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. 2020 Nov 24:11:604018.
doi: 10.3389/fphys.2020.604018. eCollection 2020.

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

Andreas Fahlman  1   2 , Bruno Cozzi  3 , Mercy Manley  4 , Sandra Jabas  4 , Marek Malik  5   6 , Ashley Blawas  7 , Vincent M Janik  8
Affiliations

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

Andreas Fahlman et al. Front Physiol. .

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.

Keywords: adaptation; cardiovascular function; cardiovascular physiology; dive response; diving physiology; marine mammal; reflex; selective gas exchange hypothesis.

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Conflict of interest statement

AF was affiliated with the company Global Diving Research Inc., while completing this work but received no financial compensation. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

FIGURE 1
FIGURE 1
Instantaneous heart rate (ifH) against time before (time –20 to 0) and up to A) 230 s or 40 s during a breath-hold for dolphin B) D1, C) D2, D) D3 (Table 1). Data are average (±s.e.m., n = 3) ifH for LONG (n = 58) and SHORT (n = 58) dives that were preceded by a symbol and with pre-determined dive duration, and dives without a symbol (NS, n = 48) in which dive duration was determined by the dolphin. (A–D) The solid vertical black line is the start of the breath-hold (BH) which is when the dolphin took the last breath before submerging. (A) The average time for the end of the breath-hold, the time of the first breath after the breath-hold, is indicated as broken vertical lines for the SHORT, NS and LONG dives (from left to right).
FIGURE 2
FIGURE 2
Examples of instantaneous heart rate (ifH) responses from individual dolphins against time before (time –20 to 0) and up to 40 s (time 0 to 40 s) during a breath-hold. (A) ifH for a LONG and SHORT dive (each preceded by a symbol with a pre-determined dive duration), and a dive without a symbol (NS), where dive duration was determined by the dolphin. (B) ifH variation during a breath-hold for 3 NS dives in dolphin D3 (Table 1). The dive durations, the time from the last breath before and first breath after a breath-hold is indicated in parenthesis.
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