Novel locomotor muscle design in extreme deep-diving whales

Abstract

SUMMARYMost marine mammals are hypothesized to routinely dive within their aerobic dive limit (ADL). Mammals that regularly perform deep, long-duration dives have locomotor muscles with elevated myoglobin concentrations that are composed of predominantly large, slow-twitch (Type I) fibers with low mitochondrial volume densities (V mt ). These features contribute to extending ADL by increasing oxygen stores and decreasing metabolic rate. Recent tagging studies, however, have challenged the view that two groups of extreme deep-diving cetaceans dive within their ADLs. Beaked whales (including Ziphius cavirostris and Mesoplodon densirostris) routinely perform the deepest and longest average dives of any air-breathing vertebrate, and short-finned pilot whales (Globicephala macrorhynchus) perform high-speed sprints at depth. We investigated the locomotor muscle morphology and estimated total body oxygen stores of several species within these two groups of cetaceans to determine whether they (1) shared muscle design features with other deep divers and (2) performed dives within their calculated ADLs. Muscle of both cetaceans displayed high myoglobin concentrations and large fibers, as predicted, but novel fiber profiles for diving mammals. Beaked whales possessed a sprinterʼs fiber-type profile, composed of ~80% fast-twitch (Type II) fibers with low V mt . Approximately one-third of the muscle fibers of short-finned pilot whales were slow-twitch, oxidative, glycolytic fibers, a rare fiber type for any mammal. The muscle morphology of beaked whales likely decreases the energetic cost of diving, while that of short-finned pilot whales supports high activity events. Calculated ADLs indicate that, at low metabolic rates, both beaked and short-finned pilot whales carry sufficient onboard oxygen to aerobically support their dives. Supplementary material available online at

Muscle biochemistry of a pelagic delphinid (Stenella longirostris longirostris): insight into fishery-induced separation of mothers and calves

“…Indeed, comparisons between the pelagic spinner dolphin and coastal bottlenose dolphin indicated that myoglobin contents of the pelagic species were consistently higher than the corresponding age class of the coastal species (Table 2). Furthermore, the myoglobin levels (range from 6.00 to 7.10 g Mb per 100 g wet muscle mass) of adult pelagic delphinids [spinner ( present study) and Fraser's dolphin, Lagenodelphis hosei (Dolar et al, 1999)] fall within the range (6.82-7.41 g Mb per 100 g wet muscle mass) measured for deepdiving cetaceans, such as short-finned pilot whales (Globicephala macrorhynchus; Velten et al 2013) and Gervais' beaked whales (Mesoplodon europaeus; Velten et al 2013). Myoglobin levels of adult pelagic delphinids also fall within the range (6.91-7.87 g Mb per 100 g wet muscle mass) reported for adult Arctic dwelling cetaceans, such as the narwhal (Monodon Monoceros; Williams et al, 2011) and beluga whale (Noren and Suydam, 2016), that must transit under sea ice.…”

Swimming and diving energetics in dolphins: a stroke-by-stroke analysis for predicting the cost of flight responses in wild odontocetes

“…Currently, this class of deep-diving odontocete is considered unique in terms of the comparatively high levels of muscle myoglobin in the skeletal muscle as well as the high proportion of body mass composed of muscle (Velten et al, 2013). To account for this, we assumed that skeletal muscle mass of the Cuvier's beaked whale was proportionately the same as reported for other deep-diving beaked whales (48% of body mass) and that myoglobin content was 73.4 g Mb kg −1 muscle (Velten et al, 2013). Multiplying by the oxygen carrying capacity of mammalian myoglobin (1.34 ml O 2 g -1 Mb) results in 118 liters of O 2 available in the beaked whale's skeletal muscles.…”

“…Multiplying by the oxygen carrying capacity of mammalian myoglobin (1.34 ml O 2 g -1 Mb) results in 118 liters of O 2 available in the beaked whale's skeletal muscles. This muscle oxygen store is only a portion of the total body oxygen store of the odontocete, which ranges from 30% of the total store (Noren and Williams, 2000) to 54% (Velten et al, 2013); we used a mean value of 40% as the conservative estimate for this study, with a resulting total body oxygen store of 295 liters of O 2 for a 2500 kg Cuvier's beaked whale.…”

Gait switches in deep-diving beaked whales: biomechanical strategies for long-duration dives

“…Two fibre types are found in the musculature of fish : slow-twitch oxidative fibres (red muscle or Type I) are used for slow steady swimming, while fast-twitch fibres (white muscle or Type II) are recruited to power brief bursts of fast swimming during predator avoidance or prey capture (Alexander and Goldspink, 1977). Type I and II muscle fibres are also present in the swimming muscles of marine mammals but less is known about how these are employed (Kanatous et al, 2008;Velten et al, 2013). It is generally assumed that diving mammals minimize their reliance on anaerobic metabolism by choosing dive durations in keeping with their activity levels (Butler and Jones, 1997).…”

“…Like other deep-diving marine mammals, beaked whales also have physiological adaptations that prolong their ADL: high lipid volume density and myoglobin concentrations increase oxygen stores while extremely low mitochondrial volume densities and large fibre diameters reduce the metabolic rate (Velten et al, 2013;Davis, 2014). Nonetheless, it is likely that the two smallest ziphiid species studied to date, Cuvier's and Blainville's beaked whales, routinely dive beyond their ADL, powering some portion of locomotion in deep dives anaerobically Velten et al, 2013). Despite this, both species make distinctive and enigmatic low-pitch ascents from deep dives.…”