Brian L. Bostrom

Estimating the effect of lung collapse and pulmonary shunt on gas exchange during breath-hold diving: The Scholander and Kooyman legacy

We developed a mathematical model to investigate the effect of lung compression and collapse (pulmonary shunt) on the uptake and removal of O(2), CO(2) and N(2) in blood and tissue of breath-hold diving mammals. We investigated the consequences of pressure (diving depth) and respiratory volume on pulmonary shunt and gas exchange as pressure compressed the alveoli. The model showed good agreement with previous studies of measured arterial O(2) tensions (Pa(O)(2)) from freely diving Weddell seals and measured arterial and venous N(2) tensions from captive elephant seals compressed in a hyperbaric chamber. Pulmonary compression resulted in a rapid spike in Pa(O)(2) and arterial CO(2) tension, followed by cyclical variation with a periodicity determined by Q(tot). The model showed that changes in diving lung volume are an efficient behavioural means to adjust the extent of gas exchange with depth. Differing models of lung compression and collapse depth caused major differences in blood and tissue N(2) estimates. Our integrated modelling approach contradicted predictions from simple models, and emphasised the complex nature of physiological interactions between circulation, lung compression and gas exchange. Overall, our work suggests the need for caution in interpretation of previous model results based on assumed collapse depths and all-or-nothing lung collapse models.

Deep diving mammals: Dive behavior and circulatory adjustments contribute to bends avoidance

A mathematical model was created that predicted blood and tissue N(2) tension (P(N2)) during breath-hold diving. Measured muscle P(N2) from the bottlenose dolphin after diving repeatedly to 100 m (Tursiops truncatus [Ridgway and Howard, 1979, Science, 4423, 1182-1183]) was compared with predictions from the model. Lung collapse was modelled as a 100% pulmonary shunt which yielded tissue P(N2) similar to those reported for the dolphin. On the other hand, predicted muscle P(N2) for an animal with a dive response, reducing cardiac output by 66% from surface values (20.5 to 6.8l x min(-1)), also agreed well with observed values in the absence of lung collapse. In fact, modelling indicated that both cardiovascular adjustments and dive behaviour are important in reducing N2 uptake during diving and enhancing safe transfer of tissue and blood N2 back to the lung immediately before coming to the surface. In particular, diving bradycardia during the descent and bottom phase together with a reduced ascent rate and increase in heart rate reduced mixed venous P(N2) upon return to the surface by as much as 45%. This has important implications as small reductions in inert gas load (approximately 5%) can substantially reduce decompression sickness (DCS) risk by as much as 50% (Fahlman et al., 2001, J. Appl. Physiol. 91, 2720-2729).

Tracheal compression delays alveolar collapse during deep diving in marine mammals

Marine mammals have very compliant alveoli and stiff upper airways; an adaptation that allows air to move from the alveoli into the upper airways, during breath-hold diving. Alveolar collapse is thought occur between 30 and 100 m and studies that have attempted to estimate gas exchange at depth have used the simplifying assumption that gas exchange ceases abruptly at the alveolar collapse depth. Here we develop a mathematical model that uses compliance values for the alveoli and upper airspaces, estimated from the literature, to predict volumes of the respiratory system at depth. Any compressibility of the upper airways decreases the volume to contain alveolar air yielding lung collapse pressures 2x that calculated assuming an incompressible upper airway. A simple relationship with alveolar volume was used to predict relative pulmonary shunt at depth. The results from our model agree with empirical data on gas absorption at depth as well as the degree of tracheal compression in forced and free diving mammals.

Calculating the ecological impacts of animal‐borne instruments on aquatic organisms

Summary 1. Animal-borne instruments provide researchers with valuable data to address important questions on wildlife ecology and conservation. However, these devices have known impacts on animal behaviour and energetics. Tags deployed on migrating animals may reduce reproductive output through increased energy demands or cause phenological mismatches of foraging and nesting events. For marine organisms, the only tagging guidelines that exist are based on lift and thrust impacts on birds – concepts that do not translate well to aquatic animals. Herein, we provide guidelines on assessing drag from animal-borne instruments and discuss the ecological impacts on marine organisms. Of particular concern is the effect of drag from instruments to the welfare of the animals and for the applicability of collected data to wild populations. 2. To help understand how drag from electronic tags affects marine animals in the wild, we used marine turtles as model aquatic organisms and conducted wind tunnel experiments to measure the fluid drag of various marine turtle body types with and without commercially available electronic tags (e.g. satellite, TDR, video cameras). We quantified the drag associated with carrying biotelemetry devices of varying frontal area and design (squared or tear drop shaped) and generated contour plots depicting percentage drag increase as a framework for evaluating tag drag by scientists and wildlife managers. Then, using concepts of fluid dynamics, we derived a universal equation estimating drag impacts from instruments across marine taxa. 3. The drag of the marine turtle casts was measured in wind speeds from 2 to 30 m s 1 (Re 30 9 10 4 – 19 9 10 6 ), equivalent to 01–1 9ms 1 in seawater. The drag coefficient (CD) of the marine turtles ranged from 011 to 022, which is typical of other large, air-breathing, marine vertebrates (008–026). The CD of tags in reference to the turtle casts was 091 018 and most tags caused minimal additional drag ( 100%). The sensitivity of aquatic animals to instrument drag is a dynamic relationship between the fluid flow patterns, or CD, and the frontal area ratio of the animal and tag. 4. In this paper, we have outlined methods for quantifying the drag costs from animal-borne instrumentation considering the instrument retention time (time to release from the animal) and the activity of the instrumented animal. With this valuable tool, researchers can quantify the drag costs from animal-borne instrumentation and choose appropriate tags for their intended study organism and question. Reducing drag will ultimately reduce the impact on the instrumented animals and lead to greater biological realism in the collected data.

Behaviour and Physiology: The Thermal Strategy of Leatherback Turtles

Background Adult leatherback turtles (Dermochelys coriacea) exhibit thermal gradients between their bodies and the environment of ≥8°C in sub-polar waters and ≤4°C in the tropics. There has been no direct evidence for thermoregulation in leatherbacks although modelling and morphological studies have given an indication of how thermoregulation may be achieved. Methodology/Principal Findings We show for the first time that leatherbacks are indeed capable of thermoregulation from studies on juvenile leatherbacks of 16 and 37 kg. In cold water (< 25°C), flipper stroke frequency increased, heat loss through the plastron, carapace and flippers was minimized, and a positive thermal gradient of up to 2.3°C was maintained between body and environment. In warm water (25 – 31°C), turtles were inactive and heat loss through their plastron, carapace and flippers increased. The thermal gradient was minimized (0.5°C). Using a scaling model, we estimate that a 300 kg adult leatherback is able to maintain a maximum thermal gradient of 18.2°C in cold sub-polar waters. Conclusions/Significance In juvenile leatherbacks, heat gain is controlled behaviourally by increasing activity while heat flux is regulated physiologically, presumably by regulation of blood flow distribution. Hence, harnessing physiology and behaviour allows leatherbacks to keep warm while foraging in cold sub-polar waters and to prevent overheating in a tropical environment.

Validation of the use of doubly labeled water for estimating metabolic rate in the green turtle (Chelonia mydas L.): a word of caution.

SUMMARY Marine turtles often have extremely high water turnover accompanied by a low field metabolic rate (FMR), a combination that can contraindicate the use of doubly labelled water (DLW). Therefore, we conducted a validation study to assess the suitability of the DLW technique for determining FMR of marine turtles. Six green turtles (22.42±3.13 kg) were injected with DLW and placed in a tank of seawater with a respirometer for continuous monitoring of oxygen consumption (MR) over a 5-day period. Trials were conducted for turtles in both fed and fasted states. Respiratory exchange ratio (RER) was determined in a dry respirometer and used to calculate energy expenditure. For fed and fasted turtles, total body water (TBW) was 66.67±3.37% and 58.70±7.63% of body mass, and water flux rates were 9.57±1.33% and 6.14±0.65% TBW day–1, respectively. Water turnover in fasted turtles was 36% lower than that of fed turtles but MR (from oxygen consumption) of fasted turtles (13.77±1.49 kJ kg–1 day–1) was 52% lower than in fed turtles (28.66±5.31 kJ kg–1 day–1). Deuterium to oxygen-18 turnover rate (kd:ko) ratios averaged 0.91±0.02 for fed turtles and 1.07±0.16 for fasted turtles. Fed turtles had a mean group difference of 8% and a mean individual difference of 53% between DLW and respirometry. The DLW method gave negative MR values in fasted turtles and could not be compared with respirometry data. Researchers should use caution when applying the DLW method in marine reptiles, especially when high water flux causes >90% of the labeled oxygen turnover to be due to water exchange.

Resource Requirements of the Pacific Leatherback Turtle Population

The Pacific population of leatherback sea turtles (Dermochelys coriacea) has drastically declined in the last 25 years. This decline has been linked to incidental capture by fisheries, egg and meat harvesting, and recently, to climate variability and resource limitation. Here we couple growth rates with feeding experiments and food intake functions to estimate daily energy requirements of leatherbacks throughout their development. We then estimate mortality rates from available data, enabling us to raise food intake (energy requirements) of the individual to the population level. We place energy requirements in context of available resources (i.e., gelatinous zooplankton abundance). Estimated consumption rates suggest that a single leatherback will eat upward of 1000 metric tonnes (t) of jellyfish in its lifetime (range 924–1112) with the Pacific population consuming 2.1×106 t of jellyfish annually (range 1.0–3.7×106) equivalent to 4.2×108 megajoules (MJ) (range 2.0–7.4×108). Model estimates suggest 2–7 yr-old juveniles comprise the majority of the Pacific leatherback population biomass and account for most of the jellyfish consumption (1.1×106 t of jellyfish or 2.2×108 MJ per year). Leatherbacks are large gelatinous zooplanktivores with consumption to biomass ratios of 96 (up to 192 if feeding strictly on low energy density Cnidarians); they, therefore, have a large capacity to impact gelatinous zooplankton landscapes. Understanding the leatherbacks needs for gelatinous zooplankton, versus the availability of these resources, can help us better assess population trends and the influence of climate induced resource limitations to reproductive output.

The Genetic Component of the Forced Diving Bradycardia Response in Mammals

We contrasted the forced diving bradycardia between two genetically similar (inbred) rat strains (Fischer and Buffalo), compared to that of outbred rats (Wistar). The animals were habituated to forced diving for 4 weeks. Each animal was then tested during one 40 s dive on each of 3 days. The heart rate (fH) was measured before, during, and after each dive. Fischer and Buffalo exhibited marked difference in dive bradycardia (Fischer: 120.9 ± 14.0 beats min−1 vs. Buffalo: 92.8 ± 12.8 beats min−1, P < 0.05). Outbred rats showed an intermediate response (103.0 ± 30.9 beats min−1) but their between-animal variability in mean dive fH and pre-diving resting fH were higher than the inbred strains (P < 0.05), which showed no difference (P > 0.05). The decreased variability in fH in inbred rats as compared with the outbred group indicates that reduced genetic variability minimizes variability of the diving bradycardia between individuals. Heritability within strains was assessed by the repeatability (R) index and was 0.93 ± 0.05 for the outbred, 0.84 ± 0.16 for Buffalo, and 0.80 ± 0.12 for Fischer rats for fH during diving. Our results suggest that a portion of the mammalian diving bradycardia may be a heritable trait.

To what extent might N2 limit dive performance in king penguins

SUMMARY A mathematical model was used to explore if elevated levels of N2, and risk of decompression sickness (DCS), could limit dive performance (duration and depth) in king penguins (Aptenodytes patagonicus). The model allowed prediction of blood and tissue (central circulation, muscle, brain and fat) N2 tensions (PN2) based on different cardiac outputs and blood flow distributions. Estimated mixed venous PN2 agreed with values observed during forced dives in a compression chamber used to validate the assumptions of the model. During bouts of foraging dives, estimated mixed venous and tissue PN2 increased as the bout progressed. Estimated mean maximum mixed venous PN2 upon return to the surface after a dive was 4.56±0.18 atmospheres absolute (ATA; range: 4.37–4.78 ATA). This is equivalent to N2 levels causing a 50% DCS incidence in terrestrial animals of similar mass. Bout termination events were not associated with extreme mixed venous N2 levels. Fat PN2 was positively correlated with bout duration and the highest estimated fat PN2 occurred at the end of a dive bout. The model suggested that short and shallow dives occurring between dive bouts help to reduce supersaturation and thereby DCS risk. Furthermore, adipose tissue could also help reduce DCS risk during the first few dives in a bout by functioning as a sink to buffer extreme levels of N2.