Adrian C. Gleiss

Tri-Axial Dynamic Acceleration as a Proxy for Animal Energy Expenditure; Should We Be Summing Values or Calculating the Vector?

Dynamic body acceleration (DBA) has been used as a proxy for energy expenditure in logger-equipped animals, with researchers summing the acceleration (overall dynamic body acceleration - ODBA) from the three orthogonal axes of devices. The vector of the dynamic body acceleration (VeDBA) may be a better proxy so this study compared ODBA and VeDBA as proxies for rate of oxygen consumption using humans and 6 other species. Twenty-one humans on a treadmill ran at different speeds while equipped with two loggers, one in a straight orientation and the other skewed, while rate of oxygen consumption () was recorded. Similar data were obtained from animals but using only one (straight) logger. In humans, both ODBA and VeDBA were good proxies for with all r2 values exceeding 0.88, although ODBA accounted for slightly but significantly more of the variation in than did VeDBA (P<0.03). There were no significant differences between ODBA and VeDBA in terms of the change in estimated by the acceleration data in a simulated situation of the logger being mounted straight but then becoming skewed (P = 0.744). In the animal study, ODBA and VeDBA were again good proxies for with all r2 values exceeding 0.70 although, again, ODBA accounted for slightly, but significantly, more of the variation in than did VeDBA (P<0.03). The simultaneous contraction of muscles, inserted variously for limb stability, may produce muscle oxygen use that at least partially equates with summing components to derive DBA. Thus, a vectorial summation to derive DBA cannot be assumed to be the more ‘correct’ calculation. However, although within the limitations of our simple study, ODBA appears a marginally better proxy for . In the unusual situation where researchers are unable to guarantee at least reasonably consistent device orientation, they should use VeDBA as a proxy for .

Key Questions in Marine Megafauna Movement Ecology

It is a golden age for animal movement studies and so an opportune time to assess priorities for future work. We assembled 40 experts to identify key questions in this field, focussing on marine megafauna, which include a broad range of birds, mammals, reptiles, and fish. Research on these taxa has both underpinned many of the recent technical developments and led to fundamental discoveries in the field. We show that the questions have broad applicability to other taxa, including terrestrial animals, flying insects, and swimming invertebrates, and, as such, this exercise provides a useful roadmap for targeted deployments and data syntheses that should advance the field of movement ecology.

High activity and Levy searches: jellyfish can search the water column like fish

Over-fishing may lead to a decrease in fish abundance and a proliferation of jellyfish. Active movements and prey search might be thought to provide a competitive advantage for fish, but here we use data-loggers to show that the frequently occurring coastal jellyfish (Rhizostoma octopus) does not simply passively drift to encounter prey. Jellyfish (327 days of data from 25 jellyfish with depth collected every 1 min) showed very dynamic vertical movements, with their integrated vertical movement averaging 619.2 m d−1, more than 60 times the water depth where they were tagged. The majority of movement patterns were best approximated by exponential models describing normal random walks. However, jellyfish also showed switching behaviour from exponential patterns to patterns best fitted by a truncated Lévy distribution with exponents (mean μ = 1.96, range 1.2–2.9) close to the theoretical optimum for searching for sparse prey (μopt ≈ 2.0). Complex movements in these ‘simple’ animals may help jellyfish to compete effectively with fish for plankton prey, which may enhance their ability to increase in dominance in perturbed ocean systems.

Convergent evolution in locomotory patterns of flying and swimming animals

Locomotion is one of the major energetic costs faced by animals and various strategies have evolved to reduce its cost. Birds use interspersed periods of flapping and gliding to reduce the mechanical requirements of level flight while undergoing cyclical changes in flight altitude, known as undulating flight. Here we equipped free-ranging marine vertebrates with accelerometers and demonstrate that gait patterns resembling undulating flight occur in four marine vertebrate species comprising sharks and pinnipeds. Both sharks and pinnipeds display intermittent gliding interspersed with powered locomotion. We suggest, that the convergent use of similar gait patterns by distinct groups of animals points to universal physical and physiological principles that operate beyond taxonomic limits and shape common solutions to increase energetic efficiency. Energetically expensive large-scale migrations performed by many vertebrates provide common selection pressure for efficient locomotion, with potential for the convergence of locomotory strategies by a wide variety of species.

Multi-Channel Data-Logging: Towards Determination of Behaviour and Metabolic Rate in Free-Swimming Sharks

Elucidation of the behavioural ecology of elasmobranchs is essential to further our understanding of the role of this order of vertebrates in marine ecosystems and therefore facilitate their conservation. Methodologies employed so far often rely on untested assumptions due to technological problems in resolving location, and orientation in three-dimensional space. This highlights the importance developing systems to resolve elasmobranch behaviour in the field. To that end semi-captive trials were conducted on two lemon sharks (Negaprion brevirostris) at Bimini Bahamas, where these individuals were equipped with archival-tags measuring 13 parameters (tri-axial acceleration, tri-axial magnetic field strength and a suite of environmental factors). Using tri-axial acceleration and tri-axial magnetic field strength, four behaviours and their intensities could be distinguished; resting, initiation of swimming after rest, steady-swimming, and fast-start swimming. Each behaviour could be characterised by the parameters measured (frequency and amplitude of acceleration peaks, changes in compass orientation). During steady swimming, animals displayed a wide range of tail-beat frequencies (0.4–1.2 Hz) and tail-beat acceleration amplitudes (0.002–0.16g). Overall dynamic body acceleration (ODBA), which is correlated with activity-specific metabolic-rate in terrestrial animals, showed a positive linear relationship with tail-beat frequency, indicating its potential as a proxy for energy expenditure in sharks. Comparison of ODBA for four distinct behaviours revealed it to be highest during fast-start swimming, and lowest during resting phases.

Does prey size matter? Novel observations of feeding in the leatherback turtle (Dermochelys coriacea) allow a test of predator–prey size relationships

Optimal foraging models predict that large predators should concentrate on large prey in order to maximize their net gain of energy intake. Here, we show that the largest species of sea turtle, Dermochelys coriacea, does not strictly adhere to this general pattern. Field observations combined with a theoretical model suggest that a 300 kg leatherback turtle would meet its energetic requirements by feeding for 3–4 h a day on 4 g jellyfish, but only if prey were aggregated in high-density patches. Therefore, prey abundance rather than prey size may, in some cases, be the overriding parameter for foraging leatherbacks. This is a classic example where the presence of small prey in the diet of a large marine predator may reflect profitable foraging decisions if the relatively low energy intake per small individual prey is offset by high encounter rates and minimal capture and handling costs. This study provides, to our knowledge, the first quantitative estimates of intake rate for this species.

Behaviour and buoyancy regulation in the deepest-diving reptile : the leatherback turtle

SUMMARY In the face of the physical and physiological challenges of performing breath-hold deep dives, marine vertebrates have evolved different strategies. Although behavioural strategies in marine mammals and seabirds have been investigated in detail, little is known about the deepest-diving reptile – the leatherback turtle (Dermochelys coriacea). Here, we deployed tri-axial accelerometers on female leatherbacks nesting on St Croix, US Virgin Islands, to explore their diving strategy. Our results show a consistent behavioural pattern within dives among individuals, with an initial period of active swimming at relatively steep descent angles (∼–40 deg), with a stroke frequency of 0.32 Hz, followed by a gliding phase. The depth at which the gliding phase began increased with the maximum depth of the dives. In addition, descent body angles and vertical velocities were higher during deeper dives. Leatherbacks might thus regulate their inspired air-volume according to the intended dive depth, similar to hard-shelled turtles and penguins. During the ascent, turtles actively swam with a stroke frequency of 0.30 Hz but with a low vertical velocity (∼0.40 ms–1) and a low pitch angle (∼+26 deg). Turtles might avoid succumbing to decompression sickness (‘the bends’) by ascending slowly to the surface. In addition, we suggest that the low body temperature of this marine ectotherm compared with that of endotherms might help reduce the risk of bubble formation by increasing the solubility of nitrogen in the blood. This physiological advantage, coupled with several behavioural and physical adaptations, might explain the particular ecological niche the leatherback turtle occupies among marine reptiles.

Assessing the role of reproduction and stress in the spring emergence of Haematozoan parasites in birds

A spring emergence of avian haemosporidian infections is nearly universal among temperate zone birds and is often described as a cost of reproductive effort. We take advantage of the opportunistic (i.e. aseasonal) breeding schedule of the red crossbill (Loxia curvirostra) to determine the relative contributions of season versus host physiology to the timing and intensity of Haemoproteus infections in the temperate zone. Despite breeding activity in both the winter and summer, Haemoproteus infections were highly seasonal – occurring largely from May through September – and measures of host physiology (i.e. reproductive condition and stress parameters) did not explain parasite prevalence. However, within the spring–summer peak, infection intensity (i.e. parasite density) was positively correlated with plasma levels of testosterone and free corticosterone and negatively correlated with corticosterone binding globulin capacity. These data are discussed in terms of the behavioral ecology of host and vector, and suggest that both seasonal increases in vector activity and relapse of latent (i.e. dormant) infections contribute to the spring emergence in birds. Relapse of latent infections does not appear to be induced by reproductive activity or increased allostatic (i.e. energy) load, but rather by a season-specific change in host or parasite physiology (e.g. melatonin or endogenous rhythms).

Harnessing the Sun: Testing a Novel Attachment Method to Record Fine Scale Movements in Ocean Sunfish (Mola mola)

Ocean sunfish (Mola mola) are a little studied fish species which are prone to exceptionally high levels of incidental by-catch. To facilitate future studies of this species we report on a novel method for short-term deployments of high-resolution data loggers to ocean sunfish. Trials were conducted under captive (n = 1 fish) and field conditions (n = 3 fish) during 2006 and 2007 in County Kerry, Ireland. Our principal aims were: (1) to develop a low-impact harness system with an automated release mechanism; (2) retrieve the detached devices at sea; (3) to assess whether this approach enabled the collection of fine-scale behavioural data from multi-channel data loggers (daily diaries). Both the attachment and retrieval mechanisms worked well at sea with the successful relocation of all devices. The harness additionally functioned well by keeping the data logger in a fixed-position at all times (except during periods of extremely fast evasive swimming) with high resolution data retrieved for a range of variables suggesting significant potential for use on other fish species. Nonetheless, as each deployment was < 2 h it was not our objective to critically define the behaviour of ocean sunfish, but simply to obtain qualitative data upon which to base future studies. Despite the short-term deployments, provisional analysis revealed some unusual swimming behaviour suggesting that body roll, in addition to pitch and sway amplitude was intrinsically linked with vertical velocity whilst the allometric relationship between body sway and frequency (taken as a proxy for fin strokes) appeared converse to previous studies of teleost locomotion.

Correlations of metabolic rate and body acceleration in three species of coastal sharks under contrasting temperature regimes

ABSTRACT The ability to produce estimates of the metabolic rate of free-ranging animals is fundamental to the study of their ecology. However, measuring the energy expenditure of animals in the field has proved difficult, especially for aquatic taxa. Accelerometry presents a means of translating metabolic rates measured in the laboratory to individuals studied in the field, pending appropriate laboratory calibrations. Such calibrations have only been performed on a few fish species to date, and only one where the effects of temperature were accounted for. Here, we present calibrations between activity, measured as overall dynamic body acceleration (ODBA), and metabolic rate, measured through respirometry, for nurse sharks (Ginglymostoma cirratum), lemon sharks (Negaprion brevirostris) and blacktip sharks (Carcharhinus limbatus). Calibrations were made at a range of volitional swimming speeds and experimental temperatures. Linear mixed models were used to determine a predictive equation for metabolic rate based on measured ODBA values, with the optimal model using ODBA in combination with activity state and temperature to predict metabolic rate in lemon and nurse sharks, and ODBA and temperature to predict metabolic rate in blacktip sharks. This study lays the groundwork for calculating the metabolic rate of these species in the wild using acceleration data. Summary: Calibrations between metabolic rate, body acceleration and temperature in three coastal sharks offer a tool to estimate field metabolic rates in these species.