A Scaling Approach to Understand the Dynamics of Fat and Lean Mass in Refueling Migrant Songbirds Measured by Quantitative Magnetic Resonance

Abstract

Fat contributes most of the energy for migratory flight of birds, whereas lean body tissues (muscles and organs) contribute amino acids and water to maintain metabolic and osmotic homeostasis. During refueling at stopover sites, both fat and lean mass are recovered, but the dynamics of this recovery are poorly understood. We used non-invasive quantitative magnetic resonance (QMR) analysis to measure fat and lean mass of > 3,500 individuals of 25 songbird species during six spring and three autumn migration seasons between 2009 and 2019 at Long Point, ON, Canada. We used allometric scaling analysis and linear mixed-effects modeling of body composition data at both the population level (single capture) and the individual level (recapture). In the population-level analysis, lean mass scaled hypoallometrically with body mass, such that for every 20% increase in body mass, lean mass was predicted to increase by 12.1% in spring and 12.8% in autumn. Fat scaled hyperallometrically with body mass, such that for every 20% increase in body mass, fat mass was predicted to increase by 144% in spring and 136% in autumn. At the individual level, these allometric relationships were more extreme. As a result of this differential allometry, at low body masses, lean and fat mass contributes nearly equally to changes in mass, but at high body mass fat deposition becomes progressively more dominant. Spring migrants deposited relatively more fat than autumn migrants, and in autumn juvenile birds tended to have greater lean mass than adults. Our findings show that lean mass deposition during refueling by songbirds is substantial, and in line with the losses of protein expected in flight. The process of fat and lean mass deposition is characterized by non-linear dynamics which are influenced by the current body composition, season, and, to a lesser extent, age. The patterns suggest that the need for dietary protein to rebuild lean mass will be greater when body mass is low, during autumn migration, and in juvenile birds.

Riding out the storm: depleted fat stores and elevated hematocrit in a small bodied endotherm exposed to severe weather

“…QMR has previously been used to understand relationships between body composition, energetics and migration in birds and bats (e.g. McGuire et al, 2018 ; Kelsey et al, 2019 ; Guglielmo et al, 2022 ). Furthermore, the use of QMR to quickly and accurately quantify the body composition of live animals has been validated and is repeatable with < 3% coefficients of variation for each measure ( Guglielmo et al, 2011 ).…”

“…muscles and organs; ( Guglielmo and Williams, 2003 ; Gerson and Guglielmo, 2011a ), but gram for gram, mobilization of lean mass yields less energy than fat. Carbohydrates, fat and protein can be used to increase fat stores, while lean mass growth requires a protein rich diet ( Guglielmo et al, 2022 ), and thus, lean mass may respond to environmental stressors more slowly than fat mass due to the need of a more protein-rich diet. Depleted lean mass typically represents either a weight-saving strategy or a source of metabolic water during flight, or more severe energy depletion under starvation conditions ( Karasov and Pinshow, 1998 ; Gerson and Guglielmo, 2011b ).…”