Yuuki Y. Watanabe

Stroke frequency, but not swimming speed, is related to body size in free-ranging seabirds, pinnipeds and cetaceans

It is obvious, at least qualitatively, that small animals move their locomotory apparatus faster than large animals: small insects move their wings invisibly fast, while large birds flap their wings slowly. However, quantitative observations have been difficult to obtain from free-ranging swimming animals. We surveyed the swimming behaviour of animals ranging from 0.5 kg seabirds to 30 000 kg sperm whales using animal-borne accelerometers. Dominant stroke cycle frequencies of swimming specialist seabirds and marine mammals were proportional to mass−0.29 (R2=0.99, n=17 groups), while propulsive swimming speeds of 1–2 m s−1 were independent of body size. This scaling relationship, obtained from breath-hold divers expected to swim optimally to conserve oxygen, does not agree with recent theoretical predictions for optimal swimming. Seabirds that use their wings for both swimming and flying stroked at a lower frequency than other swimming specialists of the same size, suggesting a morphological trade-off with wing size and stroke frequency representing a compromise. In contrast, foot-propelled diving birds such as shags had similar stroke frequencies as other swimming specialists. These results suggest that muscle characteristics may constrain swimming during cruising travel, with convergence among diving specialists in the proportions and contraction rates of propulsive muscles.

Linking animal-borne video to accelerometers reveals prey capture variability

Understanding foraging is important in ecology, as it determines the energy gains and, ultimately, the fitness of animals. However, monitoring prey captures of individual animals is difficult. Direct observations using animal-borne videos have short recording periods, and indirect signals (e.g., stomach temperature) are never validated in the field. We took an integrated approach to monitor prey captures by a predator by deploying a video camera (lasting for 85 min) and two accelerometers (on the head and back, lasting for 50 h) on free-swimming Adélie penguins. The movies showed that penguins moved the heads rapidly to capture krill in midwater and fish (Pagothenia borchgrevinki) underneath the sea ice. Captures were remarkably fast (two krill per second in swarms) and efficient (244 krill or 33 P. borchgrevinki in 78–89 min). Prey captures were detected by the signal of head acceleration relative to body acceleration with high sensitivity and specificity (0.83–0.90), as shown by receiver-operating characteristic analysis. Extension of signal analysis to the entire behavioral records showed that krill captures were spatially and temporally more variable than P. borchgrevinki captures. Notably, the frequency distribution of krill capture rate closely followed a power-law model, indicating that the foraging success of penguins depends on a small number of very successful dives. The three steps illustrated here (i.e., video observations, linking video to behavioral signals, and extension of signal analysis) are unique approaches to understanding the spatial and temporal variability of ecologically important events such as foraging.

Body density affects stroke patterns in Baikal seals

SUMMARY Buoyancy is one of the primary external forces acting on air-breathing divers and it can affect their swimming energetics. Because the body composition of marine mammals (i.e. the relative amounts of lower-density lipid and higher-density lean tissue) varies individually and seasonally, their buoyancy also fluctuates widely, and individuals would be expected to adjust their stroke patterns during dives accordingly. To test this prediction, we attached acceleration data loggers to four free-ranging Baikal seals Phoca sibirica in Lake Baikal and monitored flipper stroking activity as well as swimming speed, depth and inclination of the body axis (pitch). In addition to the logger, one seal (Individual 4) was equipped with a lead weight that was jettisoned after a predetermined time period so that we had a set of observations on the same individual with different body densities. These four data sets revealed the general diving patterns of Baikal seals and also provided direct insights into the influence of buoyancy on these patterns. Seals repeatedly performed dives of a mean duration of 7.0 min (max. 15.4 min), interrupted by a mean surface duration of 1.2 min. Dive depths were 66 m on average, but varied substantially, with a maximum depth of 324 m. The seals showed different stroke patterns among individuals; some seals stroked at lower rates during descent than ascent, while the others had higher stroke rates during descent than ascent. When the lead weight was detached from Individual 4, the seal increased its stroke rate in descent by shifting swimming mode from prolonged glides to more stroke-and-glide swimming, and decreased its stroke rate in ascent by shifting from continuous stroking to stroke-and-glide swimming. We conclude that seals adopt different stroke patterns according to their individual buoyancies. We also demonstrate that the terminal speed reached by Individual 4 during prolonged glide in descent depended on its total buoyancy and pitch, with higher speeds reached in the weighted condition and at steeper pitch. A simple physical model allowed us to estimate the body density of the seal from the speed and pitch (1027-1046 kg m-3, roughly corresponding to 32-41% lipid content, for the weighted condition; 1014-1022 kg m-3, 43-47% lipid content, for the unweighted condition).

Northern elephant seals adjust gliding and stroking patterns with changes in buoyancy: validation of at-sea metrics of body density

SUMMARY Many diving animals undergo substantial changes in their body density that are the result of changes in lipid content over their annual fasting cycle. Because the size of the lipid stores reflects an integration of foraging effort (energy expenditure) and foraging success (energy assimilation), measuring body density is a good way to track net resource acquisition of free-ranging animals while at sea. Here, we experimentally altered the body density and mass of three free-ranging elephant seals by remotely detaching weights and floats while monitoring their swimming speed, depth and three-axis acceleration with a high-resolution data logger. Cross-validation of three methods for estimating body density from hydrodynamic gliding performance of freely diving animals showed strong positive correlation with body density estimates obtained from isotope dilution body composition analysis over density ranges of 1015 to 1060 kg m–3. All three hydrodynamic models were within 1% of, but slightly greater than, body density measurements determined by isotope dilution, and therefore have the potential to track changes in body condition of a wide range of freely diving animals. Gliding during ascent and descent clearly increased and stroke rate decreased when buoyancy manipulations aided the direction of vertical transit, but ascent and descent speed were largely unchanged. The seals adjusted stroking intensity to maintain swim speed within a narrow range, despite changes in buoyancy. During active swimming, all three seals increased the amplitude of lateral body accelerations and two of the seals altered stroke frequency in response to the need to produce thrust required to overcome combined drag and buoyancy forces.

Scaling of swim speed in breath-hold divers.

1. Breath-hold divers are widely assumed to descend and ascend at the speed that minimizes energy expenditure per distance travelled (the cost of transport (COT)) to maximize foraging duration at depth. However, measuring COT with captive animals is difficult, and empirical support for this hypothesis is sparse. 2. We examined the scaling relationship of swim speed in free-ranging diving birds, mammals and turtles (37 species; mass range, 0·5-90,000 kg) with phylogenetically informed statistical methods and derived the theoretical prediction for the allometric exponent under the COT hypothesis by constructing a biomechanical model. 3. Swim speed significantly increased with mass, despite considerable variations around the scaling line. The allometric exponent (0·09) was statistically consistent with the theoretical prediction (0·05) of the COT hypothesis. 4. Our finding suggests a previously unrecognized advantage of size in divers: larger animals swim faster and thus could travel longer distance, search larger volume of water for prey and exploit a greater range of depths during a given dive duration. 5. Furthermore, as predicted from the model, endotherms (birds and mammals) swam faster than ectotherms (turtles) for their size, suggesting that metabolic power production limits swim speed. Among endotherms, birds swam faster than mammals, which cannot be explained by the model. Reynolds numbers of small birds (<2 kg) were close to the lower limit of turbulent flow (∼ 3 × 10(5) ), and they swam fast possibly to avoid the increased drag associated with flow transition.

Comparative analyses of animal-tracking data reveal ecological significance of endothermy in fishes

Significance Most fishes are cold-blooded, but tunas and some sharks (e.g., white sharks) maintain their exercising muscles warmer than ambient waters. This ability is a remarkable example of convergent evolution because bony and cartilaginous fishes diverged as long as 450 million years ago. What are the ecological benefits driving the evolution of warm muscles in fishes? Despite extensive discussion, no previous studies have tested a simple possibility that fishes with warm muscles may swim faster in nature. We demonstrate that fishes with warm muscles swim faster and perform larger-scale annual migrations than similar-sized cold-blooded fishes. Our results suggest that warm muscles enhance power output and, thus, cruising speeds, which may enable longer-distance migrations and potentially greater access to seasonally available resources. Despite long evolutionary separations, several sharks and tunas share the ability to maintain slow-twitch, aerobic red muscle (RM) warmer than ambient water. Proximate causes of RM endothermy are well understood, but ultimate causes are unclear. Two advantages often proposed are thermal niche expansion and elevated cruising speeds. The thermal niche hypothesis is generally supported, because fishes with RM endothermy often exhibit greater tolerance to broad temperature ranges. In contrast, whether fishes with RM endothermy cruise faster, and achieve any ecological benefits from doing so, remains unclear. Here, we compiled data recorded by modern animal-tracking tools for a variety of free-swimming marine vertebrates. Using phylogenetically informed allometry, we show that both cruising speeds and maximum annual migration ranges of fishes with RM endothermy are 2–3 times greater than fishes without it, and comparable to nonfish endotherms (i.e., penguins and marine mammals). The estimated cost of transport of fishes with RM endothermy is twice that of fishes without it. We suggest that the high energetic cost of RM endothermy in fishes is offset by the benefit of elevated cruising speeds, which not only increase prey encounter rates, but also enable larger-scale annual migrations and potentially greater access to seasonally available resources.

Sink fast and swim harder! Round-trip cost-of-transport for buoyant divers.

SUMMARY Efficient locomotion between prey resources at depth and oxygen at the surface is crucial for breath-hold divers to maximize time spent in the foraging layer, and thereby net energy intake rates. The body density of divers, which changes with body condition, determines the apparent weight (buoyancy) of divers, which may affect round-trip cost-of-transport (COT) between the surface and depth. We evaluated alternative predictions from external-work and actuator-disc theory of how non-neutral buoyancy affects round-trip COT to depth, and the minimum COT speed for steady-state vertical transit. Not surprisingly, the models predict that one-way COT decreases (increases) when buoyancy aids (hinders) one-way transit. At extreme deviations from neutral buoyancy, gliding at terminal velocity is the minimum COT strategy in the direction aided by buoyancy. In the transit direction hindered by buoyancy, the external-work model predicted that minimum COT speeds would not change at greater deviations from neutral buoyancy, but minimum COT speeds were predicted to increase under the actuator disc model. As previously documented for grey seals, we found that vertical transit rates of 36 elephant seals increased in both directions as body density deviated from neutral buoyancy, indicating that actuator disc theory may more closely predict the power requirements of divers affected by gravity than an external work model. For both models, minor deviations from neutral buoyancy did not affect minimum COT speed or round-trip COT itself. However, at body-density extremes, both models predict that savings in the aided direction do not fully offset the increased COT imposed by the greater thrusting required in the hindered direction.

From physiology to physics: are we recognizing the flexibility of biologging tools?

The remote measurement of data from free-ranging animals has been termed ‘biologging’ and in recent years this relatively small set of tools has been instrumental in addressing remarkably diverse questions – from ‘how will tuna respond to climate change?’ to ‘why are whales big?’. While a single biologging dataset can have the potential to test hypotheses spanning physiology, ecology, evolution and theoretical physics, explicit illustrations of this flexibility are scarce and this has arguably hindered the full realization of the power of biologging tools. Here we present a small set of examples from studies that have collected data on two parameters widespread in biologging research (depth and acceleration), but that have interpreted their data in the context of extremely diverse phenomena: from tests of biomechanical and diving-optimality models to identifications of feeding events, Lévy flight foraging strategies and expanding oxygen minimum zones. We use these examples to highlight the remarkable flexibility of biologging tools, and identify several mechanisms that may enhance the scope and dissemination of future biologging research programs.

Scaling of swim speed and stroke frequency in geometrically similar penguins: they swim optimally to minimize cost of transport

It has been predicted that geometrically similar animals would swim at the same speed with stroke frequency scaling with mass−1/3. In the present study, morphological and behavioural data obtained from free-ranging penguins (seven species) were compared. Morphological measurements support the geometrical similarity. However, cruising speeds of 1.8–2.3 m s−1 were significantly related to mass0.08 and stroke frequencies were proportional to mass−0.29. These scaling relationships do not agree with the previous predictions for geometrically similar animals. We propose a theoretical model, considering metabolic cost, work against mechanical forces (drag and buoyancy), pitch angle and dive depth. This new model predicts that: (i) the optimal swim speed, which minimizes the energy cost of transport, is proportional to (basal metabolic rate/drag)1/3 independent of buoyancy, pitch angle and dive depth; (ii) the optimal speed is related to mass0.05; and (iii) stroke frequency is proportional to mass−0.28. The observed scaling relationships of penguins support these predictions, which suggest that breath-hold divers swam optimally to minimize the cost of transport, including mechanical and metabolic energy during dive.

Functional Dorsoventral Symmetry in Relation to Lift- Based Swimming in the Ocean Sunfish Mola mola

The largest (up to 2 tons) and a globally distributed teleost—the ocean sunfish Mola mola—is commonly regarded as a planktonic fish because of its unusual shape including absence of caudal fin. This common view was recently questioned because the horizontal movements of the ocean sunfish tracked by acoustic telemetry were independent of ocean currents. However, direct information regarding their locomotor performance under natural conditions is still lacking. By using multi-sensor tags, we show that sunfish indeed swam continuously with frequent vertical movements at speeds of 0.4–0.7 m s–1, which is similar to the records of other large fishes such as salmons, marlins, and pelagic sharks. The acceleration data revealed that they stroked their dorsal and anal fins synchronously (dominant frequency, 0.3–0.6 Hz) to generate a lift-based thrust, as penguins do using two symmetrical flippers. Morphological studies of sunfish (mass, 2–959 kg) showed that the dorsal and anal fins had similar external (symmetrical shape and identical area) and internal (identical locomotory muscle mass) features; however, the muscle shape differed markedly. We conclude that ocean sunfish have functional dorsoventral symmetry with regards to the non-homologous dorsal and anal fins that act as a pair of vertical hydrofoils. Although sunfish lack a swimbladder, we found that they are neutrally buoyant independent of depth because of their subcutaneous gelatinous tissue that has low density and is incompressible. Efficient lift-based swimming in conjunction with neutral buoyancy enables sunfish to travel long distances both horizontally and vertically.