Energetic Extremes in Aquatic Locomotion by Coral Reef Fishes

Underwater locomotion is challenging due to the high friction and resistance imposed on a body moving through water and energy lost in the wake during undulatory propulsion. While aquatic organisms have evolved streamlined shapes to overcome such resistance, underwater locomotion has long been considered a costly exercise. Recent evidence for a range of swimming vertebrates, however, has suggested that flapping paired appendages around a rigid body may be an extremely efficient means of aquatic locomotion. Using intermittent flow-through respirometry, we found exceptional energetic performance in the Bluelined wrasse Stethojulis bandanensis, which maintains tuna-like optimum cruising speeds (up to 1 metre s(-1)) while using 40% less energy than expected for their body size. Displaying an exceptional aerobic scope (22-fold above resting), streamlined rigid-body posture, and wing-like fins that generate lift-based thrust, S. bandanensis literally flies underwater to efficiently maintain high optimum swimming speeds. Extreme energetic performance may be key to the colonization of highly variable environments, such as the wave-swept habitats where S. bandanensis and other wing-finned species tend to occur. Challenging preconceived notions of how best to power aquatic locomotion, biomimicry of such lift-based fin movements could yield dramatic reductions in the power needed to propel underwater vehicles at high speed.Funding was provided by the Australian Research Council (to CJF) and the Danish Agency for Science, Technology and Innovation (to JFS). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript

Maximum salinity tolerance and osmoregulatory capabilities of European perch <i>Perca fluviatilis</i> populations originating from different salinity habitats

Brackish water European perch tolerates significantly higher salinities than freshwater conspecifics due to a physiological specialization. Therefore, brackish water European perch populations may not receive recruitment from freshwater, which raises conservation issues regarding brackish water perch populations due to climate change and fisheries. Although considered a stenohaline freshwater species, European perch ( Perca fluviatilis ) inhabit brackish waters. The present study determined the maximum salinity tolerance and osmoregulatory capability on individuals originating from brackish water and from freshwater populations. The fish were acclimated for 3 weeks to salinities of 0, 10, 12.5, 15, 17.5 and 20 after an initial stepwise increase to the target salinity. The maximum salinity tolerance was determined as the test salinity below which the fish could not acclimate and lost equilibrium. Blood plasma osmolality was measured if the fish had not lost equilibrium after the acclimation period. The maximum salinity tolerance was 17.5 for brackish water European perch and 10 for fresh water European perch. The high salinity tolerance of the brackish water European perch was caused by their ability to both hyper- and hypo-osmoregulate, whereas the freshwater originating fish could only hyper-osmoregulate. The results showed that maximum salinity tolerances and osmoregulatory capabilities depends on the origin habitat salinity. Due to genetic differentiation between European perch populations in brackish and fresh water, the possibility of brackish water European perch being a subspecies of European perch is discussed, yet vital knowledge concerning heritability of salinity tolerance traits is still missing. Regardless of species status, within-species plasticity in the ability to cope with varying salinities have substantial ecological and conservation implications and underlines the need for managing brackish water and freshwater European perch stocks separately

Fish swimming in schools save energy regardless of their spatial position

For animals, being a member of a group provides various advantages, such as reduced vulnerability to predators, increased foraging opportunities and reduced energetic costs of locomotion. In moving groups such as fish schools, there are benefits of group membership for trailing individuals, who can reduce the cost of movement by exploiting the flow patterns generated by the individuals swimming ahead of them. However, whether positions relative to the closest neighbours (e.g. ahead, sided by side or behind) modulate the individual energetic cost of swimming is still unknown. Here, we addressed these questions in grey mullet Liza aurata by measuring tail-beat frequency and amplitude of 15 focal fish, swimming in separate schools, while swimming in isolation and in various positions relative to their closest neighbours, at three speeds. Our results demonstrate that, in a fish school, individuals in any position have reduced costs of swimming, compared to when they swim at the same speed but alone. Although fish swimming behind their neighbours save the most energy, even fish swimming ahead of their nearest neighbour were able to gain a net energetic benefit over swimming in isolation, including those swimming at the front of a school. Interestingly, this energetic saving was greatest at the lowest swimming speed measured in our study. Because any member of a school gains an energetic benefit compared to swimming alone, we suggest that the benefits of membership in moving groups may be more strongly linked to reducing the costs of locomotion than previously appreciated

Intra-Specific Difference in the Effect of Salinity on Physiological Performance in European Perch (<i>Perca fluviatilis</i>) and Its Ecological Importance for Fish in Estuaries

Changes in environmental salinity challenge fish homeostasis and may affect physiological performance, such as swimming capacity and metabolism, which are important for foraging, migration, and escaping predators in the wild. The effects of salinity stress on physiological performance are largely species specific, but may also depend on intra-specific differences in physiological capabilities of sub-populations. We measured critical swimming speed (U crit ) and metabolic rates during swimming and at rest at salinities of 0 and 10 in European perch ( Perca fluviatilis ) from a low salinity tolerance population (LSTP) and a high salinity tolerance population (HSTP). U crit of LSTP was significantly reduced at a salinity of 10 yet was unaffected by salinity change in HSTP. We did not detect a significant cost of osmoregulation, which should theoretically be apparent from the metabolic rates during swimming and at rest at a salinity of 0 compared to at a salinity of 10 (iso-osmotic). Maximum metabolic rates were also not affected by salinity, indicating a modest tradeoff between respiration and osmoregulation (osmo-respiratory compromise). Intra-specific differences in effects of salinity on physiological performance are important for fish species to maintain ecological compatibility in estuarine environments, yet render these sub-populations vulnerable to fisheries. The findings of the present study are therefore valuable knowledge in conservation and management of estuarine fish populations

Adapt, move, or die: how will tropical coral reef fishes cope with ocean warming?

Previous studies hailed thermal tolerance and the capacity for organisms to acclimate and adapt as the primary pathways for species survival under climate change. Here we challenge this theory. Over the past decade more than 365 tropical stenothermal fish species have been documented moving pole-ward, away from ocean warming hotspots where temperatures 2-3 °C above long-term annual means can compromise critical physiological processes. We examined the capacity of a model species - a thermally-sensitive coral reef fish, Chromis viridis (Pomacentridae) – to use preference behaviour to regulate its body temperature. Movement could potentially circumvent the physiological stress response associated with elevated temperatures and may be a strategy relied upon before genetic adaptation can be effectuated. Individuals were maintained at one of six temperatures (23, 25, 27, 29, 31 and 33 °C) for at least six weeks. We compared the relative importance of acclimation temperature to changes in upper critical thermal limits, aerobic metabolic scope, and thermal preference. While acclimation temperature positively affected the upper critical thermal limit, neither aerobic metabolic scope nor thermal preference exhibited such plasticity. Importantly, when given the choice to stay in a habitat reflecting their acclimation temperatures or relocate, fish acclimated to end-of-century predicted temperatures (i.e., 31 or 33 °C) preferentially sought out cooler temperatures, those equivalent to long-term summer averages in their natural habitats (~29 °C). This was also the temperature providing the greatest aerobic metabolic scope and body condition across all treatments. Consequently, acclimation can confer plasticity in some performance traits, but may be an unreliable indicator of the ultimate survival and distribution of mobile stenothermal species under global warming. Conversely, thermal preference can arise long before, and remain long after, the harmful effects of elevated ocean temperatures take hold and may be the primary driver of the escalating pole-ward migration of species

Habitat complexity influences selection of thermal environment in a common coral reef fish

Coral reef species, like most tropical species, are sensitive to increasing environmental temperatures, with many species already living close to their thermal maxima. Ocean warming and the increasing frequency and intensity of marine heatwaves are challenging the persistence of reef-associated species through both direct physiological effects of elevated water temperatures and the degradation and loss of habitat structure following disturbance. Understanding the relative importance of habitat degradation and ocean warming in shaping species distributions is critical in predicting the likely biological effects of global warming. Using an automated shuttle box system, we investigated how habitat complexity influences the selection of thermal environments for a common coral reef damselfish, Chromis atripectoralis. In the absence of any habitat (i.e. control), C. atripectoralis avoided temperatures below 22.9 ± 0.8°C and above 31.9 ± 0.6°C, with a preferred temperature (Tpref) of 28.1 ± 0.9°C. When complex habitat was available, individual C. atripectoralis occupied temperatures down to 4.3°C lower (mean ± SE; threshold: 18.6 ± 0.7°C; Tpref: 18.9 ± 1.0°C) than control fish. Conversely, C. atripectoralis in complex habitats occupied similar upper temperatures as control fish (threshold: 31.7 ± 0.4°C; preference: 28.3 ± 0.7°C). Our results show that the availability of complex habitat can influence the selection of thermal environment by a coral reef fish, but only at temperatures below their thermal preference. The limited scope of C. atripectoralis to occupy warmer environments, even when associated with complex habitat, suggests that habitat restoration efforts in areas that continue to warm may not be effective in retaining populations of C. atripectoralis and similar species. This species may have to move to cooler (e.g. deeper or higher latitude) habitats under predicted future warming. The integration of habitat quality and thermal environment into conservation efforts will be essential to conserve of coral reef fish populations under future ocean warming scenarios

Shuttle-box systems for studying preferred environmental ranges by aquatic animals

Animals’ selection of environments within a preferred range is key to understanding their habitat selection, tolerance to stressors and responses to environmental change. For aquatic animals, preferred environmental ranges can be studied in so-called shuttle-boxes, where an animal can choose its ambient environment by shuttling between separate choice chambers with differences in an environmental variable. Over time, researchers have refined the shuttle-box technology and applied them in many different research contexts, and we here review the use of shuttle-boxes as a research tool with aquatic animals over the past 50 years. Most studies on the methodology have been published in the latest decade, probably due to an increasing research interest in the effects of environmental change, which underlines the current popularity of the system. The shuttle-box has been applied to a wide range of research topics with regards to preferred ranges of temperature, CO2, salinity and O2 in a vast diversity of species, showing broad applicability for the system. We have synthesized the current state-of-the-art of the methodology and provided best practice guidelines with regards to setup, data analyses, experimental design and study reporting. We have also identified a series of knowledge gaps, which can and should be addressed in future studies. We conclude with highlighting directions for research using shuttle-boxes within evolutionary biology and behavioural and physiological ecology

Turbulent flow reduces oxygen consumption in the labriform swimming shiner perch, Cymatogaster aggregata

Fish swimming energetics are often measured in laboratory environments which attempt to minimize turbulence, though turbulent flows are common in the natural environment. To test whether the swimming energetics and kinematics of shiner perch Cymatogaster aggregata (a labriform swimmer) were affected by turbulence, two flow conditions were constructed in a swim-tunnel respirometer. A low-turbulence flow was created using a common swim-tunnel respirometry setup with a flow straightener and fine-mesh grid to minimize velocity fluctuations. A high-turbulence flow condition was created by allowing large velocity fluctuations to persist without a flow straightener or fine grid. The two conditions were tested with Particle Image Velocimetry to confirm significantly different turbulence properties throughout a range of mean flow speeds. Oxygen consumption rates of the swimming fish increased with swimming speeds and pectoral fin beat frequencies in both flow conditions. Higher turbulence also caused a greater positional variability in swimming individuals (vs. low-turbulence flow) at medium and high speeds. Surprisingly, fish used less oxygen in high turbulence compared to low-turbulence flow at medium and high swimming speeds. Simultaneous measurements of swimming kinematics indicated that these reductions in oxygen consumption could not be explained by specific known flow-adaptive behaviours such as Kármán-gaiting or entraining. Therefore, fish in high-turbulence flow may take advantage of the high variability in turbulent energy through time. These results suggest that swimming behavior and energetics measured in the lab in straightened flow, typical of standard swimming respirometers, might differ from that of more turbulent, semi-natural flow conditions.PostprintPeer reviewe