Kagari Aoki

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.

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.

Neutral buoyancy is optimal to minimize the cost of transport in horizontally swimming seals

Flying and terrestrial animals should spend energy to move while supporting their weight against gravity. On the other hand, supported by buoyancy, aquatic animals can minimize the energy cost for supporting their body weight and neutral buoyancy has been considered advantageous for aquatic animals. However, some studies suggested that aquatic animals might use non-neutral buoyancy for gliding and thereby save energy cost for locomotion. We manipulated the body density of seals using detachable weights and floats, and compared stroke efforts of horizontally swimming seals under natural conditions using animal-borne recorders. The results indicated that seals had smaller stroke efforts to swim a given speed when they were closer to neutral buoyancy. We conclude that neutral buoyancy is likely the best body density to minimize the cost of transport in horizontal swimming by seals.

The social context of individual foraging behaviour in long-finned pilot whales (Globicephala melas)

Long-finned pilot whales (Globicephala melas) are highly social cetaceans that live in matrilineal groups and acquire their prey during deep foraging dives. We tagged individual pilot whales to record their diving behaviour. To describe the social context of this individual behaviour, the tag data were matched with surface observations at the group level using a novel protocol. The protocol comprised two key components: a dynamic definition of the group centred around the tagged individual, and a set of behavioural parameters quantifying visually observable characteristics of the group. Our results revealed that the diving behaviour of tagged individuals was associated with distinct group-level behaviour at the water’s surface. During foraging, groups broke up into smaller and more widely spaced units with a higher degree of milling behaviour. These data formed the basis for a classification model, using random forest decision trees, which accurately distinguished between bouts of shallow diving and bouts of deep foraging dives based on group behaviour observed at the surface. The results also indicated that members of a group to a large degree synchronised the timing of their foraging periods. This was confirmed by pairs of tagged individuals that nearly always synchronized their diving bouts. Hence, our study illustrates that integration of individual-level and group-level observations can shed new light on the social context of the individual foraging behaviour of animals living in groups.

Body contact and synchronous diving in long-finned pilot whales

Synchronous behavior, as a form of social interaction, has been widely reported for odontocete cetaceans observed at the sea surface. However, few studies have quantified synchronous behavior underwater. Using data from an animal-borne data recorder and camera, we described how a pair of deep-diving odontocetes, long-finned pilot whales, coordinated diving behavior. Diving data during overlapping periods of 3.7 h were obtained from two whales within a stable trio. The tagged whales made highly synchronous movements, and their dive durations differed only slightly (3±3 s). The pair of whales maintained a constant and narrow vertical separation (ca. 3 m) throughout synchronous dives. The overall fluking rate for the same travel speed during synchronous dives was virtually the same as that during asynchronous dives, suggesting that synchronous behavior did not affect locomotion effort. In addition, a possible affiliative behavior was recorded by the animal-borne camera: another individual appeared in 8% of the frames, both with and without body contact to the tagged whale. The primary type of body contact was flipper-to-body. Our study, the first on underwater synchronous behavior and body contact of pilot whales, highlights the utility of using animal-borne devices for enabling new insights into social interactions.

Measurement of swimming speed in sperm whales

Cetaceans spend their entire life in the water. Hence these animals represent important models for studying adaptations for aquatic environment. Although many scientists have been interested in how fast they can swim, accurate swimming speed measurements of free-ranging cetaceans are rare because it is difficult to observe them continuously. In particular, little is known about routine swimming speed of deep diver, such as sperm whales. To measure swimming speed of the sperm whales, we attached two-type suction-cup-attached tags including a data logger to sperm whales. One type was similar to that employed in several other studies (Type A). The other type was modified by us to get more precious velocity data (Type B). We attached the two-type tag to a total of 11 sperm whales (8 Type A and 3 Type B) and, obtained accurate swimming speed with 8 whales of them (5 Type A and 3 Type B). A total of 136 hours of accurate swimming speed data including 137 dives was obtained. Average velocity during the dive was 1.77 plusmn 0.39 m s-1 (n =137). Maximum velocity of each whale was 4.2-9.6 m s-1 (n = 8). In addition, we found the oscillations caused by the tail beat in the time-series velocity data, which was obtained by modified suction-cup-attached tags (Type B). The modified tags provide us routine and maximum swimming speed of the whales as well as the information of the tail beat.

Body density and diving gas volume of the northern bottlenose whale (Hyperoodon ampullatus)

ABSTRACT Diving lung volume and tissue density, reflecting lipid store volume, are important physiological parameters that have only been estimated for a few breath-hold diving species. We fitted 12 northern bottlenose whales with data loggers that recorded depth, 3-axis acceleration and speed either with a fly-wheel or from change of depth corrected by pitch angle. We fitted measured values of the change in speed during 5 s descent and ascent glides to a hydrodynamic model of drag and buoyancy forces using a Bayesian estimation framework. The resulting estimate of diving gas volume was 27.4±4.2 (95% credible interval, CI) ml kg−1, closely matching the measured lung capacity of the species. Dive-by-dive variation in gas volume did not correlate with dive depth or duration. Estimated body densities of individuals ranged from 1028.4 to 1033.9 kg m−3 at the sea surface, indicating overall negative tissue buoyancy of this species in seawater. Body density estimates were highly precise with ±95% CI ranging from 0.1 to 0.4 kg m−3, which would equate to a precision of <0.5% of lipid content based upon extrapolation from the elephant seal. Six whales tagged near Jan Mayen (Norway, 71°N) had lower body density and were closer to neutral buoyancy than six whales tagged in the Gully (Nova Scotia, Canada, 44°N), a difference that was consistent with the amount of gliding observed during ascent versus descent phases in these animals. Implementation of this approach using longer-duration tags could be used to track longitudinal changes in body density and lipid store body condition of free-ranging cetaceans. Summary: Body density and diving gas volume, two important but poorly understood physiological characteristics of beaked whales, are revealed through analysis of hydrodynamic performance during glides.

Swim Speed and Acceleration Measurements of Short-Finned Pilot Whales (Globicephala macrorhynchus) in Hawai'i

Cascadia Research Collective, 218 1/2 W. 4th Avenue, Olympia, WA 98501, USAOver the last few years, studies of top predators inmarine ecosystems have benefited from the use of bio-logging systems (Naito 2004; Rutz and Hays 2009). Forexample, researchers use these techniques to study ani-mal foraging tactics and diving physiology by analyzingacceleration (body angle and stroke), and parameterssuch as swim depth and swim speeds (e.g., Sato et al.2003, 2007; Sakamoto et al. 2009).Short-finned pilot whale (Globicephala macrorhynchus),a top predator, is found worldwide in tropical and warmtemperate waters. Mature males are from 4.5 to 7 m inlength and mature females are from 3.5 to 5 m in length(Bernard and Reilly 1999). Previous studies suggestedthey are foraging during deep dives which cannot beobserved visually. Their primary prey are squid and inHawai‘i they are known to make deep dives (600–800 m)during the day, but also spend considerable periods oftime shallow diving or surface resting during the day(Baird et al. 2003). Amano and Baird (1998) recordeddeep dives over 100 m off Japan. Soto et al. (2008)recorded sound, depth, and orientation from triaxialaccelerometers and magnetometers, and suggested preychasing behavior by analyzing vertical speed and soundemission during deep dives. For a better understandingof foraging tactics and diving physiology of this species,for example studying prey pursuit in a horizontal direc-tion, stroking patterns and body angle, or assessingbehavior by acceleration, we need to record accelerationand swim speed simultaneously. However, swim speedfor short-finned pilot whales has not yet been recorded.We used remotely deployed suction-cup tags formeasuring swim speed and acceleration of short-finnedpilot whales. The understanding of toothed whale be-havior has been advanced by using suction-cup attacheddata loggers (for a review see Hooker and Baird 2001).There are several types of suction-cup attached tag: oneattached with multiple suction-cups that fixed a datalogger in place (e.g., Soto et al. 2008), which with asingle suction-cup connected to a data logger with aflexible plastic tube (Baird et al. 2005), and one with asingle suction-cup that fixed a data logger in place.With removely-deployed tags, it is difficult to set thetag parallel to the water flow. Therefore it would behard to record swim speed using a propeller with amultiple suction-cup tag. A tag using a flexible plastictube cannot record acceleration caused by the animalprecisely because it is not fixed on the animal’s body.A tag fixed on a suction-cup has been demonstratedto record swim speed and acceleration simultaneouslyin previous studies (finless porpoises, Neophocaenaphocaenoides, Akamatsu et al. 2005; sperm whales,Physeter macrocephalus, Aoki 2008). The purpose ofour work was to determine whether this type of suction-cup tag is appropriate for studying swim speed andacceleration in short-finned pilot whales, and whetherit was possible to determine behavior types based onthe data collected.

High diving metabolic rate indicated by high-speed transit to depth in negatively buoyant long-finned pilot whales

ABSTRACT To maximize foraging duration at depth, diving mammals are expected to use the lowest cost optimal speed during descent and ascent transit and to minimize the cost of transport by achieving neutral buoyancy. Here, we outfitted 18 deep-diving long-finned pilot whales with multi-sensor data loggers and found indications that their diving strategy is associated with higher costs than those of other deep-diving toothed whales. Theoretical models predict that optimal speed is proportional to (basal metabolic rate/drag)1/3 and therefore to body mass0.05. The transit speed of tagged animals (2.7±0.3 m s−1) was substantially higher than the optimal speed predicted from body mass (1.4–1.7 m s−1). According to the theoretical models, this choice of high transit speed, given a similar drag coefficient (median, 0.0035) to that in other cetaceans, indicated greater basal metabolic costs during diving than for other cetaceans. This could explain the comparatively short duration (8.9±1.5 min) of their deep dives (maximum depth, 444±85 m). Hydrodynamic gliding models indicated negative buoyancy of tissue body density (1038.8±1.6 kg m–3, ±95% credible interval, CI) and similar diving gas volume (34.6±0.6 ml kg−1, ±95% CI) to those in other deep-diving toothed whales. High diving metabolic rate and costly negative buoyancy imply a ‘spend more, gain more’ strategy of long-finned pilot whales, differing from that in other deep-diving toothed whales, which limits the costs of locomotion during foraging. We also found that net buoyancy affected the optimal speed: high transit speeds gradually decreased during ascent as the whales approached neutral buoyancy owing to gas expansion. Highlighted Article: High diving metabolic rate indicated by high-speed transit to depth and negative buoyancy of long-finned pilot whales implies a costly diving strategy compared with that in other deep-diving toothed whales.