Navigating under sea ice promotes rapid maturation of diving physiology and performance in beluga whales

Abstract

Little is known about the postnatal development of the physiological characteristics that support breath-hold in cetaceans, despite their need to swim and dive at birth. Arctic species have the additional demand of avoiding entrapment while navigating under sea ice, where breathing holes are patchily distributed and ephemeral. This is the first investigation of the ontogeny of the biochemistry of the locomotor muscle in a year-round Arctic-dwelling cetacean (beluga whale, Delphinapterus leucas). Compared with what we know about other cetaceans, belugas are born with high myoglobin content (1.56±0.02 g 100 g −1 wet muscle mass, N=2) that matures rapidly. Myoglobin increased by 452% during the first year after birth and achieved adult levels (6.91±0.35 g 100 g −1 wet muscle mass, N=9) by 14 months postpartum. Buffering capacity was 48.88±0.69 slykes (N=2) at birth; adult levels (84.31±1.38 slykes, N=9) were also achieved by 14 months postpartum. As the oxygen stores matured, calculated aerobic dive limit more than doubled over the first year of life, undoubtedly facilitating the movements of calves under sea ice. Nonetheless, small body size theoretically continues to constrain the diving ability of newly weaned 2 year olds, as they only had 74% and 69% of the aerobic breath-hold capacity of larger adult female and male counterparts. These assessments enhance our knowledge of the biology of cetaceans and provide insight into age-specific flexibility to alter underwater behaviors, as may be required with the ongoing alterations in the Arctic marine ecosystem associated with climate change and increased anthropogenic activities.

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

“…However, recent research on pigeon guillemot (Cepphus columba; Haggblom et al, 1988), penguins (Weber et al, 1974;Ponganis et al, 1999;Noren et al, 2001), sea otter (Enhydra lutris nereis; Thometz et al, 2015), pinnipeds (seals, sea lions and walruses; P. H. Thorson, Development of diving in the northern elephant seal, PhD thesis, University of California, Santa Cruz, 1993;Noren et al, 2005Noren et al, , 2015Burns et al, 2005Burns et al, , 2007Richmond et al, 2006;Fowler et al, 2007;Weise and Costa, 2007;Kanatous et al, 2008;Lestyk et al, 2009;Verrier et al, 2011) and cetaceans (whales and dolphins; Dolar et al, 1999;Etnier et al, 2004;Noren, 2004;Noren et al, 2001Noren et al, , 2014Cartwright et al, 2016;Noren and Suydam, 2016; B. P. Velten, A comparative study of the locomotor muscle of extreme deep-diving cetaceans, MSc thesis, University of North Carolina, Wilmington, 2012) have shown that a period of postnatal development is required in order to achieve mature muscle myoglobin content and muscle buffering capacity after birth. It was anticipated that the immediate demands of hypoxia should promote rapid muscle maturation in cetaceans since they are born directly into the ocean, compared with pinnipeds that are born on land and typically spend several months to years on land before foraging on their own (for reviews, see Noren et al, 2005Noren et al, , 2015.…”

“…It was anticipated that the immediate demands of hypoxia should promote rapid muscle maturation in cetaceans since they are born directly into the ocean, compared with pinnipeds that are born on land and typically spend several months to years on land before foraging on their own (for reviews, see Noren et al, 2005Noren et al, , 2015. Yet it was discovered that cetaceans can take approximately 1-3 years after birth to achieve mature myoglobin content (Dolar et al, 1999;Noren et al, 2001Noren et al, , 2014Noren and Suydam, 2016) and buffering capacity (Noren, 2004;Noren et al, 2014;Noren and Suydam, 2016) in the muscle.…”

“…Interestingly, recent investigations on Arctic marine mammal species [Pacific walruses (Odobenus rosmarus divergens; Noren et al, 2015) and beluga whales (Delphinapterus leucas; Noren and Suydam, 2016)] suggested that habitat influences the postnatal development of muscle biochemistry. Walruses and belugas achieved mature muscle properties well before the age of weaning.…”

“…Walruses and belugas achieved mature muscle properties well before the age of weaning. The disconnect between the age of nutritional independence and age of muscle maturation in these species was attributed to the requisite need of walrus and beluga calves to transit amongst sea ice, where breathing holes are patchily distributed and ephemeral (Noren et al, 2015;Noren and Suydam, 2016).…”

“…Adequate sample sizes to provide an estimate of the age in which the muscle biochemistry is fully matured is only available for three species, a delphinid (Noren et al, 2001;Noren, 2004), phocoenid (Noren et al, 2014) and monodontid (Noren and Suydam, 2016). Yet there are 88 cetacean species recognized by the International Union for Conservation of Nature that live in very diverse habitats (e.g.…”