Air-breathing Divers Research Articles

Effects of Hyperbaric Nitrogen Narcosis on Cognitive Performance in Recreational air SCUBA Divers: An Auditory Event-related Brain Potentials Study.

The narcotic effect of hyperbaric nitrogen is most pronounced in air-breathing divers because it impairs diver's cognitive and behavioral performance, and limits the depth of dive profiles. We aimed to investigate the cognitive effects of simulated (500 kPa) air environments in recreational SCUBA divers, revealed by auditory event-related potentials (AERPs). A total of 18 healthy volunteer recreational air SCUBA divers participated in the study. AERPs were recorded in pre-dive, deep-dive, and post-dive sessions. False-positive score variables were found with significantly higher differences and longer reaction times of hits during deep-dive and post-dive than pre-dive sessions. Also, P3 amplitudes were significantly reduced and peak latencies were prolonged during both deep-dive and post-dive compared with pre-dive sessions. We observed that nitrogen narcosis at 500 kPa pressure in the dry hyperbaric chamber has a mild-to-moderate negative effect on the cognitive performance of recreational air SCUBA divers, which threatened the safety of diving. Although relatively decreased, this effect also continued in the post-dive sessions. These negative effects are especially important for divers engaged in open-sea diving. Our results show crucial implications for the kinds of control measures that can help to prevent nitrogen narcosis and diving accidents at depths up to 40 msw.

Acceleration predicts energy expenditure in a fat, flightless, diving bird

Energy drives behaviour and life history decisions, yet it can be hard to measure at fine scales in free-moving animals. Accelerometry has proven a powerful tool to estimate energy expenditure, but requires calibration in the wild. This can be difficult in some environments, or for particular behaviours, and validations have produced equivocal results in some species, particularly air-breathing divers. It is, therefore, important to calibrate accelerometry across different behaviours to understand the most parsimonious way to estimate energy expenditure in free-living conditions. Here, we combine data from miniaturised acceleration loggers on 58 free-living Adélie penguins with doubly labelled water (DLW) measurements of their energy expenditure over several days. Across different behaviours, both in water and on land, dynamic body acceleration was a good predictor of independently measured DLW-derived energy expenditure (R2 = 0.72). The most parsimonious model suggested different calibration coefficients are required to predict behaviours on land versus foraging behaviour in water (R2 = 0.75). Our results show that accelerometry can be used to reliably estimate energy expenditure in penguins, and we provide calibration equations for estimating metabolic rate across several behaviours in the wild.

Thermoregulatory Strategies of Diving Air-Breathing Marine Vertebrates: A Review

The aquatic habitat of marine “air-breathing” vertebrates provides a significant thermoregulatory challenge due to the high thermal conductivity of water. In addition to temperature changes across their range, air-breathing vertebrates experience temperature changes on the timescale of seconds to minutes as they perform dives to access two critical resources: air at the surface and food at depth. In response to these challenges, air-breathing vertebrates have developed morphological and physiological adaptations that align with their life histories and phylogenies and contribute to homeostasis. However, the physiological and behavioral mechanisms used to maintain thermal balance while diving is still poorly understood. The cardiovascular system is integral to the physiological responses associated with the dive response, exercise, digestion, and thermoregulation. The adjustments required to meet one physiological demand may not be compatible with another and can result in a potential conflict between the various physiological demands imposed on air-breathing divers. We reviewed the literature on thermoregulation while diving in an effort to synthesize our current understanding of the thermoregulatory strategies of diving air-breathing marine vertebrates. Studies have demonstrated that thermoregulatory strategies can involve the temporal separation of two conflicting responses, a compromise in the performance of one response over another, or coordination of synergistic responses. We hope that a review and synthesis of both laboratory and field studies will stimulate future research efforts at the intersection of thermoregulation and diving physiology. Expanding the use of physiological biologgers, particularly to understudied species, will enhance our understanding of how these animals coordinate various physiological demands to maintain homeostasis in a thermally challenging environment.

Age‐ and Muscle‐Specific Oxidative Stress Management Strategies in a Long‐Lived Diver, the Weddell Seal

The free radical theory of aging purports that the accumulation of cellular oxidative damage leads to aging. While this process is not expected to manifest in wild populations, which can suffer from early predation or injury‐induced mortality, physically active long‐lived mammals are a model in which cellular aging may occur. Air breathing divers such as seals experience repeated bouts of ischemia‐reperfusion, potentially exposing their tissues to oxidative stress and thus damage and accelerated aging. We have previously demonstrated that skeletal muscle cellular morphology “ages” in Weddell seals without a corresponding decrease in diving behavior. This suggests stress response may protect against oxidative damage and functional impairment, providing insight into mechanisms for managing oxidative stress. We studied whether muscular senescence might arise from oxidative damage by comparing muscle from old (age 17–27 years) and young (age 9–16 years) cohorts of adult Weddell seals. Muscle biopsies were collected from healthy, active, non‐reproductive seals and frozen in liquid nitrogen. Apoptosis was examined with a cell‐death ELISA, while markers of oxidative damage to lipids (FOX assay) and proteins (4‐HNE western blot) were contrasted with antioxidant profiles (kinetic activity assays or western blots). These variables were statistically compared between age cohorts with an ANOVA model that included animal sex and biopsy site as cofactors. Old seals exhibited a 43% increase (p = 0.002) in apoptosis over young animals. Lipid peroxidation and oxidative protein damage, however, did not differ with age, suggesting that apoptotic differences were not due to oxidative stress. We also assessed antioxidant profiles and found that glutathione peroxidase (GPx) activity was 22% higher in the old cohort (p = 0.026). GPx reduces lipid hydroperoxides; this enhanced antioxidant protection may limit lipid peroxidation and downstream protein modification in old seals. The locomotory (longissimus dorsi, LD) and maneuvering (pectoralis, P) muscles of Weddell seals are perfused differently from one another during a dive, thus we also considered whether oxidative damage and antioxidant patterns are distinct between muscles using the same ANOVA. Lipid peroxidation was highest in LD (24% increase, p = 0.001), though no difference in protein modification was detected. Antioxidant protein levels revealed increased superoxide dismutase (SOD2, p = 0.009), thioredoxin reductase (TRXR2, p = 0.027) and heat shock protein 70 (HSP70, p = 0.00001) in LD. On the other hand, P exhibited a 14% increase in glutathione S‐transferase (GST, p = 0.004), which is consistent with regionally lower levels of oxidized lipid. Together, these findings illustrate that long‐lived air breathing divers display enhanced antioxidant and stress responses, possibly utilizing the pre‐conditioning effect of repeated diving. Thus, the aging Weddell seal is a compelling model for studying the successful management of oxidative stress.Support or Funding InformationNational Science Foundation Office of Polar ProgramsThis abstract is from the Experimental Biology 2018 Meeting. There is no full text article associated with this abstract published in The FASEB Journal.

Surfacers change their dive tactics depending on the aim of the dive: evidence from simultaneous measurements of breaths and energy expenditure.

Air-breathing divers are assumed to have evolved to apportion their time between surface and underwater periods to maximize the benefit gained from diving activities. However, whether they change their time allocation depending on the aim of the dive is still unknown. This may be particularly crucial for 'surfacers' because they dive for various purposes in addition to foraging. In this study, we counted breath events at the surface and estimated oxygen consumption during resting, foraging and other dives in 11 green turtles (Chelonia mydas) in the wild. Breath events were counted by a head-mounted acceleration logger or direct observation based on an animal-borne video logger, and oxygen consumption was estimated by measuring overall dynamic body acceleration. Our results indicate that green turtles maximized their submerged time, following this with five to seven breaths to replenish oxygen for resting dives. However, they changed their dive tactic during foraging and other dives; they surfaced without depleting their estimated stores of oxygen, followed by only a few breaths for effective foraging and locomotion. These dichotomous surfacing tactics would be the result of behavioural modifications by turtles depending on the aim of each dive.

Variable wind, pack ice, and prey dispersion affect the long‐term adequacy of protected areas for an Arctic sea duck

With changing climate, delineation of protected areas for sensitive species must account for long-term variability and geographic shifts of key habitat elements. Projecting the future adequacy of protected areas requires knowing major factors that drive such changes, and how readily the animals adjust to altered resources. In the Arctic, the viability of habitats for marine birds and mammals often depends on sea ice to dissipate storm waves and provide platforms for resting. However, some wind conditions (including weak winds during extreme cold) can consolidate pack ice into cover so dense that air-breathing divers are excluded from the better feeding areas. Spectacled Eiders (Somateria fischeri) winter among leads (openings) in pack ice in areas where densities of their bivalve prey are quite high. During winter 2009, however, prevailing winds created a large region of continuous ice with inadequate leads to allow access to areas of dense preferred prey. Stable isotope and fatty acid biomarkers indicated that, under these conditions, the eiders did not diversify their diet to include abundant non-bivalve taxa but did add a smaller, less preferred, bivalve species. Consistent with a computer model of eider energy balance, the body fat of adult eiders in 2009 was 33-35% lower than on the same date (19 March) in 2001 when ice conditions allowed access to higher bivalve densities. Ice cover data suggest that the eiders were mostly excluded from areas of high bivalve density from January to March in about 30% of 14 winters from 1998 to 2011. Thus, even without change in total extent of ice, shifts in prevailing winds can alter the areal density of ice to reduce access to important habitats. Because changes in wind-driven currents can also rearrange the dispersion of prey, the potential for altered wind patterns should be an important concern in projecting effects of climate change on the adequacy of marine protected areas for diving endotherms in the Arctic.

The regularity of dive performance in sea turtles: a new perspective from precise activity data

Air-breathing divers are assumed to dive and surface in a way that maximizes their realized benefit. Dive duration in diving animals seems to depend on the purpose of the dive. Although the purpose of dives in most marine mammals and birds is undoubtedly foraging, this is not always true for so-called ‘surfacers’ that spend most of their time underwater for various purposes (e.g. foraging, resting, mating and migration). In this study, we investigated the relationships among dive duration, the amount of activity per unit time, the air volume in the lungs and postdive surface duration of four hawksbill turtles, Eretmochelys imbricata, which are surfacers, using multisensor data loggers. Our results demonstrated that hawksbills generally perform dives with consistent relationships between dive duration, the amount of activity per unit time and the air volume in the lungs, and that dives are followed by short periods at the surface, indicating that hawksbills rarely perform anaerobic dives. This longer dive duration compared to the length of surface resting indicates that the diving strategy of hawksbill turtles maximizes their time spent submerged. This strategy seems unique to sea turtles and surfacers in general.

Adaptations for marine habitat and the effect of Triassic and Jurassic predator pressure on development of decompression syndrome in ichthyosaurs

Decompression syndrome (caisson disease or the "the bends") resulting in avascular necrosis has been documented in mosasaurs, sauropterygians, ichthyosaurs, and turtles from the Middle Jurassic to Late Cretaceous, but it was unclear that this disease occurred as far back as the Triassic. We have examined a large Triassic sample of ichthyosaurs and compared it with an equally large post-Triassic sample. Avascular necrosis was observed in over 15% of Late Middle Jurassic to Cretaceous ichthyosaurs with the highest occurrence (18%) in the Early Cretaceous, but was rare or absent in geologically older specimens. Triassic reptiles that dive were either physiologically protected, or rapid changes of their position in the water column rare and insignificant enough to prevent being recorded in the skeleton. Emergency surfacing due to a threat from an underwater predator may be the most important cause of avascular necrosis for air-breathing divers, with relative frequency of such events documented in the skeleton. Diving in the Triassic appears to have been a "leisurely" behavior until the evolution of large predators in the Late Jurassic that forced sudden depth alterations contributed to a higher occurrence of bends.

Measuring energy expenditure in sub-adult and hatchling sea turtles via accelerometry.

Measuring the metabolic of sea turtles is fundamental to understanding their ecology yet the presently available methods are limited. Accelerometry is a relatively new technique for estimating metabolic rate that has shown promise with a number of species but its utility with air-breathing divers is not yet established. The present study undertakes laboratory experiments to investigate whether rate of oxygen uptake ( o 2) at the surface in active sub-adult green turtles Chelonia mydas and hatchling loggerhead turtles Caretta caretta correlates with overall dynamic body acceleration (ODBA), a derivative of acceleration used as a proxy for metabolic rate. Six green turtles (25–44 kg) and two loggerhead turtles (20 g) were instrumented with tri-axial acceleration logging devices and placed singly into a respirometry chamber. The green turtles were able to submerge freely within a 1.5 m deep tank and the loggerhead turtles were tethered in water 16 cm deep so that they swam at the surface. A significant prediction equation for mean o 2 over an hour in a green turtle from measures of ODBA and mean flipper length (R2 = 0.56) returned a mean estimate error across turtles of 8.0%. The range of temperatures used in the green turtle experiments (22–30°C) had only a small effect on o 2. A o 2-ODBA equation for the loggerhead hatchling data was also significant (R2 = 0.67). Together these data indicate the potential of the accelerometry technique for estimating energy expenditure in sea turtles, which may have important applications in sea turtle diving ecology, and also in conservation such as assessing turtle survival times when trapped underwater in fishing nets.

Buoyed up and slowed down: speed limits for diving birds in shallow water

In air-breathing animals, the time and energy costs of each dive are primarily deter- mined by depth-related upthrust, swim speed and temperature. While studies have previously investigated how animals should optimise their behaviour in relation to either upthrust or speed they have rarely been examined in tandem. We took overall dynamic body acceleration (ODBA) as a proxy for the mechanical power used during the bottom phases of dives of imperial shags Phalacrocorax atriceps, as these birds forage benthically, in order to define: (1) the minimum power required for swimming at depth and (2) how the use of power above this threshold varied with dive depth. Results showed that ODBA declined with increasing dive depth in a manner cor- related with the reduction in upthrust, and that the use of power above that required for prey searching increased with increasing dive depth. This may constitute a response to depth-related patterns in prey availability. We present a model to investigate an alternative hypothesis that the ability of birds to produce burst speeds is also inversely related to the power required to counter buoyancy. Under the model assumptions, achievable burst speeds vary up to 0.7 m s -1 across dive depths from 5 to 60 m. Ultimately, prey preferences cannot be separated from prey fields, but we suggest that this model may provide insight into the ability of air-breathing divers to pursue vari- ous prey types according to dive depth.

Prolonged deep dives by the leatherback turtle Dermochelys coriacea: pushing their aerobic dive limits

Air-breathing diving animals are capable of maintaining activity during prolonged dives fuelled by on-board oxygen stores. Leatherback turtles ( Dermochelys coriacea ) perform the deepest and longest dives among sea turtles, and are among the most prolific air-breathing divers. Here we report the longest dive duration for D. coriacea during an extremely deep dive (1186 m) that lasted 86.5 minutes. This dive duration exceeded previously published calculated aerobic dive limits by almost two-fold and extends our knowledge of the diving capacity of this species.

The Scaling of Diving Time Budgets: Insights from an Optimality Approach

Simple scaling arguments suggest that, among air-breathing divers, dive duration should scale approximately with mass to the one-third power. Recent phylogenetic analyses appear to confirm this. The same analyses showed that duration of time spent at the surface between dives has scaling very similar to that of dive duration, with the result that the ratio of dive duration to surface pause duration is approximately mass invariant. This finding runs counter to other arguments found in the diving literature that suggest that surface pause duration should scale more positively with mass, leading to a negative scaling of the dive-pause ratio. We use a published model of optimal time allocation in the dive cycle to show that optimal decisions can predict approximate mass invariance in the dive-pause ratio, especially if metabolism scales approximately with mass to the two-thirds power (as indicated by some recent analyses) and oxygen uptake is assumed to have evolved to supply the body tissues at the required rate. However, emergent scaling rules are sensitive to input parameters, especially to the relationship between the scaling of metabolism and oxygen uptake rate at the surface. Our results illustrate the utility of an optimality approach for developing predictions and identifying key areas for empirical research on the allometry of diving behavior.

How long does a dive last? Foraging decisions by breath-hold divers in a patchy environment: a test of a simple model

Many theoretical models have been proposed to explain and predict the behaviour of air-breathing divers exploiting a food resource underwater. Many field observations of the behaviour of divers do not fit with the prediction that to maximize energetic gain divers should dive close to their aerobic diving limits. In an attempt to explain this paradox, Thompson & Fedak (2001, Animal Behaviour, 61, 286–297) proposed a model of diving behaviour that takes into account patchily distributed prey patches of varying quality. We tested this model experimentally in a simulated foraging set-up. We measured the diving behaviour of grey seals, Halichoerus grypus, diving to patches of varying prey density and distance from the surface. Our results were equivocal with respect to the model predictions. Seals responded to prey density, leaving low-quality patches earlier. However, this pattern was still evident at long dive distances, contrary to the prediction that during deep dives seals should stay at a patch regardless of prey density. While seals maximized dive durations at high prey densities and long distances, they did not do so at short distances. The apparent quitting strategy of the seals always produced higher net rates of energy gain than would have been achieved if they had remained at the foraging site up to their aerobic dive limit on every dive. These results indicate that seals' diving behaviour, particularly bottom duration, may indicate the relative prey availability in their environment.

A novel technique for measuring heart rate in a free swimming marine vertebrate

A mouth opening sensor incorporating a magnet and Hall sensor attached to a data logging unit was used to monitor the breathing and foraging behavior of a free-swimming leatherback sea turtle ( Dermochelys coriacea). Analysis of these data revealed a rhythmic low amplitude oscillation. Further investigation of the frequency of this signal lead us to believe that the movements (< 0.1 mm) are caused by the movement of blood through the nearby blood vessels. Putative heart rate decreased during dive descent and increased considerably during dive ascent reflecting the bradycardia and anticipatory tachycardia recorded by other means in other air-breathing divers. Oscillation frequencies were also comparable to the heart rate recorded in leatherbacks by means of implanted electrodes. We therefore propose that this device which was already known to reliably record behaviour such as breathing, feeding and buccal oscillations in sea turtles also has potential for recording other signals which cause movement on the external surface of an animal.

Optimal descent angles for shallow-diving cormorants

Air-breathing divers should attempt to maximize foraging efficiency under the constraint of limited oxygen availability. For diving water birds, high buoyancy (owing to the air in the plumage) and the associated change in buoyancy with diving depth impose further constraints on the adaptation to aquatic life. Diving birds are expected to descend as fast as possible to escape the higher buoyancy near the water surface, but in practice, shallow-diving cormorants (genus Phalacrocorax Brisson, 1760) are often observed descending the water column in relatively small angles with respect to the water surface. We derive a theoretical biomechanical model for the energetics of the descent phase of a dive of foot-propelled cormorants feeding on benthic prey at shallow depth. The model shows that visually guided benthic feeders benefit energetically from diving at small descent angles when optical conditions and bottom depth allow. The model also explains the high variation in descent angles observed in free-ranging birds, as well as the observed correlation between descent angle and bottom depth in cormorants.

Body density affects stroke patterns in Baikal seals

Buoyancy is one of the primary external forces acting on air-breathing divers and it can affect their swimming energetics. Because the body composition of marine mammals (i.e. the relative amounts of lower-density lipid and higher-density lean tissue) varies individually and seasonally, their buoyancy also fluctuates widely, and individuals would be expected to adjust their stroke patterns during dives accordingly. To test this prediction, we attached acceleration data loggers to four free-ranging Baikal seals Phoca sibirica in Lake Baikal and monitored flipper stroking activity as well as swimming speed, depth and inclination of the body axis (pitch). In addition to the logger, one seal (Individual 4) was equipped with a lead weight that was jettisoned after a predetermined time period so that we had a set of observations on the same individual with different body densities. These four data sets revealed the general diving patterns of Baikal seals and also provided direct insights into the influence of buoyancy on these patterns. Seals repeatedly performed dives of a mean duration of 7.0 min (max. 15.4 min), interrupted by a mean surface duration of 1.2 min. Dive depths were 66 m on average, but varied substantially, with a maximum depth of 324 m. The seals showed different stroke patterns among individuals; some seals stroked at lower rates during descent than ascent, while the others had higher stroke rates during descent than ascent. When the lead weight was detached from Individual 4, the seal increased its stroke rate in descent by shifting swimming mode from prolonged glides to more stroke-and-glide swimming, and decreased its stroke rate in ascent by shifting from continuous stroking to stroke-and-glide swimming. We conclude that seals adopt different stroke patterns according to their individual buoyancies. We also demonstrate that the terminal speed reached by Individual 4 during prolonged glide in descent depended on its total buoyancy and pitch, with higher speeds reached in the weighted condition and at steeper pitch. A simple physical model allowed us to estimate the body density of the seal from the speed and pitch (1,027-1,046 kg m(-3), roughly corresponding to 32-41% lipid content, for the weighted condition; 1,014-1,022 kg m(-3), 43-47% lipid content, for the unweighted condition).

THE IMPLICATIONS OF LUNG-REGULATED BUOYANCY CONTROL FOR DIVE DEPTH AND DURATION

Among air-breathing divers, control of buoyancy through lung volume regulation may be most highly developed in marine turtles. In short, the turtle lung may serve a dual role as both an oxygen store and in buoyancy control. A simple model is developed to show that, for turtles diving up to the maximum depth at which they can still use their lungs to attain neutral buoyancy, the total oxygen store will increase greatly with dive depth, and hence a corresponding increase in dive duration is predicted. Time–depth recorders attached to free-living green turtles (Chelonia mydas) at Ascension Island confirmed a marked increase in dive duration with depth, with the gradient of this relationship being >10 times that seen in diving birds and mammals. Consistent with the prediction that the lungs serve a dual role, we found that, when lead weights were added to some turtles to increase their specific gravity, the mean depth of dives decreased, but for dives to the same depth, weighted animals dived for longer. The depth distribution of green turtles seems to be generally constrained by the maximum depth at which they can still attain close to neutral buoyancy.

First records of flipper beat frequency during sea turtle diving

Depth and flipper movements were simultaneously measured during 23 dives for a free-swimming green turtle ( Chelonia mydas) at Ascension Island. A few characteristic dive profiles that have been widely reported in hard-shelled turtles were recorded. Flipper movements revealed that, on dives to midwater, there was generally active swimming, compared to long periods of inactivity on dives to the seafloor. During all dives, there were clear changes in the flipper beat frequency during the descent. On leaving the surface, flippers beats occurred quickly (typically 30–40 beats min −1) and then as the descent continued the frequency declined (typically to about 10–14 beats min −1). These observations match the general pattern reported for other air-breathing divers for increased effort at the start of the descent to overcome initial positive buoyancy.

Testing optimal foraging models for air-breathing divers

Models of diving optimality qualitatively predict diving behaviours of aquatic birds and mammals. However, none of them has been empirically tested. We examined the quantitative predictions of optimal diving models by combining cumulative oxygen uptake curves with estimates of power costs during the dives of six tufted ducks, Aythya fuligula. The effects of differing foraging costs on dive duration and rate of oxygen uptake (VO2up) at the surface were measured during bouts of voluntary dives to a food tray. The birds were trained to surface into a respirometer after each dive, so that changes in VO2up over time could be measured. The tray held either just food or closely packed stones on top of the food to make foraging energetically more costly. In contrast to predictions from the Houston & Carbone model, foraging time (tf) increased after dives incorporating higher foraging energy costs but surface time (ts) remained the same. While optimal diving models have assumed that the cumulative oxygen uptake curve is fixed, VO2up increased when the energy cost of the dive increased. The optimal breathing model quantitatively predicted ts in both conditions and oxygen consumption during foraging (m2tf) in the control condition, for the mean of all ducks. This offers evidence that the ducks were diving optimally and supports the fundamentals of optimal diving theory. However, the model did not consistently predictts or m2tf for individual birds. We discuss the limits of optimal foraging models for air-breathing divers caused by individual variation. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.

Task performance under water: An evaluation of manual dexterity efficiency in the open ocean underwater environment

The present review examines studies which have reported on the performance of submerged operators on manual dexterity tasks in the practical arena of the open ocean underwater environment. The previous emphasis on the primacy of the factor situational anxiety, in degrading efficiency, is questioned. The case for environmentally-based factors and performer skill level as potent influences on performance is advanced. In postulating a potential linear relationship between depth of operation and performance decrement for air-breathing divers, the review seeks to stimulate further experimental examination of this important applied issue.