes and employ a unique lunge-feeding mechanism whereby engulfment and filtration are temporally decoupled. As a result, lunge feeding confers the ability to rapidly engulf large prey aggregations, such as krill or schooling fish, followed by a prolonged filter phase. In contrast, engulfment and filtration occur at the same time in all other gigantic filter feeders (e.g. basking sharks, whale sharks) at slow speeds. Although lunges in rorquals occur at higher speeds, the extreme predator-prey ratios at play suggest that whales may not be able to overcome the escape abilities of scattering prey. These types of prey have been engaged in evolutionary arms races with smaller predators for tens of millions of years prior to the rise of today's ocean giants. Extant rorqual whales evolved gigantism only in the last few million years; thus, they represent rare enemies of small prey such that flight responses may be delayed until escape is less likely. Data from whale-borne movement-sensing tags, looming stimulus experiments and stomach contents suggest a potential trade-off in capture efficiency for different prey types (e.g. fish versus krill) with increasing whale body size. Such constraints likely shaped the ecology and energetics of foraging at the largest scales.

Understanding animal movement is at the core of ecology, evolution and conservation science. Big data approaches for animal tracking have facilitated impactful synthesis research on spatial biology and behavior in ecologically important and human-impacted regions. Similarly, databases of animal traits (e.g. body size, limb length, locomotion method, lifespan) have been used for a wide range of comparative questions, with emerging data being shared at the level of individuals and populations. Here, we argue that the proliferation of both types of publicly available data creates exciting opportunities to unlock new avenues of research, such as spatial planning and ecological forecasting. We assessed the feasibility of combining animal tracking and trait databases to develop and test hypotheses across geographic, temporal and biological allometric scales. We identified multiple research questions addressing performance and distribution constraints that could be answered by integrating trait and tracking data. For example, how do physiological (e.g. metabolic rates) and biomechanical traits (e.g. limb length, locomotion form) influence migration distances? We illustrate the potential of our framework with three case studies that effectively integrate trait and tracking data for comparative research. An important challenge ahead is the lack of taxonomic and spatial overlap in trait and tracking databases. We identify critical next steps for future integration of tracking and trait databases, with the most impactful being open and interlinked individual-level data. Coordinated efforts to combine trait and tracking databases will accelerate global ecological and evolutionary insights and inform conservation and management decisions in our changing world.

Animal migrations, or long-distance movements, on land, through water or in the air, are considered energetically costly because of the investment in persistent locomotion typical for migration. Diverse strategies exist to manage these energetic costs. Yet migration is only one stage in an annual cycle and may not be the most energetically costly. To better understand how free-ranging animals adaptively organize energy expenditure and locomotion, an annual cycle perspective is needed. Bio-logging data are collected for a range of animal species and could facilitate a life cycle approach to study energy expenditure. We provide examples from several studies across different taxa, as well as a more in-depth exploration from our own recent research on time activity budgets based on field observations and bio-logging data to estimate daily energy expenditure in a migratory seabird throughout a year. Our research has shown that daily energy expenditure is highest (1.7× average daily energy expenditure) during the spring migration of long-distance migratory gulls, whereas short-distance migrants expend the most energy (1.4× average daily energy expenditure) during the breeding season. Based on the examples provided, we show how bio-energetic models create exciting opportunities to study daily energetics and behaviour of migratory animals, although limitations also still exist. Such studies can reveal when, where and why peaks and lulls in energy expenditure arise over the annual cycle of a migrant, if long-distance movements are indeed energetically expensive and how animals can adapt to fluctuating demands in their natural environment throughout the year.

Drosophila's innate response to gravity, geotaxis, has been used to assess the impact of aging and disease on motor performance. Despite its rich history, fly geotaxis continues to be largely measured manually and assessed through simplistic metrics, limiting analytic insights into the behavior. Here, we have constructed a fully programmable apparatus and developed a multi-object tracking software capable of following sub-second movements of individual flies, thus allowing quantitative analysis of geotaxis. The apparatus monitors 10 fly cohorts simultaneously, with each cohort consisting of up to 7 flies. The software tracks single flies during the entire run with ∼97% accuracy, yielding detailed climbing curve, speed and movement direction with 1/30 s resolution. Our tracking permits the construction of multi-variable metrics and the detection of transitory movement phenotypes, such as slips and falls. The platform is therefore poised to advance Drosophila geotaxis assay into a comprehensive assessment of locomotor behavior.

Non-dimensional groups of measured quantities enable comparison between measurements of animals under different conditions and comparison between species. One of the most used such groups is the Reynolds number, which compares inertial and viscous contributions to forces on swimming animals. This group includes two quantities that are chosen by the researcher: a typical length and speed. Choosing these parameters will affect the numerical value of the Reynolds number, defining the state of the fluid flow. For example, by choosing fish body length as opposed to propulsive fin chord, results may vary by an order of magnitude with consequences for analysis and hydrodynamic regimes. Here, we suggest a standardized set of lengths and speeds to be used for aquatic animal locomotion to enable confident utilization of data from different sources. This framework aims to improve comparative studies within the field.