Improving estimates of diving lung volume in air-breathing marine vertebrates

The air volume in the respiratory system of marine tetrapods provides a store of O2 to fuel aerobic metabolism during dives; however, it can also be a liability, as the associated N2 can increase the risk of decompression sickness. In order to more fully understand the physiological limitations of different air-breathing marine vertebrates, it is therefore important to be able to accurately estimate the air volume in the respiratory system during diving. One method that has been used to do so is to calculate the air volume from glide phases - periods of movement during which no thrust is produced by the animal - which many species conduct during ascent periods, when gases are expanding owing to decreasing hydrostatic pressure. This method assumes that there is conservation of mass in the respiratory system, with volume changes only driven by pressure. In this Commentary, we use previously published data to argue that both the respiratory quotient and differences in tissue and blood gas solubility potentially alter the mass balance in the respiratory system throughout a dive. Therefore, near the end of a dive, the measured volume of gas at a given pressure may be 12-50% less than from the start of the dive; the actual difference will depend on the length of the dive, the cardiac output, the pulmonary shunt and the metabolic rate. Novel methods and improved understanding of diving physiology will be required to verify the size of the effects described here and to more accurately estimate the volume of gas inhaled at the start of a dive.Publisher PDFPeer reviewe

How do marine mammals manage and usually avoid gas emboli formation and gas embolic pathology? critical clues from studies of wild dolphins

© The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Fahlman, A., Moore, M. J., & Wells, R. S. How do marine mammals manage and usually avoid gas emboli formation and gas embolic pathology? critical clues from studies of wild dolphins. Frontiers in Marine Science, 8, (2021): 598633, https://doi.org/10.3389/fmars.2021.598633.Decompression theory has been mainly based on studies on terrestrial mammals, and may not translate well to marine mammals. However, evidence that marine mammals experience gas bubbles during diving is growing, causing concern that these bubbles may cause gas emboli pathology (GEP) under unusual circumstances. Marine mammal management, and usual avoidance, of gas emboli and GEP, or the bends, became a topic of intense scientific interest after sonar-exposed, mass-stranded deep-diving whales were observed with gas bubbles. Theoretical models, based on our current understanding of diving physiology in cetaceans, predict that the tissue and blood N2 levels in the bottlenose dolphin (Tursiops truncatus) are at levels that would result in severe DCS symptoms in similar sized terrestrial mammals. However, the dolphins appear to have physiological or behavioral mechanisms to avoid excessive blood N2 levels, or may be more resistant to circulating bubbles through immunological/biochemical adaptations. Studies on behavior, anatomy and physiology of marine mammals have enhanced our understanding of the mechanisms that are thought to prevent excessive uptake of N2. This has led to the selective gas exchange hypothesis, which provides a mechanism how stress-induced behavioral change may cause failure of the normal physiology, which results in excessive uptake of N2, and in extreme cases may cause formation of symptomatic gas emboli. Studies on cardiorespiratory function have been integral to the development of this hypothesis, with work initially being conducted on excised tissues and cadavers, followed by studies on anesthetized animals or trained animals under human care. These studies enabled research on free-ranging common bottlenose dolphins in Sarasota Bay, FL, and off Bermuda, and have included work on the metabolic and cardiorespiratory physiology of both shallow- and deep-diving dolphins and have been integral to better understand how cetaceans can dive to extreme depths, for long durations.Many of the studies that have resulted in the data in this review, and that have been integral to develop the selective gas exchange hypothesis have been funded by the Office of Naval Research (ONR Awards # N000141010159, N000141613088, N000141410563, N000140811220, and ONR YIP Award # N000141410563), and Dolphin Quest. The authors declare that Dolphin Quest was not involved in the study design, collection, analysis, interpretation of data, the writing of this article or the decision to submit it for publication

Pulmonary ventilation–perfusion mismatch : a novel hypothesis for how diving vertebrates may avoid the bends

© The Author(s), 2018. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Proceedings of the Royal Society B: Biological Sciences 285 (2018): 20180482, doi:10.1098/rspb.2018.0482.Hydrostatic lung compression in diving marine mammals, with collapsing alveoli blocking gas exchange at depth, has been the main theoretical basis for limiting N2 uptake and avoiding gas emboli (GE) as they ascend. However, studies of beached and bycaught cetaceans and sea turtles imply that air-breathing marine vertebrates may, under unusual circumstances, develop GE that result in decompression sickness (DCS) symptoms. Theoretical modelling of tissue and blood gas dynamics of breath-hold divers suggests that changes in perfusion and blood flow distribution may also play a significant role. The results from the modelling work suggest that our current understanding of diving physiology in many species is poor, as the models predict blood and tissue N2 levels that would result in severe DCS symptoms (chokes, paralysis and death) in a large fraction of natural dive profiles. In this review, we combine published results from marine mammals and turtles to propose alternative mechanisms for how marine vertebrates control gas exchange in the lung, through management of the pulmonary distribution of alveolar ventilation (Embedded Image) and cardiac output/lung perfusion (Embedded Image), varying the level of Embedded Image in different regions of the lung. Man-made disturbances, causing stress, could alter the Embedded Image mismatch level in the lung, resulting in an abnormally elevated uptake of N2, increasing the risk for GE. Our hypothesis provides avenues for new areas of research, offers an explanation for how sonar exposure may alter physiology causing GE and provides a new mechanism for how air-breathing marine vertebrates usually avoid the diving-related problems observed in human divers.Funding to support a portion of this work was obtained by the Fundación Oceanogràfic and by the Office of Naval Research (ONR YIP Award no. N000141410563 and Award no. N000140811220)

Resting metabolic rate and lung function in wild offshore common bottlenose dolphins, Tursiops truncatus, near Bermuda

© The Author(s), 2018. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Frontiers in Physiology 9 (2018): 886, doi:10.3389/fphys.2018.00886.Diving mammals have evolved a suite of physiological adaptations to manage respiratory gases during extended breath-hold dives. To test the hypothesis that offshore bottlenose dolphins have evolved physiological adaptations to improve their ability for extended deep dives and as protection for lung barotrauma, we investigated the lung function and respiratory physiology of four wild common bottlenose dolphins (Tursiops truncatus) near the island of Bermuda. We measured blood hematocrit (Hct, %), resting metabolic rate (RMR, l O2 ⋅ min-1), tidal volume (VT, l), respiratory frequency (fR, breaths ⋅ min-1), respiratory flow (l ⋅ min-1), and dynamic lung compliance (CL, l ⋅ cmH2O-1) in air and in water, and compared measurements with published results from coastal, shallow-diving dolphins. We found that offshore dolphins had greater Hct (56 ± 2%) compared to shallow-diving bottlenose dolphins (range: 30–49%), thus resulting in a greater O2 storage capacity and longer aerobic diving duration. Contrary to our hypothesis, the specific CL (sCL, 0.30 ± 0.12 cmH2O-1) was not different between populations. Neither the mass-specific RMR (3.0 ± 1.7 ml O2 ⋅ min-1 ⋅ kg-1) nor VT (23.0 ± 3.7 ml ⋅ kg-1) were different from coastal ecotype bottlenose dolphins, both in the wild and under managed care, suggesting that deep-diving dolphins do not have metabolic or respiratory adaptations that differ from the shallow-diving ecotypes. The lack of respiratory adaptations for deep diving further support the recently developed hypothesis that gas management in cetaceans is not entirely passive but governed by alteration in the ventilation-perfusion matching, which allows for selective gas exchange to protect against diving related problems such as decompression sickness.Funding for this project was provided by the Office of Naval Research (ONR YIP Award No. N000141410563, and Dolphin Quest, Inc. FHJ was supported by the Office of Naval Research (Award No. N00014-1410410) and an AIAS-COFUND fellowship from Aarhus Institute of Advanced Studies under the FP7 program of the EU (Agreement No. 609033)

Modeling tissue and blood gas kinetics in coastal and offshore common bottlenose dolphins, Tursiops truncatus

AF (N00014-17-1-2756), PT (N000141512553) and FHJ (N00014-14-1-0410) were supported by the Office of Naval Research, and FHJ by an AIASCOFUND fellowship from Aarhus Institute of Advanced Studies, Aarhus University, under EU's FP7 program (Agreement No. 609033). PT received funding from the MASTS pooling initiative (The Marine Alliance for Science and Technology for Scotland) and their support is gratefully acknowledged. MASTS is funded by the Scottish Funding Council (grant reference HR09011) and contributing institutions. Funding for the Sarasota Bay and Bermuda field-work was provided by Dolphin Quest, Inc., and Office of Naval Research (N00014-14-1-0563).Bottlenose dolphins (Tursiops truncatus) are highly versatile breath-holding predators that have adapted to a wide range of foraging niches from rivers and coastal ecosystems to deep-water oceanic habitats. Considerable research has been done to understand how bottlenose dolphins manage O2 during diving, but little information exists on other gases or how pressure affects gas exchange. Here we used a dynamic multi-compartment gas exchange model to estimate blood and tissue O2, CO2, and N2 from high-resolution dive records of two different common bottlenose dolphin ecotypes inhabiting shallow (Sarasota Bay) and deep (Bermuda) habitats. The objective was to compare potential physiological strategies used by the two populations to manage shallow and deep diving life styles. We informed the model using species-specific parameters for blood hematocrit, resting metabolic rate, and lung compliance. The model suggested that the known O2 stores were sufficient for Sarasota Bay dolphins to remain within the calculated aerobic dive limit (cADL), but insufficient for Bermuda dolphins that regularly exceeded their cADL. By adjusting the model to reflect the body composition of deep diving Bermuda dolphins, with elevated muscle mass, muscle myoglobin concentration and blood volume, the cADL increased beyond the longest dive duration, thus reflecting the necessary physiological and morphological changes to maintain their deep-diving life-style. The results indicate that cardiac output had to remain elevated during surface intervals for both ecotypes, and suggests that cardiac output has to remain elevated during shallow dives in-between deep dives to allow sufficient restoration of O2 stores for Bermuda dolphins. Our integrated modeling approach contradicts predictions from simple models, emphasizing the complex nature of physiological interactions between circulation, lung compression, and gas exchange.Publisher PDFPeer reviewe

Editorial: Ecology and behaviour of free-ranging animals studied by advanced data-logging and tracking techniques

© The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Wassmer, T., Jensen, F. H., Fahlman, A., & Murray, D. L. Editorial: Ecology and behaviour of free-ranging animals studied by advanced data-logging and tracking techniques. Frontiers in Ecology and Evolution, 8, (2020): 113, doi:10.3389/fevo.2020.00113.Many details of the behavior, life history and eco-physiology of animals, even among intensively-studied species, remain unknown. Direct observation is a laborious process only amenable for accessible and non-cryptic species, whereas traditional radio telemetry does not directly provide information on the diversity and complexity of animal physiology and behavior. Further, both methods are laborious and/or expensive, and may lead to biased data when physiology and/or behaviors are altered by marking or tracking (Boyer-Ontl and Pruetz, 2014; Nowak et al., 2014; Welch et al., 2018; see also Le Grand et al.). Ultimately, these methods provide only a fragmentary overview of animal behavior patterns during periods when individuals can be readily detected and surveyed while leaving activities during other times obscured. However, the ongoing miniaturization, sensor development, and increased affordability of data logging and advanced telemetric devices offers the potential for continuous and intensive data collection, thereby potentially allowing researchers to more rigorously investigate both physiology and behavior of animals that are difficult to study using traditional observational methods. Owing to these new technologies, we are at the cusp of a truly revolutionary opportunity to address important and longstanding knowledge gaps in animal eco-physiology. To that end, the special section entitled Ecology and Behaviour of Free-Ranging Animals Studied by Advanced Data-Logging and Tracking Techniques includes 22 papers that report on and quantify otherwise hidden aspects of the biology of a variety of mammals, birds, and even invertebrates, across diverse environments including land, water, and air. The highlighted studies focus on fields ranging from basic animal behavior and ecology to eco-physiology; several papers adopt an integrative approach, providing a rather comprehensive understanding of individual time budgets and their implications. Ultimately and collectively, these contributions serve as testament to the drastic improvement in the level of ecological inference that can be derived from research studies involving the use of data-logging and tracking devices that are currently available

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

Using Respiratory Sinus Arrhythmia to Estimate Inspired Tidal Volume in the Bottlenose Dolphin (Tursiops truncatus)

Man-made environmental change may have significant impact on apex predators, like marine mammals. Thus, it is important to assess the physiological boundaries for survival in these species, and assess how climate change may affect foraging efficiency and the limits for survival. In the current study, we investigated whether the respiratory sinus arrhythmia (RSA) could estimate tidal volume (VT) in resting bottlenose dolphins (Tursiops truncatus). For this purpose, we measured respiratory flow and electrocardiogram (ECG) in five adult bottlenose dolphins at rest while breathing voluntarily. Initially, an exponential decay function, using three parameters (baseline heart rate, the change in heart rate following a breath, and an exponential decay constant) was used to describe the temporal change in instantaneous heart rate following a breath. The three descriptors, in addition to body mass, were used to develop a Generalized Additive Model (GAM) to predict the inspired tidal volume (VTinsp). The GAM allowed us to predict VTinsp with an average ( ± SD) overestimate of 3 ± 2%. A jackknife sensitivity analysis, where 4 of the five dolphins were used to fit the GAM and the 5th dolphin used to make predictions resulted in an average overestimate of 2 ± 10%. Future studies should be used to assess whether similar relationships exist in active animals, allowing VT to be studied in free-ranging animals provided that heart rate can be measured

Hyperbaric tracheobronchial compression in cetaceans and pinnipeds

Author Posting. © Company of Biologists, 2020. This article is posted here by permission of Company of Biologists for personal use, not for redistribution. The definitive version was published in Journal of Experimental Biology 223 (2020): jeb217885, doi:10.1242/jeb.217885.Assessment of the compressibility of marine mammal airways at depth is crucial to understanding vital physiological processes such as gas exchange during diving. Very few studies have directly assessed changes in cetacean and pinniped tracheobronchial shape, and none have quantified changes in volume with increasing pressure. A harbor seal, gray seal, harp seal, harbor porpoise and common dolphin were imaged promptly post mortem via computed tomography in a radiolucent hyperbaric chamber. Volume reconstructions were performed of segments of the trachea and bronchi of the pinnipeds and bronchi of the cetaceans for each pressure treatment. All specimens examined demonstrated significant decreases in airway volume with increasing pressure, with those of the harbor seal and common dolphin nearing complete collapse at the highest pressures. The common dolphin bronchi demonstrated distinctly different compression dynamics between 50% and 100% lung inflation treatments, indicating the importance of air in maintaining patent airways, and collapse occurred caudally to cranially in the 50% treatment. Dynamics of the harbor seal and gray seal airways indicated that the trachea was less compliant than the bronchi. These findings indicate potential species-specific variability in airway compliance, and cessation of gas exchange may occur at greater depths than those predicted in models assuming rigid airways. This may potentially increase the likelihood of decompression sickness in these animals during diving.This research received no specific grant from any funding agency in the public, commercial or not-for-profit sectors.2021-02-1