The diving physiology of bottlenose dolphins (Tursiops truncatus). II. Biomechanics and changes in buoyancy at depth

During diving, marine mammals must balance the conservation of limited oxygen reserves with the metabolic costs of swimming exercise. As a result, energetically efficient modes of locomotion provide an advantage during periods of submergence and will presumably increase in importance as the animals perform progressively longer dives. To determine the effect of a limited oxygen supply on locomotor performance, we compared the kinematics and behavior of swimming and diving bottlenose dolphins. Adult bottlenose dolphins (Tursiops truncatus) were trained to swim horizontally near the water surface or submerged at 5 m and to dive to depths ranging from 12 to 112 m. Swimming kinematics (preferred swimming mode, stroke frequency and duration of glides) were monitored using submersible video cameras (Sony Hi-8) held by SCUBA divers or attached to a pack on the dorsal fin of the animal. Drag and buoyant forces were calculated from patterns of deceleration for horizontally swimming and vertically diving animals. The results showed that dolphins used a variety of swimming gaits that correlated with acceleration. The percentage of time spent gliding during the descent phase of dives increased with depth. Glide distances ranged from 7.1+/−1.9 m for 16 m dives to 43.6+/−7.0 m (means +/− s.e.m.) for 100 m dives. These gliding patterns were attributed to changes in buoyancy associated with lung compression at depth. By incorporating prolonged glide periods, the bottlenose dolphin realized a theoretical 10–21 % energetic savings in the cost of a 100 m dive in comparison with dives based on neutral buoyancy models. Thus, modifying locomotor patterns to account for physical changes with depth appears to be one mechanism that enables diving mammals with limited oxygen stores to extend the duration of a dive.

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Occurrence of Brucella ceti in stranded bottlenose dolphins Tursiops truncatus coincides with calving season

Diseases of Aquatic Organisms ◽

10.3354/dao03526 ◽

2020 ◽

Vol 141 ◽

pp. 185-193

Author(s):

WE McFee ◽

D Wu ◽

K Colegrove ◽

K Terio ◽

L Balthis ◽

...

Keyword(s):

South Carolina ◽

Tursiops Truncatus ◽

Marine Mammals ◽

Marine Bacterium ◽

Bottlenose Dolphins ◽

Global Public Health ◽

Terrestrial Species ◽

Long Term Study ◽

Calving Season

Brucellosis is a disease caused by the Gram-negative facultative intracellular bacterium Brucella spp. In terrestrial species, this zoonotic bacterium is a global public health risk, but there is also concern over the zoonotic potential of marine forms, such as B. ceti, which affects cetaceans. Due to the detection of B. ceti in samples from bottlenose dolphins Tursiops truncatus during the 2010-2014 Gulf of Mexico Unusual Mortality Event, a long-term study of the prevalence of Brucella in stranded bottlenose dolphins from South Carolina, USA, was conducted. From 2012 through 2017, 282 stranded bottlenose dolphins were tested for B. ceti via real-time PCR. Nearly 32% of the dolphins tested positive in at least one sample (brain, lung, blowhole swab). Very little information exists in the literature on the occurrence of Brucella spp. in marine mammals, though in terrestrial species, such as cattle and elk, higher prevalence is often reported in spring. Similar results were found in this study with the peak occurrence being between March and June, a known period of calving in South Carolina. Results from this study provide important insights into the occurrence of the marine bacterium B. ceti.

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The diving physiology of bottlenose dolphins (Tursiops truncatus). I. Balancing the demands of exercise for energy conservation at depth

Journal of Experimental Biology ◽

10.1242/jeb.202.20.2739 ◽

1999 ◽

Vol 202 (20) ◽

pp. 2739-2748 ◽

Cited By ~ 10

Author(s):

T.M. Williams ◽

J.E. Haun ◽

W.A. Friedl

Keyword(s):

Heart Rate ◽

Blood Lactate ◽

Tursiops Truncatus ◽

Marine Mammals ◽

Bottlenose Dolphins ◽

Lactate Concentration ◽

Blood Lactate Concentration ◽

Energetic Cost ◽

Breath Holding ◽

Breath Hold

During diving, marine mammals must rely on the efficient utilization of a limited oxygen reserve sequestered in the lungs, blood and muscles. To determine the effects of exercise and apnea on the use of these reserves, we examined the physiological responses of adult bottlenose dolphins (Tursiops truncatus) trained to breath-hold on the water surface or to dive to submerged targets at depths between 60 and 210 m. Changes in blood lactate levels, in partial pressures of oxygen and carbon dioxide and in heart rate were assessed while the dolphins performed sedentary breath-holds. The effects of exercise on breath-hold capacity were examined by measuring heart rate and post-dive respiration rate and blood lactate concentration for dolphins diving in Kaneohe Bay, Oahu, Hawaii. Ascent and descent rates, stroke frequency and swimming patterns were monitored during the dives. The results showed that lactate concentration was 1.1+/−0.1 mmol l(−1) at rest and increased non-linearly with the duration of the sedentary breath-hold or dive. Lactate concentration was consistently higher for the diving animals at all comparable periods of apnea. Breakpoints in plots of lactate concentration and blood gas levels against breath-hold duration (P(O2), P(CO2)) for sedentary breath-holding dolphins occurred between 200 and 240 s. In comparison, the calculated aerobic dive limit for adult dolphins was 268 s. Descent and ascent rates ranged from 1.5 to 2.5 m s(−1) during 210 m dives and were often outside the predicted range for swimming at low energetic cost. Rather than constant propulsion, diving dolphins used interrupted modes of swimming, with more than 75 % of the final ascent spent gliding. Physiological and behavioral measurements from this study indicate that superimposing swimming exercise on apnea was energetically costly for the diving dolphin but was circumvented in part by modifying the mode of swimming.

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Investigation of Environmentally Dependent Movement of Bottlenose Dolphins (Tursiops truncatus)

Journal of Zoological and Botanical Gardens ◽

10.3390/jzbg2030023 ◽

2021 ◽

Vol 2 (3) ◽

pp. 335-348

Author(s):

Zining Zhang ◽

Ding Zhang ◽

Joaquin Gabaldon ◽

Kari Goodbar ◽

Nicole West ◽

...

Keyword(s):

Animal Behavior ◽

Network Architecture ◽

Tursiops Truncatus ◽

Bottlenose Dolphins ◽

Video Frame ◽

Neural Network Architecture ◽

Environmental Stimuli ◽

And Behavior ◽

Lagoon Environment ◽

Persistent Monitoring

How environmental features (e.g., people, enrichment, or other animals) affect movement is an important element for the study of animal behavior, biomechanics, and welfare. Here we present a stationary overhead camera-based persistent monitoring framework for the investigation of bottlenose dolphin (Tursiops truncatus) response to environmental stimuli. Mask R-CNN, a convolutional neural network architecture, was trained to automatically detect 3 object types in the environment: dolphins, people, and enrichment floats that were introduced to stimulate and engage the animals. Detected objects within each video frame were linked together to create track segments across frames. The animals’ tracks were used to parameterize their response to the presence of environmental stimuli. We collected and analyzed data from 24 sessions from bottlenose dolphins in a managed lagoon environment. The seasons had an average duration of 1 h and around half of them had enrichment (42%) while the rest (58%) did not. People were visible in the environment for 18.8% of the total time (∼4.5 h), more often when enrichment was present (∼3 h) than without (∼1.5 h). When neither enrichment nor people were present, the animals swam at an average speed of 1.2 m/s. When enrichment was added to the lagoon, average swimming speed decreased to 1.0 m/s and the animals spent more time moving at slow speeds around the enrichment. Animals’ engagement with the enrichment also decreased over time. These results indicate that the presence of enrichment and people in, or around, the environment attracts the animals, influencing habitat use and movement patterns as a result. This work demonstrates the ability of the proposed framework for the quantification and persistent monitoring of bottlenose dolphins’ movement, and will enable new studies to investigate individual and group animal locomotion and behavior.

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Total energy expenditure of bottlenose dolphins (Tursiops truncatus) of different ages

Journal of Experimental Biology ◽

10.1242/jeb.242218 ◽

2021 ◽

Author(s):

Rebecca Rimbach ◽

Ahmad Amireh ◽

Austin Allen ◽

Brian Hare ◽

Emily Guarino ◽

...

Keyword(s):

Energy Expenditure ◽

Total Energy ◽

Body Mass ◽

Tursiops Truncatus ◽

Marine Mammals ◽

Bottlenose Dolphins ◽

Large Body ◽

Total Energy Expenditure ◽

Natural Seawater ◽

Terrestrial Mammals

Marine mammals are thought to have an energetically expensive lifestyle because endothermy is costly in marine environments. However, measurements of total energy expenditure (TEE; kcal/day) are available only for a limited number of marine mammals, because large body size and inaccessible habitats make TEE measurements expensive and difficult for many taxa. We measured TEE in 10 adult common bottlenose dolphins (Tursiops truncatus) living in natural seawater lagoons at two facilities (Dolphin Research Center and Dolphin Quest) using the doubly labeled water method. We assessed the relative effects of body mass, age, and physical activity on TEE. We also examined whether TEE of bottlenose dolphins, and more generally marine mammals, differs from that expected for their body mass compared to other eutherian mammals, using phylogenetic least squares (PGLS) regressions. There were no differences in body mass or TEE (unadjusted TEE and TEE adjusted for fat free mass (FFM)) between dolphins from both facilities. Our results show that Adjusted TEE decreased and fat mass (FM) increased with age. Different measures of activity were not related to age, body fat or Adjusted TEE. Both PGLS and the non-phylogenetic linear regression indicate that marine mammals have an elevated TEE compared to terrestrial mammals. However, bottlenose dolphins expended 17.1% less energy than other marine mammals of similar body mass. The two oldest dolphins (>40 years) showed a lower TEE, similar to the decline in TEE seen in older humans. To our knowledge, this is the first study to show an age-related metabolic decline in a large non-human mammal.

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The lipid composition of the blood of marine mammals—II. Atlantic bottlenose dolphins, Tursiops truncatus and two species of seals, Halichoerus grypus and Phoca vitulina

Comparative Biochemistry and Physiology Part B Comparative Biochemistry ◽

10.1016/0305-0491(71)90226-4 ◽

1971 ◽

Vol 40 (2) ◽

pp. 423-432 ◽

Cited By ~ 4

Author(s):

Gary J. Nelson

Keyword(s):

Lipid Composition ◽

Tursiops Truncatus ◽

Marine Mammals ◽

Bottlenose Dolphins ◽

Phoca Vitulina ◽

Halichoerus Grypus

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Whistle rates of wild bottlenose dolphins (Tursiops truncatus): Influences of group size and behavior.

Journal of Comparative Psychology ◽

10.1037/0735-7036.122.3.305 ◽

2008 ◽

Vol 122 (3) ◽

pp. 305-311 ◽

Cited By ~ 62

Author(s):

Nicola J. Quick ◽

Vincent M. Janik

Keyword(s):

Group Size ◽

Tursiops Truncatus ◽

Bottlenose Dolphins ◽

And Behavior

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Conditioned Variation in Heart Rate During Static Breath-Holds in the Bottlenose Dolphin (Tursiops truncatus)

Frontiers in Physiology ◽

10.3389/fphys.2020.604018 ◽

2020 ◽

Vol 11 ◽

Cited By ~ 2

Author(s):

Andreas Fahlman ◽

Bruno Cozzi ◽

Mercy Manley ◽

Sandra Jabas ◽

Marek Malik ◽

...

Keyword(s):

Heart Rate ◽

Tursiops Truncatus ◽

Marine Mammals ◽

Bottlenose Dolphins ◽

Bubble Formation ◽

Rate Of Change ◽

Breath Hold ◽

Short Breath ◽

Breath Hold Duration ◽

Spontaneous Breath

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 (difH/dt) during the first 20 s of the breath-hold differed between breath-hold types. In addition, the minimum instantaneous fH (ifHmin), and the average instantaneous fH during the last 10 s (ifHend) also differed between breath-hold types. The difH/dt was greater, and the ifHstart, ifHmin, and ifHend were lower during a LONG as compared with either a SHORT, or an NS breath-hold (P < 0.05). Even though the NS breath-hold dives were longer in duration as compared with SHORT breath-hold dives, the difH/dt was greater and the ifHstart, ifHmin, and ifHend were lower during the latter (P < 0.05). In addition, when the dolphin determined the breath-hold duration (NS), the fH was more variable within and between individuals and trials, suggesting a conditioned capacity to adjust the fH-response. These results suggest that dolphins have the capacity to selectively alter the fH-response during diving and provide evidence for significant cardiovascular plasticity in dolphins.

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Anaemia, hypothyroidism and immune suppression associated with polychlorinated biphenyl exposure in bottlenose dolphins ( Tursiops truncatus )

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2011.0665 ◽

2011 ◽

Vol 279 (1726) ◽

pp. 48-57 ◽

Cited By ~ 86

Author(s):

Lori H. Schwacke ◽

Eric S. Zolman ◽

Brian C. Balmer ◽

Sylvain De Guise ◽

R. Clay George ◽

...

Keyword(s):

Tursiops Truncatus ◽

Marine Mammals ◽

Polychlorinated Biphenyl ◽

Bottlenose Dolphins ◽

Endocrine System ◽

T Lymphocyte Proliferation ◽

Total Thyroxine ◽

High Concentrations ◽

High Doses ◽

Primate Laboratory

Polychlorinated biphenyls (PCBs), persistent chemicals widely used for industrial purposes, have been banned in most parts of the world for decades. Owing to their bioaccumulative nature, PCBs are still found in high concentrations in marine mammals, particularly those that occupy upper trophic positions. While PCB-related health effects have been well-documented in some mammals, studies among dolphins and whales are limited. We conducted health evaluations of bottlenose dolphins ( Tursiops truncatus ) near a site on the Georgia, United States coast heavily contaminated by Aroclor 1268, an uncommon PCB mixture primarily comprised of octa- through deca-chlorobiphenyl congeners. A high proportion (26%) of sampled dolphins suffered anaemia, a finding previously reported from primate laboratory studies using high doses of a more common PCB mixture, Aroclor 1254. In addition, the dolphins showed reduced thyroid hormone levels and total thyroxine, free thyroxine and triiodothyronine negatively correlated with PCB concentration measured in blubber ( p = 0.039, < 0.001, 0.009, respectively). Similarly, T-lymphocyte proliferation and indices of innate immunity decreased with blubber PCB concentration, suggesting an increased susceptibility to infectious disease. Other persistent contaminants such as DDT which could potentially confound results were similar in the Georgia dolphins when compared with previously sampled reference sites, and therefore probably did not contribute to the observed correlations. Our results clearly demonstrate that dolphins are vulnerable to PCB-related toxic effects, at least partially mediated through the endocrine system. The severity of the effects suggests that the PCB mixture to which the Georgia dolphins were exposed has substantial toxic potential and further studies are warranted to elucidate mechanisms and potential impacts on other top-level predators, including humans, who regularly consume fish from the same marine waters.

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Respiratory sinus arrhythmia and submersion bradycardia in bottlenose dolphins (Tursiops truncatus)

Journal of Experimental Biology ◽

10.1242/jeb.234096 ◽

2020 ◽

Vol 224 (1) ◽

pp. jeb234096

Author(s):

Ashley M. Blawas ◽

Douglas P. Nowacek ◽

Austin S. Allen ◽

Julie Rocho-Levine ◽

Andreas Fahlman

Keyword(s):

Heart Rate ◽

Gas Exchange ◽

Respiratory Sinus Arrhythmia ◽

Tursiops Truncatus ◽

Marine Mammals ◽

Bottlenose Dolphins ◽

Sinus Arrhythmia ◽

The Many ◽

Spontaneously Breathing ◽

The Relationship

ABSTRACTAmong 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 (fH) in six adult male bottlenose dolphins (Tursiops truncatus) spontaneously breathing at the surface to quantify the relationship between respiration and fH, and compared this with fH during submerged breath-holds. We found that dolphins exhibit a pronounced respiratory sinus arrhythmia (RSA) during surface breathing, resulting in a rapid increase in fH after a breath followed by a gradual decrease over the following 15–20 s to a steady fH that is maintained until the following breath. RSA resulted in a maximum instantaneous fH (ifH) of 87.4±13.6 beats min−1 and a minimum ifH of 56.8±14.8 beats min−1, and the degree of RSA was positively correlated with the inter-breath interval (IBI). The minimum ifH during 2 min submerged breath-holds where dolphins exhibited submersion bradycardia (36.4±9.0 beats min−1) was lower than the minimum ifH observed during an average IBI; however, during IBIs longer than 30 s, the minimum ifH (38.7±10.6 beats min−1) was not significantly different from that during 2 min breath-holds. These results demonstrate that the fH 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 fH variability and emphasize the need to understand its relationship to submersion bradycardia.

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