Migratory songbirds exhibit seasonal modulation of the oxygen cascade

Abstract

Migratory flight requires birds to maintain intensive aerobic exercise for many hours or days. Maintaining O2 supply to flight muscles is therefore important during migration, especially since migratory songbirds have been documented flying at altitudes greater than 5000 m above sea level, where O2 is limited. Whether songbirds exhibit seasonal plasticity of the O2 cascade to maintain O2 uptake and transport during migratory flight is not well understood. We investigated changes in the hypoxic ventilatory response, haematology and pectoralis (flight) muscle phenotype of 6 songbird species from 3 families during migratory and non-migratory conditions. Songbirds were captured during southbound migration in southern Ontario, Canada. Half of the birds were assessed during migration, and the rest were transitioned onto a winter photoperiod to induce a non-migratory phenotype and measured. All species exhibited seasonal plasticity at various stages along the O2 cascade, but not all species exhibited the same responses. Songbirds tended to be more hypoxia tolerant during migration, withstanding 5 kPa O2 and breathed more effectively through slower, deeper breaths. Warblers had a stronger haemoglobin-O2 affinity during autumn migration (decrease of ∼4.7 Torr), while the opposite was observed in thrushes (increase of ∼2.6 Torr). In the flight muscle there was an ∼1.2-fold increase in the abundance of muscle fibres with smaller fibre transverse areas during autumn migration, but no changes in capillary:fibre ratio. These adjustments would enhance O2 uptake and transport to the flight muscle. Our findings demonstrate that in the O2 cascade there is no ideal migratory phenotype for all songbirds.

Keywords: Control of breathing; Haematology; Muscle morphology; Thrushes; Vireos; Warblers.

Fig. 1.

Body mass and fat measurements are influenced by migration state in most species of songbirds. (A) Body mass and (B) % fat and % wet lean mass of body mass. Within family, long-distance migrants (red-eyed vireos, blackpoll warblers and Swainson's thrushes) are all heavier than the short-distance migrants (warbling vireos, myrtle yellow-rumped warblers, hermit thrushes). Reductions in body mass during autumn migration are associated with reduced percentages of fat and increased percentages of wet lean mass. Individual values are plotted in A, in addition to mean±s.e.m. φ represents a significant difference between species within a family; * represents a significant difference between migrating and non-migrating conditions within a species, after a two-factor ANOVA within each family; P<0.05. N for all figures (migratory, non-migratory): warbling vireo=6, 6; red-eyed vireo=6, 5; yellow-rumped warbler=7, 7; blackpoll warbler=8, 7; hermit thrush=8, 8; Swainson's thrush=8, 8.

Fig. 2.

Breathing responses to progressive hypoxia in vireos, warblers and thrushes during migratory and non-migratory conditions. Breathing responses to progressive hypoxia (21, 16, 12, 9, 7, 5 kPa O₂) in vireos (A,D,G), warblers (B,E,H) and thrushes (C,F,I) during migratory (solid symbols) and non-migratory (open symbols) conditions. Increases in total ventilation (A–C) during hypoxia challenge are driven primarily by increases in breathing frequency (D–F) in all species, while tidal volume remains constant (G–I). Grey symbols (graphs on left in each panel) represent short-distance migrants and black symbols (right) represent long-distance migrants. Values are means±s.e.m.; * represents a significant main effect of season (migratory versus non-migratory); * represents a significant pairwise difference between migratory and non-migratory conditions within a P_O2 level, based on a two-factor ANCOVA within each species; P<0.05.

Fig. 3.

Breathing and metabolic responses to progressive hypoxia in vireos, warblers and thrushes during migratory and non-migratory conditions. Oxygen consumption increased during non-migratory conditions in many species (A–C), resulting in reduced air convection requirements (D–F) and greater pulmonary oxygen extraction (G–I) compared with migratory conditions. Grey symbols represent short-distance migrants and black symbols represent long-distance migrants. Values are means±s.e.m.; * represents a significant main effect of season (migratory versus non-migratory); * represents a significant pairwise difference between migratory and non-migratory conditions within a P_O2 level, based on a two-factor ANCOVA within each species.

Fig. 4.

Body temperature responses to progressive hypoxia in vireos, warblers and thrushes during migratory and non-migratory conditions. Resting body temperature (normoxia) was significantly lower during the migratory season in most species, but season did not significantly influence the decline in body temperature in hypoxia. Grey symbols represent short-distance migrants and black symbols represent long-distance migrants. Values are means±s.e.m.; * represents a significant pairwise difference between migratory and non-migratory conditions within a P_O2 level, based on a two-factor ANCOVA within each species.

Fig. 5.

Haemoglobin-oxygen binding affinity (P₅₀) in warblers and thrushes during migratory and non-migratory conditions. Hb–O₂ affinity was influenced by season in some species. Values are means±s.e.m.; groups that do not share letters within a songbird family represent a significant pairwise difference between season and species; * represents a significant main effect of season within a family after a two-factor ANOVA within each family.

Fig. 6.

Representative images of the pectoralis muscle of myrtle yellow-rumped warblers and blackpoll warblers during autumn migration and non-migratory conditions. Fluorescence immunohistochemistry was used to identify muscle boundaries (laminin, in magenta) and capillaries (Griffonia simplicifolia lectin 1, in yellow). Scale bar: 100 μm.

Fig. 7.

Fibre and capillary histology of the pectoralis muscle in vireos, warblers and thrushes during migratory and non-migratory conditions. Fibre density (A), transverse area (B) and capillary density (C) are influenced by season in warblers and thrushes, and mainly in the short-distance migrants (those that stay within North America), but capillary-fibre ratio is not altered with season (D). Values are means±s.e.m.; * represents a significant pairwise difference between migratory and non-migratory conditions within a species; * represents a significant main effect of season within a family after a two-factor ANOVA within each family.