Atlantic Grey Seal Milk Shows Continuous Changes in Key Metabolites and Indicators of Metabolic Transition in Pups From Birth to Weaning

David G Watson,Malcolm W Kennedy,Patrick P Pomeroy

doi:10.3389/fmars.2020.596904

David G Watson, Malcolm W Kennedy + Show 1 more

Open Access

https://doi.org/10.3389/fmars.2020.596904

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Abstract

Mothers of the Atlantic grey seal,Halichoerus grypus, lactate for about 20 days, during which they do not feed and may have no access to water. Following weaning, they depart to sea leaving their pups unattended and unfed for up to another 40 days. We are interested in how this lactation strategy supports the pups’ rapid growth and development while also preparing them for their long fast before independently going to sea. We report a broad spectrum metabolomic analysis of whole milks of these seals that reveals continuous changes in key metabolites from birth to weaning. Certain components exhibit abbreviated appearances at the onset of lactation, followed by continuous rises or falls in others until weaning. Riboflavin/Vitamin B2, hormone-related sterol sulfates, lactose, and complex oligosaccharides all appear in milk briefly after birth then disappear. Lipids associated with cellular signaling and brain development occur at highest levels shortly after birth, then diminish. In contrast, other lipids and Vitamin B6/pyridoxine steadily increase as weaning approaches. Overall, these findings may indicate an early transition from carbohydrate to fat-based energy metabolism and establishment of gut microbiomes in pups, followed by provisioning for post-weaning development and fasting.

Highlights

Milks are a critical source of nutrition and passive immune protection for mammalian neonates
Oligosaccharides can comprise the main carbohydrates in milks, and, excepting lactose, they may not be digested or absorbed for energy metabolism (Gnoth et al, 2000; German et al, 2008; Zivkovic et al, 2011)
Some milk oligosaccharides are metabolized by gut microorganisms, such as Bifidobacterium spp., that are enriched in the gut of naturally nursed animals and humans (Zivkovic et al, 2011; Musilova et al, 2014; James et al, 2019)

Summary

Introduction

Milks are a critical source of nutrition and passive immune protection for mammalian neonates. Milks of eutherian (“placental”) mammals change dramatically in composition during the immediate post-partum period and usually resolve into stable, “mature” phases (Langer, 2009) The nature of these changes reflects the type of placenta that a species exhibits. Oceanic marine mammals produce precocial neonates that are invested with large fat reserves that provide insulation against hypothermia when birthed in water, on land in exposed coastal environments, or on ice (Berta et al, 2015a). Those that birth on land or ice are the pinnipeds (sea lions and eared seals; Ottariidae), the walruses (Odobenidae), and the true, “earless” seals (Phocidae). These seals are capital breeders whose brief, intense lactations are thought to have evolved in response to exploitation of transient pack ice for pup rearing, reduction in total energy costs of hunting and feeding vs. lactation, and predation (Schulz and Bowen, 2004, 2005; Berta et al, 2015b)

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