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1.
iScience ; 24(4): 102221, 2021 Apr 23.
Article in English | MEDLINE | ID: mdl-33997664

ABSTRACT

Advances in biologging technology have enabled 3D dead-reckoning reconstruction of marine animal movements at spatiotemporal scales of meters and seconds. Examining high-resolution 3D movements of sharks (Galeocerdo cuvier, N = 4; Rhincodon typus, N = 1), sea turtles (Chelonia mydas, N = 3), penguins (Aptenodytes patagonicus, N = 6), and marine mammals (Arctocephalus gazella, N = 4; Ziphius cavirostris, N = 1), we report the discovery of circling events where animals consecutively circled more than twice at relatively constant angular speeds. Similar circling behaviors were observed across a wide variety of marine megafauna, suggesting these behaviors might serve several similar purposes across taxa including foraging, social interactions, and navigation.

2.
J Exp Biol ; 224(Pt 4)2021 02 16.
Article in English | MEDLINE | ID: mdl-33436369

ABSTRACT

Animals with high resting metabolic rates and low drag coefficients typically have fast optimal swim speeds in order to minimise energy costs per unit travel distance. The cruising swim speeds of sea turtles (0.5-0.6 m s-1) are slower than those of seabirds and marine mammals (1-2 m s-1). This study measured the resting metabolic rates and drag coefficients of sea turtles to answer two questions: (1) do turtles swim at the optimal swim speed?; and (2) what factors control the optimal swim speed of turtles? The resting metabolic rates of 13 loggerhead and 12 green turtles were measured; then, the cruising swim speeds of 15 loggerhead and 9 green turtles were measured and their drag coefficients were estimated under natural conditions. The measured cruising swim speeds (0.27-0.50 m s-1) agreed with predicted optimal swim speeds (0.19-0.32 m s-1). The resting metabolic rates of turtles were approximately one-twentieth those of penguins, and the products of the drag coefficient and frontal area of turtles were 8.6 times higher than those of penguins. Therefore, our results suggest that both low resting metabolic rate and high drag coefficient of turtles determine their slow cruising speed.


Subject(s)
Spheniscidae , Turtles , Animals , Basal Metabolism , Energy Metabolism , Swimming
3.
Proc Biol Sci ; 288(1943): 20202307, 2021 01 27.
Article in English | MEDLINE | ID: mdl-33499785

ABSTRACT

Monitoring the body condition of free-ranging marine mammals at different life-history stages is essential to understand their ecology as they must accumulate sufficient energy reserves for survival and reproduction. However, assessing body condition in free-ranging marine mammals is challenging. We cross-validated two independent approaches to estimate the body condition of humpback whales (Megaptera novaeangliae) at two feeding grounds in Canada and Norway: animal-borne tags (n = 59) and aerial photogrammetry (n = 55). Whales that had a large length-standardized projected area in overhead images (i.e. whales looked fatter) had lower estimated tissue body density (TBD) (greater lipid stores) from tag data. Linking both measurements in a Bayesian hierarchical model to estimate the true underlying (hidden) tissue body density (uTBD), we found uTBD was lower (-3.5 kg m-3) in pregnant females compared to adult males and resting females, while in lactating females it was higher (+6.0 kg m-3). Whales were more negatively buoyant (+5.0 kg m-3) in Norway than Canada during the early feeding season, possibly owing to a longer migration from breeding areas. While uTBD decreased over the feeding season across life-history traits, whale tissues remained negatively buoyant (1035.3 ± 3.8 kg m-3) in the late feeding season. This study adds confidence to the effectiveness of these independent methods to estimate the body condition of free-ranging whales.


Subject(s)
Humpback Whale , Animals , Bayes Theorem , Canada , Female , Lactation , Lipids , Male , Norway , Photogrammetry , Pregnancy
4.
Proc Biol Sci ; 286(1899): 20182592, 2019 03 27.
Article in English | MEDLINE | ID: mdl-30890101

ABSTRACT

Impact assessments for sonar operations typically use received sound levels to predict behavioural disturbance in marine mammals. However, there are indications that cetaceans may learn to associate exposures from distant sound sources with lower perceived risk. To investigate the roles of source distance and received level in an area without frequent sonar activity, we conducted multi-scale controlled exposure experiments ( n = 3) with 12 northern bottlenose whales near Jan Mayen, Norway. Animals were tagged with high-resolution archival tags ( n = 1 per experiment) or medium-resolution satellite tags ( n = 9 in total) and subsequently exposed to sonar. We also deployed bottom-moored recorders to acoustically monitor for whales in the exposed area. Tagged whales initiated avoidance of the sound source over a wide range of distances (0.8-28 km), with responses characteristic of beaked whales. Both onset and intensity of response were better predicted by received sound pressure level (SPL) than by source distance. Avoidance threshold SPLs estimated for each whale ranged from 117-126 dB re 1 µPa, comparable to those of other tagged beaked whales. In this pristine underwater acoustic environment, we found no indication that the source distances tested in our experiments modulated the behavioural effects of sonar, as has been suggested for locations where whales are frequently exposed to sonar.


Subject(s)
Noise/adverse effects , Swimming , Whales/physiology , Acoustic Stimulation , Animals , Arctic Regions , Norway , Oceans and Seas
5.
PLoS One ; 13(7): e0200287, 2018.
Article in English | MEDLINE | ID: mdl-30001369

ABSTRACT

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.


Subject(s)
Body Composition , Humpback Whale/anatomy & histology , Animals , Bayes Theorem , Body Composition/physiology , Feeding Behavior , Female , Humpback Whale/physiology , Hydrodynamics , Male , Models, Biological , Swimming/physiology
6.
J Exp Biol ; 221(Pt 13)2018 07 09.
Article in English | MEDLINE | ID: mdl-29748215

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.


Subject(s)
Basal Metabolism/physiology , Diving/physiology , Temperature , Turtles/physiology , Animals , Japan , Pacific Ocean , Seasons
7.
J Exp Biol ; 220(Pt 20): 3802-3811, 2017 10 15.
Article in English | MEDLINE | ID: mdl-29046419

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.


Subject(s)
Diving , Energy Metabolism , Whales, Pilot/physiology , Animals , Biomechanical Phenomena , Female , Male , Swimming
9.
J Exp Biol ; 219(Pt 16): 2458-68, 2016 08 15.
Article in English | MEDLINE | ID: mdl-27296044

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.


Subject(s)
Body Composition/physiology , Diving/physiology , Gases/metabolism , Whales/physiology , Acceleration , Animals , Databases as Topic , Models, Biological
10.
Sci Rep ; 6: 28015, 2016 06 16.
Article in English | MEDLINE | ID: mdl-27305858

ABSTRACT

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.


Subject(s)
Feces/chemistry , Feeding Behavior/physiology , Feeding Behavior/psychology , Turtles/physiology , Waste Products , Water Pollutants , Animals , Eating
11.
PLoS One ; 8(6): e66043, 2013.
Article in English | MEDLINE | ID: mdl-23776603

ABSTRACT

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.


Subject(s)
Imaging, Three-Dimensional/methods , Predatory Behavior/physiology , Remote Sensing Technology/methods , Turtles/physiology , Vision, Ocular/physiology , Animals , Biomechanical Phenomena , Japan , Video Recording/methods
12.
J Exp Biol ; 215(Pt 23): 4166-74, 2012 Dec 01.
Article in English | MEDLINE | ID: mdl-22899532

ABSTRACT

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).


Subject(s)
Feeding Behavior , Head/anatomy & histology , Turtles/anatomy & histology , Turtles/physiology , Animals , Diet , Environment , Head/growth & development , Turtles/growth & development
13.
J Anim Ecol ; 80(1): 57-68, 2011 Jan.
Article in English | MEDLINE | ID: mdl-20946384

ABSTRACT

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.


Subject(s)
Birds/physiology , Diving/physiology , Mammals/physiology , Swimming/physiology , Turtles/physiology , Animals , Basal Metabolism , Birds/genetics , Body Size , Body Temperature Regulation , Humans , Mammals/genetics , Phylogeny , Turtles/genetics
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