Abstract Migration is one of the most energy-demanding behaviors observed in birds. Mitochondria are the primary source of energy used to support these long-distance movements, yet how mitochondria meet the energetic demands of migration is scarcely studied. We quantified changes in mitochondrial respiratory performance in the White-crowned Sparrow (Zonotrichia leucophrys), which has a migratory and non-migratory subspecies. We hypothesized that the long-distance migratory Gambel’s subspecies (Z. l. gambelii) would show higher mitochondrial respiratory performance compared to the non-migratory Nuttall’s subspecies (Z. l. nuttalli). We sampled Gambel’s individuals during spring pre-migration, active fall migration, and a period with no migration or breeding (winter). We sampled Nuttall’s individuals during periods coinciding with fall migration and the winter period of Gambel’s annual cycle. Overall, Gambel’s individuals had higher citrate synthase, a proxy for mitochondrial volume, than Nuttall’s individuals. This was most pronounced prior to and during migration. We found that both OXPHOS capacity (state 3) and basal respiration (state 4) of mitochondria exhibit high seasonal flexibility within Gambel’s individuals, with values highest during active migration. These values in Nuttall’s individuals were most similar to Gambel’s individuals in winter. Our observations indicate that seasonal changes in mitochondrial respiration play a vital role in migration energetics.
more »
« less
This content will become publicly available on December 1, 2025
Mitochondrial remodelling supports migration in white-crowned sparrows ( Zonotrichia leucophrys )
The migratory movements undertaken by birds are among the most energetically demanding behaviours observed in nature. Mitochondria are the source of aerobic energy production on which migration depends, but a key component of mitochondrial function, mitochondrial remodelling, has not been investigated in the context of bird migration. We measured markers of mitochondrial remodelling in the skeletal muscles of the Gambel’s (migratory) and Nuttall’s (non-migratory) white-crowned sparrows within and outside migratory periods. Gambel’s were collected in (i) a non-migration period (baseline), (ii) preparation to depart for spring migration (pre-migration) and (iii) active autumn migration (mid-migration). Nuttall’s were collected at timepoints corresponding to baseline and mid-migration in Gambel’s. Across all sampling periods, we found that migratory birds had greater mitochondrial remodelling compared with non-migratory birds. Furthermore, birds from the migratory population also displayed flexibility, increasing several markers of mitochondrial remodelling (e.g. NRF1, OPA1 and Drp1) pre- and during migration. Further, the greater levels of mitochondrial remodelling and its upregulation during migration were specific to the pectoralis muscle used in flapping flight. Our study is the first to show that mitochondrial remodelling supports migration in Gambel’s white-crowned sparrows, indicating a highly specific and efficient phenotype supporting the increased energetic demands of migration.
more »
« less
- Award ID(s):
- 2223528
- PAR ID:
- 10616829
- Publisher / Repository:
- The Royal Society
- Date Published:
- Journal Name:
- Proceedings of the Royal Society B: Biological Sciences
- Volume:
- 291
- Issue:
- 2036
- ISSN:
- 1471-2954
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Synopsis Birds exhibit a variety of migration strategies. Because sustained flapping flight requires the production of elevated levels of energy compared to typical daily activities, migratory birds are well-documented to have several physiological adaptations to support the energy demands of migration. However, even though mitochondria are the source of ATP that powers flight, the respiratory performance of the mitochondria is almost unstudied in the context of migration. We hypothesized that migratory species would have higher mitochondrial respiratory performance during migration compared to species that do not migrate. To test this hypothesis, we compared variables related to mitochondrial respiratory function between two confamilial bird species—the migratory Gray Catbird (Dumetella carolinensis) and the non-migratory Northern Mockingbird (Mimus polyglottos). Birds were captured at the same location along the Alabama Gulf Coast, where we assumed that Gray Catbirds were migrants and where resident Northern Mockingbirds live year-round. We found a trend in citrate synthase activity, which suggests that Gray Catbirds have a greater mitochondrial volume in their pectoralis muscle, but we observed no other differences in mitochondrial respiration or complex enzymatic activities between individuals from the migrant vs. the non-migrant species. However, when we assessed the catbirds included in our study using well-established indicators of migratory physiology, birds fell into two groups: a group with physiological parameters indicating a physiology of birds engaged in migration and a group with the physiology of birds not migrating. Thus, our comparison included catbirds that appeared to be outside of migratory condition. When we compared the mitochondrial performance of these three groups, we found that the mitochondrial respiratory capacity of migrating catbirds was very similar to that of Northern Mockingbirds, while the catbirds judged to be not migrating were lowest. One explanation for these observations is these species display very different daily flight behaviors. While the mockingbirds we sampled were not breeding nor migrating, they are highly active birds, living in the open and engaging in flapping flights throughout each day. In contrast, Gray Catbirds live in shrubs and fly infrequently when not migrating. Such differences in baseline energy needs likely confounded our attempt to study adaptations to migration.more » « less
-
null (Ed.)Songbirds meet the extreme metabolic demands of migration by burning both stored fat and protein. However, catabolizing these endogenous tissues for energy leads to organ atrophy, and reductions in gastrointestinal tissue can be as great as 50% of the pre-flight mass. Remarkably, during stopover refuelling birds quickly regain digestive mass and performance. Aminopep- tidase-N (APN) is a brush-border enzyme responsible for late-stage protein digestion and may critically assist tissue reconstruction during the stopover, thus compensating for reduced gut size. We hypothesized that birds recover- ing from a fast would differentially upregulate APN activity relative to disaccharidases to rapidly process and assimilate dietary protein into lean mass. We fasted 23 wild-caught migratory white-throated sparrows (Zonotrichia albicollis) for 48h to mimic mass reductions experienced during migratory flight and measured intestinal APN activity before the fast, immediately after the fast, and during recovery at 24 h and 48 h post- fast. Total fat mass, lean mass and basal metabolic rate were measured daily. We show that fasted birds maintain APN activity through the fast, despite a 30% reduction in intestine mass, but during refuelling, APN activity increases nearly twofold over pre-fasted individuals. This suggests that dynamically regulating APN may be necessary for rapid protein reconstruction during the stopover.more » « less
-
Animal social interactions have an intrinsic spatial basis as many of these interactions occur in spatial proximity. This presents a dilemma when determining causality: Do individuals interact socially because they happen to share space, or do they share space because they are socially linked? We present a method that uses demographic turnover events as a natural experiment to investigate the links between social associations and space use in the context of interannual winter site fidelity in a migratory bird. We previously found that golden-crowned sparrows ( Zonotrichia atricapilla ) show consistent flocking relationships across years, and that familiarity between individuals influences the dynamics of social competition over resources. Using long-term data on winter social and spatial behavior across 10 y, we show that i) sparrows exhibit interannual fidelity to winter home ranges on the scale of tens of meters and ii) the precision of interannual site fidelity increases with the number of winters spent, but iii) this fidelity is weakened when sparrows lose close flockmates from the previous year. Furthermore, the effect of flockmate loss on site fidelity was higher for birds that had returned in more than 2 winters, suggesting that social fidelity may play an increasingly important role on spatial behavior across the lifetime of this migratory bird. Our study provides evidence that social relationships can influence site fidelity, and shows the potential of long-term studies for disentangling the relationship between social and spatial behavior.more » « less
-
Abstract Although the endocrine system likely plays an important role in orchestrating the transition to a migratory state, the specific mechanisms by which this occurs remain poorly understood. Changes in glucocorticoid signaling are one proposed mechanism that may be important in migratory transitions. Although previous work has focused on the role of changes in circulating glucocorticoids, another potential mechanism is changes in the expression of its cognate receptors. Here, we test this hypothesis by comparing mRNA expression of the genes for the mineralocorticoid receptor ( MR ) and glucocorticoid receptor ( GR ) in two brain regions implicated in the regulation of migratory behavior (the hippocampus and hypothalamus) in pine siskins ( Spinus pinus ) sampled before or after the transition to a spring nomadic migratory state. Compared to pre-migratory birds, migratory birds had body conditions more indicative of physiological preparations for migration (e.g., larger body mass), and greater levels of nocturnal migratory restlessness. However, we found no differences between pre-migratory and migratory birds in the expression of GR or MR mRNA in either the hippocampus or hypothalamus. Thus, differences in expression of receptors for glucocorticoids do not appear to underly the observed differences in physiology and behavior across a migratory transition. Taken together with previous results showing no change in circulating corticosterone levels during this transition, our findings provide no evidence for a role of glucocorticoid signaling in the spring migratory transition of this species.more » « less
An official website of the United States government
