Andreas Fahlman

High-resolution dive depth and acceleration recordings
from nearshore (Sarasota Bay, dive depth < 30 m), and offshore
(Bermuda) bottlenose dolphins (Tursiops spp.) were
used to estimate the diving metabolic rate (DMR) and the
locomotor metabolic rate (LMR, L O2/min) during three
phases of diving (descent, bottom, and ascent). For shallow
dives (depth ≤ 30 m), we found no differences between the
two ecotypes in the LMR during diving, nor during the
postdive shallow interval between dives. For intermediate
(30 m < depth ≤ 100 m) and deep dives (depth > 100 m),
the LMR was significantly higher during ascent than during
descent and the bottom phase by 59% and 9%, respectively.
In addition, the rate of change in depth during descent and
ascent (meters/second) increased with maximal dive depth.
The dynamic aerobic dive limit (dADL) was calculated from
the estimated DMR and the estimated predive O2 stores.
For the Bermuda dolphins, the dADL decreased with dive
depth, and was 18.7, 15.4, and 11.1 min for shallow, intermediate,
and deep dives, respectively. These results provide a useful approach to understand the complex nature of
physiological interactions between aerobic metabolism,
energy use, and diving capacity.

While basal metabolic rate (BMR) scales proportionally with body mass (Mb), it remains unclear whether the relationship differs between mammals from aquatic and terrestrial habitats. We hypothesized that differences in BMR allometry would be reflected in similar differences in scaling of O2 delivery pathways through the cardiorespiratory system. We performed a comparative analysis of BMR across 63 mammalian species (20 aquatic, 43 terrestrial) with a Mb range from 10 kg to 5318 kg. Our results revealed elevated BMRs in small (>10 kg and <100 kg) aquatic mammals compared to small terrestrial mammals. The results demonstrated that minute ventilation, that is, tidal volume (VT)·breathing frequency (fR), as well as cardiac output, that is, stroke volume·heart rate, do not differ between the two habitats. We found that the “aquatic breathing strategy”, characterized by higher VT and lower fR resulting in a more effective gas exchange, and by elevated blood hemoglobin concentrations resulting in a higher volume of O2 for the same volume of blood, supported elevated metabolic requirements in aquatic mammals. The results from this study provide a possible explanation of how differences in gas exchange may serve energy demands in aquatic versus terrestrial mammals.

The dive response is well documented for marine mammals, and includes a significant reduction in heart rate (f H) during submersion as compared while breathing at the surface. In the current study we assessed the influence of the Respiratory Sinus Arrhythmia (RSA) while estimating the resting f H while breathing. Using transthoracic echocardiography we measured f H , and stroke volume (SV) during voluntary surface apneas at rest up to 255 s, and during recovery from apnea in 11 adult bottlenose dolphins (Tursiops truncatus, 9 males and 2 females, body mass range: 140-235 kg). The dolphins exhibited a significant post-respiratory tachycardia and increased SV. Therefore, only data after this RSA had stabilized were used for analysis and comparison. The average (±s.d.) f H , SV, and cardiac output (CO) after spontaneous breaths while resting at the surface were 44 ± 6 beats min −1 , 179 ± 31 ml, and 7909 ± 1814 l min −1 , respectively. During the apnea the f H , SV, and CO decreased pr...

: The objective of this study is to update a current gas dynamics model with recently acquired data for respiratory compliance (P-V), and body compartment size estimates in California sea lions. The model will be calibrated against measured arterial and venous PO2 levels from California sea lions, and estimate the error between predicted and observed values. The model will be used to investigate specific scenarios where marine mammals could be particularly prone to decompression sickness (DCS) due to changes in dive behavior or physiology.

Previous reports suggested the existence of direct somatic motor control over heart rate (fH) responses during diving in some marine mammals, as the result of a cognitive and/or learning process rather than being a reflexive response. This would be beneficial for O2 storage management, but would also allow ventilation-perfusion matching for selective gas exchange, where O2 and CO2 can be exchanged with minimal exchange of N2. Such a mechanism explains how air breathing marine vertebrates avoid diving related gas bubble formation during repeated dives, and how stress could interrupt this mechanism and cause excessive N2 exchange. To investigate the conditioned response, we measured the fH-response before and during static breath-holds in three bottlenose dolphins (Tursiops truncatus) when shown a visual symbol to perform either a long (LONG) or short (SHORT) breath-hold, or during a spontaneous breath-hold without a symbol (NS). The average fH (ifHstart), and the rate of change in fH...

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 N2levels 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 N2levels, or may be more resistant to circulating bubbles through immunological/biochemical ada...

Sea turtles, like other air-breathing diving vertebrates, commonly experience significant gas embolism (GE) when incidentally caught at depth in fishing gear and brought to the surface. To better understand why sea turtles develop GE, we built a mathematical model to estimate partial pressures of N2 (PN2), O2 (PO2), and CO2 (PCO2) in the major body-compartments of diving loggerheads (Caretta caretta), leatherbacks (Dermochelys coriacea), and green turtles (Chelonia mydas). This model was adapted from a published model for estimating gas dynamics in marine mammals and penguins. To parameterize the sea turtle model, we used values gleaned from previously published literature and 22 necropsies. Next, we applied this model to data collected from free-roaming individuals of the three study species. Finally, we varied body-condition and cardiac output within the model to see how these factors affected the risk of GE. Our model suggests that cardiac output likely plays a significant role i...

In recent decades, biologists have sought to tag animals with various sensors to study aspects of their behavior otherwise inaccessible from controlled laboratory experiments. Despite this, chemical information, both environmental and physiological, remains challenging to collect despite its tremendous potential to elucidate a wide range of animal behaviors. In this work, we explore the design, feasibility, and data collection constraints of implantable, near-infrared fluorescent nanosensors based on DNA-wrapped single-wall carbon nanotubes (SWNT) embedded within a biocompatible poly(ethylene glycol) diacrylate (PEGDA) hydrogel. These sensors are enabled by Corona Phase Molecular Recognition (CoPhMoRe) to provide selective chemical detection for marine organism biologging. Riboflavin, a key nutrient in oxidative phosphorylation, is utilized as a model analyte in in vitro and ex vivo tissue measurements. Nine species of bony fish, sharks, eels, and turtles were utilized on site at Oceanogràfic in Valencia, Spain to investigate sensor design parameters, including implantation depth, sensor imaging and detection limits, fluence, and stability, as well as acute and long-term biocompatibility. Hydrogels were implanted subcutaneously and imaged using a customized, field-portable Raspberry Pi camera system. Hydrogels could be detected up to depths of 7 mm in the skin and muscle tissue of deceased teleost fish ( Sparus aurata and Stenotomus chrysops) and a deceased catshark ( Galeus melastomus). The effects of tissue heterogeneity on hydrogel delivery and fluorescence visibility were explored, with darker tissues masking hydrogel fluorescence. Hydrogels were implanted into a living eastern river cooter ( Pseudemys concinna), a European eel ( Anguilla anguilla), and a second species of catshark ( Scyliorhinus stellaris). The animals displayed no observable changes in movement and feeding patterns. Imaging by high-resolution ultrasound indicated no changes in tissue structure in the eel and catshark. In the turtle, some tissue reaction was detected upon dissection and histopathology. Analysis of movement patterns in sarasa comet goldfish ( Carassius auratus) indicated that the hydrogel implants did not affect swimming patterns. Taken together, these results indicate that this implantable form factor is a promising technique for biologging using aquatic vertebrates with further development. Future work will tune the sensor detection range to the physiological range of riboflavin, develop strategies to normalize sensor signal to account for the optical heterogeneity of animal tissues, and design a flexible, wearable device incorporating optoelectronic components that will enable sensor measurements in moving animals. This work advances the application of nanosensors to organisms beyond the commonly used rodent and zebrafish models and is an important step toward the physiological biologging of aquatic organisms.

We measured respiratory flow, breath duration, and calculated tidal volume (V) in nine belugas (Delphinapterus leucas, mean measured body mass: 628 ± 151 kg, n = 5) housed in managed care facilities. Both spontaneous (resting at station) and trained maximal respirations (chuffs) were measured. The mean (±s.d.) inspiratory V for spontaneous breaths (16.7 ± 4.7 l, range: 7.5-18.7 l) was larger than those predicted based on respiratory scaling equations from terrestrial mammals and was 32 ± 10% of estimated total lung capacity (TLC) based on an equation from static measurements made on a range of cetaceans and pinniped lungs, and 52 ± 18% of estimated vital capacities (V, mean: 27.7 ± 8.9 l, range: 16.7-40.3 l) based on respiratory measurements obtained during trained maximal respirations. Expiratory flow (V˙, spontaneous: 26.1 ± 5.5 l s, chuff: 66.8 ± 22.5 l s) was significantly higher as compared with inspiratory flow (V˙, spontaneous: 22.3 ± 4.6 l s, chuff: 30.1 ± 8.4 l s), and the maximal expiratory flow recorded was 212 l s. The breath duration was shorter for forced breaths (Expiration: 518 ± 101 ms; Inspiration: 905 ± 170 ms; Total: 1423 ± 227 ms) as compared with spontaneous breaths (Expiration: 995 ± 176 ms; Inspiration: 1098 ± 219 ms; Total: 2093 ± 302 ms). These data provide baseline estimates of the respiratory capacity of belugas.

Fisheries interactions are the most serious threats for sea turtle populations. Despite the existence of some rescue centres providing post-traumatic care and rehabilitation, adequate treatment is hampered by the lack of understanding of the problems incurred while turtles remain entrapped in fishing gears. Recently it was shown that bycaught loggerhead sea turtles (Caretta caretta) could experience formation of gas emboli (GE) and develop decompression sickness (DCS) after trawl and gillnet interaction. This condition could be reversed by hyperbaric O2 treatment (HBOT). The goal of this study was to assess how GE alters respiratory function in bycaught turtles before recompression therapy and measure the improvement after this treatment. Specifically, we assessed the effect of DCS on breath duration, expiratory and inspiratory flow and tidal volume (VT), and the effectiveness of HBOT to improve these parameters. HBOT significantly increased respiratory flows by 32-45% while VT incr...

As marine divers, pinnipeds have a high capacity for exercise at depth while holding their breath. With finite access to oxygen, these species need to be capable of extended aerobic exercise and conservation of energy. Pinnipeds must deal with common physiological hurdles, such as hypoxia, exhaustion and acidosis, that are common to all exercising mammals. The physiological mechanisms in marine mammals used for managing oxygen and carbon dioxide have sparked much research, but access to animals and tissues is difficult and requires permits. Deceased animals that are either bycaught or stranded provide one potential source for tissues, but the validity of biochemical data from post-mortem samples has not been rigorously assessed. Tissues collected from stranded diving mammals may be a crucial source to add to our limited knowledge on the physiology of some of these animals and important to the conservation and management of these species. We aim to determine the reliability of bioche...

Several physiological factors have been suspected of affecting the risk of decompression sickness (DCS), but few have been thoroughly studied during controlled conditions. Dehydration is a potential factor that could increase the risk of DCS. It has been suggested that hydration may enhance inert gas removal or increase surface tension of the blood. Dehydration increases DCS risk. Littermate pairs of male Yorkshire swine (n=57, mean +/- 1 SD 20.6 +/- 1.7 kg) were randomized into two groups. The hydrated group received no medication and was allowed ad lib access to water during a simulated saturation dive. The dehydrated group received intravenous 2 mg x kg(-1) Lasix (a diuretic medication) without access to water throughout the dive. Animals were then compressed on air to 110 ft of seawater (fsw, 4.33 ATA) for 22 h and brought directly to the surface at a rate of 30 fsw x min(-1) (0.91 ATA x min(-1)). Outcomes of death and non-fatal central nervous system (CNS) or cardiopulmonary DCS were recorded. In the hydrated group (n=31): DCS=10, cardiopulmonary DCS=9, CNS DCS=2, Death=4. In the dehydrated group (n=26): DCS=19, cardiopulmonary DCS=19, CNS DCS=6, Death=9. Dehydration significantly increased the overall risk of severe DCS and death. Specifically, it increased the risk of cardiopulmonary DCS, and showed a trend toward increased CNS DCS. In addition, dehydrated subjects manifested cardiopulmonary DCS sooner and showed a trend toward more rapid death (p &amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;lt; 0.1). Hydration status at the time of decompression significantly influences the incidence and time to onset of DCS in this model.

The Marine Mammal Center (TMMC) cares for malnourished California sea lion (CSL) ( Zalophus californianus ) pups and yearlings every year. Hypoglycemia is a common consequence of malnutrition in young CSLs. Administering dextrose during a hypoglycemic crisis is vital to recovery. Traditional veterinary approaches to treat hypoglycemia pose therapeutic challenges in otariids, as vascular access and catheter maintenance can be difficult. The current approach to a hypoglycemic episode at TMMC is to administer dextrose intravenously (IV) by medically trained personnel. Intraperitoneal (IP) dextrose administration is an attractive alternative to IV administration because volunteer staff with basic training can administer treatment instead of waiting for trained staff to treat. This study compares the effects of IV, IP, and no dextrose administration on serum glucose and insulin in clinically healthy, euglycemic CSL yearlings. Three groups of animals, consisting of five sea lions each, we...

We examined an adjunctive treatment for severe decompression sickness (DCS) to be used when hyperbaric treatment is delayed or unavailable. It has been hypothesized that intravenous perfluorocarbon (PFC) emulsion combined with 100% inspired O2 would improve the outcome in severe DCS. Swine (n = 45) were compressed to 4.9 ATA on air for 22 h and brought directly to 1 ATA at 0.9 ATA min(-1). The animals were then randomized to three groups. The first group breathed ambient air, the second group breathed 100% O2, and a third group received 6 ml x kg(-1) of perflubron emulsion (Oxygent) intravenously and breathed 100% O2. Outcomes of neurological and cardiopulmonary DCS and death were recorded. Animals that received PFC emulsion sustained less DCS (p &amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;lt; 0.01) than the other groups (53% vs. 93%). No animals in the PFC group sustained neurological DCS, which was present in 69% of the subjects in the other two groups. O2 breathing postdive did not significantly reduce morbidity or mortality in this model. Postdive treatment with PFC emulsion and 100% O2 decreased the incidence of DCS after nonstop decompression from saturation.

Decompression sickness (DCS) risk following a simulated dive in H2 was lower in pigs with a native intestinal flora that metabolized H2. Pigs (n = 27; 19.4 +/- 0.2 kg body mass) were placed in a chamber that was pressurized to 22.2-25.5 atm (absolute; 2.2-2.6 MPa) with 84-93% H2 for 3 h. Chamber concentrations of O2, H2, He, N2, and CH4 were monitored by gas chromatography. Release of CH4 from the pigs indicated that intestinal microbes had metabolized H2 After decompressing to 11 atm, the pigs were observed for DCS. Animals with DCS released significantly less (P &lt; 0.05) methane (0.53 +/- 0.37 ppm CH4; n = 5) than those without DCS (1.40 +/- 0.17 ppm CH4; n = 22). The DCS risk reduction was attributed to the loss of roughly 12% of the total volume of H2 that could be stored in the tissues of the pigs. Thus, H2 metabolism by the native intestinal flora of pigs may protect against DCS following a simulated H2 dive.

A theory was forwarded in 1960 that humans significantly deviate in anatomy, physiology and behavior from their closest relatives, the great apes, and instead resemble diving mammals, as a result of a period of selective pressure to enter the water (Hardy, 1960). Humans can learn how to dive and in many aspects resemble diving mammals, but how similar is man when compared with aquatic species? To evaluate this, we compared diving performances in a number of aquatic, semiaquatic, and terrestrial species. As an index of aquatic diving specialization, we used maximal and average dive depth and duration, and proportion of time spent under water during repeated dives. Our analysis indicates that aquatic “deep divers” form a separate group, to which humans – and most aquatic and semi aquatic mammals – do not compare in diving specialization. Several species perform dives of intermediate duration and to intermediate depths, and form a group of “moderate divers”. A great number of species show more modest diving skills, despite being dependent on an aquatic life or food sources, and form a group of “shallow divers”. Humans fit well in this latter group and their maximum diving capacity is well within the typical ability performed by shallow near shore foragers. It may be the case that, as most accessible food is present near the shores, a great number of air breathing species have specialized to utilize this niche, while only a smaller group have developed the

ABSTRACT The behavior of gas-filled compartments and bubbles in diving mammals has been a subject of modeling, some measurement, and much recent controversy. However, direct observation of how these volumes change with pressure has been limited. Accepting inevitable concerns about changes in tissue behavior post mortem, seal and dolphin cadavers can now be imaged under pressure using a radio-lucent, glass-fiber, water-filled pressure vessel rated to 250 psi. The combined mass of the sample and the vessel substantially exceed the weight limit of available CT scanner tables. Therefore, a custom rail and counterweighted carriage system were fabricated. The vessel is magnetically linked via an actuator on the CT table and a transponder on the vessel carriage to synchronize table and vessel movement. UHR-CT protocols were employed to image excised and in situ lungs, both in and out of the vessel. There was no loss of tissue detail or resolution for images in the pressure vessel. In this way the specimen can be spirally scanned within the chamber at a range of pressures. Quantification of the change in volume of the various gas-filled structures then allows an absolute measurement of the compliance of various critical structures. The resulting data will populate a new generation of mathematical models for determining how marine mammal lung tissues respond to pressure related gaseous changes in dissolved and gas phases during deep dives.

Among the many factors that influence the cardiovascular adjustments of marine mammals is the act of respiration at the surface, which facilitates rapid gas exchange and tissue re-perfusion between dives. We measured heart rate (f H) in six adult male bottlenose dolphins (Tursiops truncatus) spontaneously breathing at the surface to quantify the relationship between respiration and f H , and compared this with f H during submerged breath-holds. We found that dolphins exhibit a pronounced respiratory sinus arrhythmia (RSA) during surface breathing, resulting in a rapid increase in f H after a breath followed by a gradual decrease over the following 15-20 s to a steady f H that is maintained until the following breath. RSA resulted in a maximum instantaneous f H (if H) of 87.4±13.6 beats min −1 and a minimum if H of 56.8±14.8 beats min −1 , and the degree of RSA was positively correlated with the inter-breath interval (IBI). The minimum if H during 2 min submerged breath-holds where dolphins exhibited submersion bradycardia (36.4±9.0 beats min −1) was lower than the minimum if H observed during an average IBI; however, during IBIs longer than 30 s, the minimum if H (38.7±10.6 beats min −1) was not significantly different from that during 2 min breath-holds. These results demonstrate that the f H patterns observed during submerged breath-holds are similar to those resulting from RSA during an extended IBI. Here, we highlight the importance of RSA in influencing f H variability and emphasize the need to understand its relationship to submersion bradycardia.

Video abstract: https://www.youtube.com/watch?v=WxqKniwIVf4
In the current study we used transthoracic echocardiography to measure stroke volume (SV), heart rate (f H) and cardiac output (CO) in adult bottlenose dolphins (Tursiops truncatus), a male beluga whale calf [Delphinapterus leucas, body mass (M b) range: 151-175 kg] and an adult female false killer whale (Pseudorca crassidens, estimated M b : 500-550 kg) housed in managed care. We also recorded continuous electrocardiogram (ECG) in the beluga whale, bottlenose dolphin, false killer whale, killer whale (Orcinus orca) and pilot whale (Globicephala macrorhynchus) to evaluate cardiorespiratory coupling while breathing spontaneously under voluntary control. The results show that cetaceans have a strong respiratory sinus arrythmia (RSA), during which both f H and SV vary within the interbreath interval, making average values dependent on the breathing frequency (f R). The RSA-corrected f H was lower for all cetaceans compared with that of similarly sized terrestrial mammals breathing continuously. As compared with terrestrial mammals, the RSA-corrected SV and CO were either lower or the same for the dolphin and false killer whale, while both were elevated in the beluga whale. When plotting f R against f H for an inactive mammal, cetaceans had a greater cardiac response to changes in f R as compared with terrestrial mammals. We propose that these data indicate an important coupling between respiration and cardiac function that enhances gas exchange, and that this RSA is important to maximize gas exchange during surface intervals, similar to that reported in the elephant seal.

video summary: https://www.youtube.com/watch?v=r93I8ffgAoI
We analysed 3680 dives from 23 satellite-linked tags deployed on Cuvier's beaked whales to assess the relationship between long duration dives and inter-deep dive intervals and to estimate aerobic dive limit (ADL). The median duration of presumed foraging dives was 59 min and 5% of dives exceeded 77.7 min. We found no relationship between the longest 5% of dive durations and the following inter-deep dive interval nor any relationship with the ventilation period immediately prior to or following a long dive. We suggest that Cuvier's beaked whales have low metabolic rates, high oxygen storage capacities and a high acid-buffering capacity to deal with the by-products of both aerobic and anaerobic metabolism, which enables them to extend dive durations and exploit their bathypelagic foraging habitats.

1. Animal behavior is elicited, in part, in response to external conditions, but understanding how animals perceive the environment and make the decisions that bring about these behavioral responses is challenging. 2. Animal heads often move during specific behaviors and, additionally, typically have sensory systems (notably vision, smell, and hearing) sampling in defined arcs (nor-mally to the front of their heads). As such, head-mounted electronic sensors consisting of accelerometers and magnetometers, which can be used to determine the movement and directionality of animal heads (where head "movement" is defined here as changes in heading [azimuth] and/or pitch [elevation angle]), can potentially provide information both on behaviors in general and also clarify which parts of the environment the animals might be prioritizing ("environmental framing"). 3. We propose a new approach to visualize the data of such head-mounted tags that combines the instantaneous outputs of head heading and pitch in a single intuitive spherical plot. This sphere has magnetic heading denoted by "longitude" position and head pitch by "latitude" on this "orientation sphere" (O-sphere). 4. We construct the O-sphere for the head rotations of a number of vertebrates with contrasting body shape and ecology (oryx, sheep, tortoises, and turtles), illustrating various behaviors, including foraging, walking, and environmental scanning. We also propose correcting head orientations for body orientations to highlight specific heading-independent head rotation, and propose the derivation of O-sphere-metrics, such as angular speed across the sphere. This should help identify the functions of various head behaviors. 5. Visualizations of the O-sphere provide an intuitive representation of animal behavior manifest via head orientation and rotation. This has ramifications for quantifying and understanding behaviors ranging from navigation through vigilance to feeding and, when used in tandem with body movement, should provide an

Lung function testing was performed each 6 months in 3 managed care dolphins (2 males, 1 female) during a 1-year period to assess whether these data provide diagnostic information about respiratory health. Pulmonary radiographs and standard clinical testing were used to evaluate the health of each dolphin. The female dolphin had chronic bronchitis and one of the male dolphins developed pneumonia before the last testing date. There were no differences in lung function parameters between test dates for the two male dolphins, but for the last lung function evaluation the breath duration and respiratory flow increased in the female. Evaluation of the flow-volume relationship during forced breaths (chuffs) in water indicated clear changes with emerging disease in the male that contracted pneumonia before the last test date. Similar flow restrictions were also seen in the flow-volume data from spontaneous breaths when this dolphin was on land for a brief period to obtain radiographs. We conclude that lung function testing may be a minimally invasive and possibly useful diagnostic tool to evaluate pulmonary health in both managed care and wild dolphins. This method should be given more attention as an alternative method that is easy to perform and quick to evaluate.