Drivers of the dive response in trained harbour porpoises<i>(Phocoena phocoena</i>)

Elmegaard, Siri L.; McDonald, Birgitte I.; Madsen, Peter T.

doi:10.1242/jeb.208637

Cited by 19 publications

(21 citation statements)

References 43 publications

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“…In addition, the pre-apnea and diving f H 's were within the range of those reported in previous studies in conditioned bottlenose dolphins (Noren et al, 2004;Fahlman et al, 2019bFahlman et al, , 2020b, and did not vary depending on the type of breath-hold (Figure 1). While the f H -response during the breath-hold in the current study is similar to that reported in the harbor porpoise, the pre-dive f H varied considerably in the harbor porpoise (Elmegaard et al, 2016(Elmegaard et al, , 2019. It is possible that a non-random design, where the animal anticipated the task beforehand resulted in changes in the breathing frequency or tidal volume, which are known to alter f H (Cauture et al, 2019;Fahlman et al, 2019bFahlman et al, , 2020b).…”

Section: Evidence For Conditioned Control Of Heart Ratesupporting

confidence: 69%

“…While it is clear that the dive response is exhibited by all vertebrates studied and that the response is heritable, its actual role and regulation within and between species is debated (Mottishaw et al, 1999;Fahlman et al, 2011;Ponganis, 2011;Ponganis et al, 2017;Parkes, 2019). A number of factors such a facial immersion (in humans), breathing frequency, tidal volume, age, blood O 2 and CO 2 tension, blood pressure, and emotional state may explain the large variability within and between individuals (Irving, 1963;Harrison et al, 1972;Lin et al, 1972;Jones et al, 1973;Moore et al, 1973;Angell-James et al, 1978Openshaw and Woodroof, 1978;Blix, 1987;Bernardi et al, 1989;Thompson and Fedak, 1993;Castellini et al, 1994a,b;Andrews et al, 2000;Fahlman et al, 2011;Elmegaard et al, 2016Elmegaard et al, , 2019Kaczmarek et al, 2018;Cauture et al, 2019). In addition, previous studies have suggested that at least some marine mammals can be conditioned to alter the f H response depending on anticipation (Elmegaard et al, 2016;Kaczmarek et al, 2018), possibly due to suprabulbar or cortical influences Jones, 1982, 1997;Panneton, 2013).…”

Section: Evidence For Conditioned Control Of Heart Ratementioning

confidence: 99%

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

Fahlman

Cozzi

Manley³

et al. 2020

Front. Physiol.

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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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Section: Evidence For Conditioned Control Of Heart Ratesupporting

confidence: 69%

Section: Evidence For Conditioned Control Of Heart Ratementioning

confidence: 99%

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

Fahlman

Cozzi

Manley³

et al. 2020

Front. Physiol.

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“…5. In the plot, we also included published data for the harbor porpoise (Phocoena phocoena), the adult beluga whale (Delphinapterus leucas) and gray whale (Eschrichtius robustus) (Bickett et al, 2019;Elmegaard et al, 2019;Ponganis and Kooyman, 1999;Wahrenbrock et al, 1974). The regression for the cetaceans was: f H =24.8+11.9f R (Fig.…”

Section: Relationship Between F R and F Hmentioning

confidence: 99%

“…By using RSA correction, comparisons within and between species and activity states (inactive, swimming, diving) could be made and be Data for bottlenose dolphin, beluga whale, false killer whale, pilot whale and killer whale are from the present study. Data for harbor porpoise (Phocoena phocoena) and gray whale (Eschrichtius robustus), and additional data for the killer whale, pilot whale and adult beluga whale are from previous studies (Bickett et al, 2019;Elmegaard et al, 2019;Ponganis and Kooyman, 1999;Wahrenbrock et al, 1974). The regression for the cetacean data was:…”

Section: Changes In Co During Rsa Are Made By Variation In Both F H Amentioning

confidence: 99%

Cardiorespiratory coupling in cetaceans; a physiological strategy to improve gas exchange?

Fahlman

Miedler²,

Martí‐Bonmatí

et al. 2020

Journal of Experimental Biology

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In the current study we used transthoracic echocardiography to measure stroke volume (SV), heart rate (fH) and cardiac output (CO) in adult bottlenose dolphins (Tursiops truncatus), a male beluga whale calf [Delphinapterus leucas, body mass (Mb) range: 151–175 kg] and an adult female false killer whale (Pseudorca crassidens, estimated Mb: 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 fH and SV vary within the interbreath interval, making average values dependent on the breathing frequency (fR). The RSA-corrected fH 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 fR against fH for an inactive mammal, cetaceans had a greater cardiac response to changes in fR 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.

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“…The elastic tissue network that surrounds the entire MESs and extends into the cartilaginous rings may serve to maintain the lumen of the terminal bronchioles open during explosive ventilation, preventing obstruction of the airways. The mechanisms by which MESs are regulated by the visceral nervous system are not known, and here we also note that, at least in some species, specific respiratory responses to diving may be under somatic control (Elmegaard et al, 2019). In this study, we describe the presence of NFs in the terminal portion of the lung of bottlenose and striped dolphins.…”

Section: Discussionmentioning

confidence: 73%

Microscopic anatomical, immunohistochemical, and morphometric characterization of the terminal airways of the lung in cetaceans

Otero-Sabio

Centelleghe

Corain

et al. 2020

Journal of Morphology

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The lungs of cetaceans undergo anatomical and physiological adaptations that facilitate extended breath‐holding during dives. Here, we present new insights on the ontogeny of the microscopic anatomy of the terminal portion of the airways of the lungs in five cetacean species: the fin whale (Balaenoptera physalus); the sperm whale (Physeter macrocephalus), the Cuvier's beaked whale (Ziphius cavirostris); the bottlenose dolphin (Tursiops truncatus); and the striped dolphin (Stenella coeruleoalba). We (a) studied the histology of the terminal portion of the airways; (b) used immunohistochemistry (IHC) to characterize the muscle fibers with antibodies against smooth muscle (sm‐) actin, sm‐myosin, and desmin; (c) the innervation of myoelastic sphincters (MESs) with an antibody against neurofilament protein; and (d) defined the diameter of the terminal bronchioles, the diameter and length of the alveoli, the thickness of the septa, the major and minor axis, perimeter and section area of the cartilaginous rings by quantitative morphometric analyses in partially inflated lung tissue. As already reported in the literature, in bottlenose and striped dolphins, a system of MESs was observed in the terminal bronchioles. Immunohistochemistry confirmed the presence of smooth muscle in the terminal bronchioles, alveolar ducts, and alveolar septa in all the examined species. Some neurofilaments were observed close to the MESs in both bottlenose and striped dolphins. In fin, sperm, and Cuvier's beaked whales, we noted a layer of longitudinal smooth muscle going from the terminal bronchioles to the alveolar sacs. The morphometric analysis allowed to quantify the structural differences among cetacean species by ranking them into groups according to the adjusted mean values of the morphometric parameters measured. Our results contribute to the current understanding of the anatomy of the terminal airways of the cetacean lung and the role of the smooth muscle in the alveolar collapse reflex, crucial for prolonged breath‐holding diving.

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Drivers of the dive response in trained harbour porpoises(Phocoena phocoena)

Cited by 19 publications

References 43 publications

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

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

Cardiorespiratory coupling in cetaceans; a physiological strategy to improve gas exchange?

Microscopic anatomical, immunohistochemical, and morphometric characterization of the terminal airways of the lung in cetaceans

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