Stereotypical diel movement and dive pattern of male sperm whales in a submarine canyon revealed by land-based and bio-logging surveys

Male sperm whales are under pressure to grow larger in order to increase their mating opportunities, which could lead them to more efficiently forage in high latitude feeding grounds. Movement patterns of male sperm whales in Nemuro Strait, Japan, were investigated horizontally and vertically using land-based observation and bio-logging methods to determine how they facilitate foraging in the narrow submarine canyon. Eleven tagged whales showed the distinct diel pattern for dive depth, as it was deeper at night than during the day. Five-year data of land-based observation and GPS data from six tagged whales revealed the tendency of whales to change the north-south direction of their horizontal movement every 4–6 h, and this movement direction was not related to the direction of the current. Their periodic heading change is thought to be a consequence of the whales making two round trips each day within the foraging area, one during the day to shallow layers and one during the night to deep layers. These tactics may help the whales to search for prey in this narrow submarine canyon efficiently. Most whales changed their direction of movement in a similar manner, which is probably due to the whales’ tendency to stay close enough to each other to obtain information about the prey environment using the echolocation clicks of other whales. The results emphasize the ability of male sperm whales to adapt their foraging tactics according to the prey environment of their habitat and intense pressure to grow faster may be the drive for this ability. The importance of social cohesion among foraging male sperm whales was also suggested

Using an omnidirectional video logger to observe the underwater life of marine animals : humpback whale resting behaviour

This study was supported by the Bio-Logging Science of the University of Tokyo (UTBLS) program, the Japan Society for the Promotion of Science Postdoctoral Fellowships Research Abroad, the Japan Society for the Promotion of Science (grant number 17H00776 K.S), the Japan Society for the Promotion of Science Bilateral Open Partnership Joint Research Program, the Mitsui and Co. Environment Fund, and The Research Grant against Global Warming of the Ichimura Foundation for New Technology.Animal-borne video loggers are powerful tools for investigating animal behaviour because they directly record immediate and extended peripheral animal activities; however, typical video loggers capture only a limited area on one side of an animal being monitored owing to their narrow field of view. Here, we investigated the resting behaviour of humpback whales using an animal-borne omnidirectional video camera combined with a behavioural data logger. In the video logger footage, two non-tagged resting individuals, which did not spread their flippers or move their flukes, were observed above a tagged animal, representing an apparent bout of group resting. During the video logger recording, the swim speed was relatively slow (0.75 m s ), and the tagged animal made only a few strokes of very low amplitude during drift diving. We report the drift dives as resting behaviour specific to baleen whales as same as seals, sperm whales and loggerhead turtles. Overall, our study shows that an omnidirectional video logger is a valuable tool for interpreting animal ecology with improved accuracy owing to its ability to record a wide field of view.Publisher PDFPeer reviewe

Persistence of skin marks on killer whales (Orcinus orca) caused by the parasitic sea lamprey (Petromyzon marinus) in Iceland

Lampreys have long been thought to be a cetacean ectoparasite, due to the observation of round marks on the skin of whales caught during whaling operations. Pike (1951), Nemoto (1955), and van Utrecht (1959) compared such marks on the skin of various cetacean species caught in the Pacific and Atlantic Oceans with the dentition of lampreys and concluded that most round marks had been caused by this parasite. However, lampreys were never collected from captured whales and, due to the lack of direct evidence, some discussion emerged as to the origin of these wounds. Jones (1971) later argued that crescent-shaped marks previously attributed to lampreys were in fact caused by cookie-cutter sharks (Isistius brasiliensis). However, he agreed that other round marks were undoubtedly caused by lampreys. Recently, photographs of sea lampreys (Petromyzon marinus) attached to northern right whales, Eubalaena glacialis (Nichols and Hamilton 2004), and minke whales, Balaenoptera acutorostrata (Nichols and Tscherter 2011), in the western North Atlantic conclusively showed that lampreys do associate with those species. Similar evidence for other cetaceans is still lacking

Non-lunge feeding behaviour of humpback whales associated with fishing boats in Norway

Funding: Ichimura Foundation of New Technology Japan Society for the Promotion of Science Postdoctoral Fellowships Research Abroad Mitsui and Co. Environment Fund.Top marine predators, such as odontocetes, pinnipeds, and seabirds, are known to forage around fishing boats as fishermen aggregate and/or discard their prey. Recently, incidents of humpback whales interacting with fishing boats have been reported. However, whether humpback whales utilise discard fish as a food source and how they forage around fishing boats is unknown. This study reports, for the first time, the foraging behaviour of a humpback whale around fishing boats. Three whales were tagged using a suction-cup tag containing a video camera, and a behavioural data logger in the coastal area of Tromsø, Norway. Video data from one tagged whale showed that the whale remained in close vicinity of fishing boats for 43 min, and revealed the presence of large numbers of dead fish, fish-eating killer whales, fishing boats, and fishing gear. In waters with large numbers of dead fish, the whale raised its upper jaw, a motion associated with engulfing discard fish from fishing boats, and this feeding behaviour differed markedly from lunge-feeding observed in two other whales in the same area. This behaviour was defined as “pick-up feeding”. No lunge feeding was seen on the data logger when the whale foraged around fishing boats. This study highlights a novel humpback whale foraging strategy: low energy gain from scattered prey but also low energy costs as high-energy lunge feeding is not required.Publisher PDFPeer reviewe

Breathing patterns indicate cost of exercise during diving and response to experimental sound exposures in long-finned pilot whales

This work was funded by NL Ministry of Defence, NOR Ministry of Defence, United States Office of Naval Research (N00014-08-1-0984, N00014-10-1-0355, and N00014-14-1-0390), and FR Ministry of Defence (DGA) (public market n°15860052). KA was supported by the Japan Society for the Promotion of Science Bilateral Open Partnership Joint Research Program.Air-breathing marine predators that target sub-surface prey have to balance the energetic benefit of foraging against the time, energetic and physiological costs of diving. Here we use on-animal data loggers to assess whether such trade-offs can be revealed by the breathing rates (BR) and timing of breaths in long-finned pilot whales (Globicephela melas). We used the period immediately following foraging dives in particular, for which respiratory behavior can be expected to be optimized for gas exchange. Breath times and fluke strokes were detected using onboard sensors (pressure, 3-axis acceleration) attached to animals using suction cups. The number and timing of breaths were quantified in non-linear mixed models that incorporated serial correlation and individual as a random effect. We found that pilot whales increased their BR in the 5-10min period prior to, and immediately following, dives that exceeded 31m depth. While pre-dive BRs did not vary with dive duration, the initial post-dive BR was linearly correlated with duration of >2 min dives, with BR then declining exponentially. Apparent net diving costs were 1.7 (SE 0.2) breaths per min of diving (post-dive number of breaths, above pre-dive breathing rate unrelated to dive recovery). Every fluke stroke was estimated to cost 0.086 breaths, which amounted to 80-90% average contribution of locomotion to the net diving costs. After accounting for fluke stroke rate, individuals in the small body size class took a greater number of breaths per diving minute. Individuals reduced their breathing rate (from the rate expected by diving behavior) by 13-16% during playbacks of killer whale sounds and their first exposure to 1-2kHz naval sonar, indicating similar responses to interspecific competitor/predator and anthropogenic sounds. Although we cannot rule out individuals increasing their per-breath O2 uptake to match metabolic demand, our results suggest that behavioral responses to experimental sound exposures were not associated with increased metabolic rates in a stress response, but metabolic rates instead appear to decrease. Our results support the hypothesis that maximal performance leads to predictable (optimized) breathing patterns, which combined with further physiological measurements could improve proxies of field metabolic rates and per-stroke energy costs from animal-borne behavior data.Publisher PDFPeer reviewe

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

The US Office of Naval Research and Strategic Environmental Research and Development Program (SERDP) supported the fieldwork as a part of the 3S study collaboration. This study was also supported by the program Bio-Logging Science of the University of Tokyo (UTBLS).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.Publisher PDFPeer reviewe

Leave or stay? Video-logger revealed foraging efficiency of humpback whales under temporal change in prey density

Publisher's version (útgefin grein)Central place foraging theory (CPF) has been used to predict the optimal patch residence time for air-breathing marine predators in response to patch quality. Humpback whales (Megaptera novaeangliae) forage on densely aggregated prey, which may induce drastic change in prey density in a single feeding event. Thus, the decision whether to leave or stay after each feeding event in a single dive in response to this drastic change, should have a significant effect on prey exploitation efficiency. However, whether humpback whales show adaptive behavior in response to the diminishing prey density in a single dive has been technically difficult to test. Here, we studied the foraging behavior of humpback whales in response to change in prey density in a single dive and calculated the efficiency of each foraging dive using a model based on CPF approach. Using animal-borne accelerometers and video loggers attached to whales, foraging behavior and change in relative prey density in front of the whales were successfully quantified. Results showed diminishing rate of energy intake in consecutive feeding events, and humpback whales efficiently fed by bringing the rate of energy intake close to maximum in a single dive cycle. This video-based method also enabled us to detect the presence of other animals around the tagged whales, showing an interesting trend in behavioral changes where feeding duration was shorter when other animals were present. Our results have introduced a new potential to quantitatively investigate the effect of other animals on free-ranging top predators in the context of optimal foraging theory.Peer Reviewe

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

This study was funded by Strategic Environmental Research and Development Program (https://www.serdp-estcp.org; grant number RC-2337). In addition, the study was partly supported by Core Research for Evolutional Science and Technology by Japan Science and Technology Agency (http://www.jst.go.jp/kisoken/crest/en/index.html, grant number JPMJCR1685) and Bilateral Open Partnership Joint Research Projects by Japan Society for the Promotion of Science (http://www.jsps.go.jp/english/e-bilat/index.html; no specific grant number).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.Publisher PDFPeer reviewe

The New Era of Physio-Logging and Their Grand Challenges.

International audienc

doi:10.1098/rspb.2006.0005

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 animalborne accelerometers. Dominant stroke cycle frequencies of swimming specialist seabirds and marine mammals were proportional to mass K0.29 (R 2 Z0.99, nZ17 groups), while propulsive swimming speeds of 1-2 m s K1 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. Keywords: accelerometer; power spectral density; dive; free-ranging; scaling; optimal INTRODUCTION In a Friday Evening Discourse given at the Royal Institution in 1949 Direct observations have often been used to record movements of flying animals MATERIAL AND METHODS We compared the stroke frequencies and swimming speeds of a range of animals in relation to their body sizes. Owing to morphological differences among species, body mass was used as an index of body size. Morphological measurements were used to estimate mass for adult Weddell seals , leatherback turtles and sperm whales Field experiments using accelerometers were conducted from tropical to Antarctic regions. Detailed protocols of the field experiments were already published for the sperm whale (French Guiana, South America, May 2001. Study protocols followed those of the above-mentioned published studies. We used acceleration data loggers (D2GT and PD2GT, Little Leonardo Ltd, Tokyo; Dtag, the Woods Hole Oceanographic Institution; We could detect the duration of each stroke cycle from the time-series data, but our goal was to determine the dominant stroke cycle frequency for each animal. The periodic properties of the acceleration signal allowed us to apply a Fourier Transform to determine the dominant frequency. Power spectral density (PSD) was calculated from the entire acceleration dataset of each animal, or a subsample during identified foraging or migration behaviour to determine the dominant stroke cycle frequency using a Fast Fourier Transformation with a computer program package, IGOR PRO (WaveMetric, Inc., Lake Oswego, OR, USA). For the sperm whale, the bottom phase of the dive was not used as it is typified by body rotations, which can occur at similar rates to the fluking action. Stroke frequency and body size of animals K. Sato et al. 473 Proc. R. Soc. B (2007) 3. RESULTS Seals move their rear flippers side-to-side and these movements are detected as fluctuations in lateral acceleration along the transverse axis of the body (Mirounga angustirostris; with R 2 Z0.99 (nZ17, p!0.0001). The 95% confidence interval for the exponent was from K0.28 to K0.30. In contrast, the mean propulsive swim speed (U ) among these species was independent of body mass in the log-log analysis (UZ1.88 m K0.05 , R 2 Z0.18, nZ17, pZ0.09). Sperm whales of more than 30 tons, 300 kg seals and 0.5 kg seabirds all swam at mean swim speeds around 1-2 m s K1 during transit between the sea surface and the foraging depths (table 1). DISCUSSION According to experimental measurements based on respirometers in water tunnels and the doubly labelled water technique, the optimum swim speed was proportional to mass 0.27 Stroke frequency and body size of animals K. Sato et al. 475 Proc. R. Soc. B K1 ). Why these free-ranging animals did not follow the theoretical and experimental predictions for optimal swimming speed is a question we cannot answer now. The constructal model The isometric model proposed by According to the present study, swim speed (U ) was independent of body size, therefore the frequency is expected to be proportional to area divided by mass (S/m), which is expected to be proportional to the length K1 or mass K1/3 . Results of the present study were obtained from morphologically diverse animals. Nonetheless, f is inversely proportional to m K0.29 , close to the predicted value of mass K1/3 , implying that diving specialists among seabirds and marine mammals have evolved similar proportions of propulsive muscles and muscle contraction rates during cruising travel. The scaling relationship was very strong among swimming specialists during contexts when they were predicted to swim efficiently. Moreover, interesting deviations from the regression line (see Japanese flounders Paralichthys olivaceus had lower stroke frequencies than other swimming specialists (open pink circle i