Conditioned variation in heart rate during static breath-holds in the bottlenose dolphin (Tursiops truncatus)

Andreas Fahlman; Bruno Cozzi; Mercy Manley; Sandra Jabas; Marek Malik; Ashley Blawas; Vincent M. Janik

doi:10.3389/fphys.2020.604018

Conditioned variation in heart rate during static breath-holds in the bottlenose dolphin (Tursiops truncatus)

Andreas Fahlman^*, Bruno Cozzi, Mercy Manley, Sandra Jabas, Marek Malik, Ashley Blawas, Vincent M. Janik

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

Abstract

Previous reports suggested the existence of direct somatic motor control over heart rate (f_H) 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 f_H-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 f_H (if_Hstart), and the rate of change in f_H (dif_H/dt) during the first 20 s of the breath-hold differed between breath-hold types. In addition, the minimum instantaneous f_H (if_Hmin), and the average instantaneous f_H during the last 10 s (if_Hend) also differed between breath-hold types. The dif_H/dt was greater, and the if_Hstart, if_Hmin, and if_Hend 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 dif_H/dt was greater and the if_Hstart, if_Hmin, and if_Hend were lower during the latter (P < 0.05). In addition, when the dolphin determined the breath-hold duration (NS), the f_H was more variable within and between individuals and trials, suggesting a conditioned capacity to adjust the f_H-response. These results suggest that dolphins have the capacity to selectively alter the f_H-response during diving and provide evidence for significant cardiovascular plasticity in dolphins.

Original language	English
Article number	604018
Journal	Frontiers in Physiology
Volume	11
DOIs	https://doi.org/10.3389/fphys.2020.604018
Publication status	Published - 24 Nov 2020

Keywords

Dive response
Diving physiology
Marine mammal
Reflex
Cardiovascular physiology

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.3389/fphys.2020.604018Licence: CC BY

Fahlman_2020_FP_Conditioned_CC
Copyright © 2020 Fahlman, Cozzi, Manley, Jabas, Malik, Blawas and Janik. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
Final published version, 1.42 MBLicence: CC BY

Conditioned variation in heart rate during static breath-holds in the bottlenose dolphin (Tursiops truncatus) (dataset)
Janik, V. (Creator), OSF, 2020
https://osf.io/t8jry
Dataset

Cite this

@article{295e82d825bf4ef5b99d1bc1001ab353,

title = "Conditioned variation in heart rate during static breath-holds in the bottlenose dolphin (Tursiops truncatus)",

abstract = "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.",

keywords = "Dive response, Diving physiology, Marine mammal, Reflex, Cardiovascular physiology",

author = "Andreas Fahlman and Bruno Cozzi and Mercy Manley and Sandra Jabas and Marek Malik and Ashley Blawas and Janik, {Vincent M.}",

note = "Funding for this project was provided by the Office of Naval Research to AF (ONR Award # N00014-16-1-3088).",

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doi = "10.3389/fphys.2020.604018",

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volume = "11",

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T1 - Conditioned variation in heart rate during static breath-holds in the bottlenose dolphin (Tursiops truncatus)

AU - Fahlman, Andreas

AU - Cozzi, Bruno

AU - Manley, Mercy

AU - Jabas, Sandra

AU - Malik, Marek

AU - Blawas, Ashley

AU - Janik, Vincent M.

N1 - Funding for this project was provided by the Office of Naval Research to AF (ONR Award # N00014-16-1-3088).

PY - 2020/11/24

Y1 - 2020/11/24

N2 - 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.

AB - 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.

KW - Dive response

KW - Diving physiology

KW - Marine mammal

KW - Reflex

KW - Cardiovascular physiology

U2 - 10.3389/fphys.2020.604018

DO - 10.3389/fphys.2020.604018

M3 - Article

SN - 1664-042X

VL - 11

JO - Frontiers in Physiology

JF - Frontiers in Physiology

M1 - 604018

ER -

Conditioned variation in heart rate during static breath-holds in the bottlenose dolphin (Tursiops truncatus)

Abstract

Keywords

UN SDGs

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Conditioned variation in heart rate during static breath-holds in the bottlenose dolphin (Tursiops truncatus) (dataset)

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