Ontogeny of Oxygen Storage Capacity and Diving Ability in the Southern Sea Otter (Enhydra lutris nereis): Costs and Benefits of Large Lungs

Abstract

Small body size, large lungs, and dense pelage contribute to the unique challenges faced by diving sea otters (Enhydra lutris) when compared to other marine mammals. Here we determine the consequences of large lungs on the development of diving ability in southern sea otters (Enhydra lutris nereis) by examining the ontogeny of blood, muscle, and lung oxygen stores and calculating aerobic dive limits (cADL) for immature and mature age classes. Total oxygen storage capacity matures rapidly in sea otters, reaching adult levels by 2 mo postpartum. But this result is driven by exceptional lung capacity at birth, followed by a decrease in mass-specific lung volume with age. Blood and muscle oxygen stores remain well below adult values before weaning, with large pups exhibiting 74% and 54% of adult values, respectively. Slow muscle development limits the capacity of immature sea otters to dive against high positive buoyancy due to comparatively large lungs. Immature sea otters diving with total lung capacity (TLC) experience up to twice the mass-specific positive buoyancy as adults diving with TLC but can reduce these forces to comparable adult levels by using a smaller diving lung volume (DLV). The cADL of a juvenile with DLV is 3.62 min, while the cADL of an adult with TLC is 4.82 min. We find that the magnitude of positive buoyancy experienced by sea otters changes markedly with age and strongly influences the ontogeny of diving ability in this species.

Regional variability in diving physiology and behavior in a widely distributed air-breathing marine predator, the South American sea lionOtaria byronia

“…Similarly, across sea lion species, the Galapagos sea lion, which is the smallest sea lion, has the highest mass-specific oxygen stores of any sea lion, with values comparable to the more proficient diving phocids or true seals (Villegas-Amtmann and . Finally, the smallest marine mammal, the sea otter Enhydra lutris, has mass-specific oxygen stores that are surprisingly high and comparable to those measured for phocid seals and the Galapagos sea lion (Thometz et al, 2015).…”

“…Therefore, the ADL can be used to determine whether and when sea lions are performing dives that approach their maximum aerobic capacity, which has been reported for other benthic and deep-diving otariids (Costa et al, 2001(Costa et al, , 2004. At a population level, such a diving strategy could put a species at risk if they are unable to cope with environmental variability and fluctuations (Boyd, 1997;Costa et al, 2001;Thometz et al, 2015). Although the South American sea lion is categorized as a species of Least Concern (IUCN), the recovery of local stocks in the decades following their commercial harvest differs greatly between regions.…”

“…As the estimation of total body oxygen stores requires sampling and handling of animals, our knowledge is biased towards amphibious species that can be handled on land ( pinnipeds, penguins and reptiles), or small cetaceans and sirenians that can be sampled in captivity or post mortem (Noren et al, 2002;Noren and Williams, 2000). While the differences in oxygen stores and diving physiology caused by intrinsic factors, such as age, size and gender have been examined (Fowler et al, 2007;Hassrick et al, 2010;MacArthur et al, 2001;Ponganis et al, 1999;Richmond et al, 2006;Weise and Costa, 2007), the role of the extrinsic environmental changes on diving physiology has only recently been considered (Costa et al, 2004;Maekawa and Kato, 2015;Thometz et al, 2015;Villegas-Amtmann et al, 2012).…”

The high cost of reproduction in sea otters necessitates unique physiological adaptations

“…At 63 days postpartum, the proportion of energy demands met by a pup was modeled as a linear increase of 0.5% of pup energy demands each day. This estimation was based on the progressive increase in diving and foraging abilities documented for dependent pups (Thometz et al, 2015) and the knowledge that despite such increases, pups continue to nurse and solicit food from mothers until weaning [Payne and Jameson, 1984; M. M. Staedler, Maternal care and provisioning in the southern sea otter (Enhydra lutris nereis): reproductive consequences of diet specialization in an apex predator, Masters thesis, University of California Santa Cruz, USA, 2011]. We acknowledge that the true start time and progression of independent energy retrieval by pups is highly variable and that modeling this as a linear trend may overestimate prey retrieval initially and underestimate prey retrieval near weaning.…”

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.…”