Tomoko Narazaki

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.

Sea turtles compensate deflection of heading at the sea surface during directional travel.

SUMMARY Air-breathing marine animals, including sea turtles, utilise two fundamentally different environments (i.e. sea surface and underwater) during migration. Many satellite telemetry studies have shown travel paths at relatively large spatio-temporal scales, discussing the orientation and navigation mechanisms that guide turtles. However, as travel paths obtained by satellite telemetry only reflect movements at the surface, little is known about movements and orientation ability underwater. In this study, to assess orientation ability both at the surface and underwater, fine-scale 3-D movements of free-ranging loggerhead turtles Caretta caretta were reconstructed by using multi-sensor data loggers. Video systems (‘Crittercam’) were also used to record the behaviour of the turtles and the visual information surrounding the turtles. During August and October in 2006 and 2007, eight turtles were released from Otsuchi Bay, Japan (39°20′30N, 141°56′00E), and a total of 118 h of 3-D movements were reconstructed. Turtles maintained highly straight-line courses (straightness index >0.95) during 41% of the total duration (i.e. ‘travelling periods’). During travelling periods, turtles swam continuously, maintaining unidirectional heading throughout dives whereas turtles changed heading remarkably at the surface. Despite highly directional movements during dives, travel direction tended to shift by the end of dives lasting 10 minutes or more. Such deflections seemed to be compensated during subsequent surfacing periods because there was a negative relationship between changes in travel direction arising during dives and subsequent surfacing periods. Therefore, remarkable changes in heading at the surface could be interpreted as direction-searching behaviour. Our results suggested that turtles undertaking directional travel were more dependent on directional information that was reliable at the surface.

Loggerhead Turtles (Caretta caretta) Use Vision to Forage on Gelatinous Prey in Mid-Water

Identifying characteristics of foraging activity is fundamental to understanding an animals’ lifestyle and foraging ecology. Despite its importance, monitoring the foraging activities of marine animals is difficult because direct observation is rarely possible. In this study, we use an animal-borne imaging system and three-dimensional data logger simultaneously to observe the foraging behaviour of large juvenile and adult sized loggerhead turtles (Caretta caretta) in their natural environment. Video recordings showed that the turtles foraged on gelatinous prey while swimming in mid-water (i.e., defined as epipelagic water column deeper than 1 m in this study). By linking video and 3D data, we found that mid-water foraging events share the common feature of a marked deceleration phase associated with the capture and handling of the sluggish prey. Analysis of high-resolution 3D movements during mid-water foraging events, including presumptive events extracted from 3D data using deceleration in swim speed as a proxy for foraging (detection rate = 0.67), showed that turtles swam straight toward prey in 171 events (i.e., turning point absent) but made a single turn toward the prey an average of 5.7±6.0 m before reaching the prey in 229 events (i.e., turning point present). Foraging events with a turning point tended to occur during the daytime, suggesting that turtles primarily used visual cues to locate prey. In addition, an incident of a turtle encountering a plastic bag while swimming in mid-water was recorded. The fact that the turtle’s movements while approaching the plastic bag were analogous to those of a true foraging event, having a turning point and deceleration phase, also support the use of vision in mid-water foraging. Our study shows that integrated video and high-resolution 3D data analysis provides unique opportunities to understand foraging behaviours in the context of the sensory ecology involved in prey location.

The ontogenetic scaling of bite force and head size in loggerhead sea turtles (Caretta caretta): implications for durophagy in neritic, benthic habitats

SUMMARY Ontogenetic studies of vertebrate feeding performance can help address questions relevant to foraging ecology. Feeding morphology and performance can either limit access to food resources or open up new trophic niches in both aquatic and terrestrial systems. Loggerhead sea turtles are long-lived vertebrates with complex life histories that are marked by an ontogenetic shift from an oceanic habitat to a coastal neritic habitat, and a transition from soft oceanic prey to hard, benthic prey. Although considered durophagous and strong biters, bite performance has not been measured in loggerheads, nor has the ontogeny of bite performance been characterized. In the present study, we collected measurements of bite force in loggerhead turtles from hatchlings to adults. When subadults reach the body size at which the ontogenetic shift occurs, their crushing capability is great enough for them to consume numerous species of hard benthic prey of small sizes. As loggerheads mature and bite performance increases, larger and harder benthic prey become accessible. Loggerhead bite performance eventually surpasses the crushing capability of other durophagous carnivores, thereby potentially reducing competition for hard benthic prey. The increasing bite performance and accompanying changes in morphology of the head and jaws are likely an effective mechanism for resource partitioning and decreasing trophic competition. Simultaneous measurements of body and head size and the use of non-linear reduced major axis regression show that bite force increases with significant positive allometry relative to body size (straight carapace length, straight carapace width and mass) and head size (head width, height and length). Simple correlation showed that all recorded morphometrics were good predictors of measured bite performance, but an AICc-based weighted regression showed that body size (straight carapace width followed by straight carapace length and mass, respectively) were more likely predictors of bite force than head size morphometrics (head width and head length).

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.

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.

The feeding habit of sea turtles influences their reaction to artificial marine debris.

Ingestion of artificial debris is considered as a significant stress for wildlife including sea turtles. To investigate how turtles react to artificial debris under natural conditions, we deployed animal-borne video cameras on loggerhead and green turtles in addition to feces and gut contents analyses from 2007 to 2015. Frequency of occurrences of artificial debris in feces and gut contents collected from loggerhead turtles were 35.7% (10/28) and 84.6% (11/13), respectively. Artificial debris appeared in all green turtles in feces (25/25) and gut contents (10/10), and green turtles ingested more debris (feces; 15.8 ± 33.4 g, gut; 39.8 ± 51.2 g) than loggerhead turtles (feces; 1.6 ± 3.7 g, gut; 9.7 ± 15.0 g). In the video records (60 and 52.5 hours from 10 loggerhead and 6 green turtles, respectively), turtles encountered 46 artificial debris and ingested 23 of them. The encounter-ingestion ratio of artificial debris in green turtles (61.8%) was significantly higher than that in loggerhead turtles (16.7%). Loggerhead turtles frequently fed on gelatinous prey (78/84), however, green turtles mainly fed marine algae (156/210), and partly consumed gelatinous prey (10/210). Turtles seemed to confuse solo drifting debris with their diet, and omnivorous green turtles were more attracted by artificial debris.

Energy expenditure of adult green turtles (Chelonia mydas) at their foraging grounds and during simulated oceanic migration

Measuring the energy requirements of animals under natural conditions and determining how acquired energy is allocated to specific activities is a central theme in ecophysiology. Turtle reproductive output is fundamentally linked with their energy balance so a detailed understanding of marine turtle energy requirements during the different phases of their life cycle at sea is essential for their conservation. We used the non-invasive accelerometry technique to investigate the activity patterns and energy expenditure (EE) of adult green turtles (Chelonia mydas) foraging year-round at a seagrass meadow in Mayotte (n = 13) and during simulated oceanic migration (displacement from the nesting beach) off Moheli (n = 1), in the south-western Indian Ocean. At the foraging site, turtles divided their days between foraging benthically on the shallow seagrass meadow during daylight hours and resting at greater depth on the inner side of the reef slope at night. Estimated oxygen consumption rates (sinline image) and daily energy expenditures (DEE) at the foraging site were low (sinline image during the day was 1·6 and 1·9 times the respective resting rate at night during the austral summer and winter, respectively), which is consistent with the requirement to build up substantial energy reserves at the foraging site, to sustain the energy-demanding breeding migration and reproduction. Dive duration (but not dive depth) at the foraging site shifted significantly with season (dive duration increased with declining water temperatures, Tw), while overall activity levels remained unchanged. In parallel with a significant seasonal decline in Tw (from 28·9 ± 0·1 °C to 25·3 ± 0·4 °C), there was a moderate (˜19%) but significant decline in DEE of turtles during the austral winter (901 ± 111 kJ day−1), when compared with the austral summer (1117 ± 66 kJ day−1). By contrast, the turtle moved continuously during simulated oceanic migration, conducting short/shallow dives in the day, which (predominately at night) were interspersed with longer and deeper ‘pelagic’ dives. Estimated oxygen consumption rates during a simulated migration (1·25 ± 0·16 mL O2 min−1 kg−0·83) were found to be significantly increased over the foraging condition, equal to ˜3 times the resting rate at night (0·42 ± 0·02 mL O2 min−1 kg−0·83), and daily energy expenditure amounted to 2327 ± 292 kJ day−1, underlining the tremendous energetic effort associated with breeding migration. Our study indicates that the accelerometry technique provides a new and promising opportunity to study marine turtle energy relations in great detail and under natural conditions.

High resting metabolic rates with low thermal dependence induce active dives in overwintering Pacific juvenile loggerhead turtles

ABSTRACT The metabolic rate and activity of sea turtles generally decreases with decreasing seasonal ambient temperature. Juvenile loggerhead turtles in the Mediterranean Sea made prolonged inactive dives (>400 min), indicating a state of dormancy during the cold winter period. However, seasonal differences in dive duration were not detected in juvenile loggerheads in the western North Pacific, even though the ambient water temperature changed by more than 10°C. Thus, metabolic states might differ among populations, explaining differences in the diving behaviour of juveniles during winter. Here, we tested the hypothesis that the active overwintering behaviour of juvenile loggerheads in the western North Pacific is driven by a high resting metabolic rate (RMR) with low thermal dependence. The RMR of juveniles in the western North Pacific (N=13) was 1.4–5.7 times higher (Q10=1.8) than that of juveniles in the Mediterranean Sea (Q10=5.4). To validate the high RMR values in the western North Pacific, the difference between core body temperature and ambient water temperature (ΔTb) was estimated from measured RMR and was compared with measured ΔTb. The measured and estimated ΔTb matched each other. In addition, most of the dives conducted by the turtles in the western North Pacific were within the calculated aerobic dive limit (cADL) expected from the measured metabolic rate. Our results indicate that high RMR with low thermal dependence induces active diving during the overwintering periods of juvenile loggerheads in the western North Pacific, supporting the suggestion that metabolic states differ among populations. Summary: Active dives of juvenile loggerhead turtles in the western North Pacific during the winter period are driven by a high resting metabolic rate.

Body density of humpback whales (Megaptera novaengliae) in feeding aggregations estimated from hydrodynamic gliding performance

Many baleen whales undertake annual fasting and feeding cycles, resulting in substantial changes in their body condition, an important factor affecting fitness. As a measure of lipid-store body condition, tissue density of a few deep diving marine mammals has been estimated using a hydrodynamic glide model of drag and buoyancy forces. Here, we applied the method to shallow-diving humpback whales (Megaptera novaeangliae) in North Atlantic and Antarctic feeding aggregations. High-resolution 3-axis acceleration, depth and speed data were collected from 24 whales. Measured values of acceleration during 5 s glides were fitted to a hydrodynamic glide model to estimate unknown parameters (tissue density, drag term and diving gas volume) in a Bayesian framework. Estimated species-average tissue density (1031.6 ± 2.1 kg m-3, ±95% credible interval) indicates that humpback whale tissue is typically negatively buoyant although there was a large inter-individual variation ranging from 1025.2 to 1043.1 kg m-3. The precision of the individual estimates was substantially finer than the variation across different individual whales, demonstrating a progressive decrease in tissue density throughout the feeding season and comparably high lipid-store in pregnant females. The drag term (CDAm-1) was estimated to be relatively high, indicating a large effect of lift-related induced drag for humpback whales. Our results show that tissue density of shallow diving baleen whales can be estimated using the hydrodynamic gliding model, although cross-validation with other techniques is an essential next step. This method for estimating body condition is likely to be broadly applicable across a range of aquatic animals and environments.