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.

An integrated comparative physiology and molecular approach pinpoints mediators of breath-hold capacity in dolphins

“…C. Individual dolphin lipoxygenase activity in whole blood collected at an independent sampling date. D. Physiological measurements of heart rate for three individual dolphins (black lines from ECG data previously published in Blawas et al, 2020, dashed lines from echocardiogram data previously published in Fahlman et al, 2020) over time. Inset shows heart rate for humans performing breath-holds with facial immersion in water (dark gray in inset) overlaid on dolphin heart rate.…”

“…Dolphins and other cetaceans have evolved exquisite physiological adaptations to deal with the challenges of a fully aquatic lifestyle including having a hydrodynamic shape to reduce drag (Fish, 1993), counter-current heat exchangers for thermoregulation (Pabst et al, 1999; Scholander and Schevill, 1955), and cardiorespiratory plasticity for exquisite management of circulation and respiratory gases (Blawas et al, 2021; Fahlman et al, 2020b, 2020a, 2019b; Noren et al, 2012). The well-known dive response, a suite of adaptations that support reduced aerobic metabolism during diving, involves apnea, bradycardia, and peripheral vasoconstriction that assures maintained mean arterial blood pressure as blood flow to peripheral tissues is reduced and allows regulation of perfusion to conserve oxygen-rich blood for the brain and heart.…”

An external telemetry system for recording resting heart rate variability and heart rate in free-ranging large wild mammals

“…Finally, in all models, individual identity had a highly significant effect, suggesting individual differences in the occurrence of flats, stairs and artefacts. There are potentially many influences at play here, such as individual differences in location and micro-habitat, especially with respect to access to water [ 27 , 28 , 59 ], behaviour patterns [ 60 , 61 ], or even the possibility of cognitive control of heart rate [ 62 ] that may influence the occurrence of flats and stairs. Heart rate monitor tag ID was also retained in the best models for flats and artefacts, but we were unfortunately unable to conduct a crossed experimental design to thoroughly disentangle the effects of individual ID and tag ID.…”

The New Era of Physio-Logging and Their Grand Challenges

“…In recent years, there has been a focus on measuring physiology in free-ranging animals. For example, trained animals that are desensitized to the experimental procedures have been used to study diving energetics, cardiorespiratory and vascular physiology, and cerebrovascular physiology (Elsner, 1965 ; Olsen et al, 1969 ; Ridgway and Howard, 1979 ; Williams et al, 1993 ; Hurley and Costa, 2001 ; Fahlman et al, 2008 , 2019 , 2020a , b ; Mortola and Sequin, 2009 ; Rosen and Trites, 2013 ; Worthy et al, 2013 ; Elmegaard et al, 2016 , 2019 ; Takei et al, 2016 ; McKnight et al, 2019 ; Meir et al, 2019 ; Pedersen et al, 2020 ; Blawas et al, 2021 ). As bio-logging technologies have advanced, physiological parameters such as heart rate, respiration rate, and blood O 2 have even been measured in free-ranging fish, reptiles, birds, and mammals (Falke et al, 1985 ; Ponganis et al, 1991 ; Thompson and Fedak, 1993 ; Southwood et al, 1999 ; Andrews et al, 2000 ; Froget et al, 2004 ; Ropert-Coudert et al, 2006 , 2009b ; Meir et al, 2009 ; Yamamoto et al, 2009 ; Meir and Ponganis, 2010 ; McDonald and Ponganis, 2013 , 2014 ; Sakamoto et al, 2013 ; Duriez et al, 2014 ; Goldbogen et al, 2019a ; McKnight et al, 2019 , 2021a , b ; Sumich, 2021 ).…”