Stroke and glide of wing–propelled divers: deep diving seabirds adjust surge frequency to buoyancy change with depth

Watanuki, Yutaka; Niizuma, Yasuaki; Gabrielsen, Geir Wing; Sato, Katsufumi; Naito, Yoshiro

doi:10.1098/rspb.2002.2252

Cited by 113 publications

(152 citation statements)

References 21 publications

(23 reference statements)

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“…1B). Although mechanical costs during deep dives have been precisely measured and increase approximately linearly with dive depth (30)(31)(32), actual metabolic costs measured in the field decelerated as dive depth increased (Table 1). We suggest that physiological processes during the dive, such as oxygen store management and thermoregulation, are the dominant processes determining costs in wing-propelled divers diving to depths where buoyancy costs are minimal (22,25,27).…”

Section: Resultsmentioning

confidence: 99%

High flight costs, but low dive costs, in auks support the biomechanical hypothesis for flightlessness in penguins

Elliott

Ricklefs

Gaston

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

186

183

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Flight is a key adaptive trait. Despite its advantages, flight has been lost in several groups of birds, notably among seabirds, where flightlessness has evolved independently in at least five lineages. One hypothesis for the loss of flight among seabirds is that animals moving between different media face tradeoffs between maximizing function in one medium relative to the other. In particular, biomechanical models of energy costs during flying and diving suggest that a wing designed for optimal diving performance should lead to enormous energy costs when flying in air. Costs of flying and diving have been measured in free-living animals that use their wings to fly or to propel their dives, but not both. Animals that both fly and dive might approach the functional boundary between flight and nonflight. We show that flight costs for thickbilled murres (Uria lomvia), which are wing-propelled divers, and pelagic cormorants (Phalacrocorax pelagicus) (foot-propelled divers), are the highest recorded for vertebrates. Dive costs are high for cormorants and low for murres, but the latter are still higher than for flightless wing-propelled diving birds (penguins). For murres, flight costs were higher than predicted from biomechanical modeling, and the oxygen consumption rate during dives decreased with depth at a faster rate than estimated biomechanical costs. These results strongly support the hypothesis that function constrains form in diving birds, and that optimizing wing shape and form for wing-propelled diving leads to such high flight costs that flying ceases to be an option in larger wing-propelled diving seabirds, including penguins.light is a key adaptation that has evolved independently on many occasions (1). Despite the apparent advantages of flying, the ability to fly has been secondarily lost in several groups. Because a major advantage of flight is reduced extrinsic mortality (2), one hypothesis for the evolution of flightlessness posits that gains in efficiency in other locomotory modalities, such as diving, offset mortality risks in relatively safe environments. The high energy demands of flight also may be disadvantageous, particularly in habitats with low productivity (3, 4). The restriction of some terrestrial flightless birds to remote, predator-free islands with low productivity supports this hypothesis (3, 4). The reasoning seems less tenable for flightless diving seabirds that often exploit highly productive waters but are vulnerable to predation by seals, whales, and sharks. Moreover, many species of penguin travel long distances between their breeding and feeding grounds on a journey that could be made far more quickly by flying than by walking and swimming (5). An alternative biomechanical hypothesis suggests that flightlessness evolved in these birds because of a tradeoff in the optimization of wing-propelled locomotion in different media. In short, as wings become more efficient for swimming they become less efficient for flying, and vice versa. At some point, adaptations to increase swimming...

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Section: Resultsmentioning

confidence: 99%

High flight costs, but low dive costs, in auks support the biomechanical hypothesis for flightlessness in penguins

Elliott

Ricklefs

Gaston

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

186

183

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“…Such loggers have been used to examine, for example, the in-flight and diving behavior of birds (Yoda et al 1999(Yoda et al , 2001Watanuki et al 2003;Wilson et al 2006;Gó mez Laich et al 2008;Halsey et al 2009b), the diving and feeding behavior of marine mammals (Sato et al 2006;Viviant et al 2010), and the movement patterns of an array of species Wilson et al 2008). More recently, acceleration-data loggers have been applied to estimating energy expenditure in free-living animals by calibration of measures of acceleration with metabolic rate, which tends to be measured via respirometry as rate of oxygen consumption (…”

Section: Introductionmentioning

confidence: 99%

Assessing the Validity of the Accelerometry Technique for Estimating the Energy Expenditure of Diving Double-Crested CormorantsPhalacrocorax auritus

Halsey¹,

White²,

Enstipp³

et al. 2011

Physiological and Biochemical Zoology

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JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact support@jstor.org.. The University of Chicago Press ABSTRACTOver the past few years, acceleration-data loggers have been used to provide calibrated proxies of energy expenditure: the accelerometry technique. Relationships between rate of oxygen consumption and a derivation of acceleration data termed "overall dynamic body acceleration" (ODBA) have now been generated for a range of species, including birds, mammals, and amphibians. In this study, we examine the utility of the accelerometry technique for estimating the energy expended by double-crested cormorants Phalacrocorax auritus to undertake a dive cycle (i.e., a dive and the subsequent pause at the surface before another dive). The results show that ODBA does not calibrate with energy expenditure in diving cormorants, where energy expenditure is calculated from measures of oxygen uptake during surface periods between dives. The possible explanations include reasons why energy expenditure may not relate to ODBA but also reasons why oxygen uptake between dives may not accurately represent energy expenditure during a dive cycle.

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“…Most breath-holding marine predators capture food in discrete feeding events (Ropert-Coudert et al 2006;Hassrick et al 2007;Aguilar Soto et al 2008), where they reduce oxygen consumption by gliding during parts of either ascent or descent (Williams et al 2000) and employ a stroke-and-glide gait at depth to prolong foraging time (Crocker et al 1997;Croll et al 2001;Williams 2001;Wilson et al 2002;Watanuki et al 2003). Thus, locomotion is a major oxygen-consuming activity using up oxygen reserves while diving, and the stroke-and-glide strategy of most air-breathing marine animals allows them to perform longer breath-hold dives, maximizing access to food resources (Crocker et al 1997;Williams et al 2000;Watanuki et al 2003).…”

Section: Introductionmentioning

confidence: 99%

Behaviour and kinematics of continuous ram filtration in bowhead whales (Balaena mysticetus)

et al. 2009

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Balaenid whales perform long breath-hold foraging dives despite a high drag from their ram filtration of zooplankton. To maximize the volume of prey acquired in a dive with limited oxygen supplies, balaenids must either filter feed only occasionally when prey density is particularly high, or they must swim at slow speeds while filtering to reduce drag and oxygen consumption. Using digital tags with three-axis accelerometers, we studied bowhead whales feeding off West Greenland and present here, to our knowledge, the first detailed data on the kinematics and swimming behaviour of a balaenid whale filter feeding at depth. Bowhead whales employ a continuous fluking gait throughout the bottom phase of foraging dives, moving at very slow speeds (less than 1 m s 21 ), allowing them to filter feed continuously at depth. Despite the slow speeds, the large mouth aperture provides a water filtration rate of approximately 3 m 3 s 21 , amounting to some 2000 tonnes of water and prey filtered per dive. We conclude that a food niche of dense, slow-moving zooplankton prey has led balaenids to evolve locomotor and filtering systems adapted to work against a high drag at swimming speeds of less than 0.07 body length s 21 using a continuous fluking gait very different from that of nekton-feeding, aquatic predators.

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Stroke and glide of wing–propelled divers: deep diving seabirds adjust surge frequency to buoyancy change with depth

Cited by 113 publications

References 21 publications

High flight costs, but low dive costs, in auks support the biomechanical hypothesis for flightlessness in penguins

High flight costs, but low dive costs, in auks support the biomechanical hypothesis for flightlessness in penguins

Assessing the Validity of the Accelerometry Technique for Estimating the Energy Expenditure of Diving Double-Crested CormorantsPhalacrocorax auritus

Behaviour and kinematics of continuous ram filtration in bowhead whales (Balaena mysticetus)

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