Blood metabolites as indicators of nutrient utilization in fasting, lactating phocid seals: does depletion of nutrient reserves terminate lactation?

Abstract

Metabolites of lipid (free fatty acids (FFA) and β-hydroxybutyrate (βHBA)) and protein (blood urea nitrogen (BUN)) oxidation were measured during lactation in 18 female grey seals (Halichoerus grypus) and 6 female hooded seals (Cystophora cristata) as indicators of nutrient depletion and possible cues for pup weaning. FFA levels were high during lactation in both grey seals (51.2 ± 2.3 mg·dL -1 ) and hooded seals (67.0 ± 8.1 mg·dL -1 ), and levels were primarily related to the rapid lipid mobilization required for their high respective milk-fat outputs (P = 0.002). βHBA concentrations were negligible throughout lactation in both species (0.30 ± 0.14 and 0.03 ± 0.01 mg·dL -1 , respectively). Grey seals exhibited a decrease in BUN levels over the course of lactation (i.e., days 0-15, 39.3 ± 1.8 -23.5 ± 3.3 mg·dL -1 , P < 0.001), which suggests protein sparing despite the added energetic cost of milk production over the 16-d lactation period. In contrast, hooded seals showed higher levels and no change in BUN levels (i.e., days 0-3, 43.2 ± 2.1 -45.8 ± 2.1 mg·dL -1 , P > 0.3), suggesting that there is less need to spare protein in a species which lactates for only 3.6 d. Females of both species weaned their pups before entering stage III fasting, therefore metabolite levels do not appear to be a physiological cue for weaning.Résumé : Les métabolites de l'oxydation des lipides (acides gras libres (FFA) et $-hydroxybutirate ($HBA)) et des protéines (azote uréique du sang (BUN)) ont été mesurés au cours de la période d'allaitement chez 18 femelles du Phoque gris (Halichoerus grypus) et 6 femelles du Phoque à capuchon (Cystophora cristata) en tant qu'indicateurs de l'épuisement des réserves de nutriments et déclencheurs possibles du sevrage des petits. Les concentrations de FFA sont élevées au cours de l'allaitement chez le Phoque gris (51,2 ± 2,3 mg·dL -1 ) et le Phoque à capuchon (67,0 ± 8,1 mg·dL -1 ) et elles sont reliées surtout à la mobilisation rapide des lipides nécessaires à une abondante production de lait (P = 0,002). La concentration de $HBA est négligeable chez les deux espèces au cours de toute la période d'allaitement (0,30 ± 0,14 et 0,03 ± 0,01 mg·dL -1 , respectivement). Les Phoques gris subissent une diminution de leur BUN durant l'allaitement (i.e., 39,3 ± 1,8 -23,5 ± 3,3 mg·dL -1 du jour 0 au jour 15; P < 0,001) ce qui indique une économie de protéines malgré les coûts énergétiques additionnels de la production de lait au cours des 16 jours de l'allaitement. En revanche, chez le Phoque à capuchon, les concentrations de BUN, plus élevées, ne changent pas (i.e., 43,2 ± 2,1 -45,8 ± 2,1 mg·dL -1 du jour 0 au jour 3; P > 0,3), probablement parce que l'économie des protéines est moins néces-saire chez une espèce dont l'allaitement ne dure que 3,6 jours. Les femelles des deux espèces sèvrent leurs petits avant d'entreprendre la phase III de leur jeûne et donc, la concentration des métabolites ne semble pas être le facteur physiologique déclencheur du sevrage.[Traduit par la Rédaction] Mellish and Iverson 311

Energetic limits: Defining the bounds and trade‐offs of successful energy management in a capital breeder

“…by investigating metabolite trends leading up to weaning; Mellish & Iverson, 2001;Watson, Pomeroy, Al-Tannak, & Kennedy, 2020).…”

“…Previous work has demonstrated that female seals may adjust their reproductive output between years, when faced with changing environmental conditions prior to the lactation period, in order to maximize lifetime reproductive output (Bowen et al, 2015; Desprez et al., 2018; Kalberer, Meise, Trillmich, & Krüger, 2018; McMahon et al., 2016; Pomeroy et al., 1999; Smout et al., 2020), but research has yet to reveal the mechanism for terminating lactation in grey seals (e.g. by investigating metabolite trends leading up to weaning; Mellish & Iverson, 2001; Watson, Pomeroy, Al‐Tannak, & Kennedy, 2020). Extended time spent applying a non‐compensatory energy strategy may result in a heightened energy debt, forcing those individuals to terminate their breeding attempt and possibly also skip the following breeding season to extend their recovery time (Pomeroy et al., 1999).…”

Response of metabolic hormones and blood metabolites to realimentation in rehabilitated harbor seal (Phoca vitulina) pups

“…Previous studies of blood metabolites and metabolic hormones in pinnipeds have focused on the physiology of fasting adaptation and determination of nutritional status in wild populations for health assessment (Costa and Ortiz 1982;Castellini and Rea 1992;Roletto 1993;Hall 1998;Mellish and Iverson 2001;Trumble et al 2006;Crocker et al 2012). However, limited research has investigated the response to realimentation in these fasting adapted species (Richmond et al 2010;Dailey et al 2016).…”

“…Serum metabolites are often used to indicate the overall condition and health status of animals in clinical settings such as rehabilitation. Blood metabolites such as blood urea nitrogen (BUN), total protein, triglycerides, and glucose provide valuable information about the nutritional status of an animal based upon the types of energy sources (protein, lipid, carbohydrate) being utilized (Bossart et al 2001;Mellish and Iverson 2001;McCue 2010).…”

Obtaining accurate glucose measurements from wild animals under field conditions: comparing a hand held glucometer with a standard laboratory technique in grey seals

“…Typically, elevated EGP is required in other mammals to support milk production ( Mohammad et al ., 2009 ). Glucose may thus be higher in grey seals earlier in lactation to support high milk output ( Mellish et al ., 1999 ; Mellish and Iverson, 2000 ). The reduction in circulating glucose later in lactation may reflect decreased EGP to protect protein reserves.…”