Locomotion in diving elephant seals: physical and physiological constraints

To better understand how elephant seals (Mirounga angustirostris) use negative buoyancy to reduce energy metabolism and prolong dive duration, we modelled the energetic cost of transit and deep foraging dives in an elephant seal. A numerical integration technique was used to model the effects of swim speed, descent and ascent angles, and modes of locomotion (i.e. stroking and gliding) on diving metabolic rate, aerobic dive limit, vertical displacement (maximum dive depth) and horizontal displacement (maximum horizontal distance along a straight line between the beginning and end locations of the dive) for aerobic transit and foraging dives. Realistic values of the various parameters were taken from previous experimental data. Our results indicate that there is little energetic advantage to transit dives with gliding descent compared with horizontal swimming beneath the surface. Other factors such as feeding and predator avoidance may favour diving to depth during migration. Gliding descent showed variable energy savings for foraging dives. Deep mid-water foraging dives showed the greatest energy savings (approx. 18%) as a result of gliding during descent. In contrast, flat-bottom foraging dives with horizontal swimming at a depth of 400m showed less of an energetic advantage with gliding descent, primarily because more of the dive involved stroking. Additional data are needed before the advantages of gliding descent can be fully understood for male and female elephant seals of different age and body composition. This type of data will require animal-borne instruments that can record the behaviour, three-dimensional movements and locomotory performance of free-ranging animals at depth.     

Metabolic limits on dive duration and swimming speed in the southern elephant seal Mirounga leonina

The ability of air-breathing marine predators to forage successfully depends on their ability to remain submerged. This is in turn related to their total O(2) stores and the rate at which these stores are used up while submerged. Body size was positively related to dive duration in a sample of 34 adult female southern elephant seals from Macquarie Island. However, there was no relationship between body size and dive depth. This indicates that smaller seals, with smaller total O(2) stores, make shorter dives than larger individuals but operate at similar depths, resulting in less time being spent at depth. Nine adult female elephant seals were also equipped with velocity time depth recorders. In eight of these seals, a plot of swimming speed against dive duration revealed a cloud of points with a clear upper boundary. This boundary could be described using regression analysis and gave a significant negative relationship in most cases. These results indicate that metabolic rate varies with activity levels, as indicated by swimming speed, and that there are quantifiable limits to the distance that a seal can travel on a dive of a given swimming speed. However, the seals rarely dive to these physiological limits, and the majority of their dives are well within their aerobic capacity. Elephant seals therefore appear to dive in a way that ensures that they have a reserve of O(2) available.     

DIVE CHARACTERISTICS OF SATELLITE-MONITORED BLUE WHALES (BALAENOPTERA MUSCULUS) OFF THE CENTRAL CALIFORNIA COAST

Dive habits of four Northeast Pacific blue whales ( Balaenoptera musculus ) were studied using satellite-monitored radio tags. Tags summarized dive-duration data into eight 3-h periods daily. One tag additionally summarized dive depth and time-at-depth information for these same periods. Tracking periods ranged from 0.6 to 12.7 d and provided data for 17 three-hour summary periods, representing 2,007 dives (788 of which provided depth information). Total number of dives during a 3-h summary period ranged from 83 to 128. Seventy-two percent of dives were ≤ 1 min long. All whales spent >94% of their time submerged. Average duration of true dives (dives >1 min) ranged from 4.2 to 7.2 min. Seventy-five percent of depth-monitored dives were to ≤16 m, accounting for 78% of that animal's time. Average depth of dives to >16 m was 105 ± 13 m.     

Respiratory frequency, dive behaviour and social interactions of leatherback turtles, Dermochelys coriacea during the inter-nesting interval

We collected simultaneous dive Time Depth Recorder (TDR) data and video images from free swimming adult female leatherback turtles, Dermochelys coriacea, during the first 24 h after nesting on the beach, in order to determine relationships between dive parameters, activity, overall respiratory frequency and behaviour.We identified three different underwater locomotory activities (subsurface swimming, V-shaped dives and U-shaped dives) from video and TDR data that varied in their mean depth, duration and a number of other parameters. Overall respiratory frequency (overall f_R) was significantly different between all locomotory activities, with turtles taking 1.7±0.1 breaths min⁻¹ while subsurface swimming, 0.78 breaths min⁻¹ after V-shaped dives and 0.57 breaths min⁻¹ after U-shaped dives. Descent rates and ascent rates were significantly faster in U-shaped dives (descent 0.19±0.010 m s⁻¹, ascent 0.28±0.015 m s⁻¹) than in V-shaped dives (descent 0.10±0.008 m s⁻¹, ascent 0.12±0.012 m s⁻¹). Flipper stroke rates were significantly lower during the bottom component of U-shaped dives (0.18±0.02 strokes s⁻¹) than during the descent (0.29±0.03 strokes s⁻¹) or ascent (0.29±0.03 strokes s⁻¹). From overall f_R and flipper stroke rate data, we inferred that turtles used less energy during U-shaped dives than the other activity types. We recorded interactions between male turtles and the study females that lasted up to 11 min, during which male turtles displayed the characteristic courtship behaviour of sea turtles. It appeared that females attempted to avoid males by aborting ascent and extending dive duration to swim to the sea floor when males were present.     

Diving behaviour in relation to water temperature in the southern elephant seal: foraging implications

Summary A time-depth-temperature recorder provided a continuous record of diving by a female southern elephant seal in relation to water temperature for 27 days (1939 dives) after completion of moult. Mean maximum dive depth was 391±2.6 m and the overall maximum was 775 m. Dives lasted on average 17.5±0.09 min. Most dives showed a rapid descent to the discontinuity between the cold surface water and warmer deep water. Consequently the seal spent 57% of its time while diving at a depth of 200–400 m when it may have been foraging. This strongly suggests that the seal was exploiting a food source at the discontinuity between vertically stratified water masses. The water temperature data also indicated that the seal was diving in waters south of the Antarctic Polar Front and at some distance from the northern edge of the pack ice. The seal spent 88% of its time under water. Normal surface intervals between dives lasted an average of 2.1 ± 0.1 min whereas 16 extended surface intervals (>10 min duration) lasted 32.7±4.6 min. Dives were deeper during the day than at night and all but one extended surface interval occurred at night. The pattern of dives was similar to records from northern elephant seals but this is the first study to show how diving behaviour relates to water temperature.     

DEVELOPMENT OF DIVING BY HARBOR SEAL PUPS IN TWO REGIONS OF ALASKA: USE OF THE WATER COLUMN

Satellite-linked dive recorders were attached to 53 harbor seal pups in Prince William Sound (PWS) and at Tugidak Island, Alaska, during 1997–1999. We used generalized additive models and bootstrap techniques to describe pup diving behavior during their first year of life. Pups increased their ability to dive during the first 3–6 mo, as indicated by increases in proportion of time in the water (time wet) and maximum dive depth achieved by a pup each day (max-depth) values. Time wet and/or max-depth later decreased, suggesting a seasonal component to diving behavior. Monthly time wet varied from an overall minimum of 0.68 at tagging in July to a maximum of 0.89 in November. Pups spent half of their time wet swimming in water <25 m deep, the shallowest 30% of the available water column. They spent only 5% of their time swimming in the deepest 30% of the available water column, at depths >60–70 m. This strongly suggests they were not feeding on or near bottom during their first year. Average max-depths and deepest actual dives were similar for PWS and Tugidak pups. PWS pups dove deeper sooner and spent less time wet than Tugidak pups during the first few months after tagging, probably as a result of regional bathymetric differences. Diving behavior and body condition suggest that food availability was not likely a major factor in the population decline in PWS during the period of this study.     

Diving behaviour of dugongs, Dugong dugon

The diving behaviour of 15 dugongs (Dugong dugon) was documented using time-depth recorders (TDRs), which logged a total of 39,507 dives. The TDRs were deployed on dugongs caught at three study sites in northern Australia: Shark Bay, the Gulf of Carpentaria and Shoalwater Bay. The average time for which the dive data were collected per dugong was 10.4±1.1 (S.E.) days. Overall, these dugongs spent 47% of their daily activities within 1.5 m of the sea surface and 72% less than 3 m from the sea surface. Their mean maximum dive depth was 4.8±0.4 m (S.E.), mean dive duration was 2.7±0.17 min and the number of dives per hour averaged 11.8±1.2. The maximum dive depth recorded was 20.5 m; the maximum dive time in water >1.5 m deep was 12.3 min. The effects of dugong sex, location (study site), time of day and tidal cycle on diving rates (dives per hour), mean maximum dive depths, durations of dives, and time spent ≤1.5 m from the surface were investigated using weighted split-plot analysis of variance. The dugongs exhibited substantial interindividual variation in all dive parameters. The interaction between location and time of day was significant for diving rates, mean maximum dive depths and time spent within 1.5 m of the surface. In all these cases, there was substantial variation among individuals within locations among times of day. Thus, it was the variation among individuals that dominated all other effects. Dives were categorised into five types based on the shape of the time-depth profile. Of these, 67% of dives were interpreted as feeding dives (square and U-shaped), 8% as exploratory dives (V-shaped), 22% as travelling dives (shallow-erratic) and 3% as shallow resting dives. There was systematic variation in the distribution of dive types among the factors examined. Most of this variation was among individuals, but this differed across both time of day and tidal state. Not surprisingly, there was a positive relationship between dive duration and depth and a negative relationship between the number of dives per hour and the time spent within 1.5 m of the surface after a dive.     

Diving depths of Shags Phalacrocorax aristotelis breeding on the Isle of May

Information on maximum dive depth and the time spent at various depths was obtained from 49 Shags Phalacrocorax aristotelis. On average, the maximum dive depth was 33–35 m; the overall maximum was 43 m. Shags dived repeatedly to the same depth and spent c. 55% of the time between 25 and 34 m which indicated that they were foraging close to the seabed. About 46% of the time underwater was spent foraging and 54% travelling. Average underwater swimming speed was 1.7-1.9 m per second.     

Acquisition of gliding skills by Weddell seal (Leptonychotes weddellii) pups during lactation

Pinnipeds give birth to their pups ashore or on ice and forage in water. Therefore, neonates initially lack the adaptations to sustain prolonged underwater diving activity. Although the physiological development for breath-holding during diving has been investigated in seal pups, little is known about the concurrent development of behavioral adaptations during lactation. In this study, multisensor data loggers were used to record diving behavior and swimming gaits of pre-weaned Weddell seal (Leptonychotes weddellii) pups. Experiments were conducted in 16 pups at the Syowa Station, Antarctica, from November to December 1999 and 2004. Swimming speeds, dive depths and flipper stroking rates were recorded for each individual for about 24 h. We found that the glide index during ascending was increased with body length, whereas the dominant stroke cycle frequency were not affected by body length, dive depth and descent or ascent phase. All pups had significantly higher stroke rates in descent than in ascent, but there was no difference between swimming speed. As we found a positive relationship between the body length and age, we considered body length as an index of growth. Therefore, we conclude that pups gradually acquire the ability to glide with utilizing positive buoyancy during ascending toward the end of lactation.     

Diving patterns and performance in the Antarctic blue-eyed shag Phalacrocorax atriceps

The pattern and characteristics of diving of two male blue-eyed shags Phalacrocorax atriceps were studied, using continuous-recording time-depth recorders, for a total of 15 consecutive days during which the depth, duration, bottom time, ascent and descent rates and surface intervals of 674 dives were recorded. Deep dives (> 35 m, averages80–90 m, max. 116 m) were twice as common (64% versus 34%) as shallow dives (< 21 m and 90% < 10 m). Deep dives were long (averages 2.7-4.1 min, max. 5.2 min) with half the time spent near maximum depth and fast travel speeds (averages 1.0-2.4 m s⁻¹). Shallow dives were short (average 0.5 min, max. 1.3 min), without bottom time and with slow travel speeds (0.1–0.6 m s⁻¹). The time spent at depth and the diet (mainly benthic fish and octopus) is consistent with benthic foraging; the function of shallow dives is uncertain. Male shags forage mainly in the afternoon in3–5 distinct bouts of diving. Within bouts (and shorter homogeneous sequences of diving) surface intervals are consistently2–3 times the preceding dive duration; in other shags the reverse is the case. Blue-eyed shag diving depth, duration and pattern is extreme amongst shags; and the relationship between dives and surface intervals suggests that they may regularly exceed their aerobic dive limit.     

DIVING BEHAVIOR AND PERFORMANCE OF HARBOR PORPOISES, PHOCOENA PHOCOENA, IN FUNKA BAY, HOKKAIDO, JAPAN

In order to monitor the diving behavior of free-ranging cetaceans, microdataloggers, with pre-programmed release mechanisms, were attached to the dorsal fins of two female harbor porpoises ( Phocoena phocoena ) in Funka Bay, Hokkaido, Japan, in 1994. The two loggers were successfully recovered and a total of 141 h of diving data (depth and water temperature in 4,671 dives) was obtained. Both porpoises dived almost continuously, rarely exhibiting long-term rest at the surface. Maximum dive depths were 98.6 m and 70.8 m, respectively, with more than 70% of diving time at 20 m or less. Most shallow dives were V-shaped with no bottom time. The V-shaped dives were significantly shallower in dive depth and shorter in dive duration than U-shaped dives. Descent rate was not constant during a dive. The deeper the dive depths, the faster the mean descent and initial descent rates. This suggests that porpoises have anticipated the depth to which they will dive before initiating the dive itself.     

Ascent exhalations of Antarctic fur seals: a behavioural adaptation for breath-hold diving?

Novel observations collected from video, acoustic and conductivity sensors showed that Antarctic fur seals consistently exhale during the last 50-85% of ascent from all dives (10-160 m, n > 8000 dives from 50 seals). The depth of initial bubble emission was best predicted by maximum dive depth, suggesting an underlying physical mechanism. Bubble sound intensity recorded from one seal followed predictions of a simple model based on venting expanding lung air with decreasing pressure. Comparison of air release between dives, together with lack of variation in intensity of thrusting movement during initial descent regardless of ultimate dive depth, suggested that inhaled diving lung volume was constant for all dives. The thrusting intensity in the final phase of ascent was greater for dives in which ascent exhalation began at a greater depth, suggesting an energetic cost to this behaviour, probably as a result of loss of buoyancy from reduced lung volume. These results suggest that fur seals descend with full lung air stores, and thus face the physiological consequences of pressure at depth. We suggest that these regular and predictable ascent exhalations could function to reduce the potential for a precipitous drop in blood oxygen that would result in shallow-water blackout.     

Vertical movement of dolphinfish <Emphasis Type="Italic">Coryphaena hippurus</Emphasis> as recorded by acceleration data-loggers in the northern East China Sea

Environmental changes influence foraging behavior for most animals. Dolphinfish, Coryphaena hippurus, are epipelagic predators and have a cosmopolitan tropical to warm-temperate (>20°C) distribution. We simultaneously obtained the ambient temperature and the foraging behavior (i.e., swimming speed, depth and tailbeat acceleration) of dolphinfish, using an acceleration data-logger in May, September, October, November 2007, June 2008, May and July 2010 for 8 individuals. Although the dolphinfish spent a mean ± standard deviation of 43.4 ± 27.7% of their time at the surface (0–5 m), dive excursions from the surface (DES) were observed in all individuals and maximum DES depths ranged from 50.1 to 95.4 m. DES events resulted dives below the thermocline for these dolphinfish, and there was a significantly positive relationship between the isothermal layer depth (ILD) and DES depth. Our results demonstrate that dolphinfish avoided the rapid thermal change beyond the thermocline, and their prey is most likely found in the upper layers of the thermocline. Gliding behavior during the DES phase was also observed and dolphinfish gradually descended to deeper waters with gliding. The gliding time was longer when the ILD was deeper, and fish tended to dive deeper. We suggest that dolphinfish adopt gliding behavior to search a broader range of depths for prey, while minimizing energy use.     

Diving heart rate development in postnatal harbour seals, Phoca vitulina

Harbour seals, Phoca vitulina, dive from birth, providing a means of mapping the development of the diving response, and so our objective was to investigate the postpartum development of diving bradycardia. The study was conducted May-July 2000 and 2001 in the St. Lawrence River Estuary (48 degrees 41'N, 68 degrees 01'W). Both depth and heart rate (HR) were remotely recorded during 86,931 dives (ages 2-42 d, n = 15) and only depth for an additional 20,300 dives (combined data covered newborn to 60 d, n = 20). The mean dive depth and mean dive durations were conservative during nursing (2.1 +/- 0.1 m and 0.57 +/- 0.01 min, range = 0-30.9 m and 0-5.9 min, respectively). The HR of neonatal pups during submersion was bimodal, but as days passed, the milder of the two diving HRs disappeared from their diving HR record. By 15 d of age, most of the dive time was spent at the lower diving bradycardia rate. Additionally, this study shows that pups are born with the ability to maintain the lower, more fully developed dive bradycardia during focused diving but do not do so during shorter routine dives.     

THREE-DIMENSIONAL DIVING BEHAVIORS OF RINGED SEALS (PHOCA HISPIDA)

Dives of five freely diving ringed seals were classified into three-dimentional movement types. Horizontally convoluted dives, defined as dives with angular velocity > 15°/sec, appeared to be foraging or social dives. Simple dives that did not include convoluted movements (angular velocity < 10°/sec) were considered to be exploration dives. Directional dives with nearly linear horizontal travel (horizontal directionality >0.6, on a scale of 0–1) were presumed to be travel dives. Each three-dimensional dive type was observed with similar frequency in dives with two distinct time-depth profiles: V-shaped profiles in which ascent immediately followed descent, and U-shaped profiles in which >7 sec were spent at depth between descent and ascent. The lack of behavioral differences between dives with distinct time-depth profiles suggested that time-depth profiles are not a reliable means of inferring dive behaviors for ringed seals.     

Diving behaviour of the Shy Albatross Diomedea cauta in Tasmania: initial findings and dive recorder assessment

The diving behaviour of the Shy Albatross Diomedea cauta was investigated using archival time-depth recorders (TDRs) and maximum depth gauges (MDGs). Data from birds carrying multiple devices and from diving simulations indicated that the degree of correspondence between TDRs and MDGs varied with the dive depth, duration and frequency, as well as with body placement. The MDGs were the most reliable when the diving depth was greater than 0.5 m, when the diving frequency was low and when gauges were placed on the birds' backs. The TDRs were used during late incubation and early chick rearing in 1994. Fifty-two dives (0.4 m) were recorded during 20 foraging trips of 15 individuals. The majority of dives were within the upper 3 m of the water column and lasted for less than 6 s. However, dives to 7.4 m and others lasting 19 s were recorded. The albatrosses dived between 07.00 h and 22.00 h, with peaks in their diving activity near midday and twilight. Mean diving depth varied throughout the day. with the deepest dives occurring between 10.00 h and 12.00 h. Two dive types were identified on the basis of the relationship between dive depth and descent rate. Plunge dives were short (5 s), and the birds reached a maximum depth of 2.9 m. Swimming dives were both longer and deeper. The characteristics of Shy Albatross plunge dives were similar to those of gannets Morus spp., which are known to be proficient plunge divers. Swimming dives suggest that Shy Albatrosses actively pursue prey underwater.     

SUCCESSFUL USE OF A TRANSLOCATION PROGRAM TO INVESTIGATE DIVING BEHAVIOR IN A MALE AUSTRALIAN FUR SEAL, ARCTOCEPHALUS PUSILLUS DORIFERUS

This study reports some of the first foraging behavior data collected for male fur seals. A nonbreeding male Australian fur seal, Arctocephalus pusillus doriferus , captured at a commercial salmon farm in southern Tasmania, Australia, was relocated 450 km from the site of capture. The animal was equipped with a geolocating time-depth recorder that recorded diving behavior and approximate location for the 14.4 d that it took the seal to travel down the east coast of Tasmania and be recaptured at the salmon farm. During its time at sea, the seal spent most of its time over the relatively shallow shelf waters. It spent 30% of its time ashore on a number of different haul-out sites. The deepest dive was 102 m and the maximum duration was 6.8 min. "Foraging" type dives made up 31.2% of the time at sea and had a median duration of 2.5 min and a median depth of 14 m. The seal performed these dives more commonly during the latter part of its time at sea, while it was on the east coast. Unlike other fur seal species studied to date, there was no evidence of a diurnal foraging pattern; it made dives at all times of the day and night.     

Buoyancy under Control: Underwater Locomotor Performance in a Deep Diving Seabird Suggests Respiratory Strategies for Reducing Foraging Effort

Background

Because they have air stored in many body compartments, diving seabirds are expected to exhibit efficient behavioural strategies for reducing costs related to buoyancy control. We study the underwater locomotor activity of a deep-diving species from the Cormorant family (Kerguelen shag) and report locomotor adjustments to the change of buoyancy with depth.

Methodology/Principal Findings

Using accelerometers, we show that during both the descent and ascent phases of dives, shags modelled their acceleration and stroking activity on the natural variation of buoyancy with depth. For example, during the descent phase, birds increased swim speed with depth. But in parallel, and with a decay constant similar to the one in the equation explaining the decrease of buoyancy with depth, they decreased foot-stroke frequency exponentially, a behaviour that enables birds to reduce oxygen consumption. During ascent, birds also reduced locomotor cost by ascending passively. We considered the depth at which they started gliding as a proxy to their depth of neutral buoyancy. This depth increased with maximum dive depth. As an explanation for this, we propose that shags adjust their buoyancy to depth by varying the amount of respiratory air they dive with.

Conclusions/Significance

Calculations based on known values of stored body oxygen volumes and on deep-diving metabolic rates in avian divers suggest that the variations of volume of respiratory oxygen associated with a respiration mediated buoyancy control only influence aerobic dive duration moderately. Therefore, we propose that an advantage in cormorants - as in other families of diving seabirds - of respiratory air volume adjustment upon diving could be related less to increasing time of submergence, through an increased volume of body oxygen stores, than to reducing the locomotor costs of buoyancy control.     

Intermittent Swimming by Mammals: A Strategy for Increasing Energetic Efficiency During Diving

The evolutionary history of marine mammals involved marked physiologicaland morphological modifications to change from terrestrial toaquatic locomotion. A consequence of this ancestry is that swimmingis energetically expensive for mammals in comparison to fish.This study examined the use of behavioral strategies by marinemammals to circumvent these elevated locomotor costs duringhorizontal swimming and vertical diving. Intermittent formsof locomotion, including wave-riding and porpoising when nearthe water surface, and prolonged gliding and a stroke and glidemode of propulsion when diving, enabled marine mammals to increasethe efficiency of aquatic locomotion. Video instrumentationpacks (8-mm camera, video recorder and time-depth microprocessor)deployed on deep diving bottlenose dolphins (Tursiops truncatus),northern elephant seals (Mirounga angustirostris), and Weddellseals (Leptonychotes weddellii) revealed exceptionally longperiods of gliding during descent to depth. Glide duration dependedon depth and represented nearly 80% of the descent for divesexceeding 200 m. Transitions in locomotor mode during divingwere attributed to buoyancy changes with compression of thelungs at depth, and were associated with a 9–60% reductionin the energetic cost of dives for the species examined. Bychanging to intermittent locomotor patterns, marine mammalsare able to increase travelling speed for little additionalenergetic cost when surface swimming, and to extend the durationof submergence despite limitations in oxygen stores when diving.     

ANALYSIS OF SWIM VELOCITIES DURING DEEP AND SHALLOW DIVES OF TWO NORTHERN FUR SEALS, CALLORHINUS URSINUS

Swim velocities at 15-sec intervals and maximum depth per dive were recorded by microprocessor units on two "mixed diver" adult female northern fur seals during summer foraging trips. These records allowed comparison of swim velocities of deep (>75 m) and shallow (<75 m) dives.
Deep dives averaged 120 m depth and 3 min duration; shallow dives averaged 30 m and 1.2 min. Mean swim velocities on deep dives were 1.8 and 1.5 m/sec for the two animals; mean swim velocities on shallow dives were 1.5 and 1.2 m/sec. The number of minutes per hour spent diving during the deep and shallow dive patterns were 11 and 27 min, respectively.
Swim velocity, and hence, relative metabolic rate, did not account for the differences in dive durations between deep and shallow dives. The long surface durations associated with deep dives, and estimates of metabolic rates for the observed swim velocities, suggest that deep dives involve significant anaerobic metabolism.