Consequences of being phenotypically mismatched with the environment: Rapid muscle ultrastructural changes in cold-shocked black-capped chickadees (Poecile atricapillus)

Phenotypic flexibility has received considerable attention in the last decade; however, whereas many studies have reported amplitude of variation in phenotypic traits, much less attention has focused on the rate at which traits can adjust in response to sudden changes in the environment. We investigated whole animal and muscle phenotypic changes occurring in black-capped chickadees (Poecile atricapillus) acclimated to cold (-5°C) and warm (20°C) temperatures in the first 3 h following a 15°C temperature drop (over 3 h). Before the temperature change, cold-acclimated birds were consuming 95% more food, were carrying twice as much body fat, and had 23% larger pectoralis muscle fiber diameters than individuals kept at 20°C. In the 3 h following the temperature drop, these same birds altered their pectoralis muscle ultrastructure by increasing the number of capillaries per fiber area and the number of nuclei per millimeter of fiber by 22%, consequently leading to a 22% decrease in myonuclear domain (amount of cytoplasm serviced per nucleus), whereas no such changes were observed in the warm-acclimated birds. To our knowledge, this is the first demonstration of such a rapid adjustment in muscle fiber ultrastructure in vertebrates. These results support the hypothesis that chickadees maintaining a cold phenotype are better prepared than warm-phenotype individuals to respond to a sudden decline in temperature, such as what may be experienced in their natural wintering environment

Snow Buntings Maintain Winter-Level Cold Endurance While Migrating to the High Arctic

Arctic breeding songbirds migrate early in the spring and can face winter environments requiring cold endurance throughout their journey. One such species, the snow bunting (Plectrophenax nivalis), is known for its significant thermogenic capacity. Empirical studies suggest that buntings can indeed maintain winter cold acclimatization into the migratory and breeding phenotypes when kept captive on their wintering grounds. This capacity could be advantageous not only for migrating in a cold environment, but also for facing unpredictable Arctic weather on arrival and during preparation for breeding. However, migration also typically leads to declines in the sizes of several body components linked to metabolic performance. As such, buntings could also experience some loss of cold endurance as they migrate. Here, we aimed to determine whether free-living snow buntings maintain a cold acclimatized phenotype during spring migration. Using a multi-year dataset, we compared body composition (body mass, fat stores, and pectoralis muscle thickness), oxygen carrying capacity (hematocrit) and metabolic performance (thermogenic capacity – Msum and maintenance energy expenditure – BMR) of birds captured on their wintering grounds (January–February, Rimouski, QC, 48°N) and during pre-breeding (April–May) in the Arctic (Alert, NU, 82°). Our results show that body mass, fat stores and Msum were similar between the two stages, while hematocrit and pectoralis muscle thickness were lower in pre-breeding birds than in wintering individuals. These results suggest that although tissue degradation during migration may affect flight muscle size, buntings are able to maintain cold endurance (i.e., Msum) up to their Arctic breeding grounds. However, BMR was higher during pre-breeding than during winter, suggesting higher maintenance costs in the Arctic

Phenotypic constraints at the top of the world: an Arctic songbird faces the cumulative cost of maintaining a winter-like phenotype during breeding

Among birds, several body composition traits typically decrease in size or mass during breeding likely as a result of competing demands during this critical life history stage. However, a recent outdoor captive study in an Arctic-breeding cold-specialist songbird (snow buntings – Plectrophenax nivalis) demonstrated that these birds maintain winter cold acclimatization during the spring and summer, despite facing summer temperatures much warmer than on their Arctic breeding grounds. This suggests that buntings may face a cumulative physiological cost during breeding: having to support a winter phenotype while also upregulating additional traits for reproduction. The current study aimed to test this hypothesis. Between 2016 and 2019, we examined how body composition and metabolic performance (thermogenic capacity and physiological maintenance costs) changed from pre-breeding to chick provisioning in free-living birds captured at the northern limit of their breeding range in the Canadian Arctic (Alert, NU, 82°). While body mass and fat reserves deceased significantly between pre-breeding and territory defense independent of thermal conditions, cold endurance and associated traits remained stable and elevated up to the nestling provisioning period, as long as ambient temperature remained below a threshold level of 0–2°C. These results indicate that snow buntings must maintain a high thermogenic capacity after arrival on the breeding grounds if temperatures remain below freezing, regardless of whether birds are actively breeding or not. In this context, our research suggests that these birds, and possibly other arctic breeding songbirds, may experience cumulative physiological costs during years with a late onset of spring, when breeding activities (i.e., egg production and incubation) begin while temperatures are still below 0–2°C

Phenotypic constraints at the top of the world: an Arctic songbird faces the cumulative cost of maintaining a winter-like phenotype during breeding

Among birds, several body composition traits typically decrease in size or mass during breeding likely as a result of competing demands during this critical life history stage. However, a recent outdoor captive study in an Arctic-breeding cold-specialist songbird (snow buntings – Plectrophenax nivalis) demonstrated that these birds maintain winter cold acclimatization during the spring and summer, despite facing summer temperatures much warmer than on their Arctic breeding grounds. This suggests that buntings may face a cumulative physiological cost during breeding: having to support a winter phenotype while also upregulating additional traits for reproduction. The current study aimed to test this hypothesis. Between 2016 and 2019, we examined how body composition and metabolic performance (thermogenic capacity and physiological maintenance costs) changed from pre-breeding to chick provisioning in free-living birds captured at the northern limit of their breeding range in the Canadian Arctic (Alert, NU, 82°). While body mass and fat reserves deceased significantly between pre-breeding and territory defense independent of thermal conditions, cold endurance and associated traits remained stable and elevated up to the nestling provisioning period, as long as ambient temperature remained below a threshold level of 0–2°C. These results indicate that snow buntings must maintain a high thermogenic capacity after arrival on the breeding grounds if temperatures remain below freezing, regardless of whether birds are actively breeding or not. In this context, our research suggests that these birds, and possibly other arctic breeding songbirds, may experience cumulative physiological costs during years with a late onset of spring, when breeding activities (i.e., egg production and incubation) begin while temperatures are still below 0–2°C

Whole genome sequencing of an avipoxvirus associated with infections in a group of aviary-housed snow buntings (Plectrophenax nivalis)

Avipoxvirus infections have been reported in both free-ranging and domestic birds worldwide. Fowlpox and canarypox viruses belong to the genus Avipoxvirus among the virus family Poxviridae. They cause cutaneous lesions with proliferative growths on the unfeathered parts of the skin and/or diphtheritic lesions generally associated with necrosis in the upper respiratory and digestive tracts. In this study, a poxvirus has been identified in wild-caught snow buntings (Plectrophenax nivalis) housed in an outdoor aviary in the region of Rimouski, Quebec. During the falls and winters of 2015 and 2016, eight snow buntings affected by this infection were examined. Macroscopic and microscopic lesions observed were characteristic of an avipoxvirus infection. Electron microscopy imaging of an ultrathin section of the histopathological lesions of two birds confirmed the presence of the poxvirus. Afterward, the presence of the poxvirus was confirmed in three birds by a specific polymerase chain reaction assay that amplified a segment of the gene encoding the fowlpox virus 4b core protein. A 576-nucleotide amplicon was obtained from one of them and sequenced. The analyses revealed a 99% homology to other previously described avipoxviruses. Using high-throughput sequencing, almost the entire viral genome of this avipoxvirus was revealed and found to possess a 359,853-nucleotide sequence in length. Bioinformatic analyses revealed that the virus was genetically related to canarypox virus. To our knowledge, this is the first confirmed case and full description of a poxviral infection in this species. This episode suggests a high susceptibility of this northern species of passerine to avipoxviruses circulating in southeastern Canada during the summer months. Even if the source of the viral infections remains undetermined, transmission by local biological vectors is suspected. Management of poxviral infections in snow buntings housed outdoors in southeastern Canada could rely on the control of biting insects

Consequences of being phenotypically mismatched with the environment: Rapid muscle ultrastructural changes in cold-shocked black-capped chickadees (Poecile atricapillus)

Phenotypic flexibility has received considerable attention in the last decade; however, whereas many studies have reported amplitude of variation in phenotypic traits, much less attention has focused on the rate at which traits can adjust in response to sudden changes in the environment. We investigated whole animal and muscle phenotypic changes occurring in black-capped chickadees (Poecile atricapillus) acclimated to cold (-5°C) and warm (20°C) temperatures in the first 3 h following a 15°C temperature drop (over 3 h). Before the temperature change, cold-acclimated birds were consuming 95% more food, were carrying twice as much body fat, and had 23% larger pectoralis muscle fiber diameters than individuals kept at 20°C. In the 3 h following the temperature drop, these same birds altered their pectoralis muscle ultrastructure by increasing the number of capillaries per fiber area and the number of nuclei per millimeter of fiber by 22%, consequently leading to a 22% decrease in myonuclear domain (amount of cytoplasm serviced per nucleus), whereas no such changes were observed in the warm-acclimated birds. To our knowledge, this is the first demonstration of such a rapid adjustment in muscle fiber ultrastructure in vertebrates. These results support the hypothesis that chickadees maintaining a cold phenotype are better prepared than warm-phenotype individuals to respond to a sudden decline in temperature, such as what may be experienced in their natural wintering environment

Wintering snow buntings elevate cold hardiness to extreme levels but show no changes in maintenance costs

Resident temperate passerines adjust their phenotypes to cope with winter constraints, with peak performance in metabolic traits typically occurring during the coldest months. However, it is sparsely known whether cold-adapted northern species make similar adjustments when faced with variable seasonal environments. Life in near-constant cold could be associated with limited flexibility in traits underlying cold endurance. We investigated this by tracking individual physiological changes over five consecutive winters in snow buntings (Plectrophenax nivalis), an Arctic-breeding migratory passerine typically confronted with nearly constant cold. Buntings were held in an outdoor aviary and exposed to seasonal temperature variation typical of temperate zone climates. We measured phenotypic changes in body composition (body, fat, and lean mass, pectoralis muscle thickness), oxygen transport capacity (hematocrit), metabolic performance (basal metabolic rate [BMR] and summit metabolic rate [Msum]), thermogenic endurance (time to reach Msum), and cold tolerance (temperature at Msum). Snow buntings showed flexibility in functions underlying thermogenic capacity and cold endurance comparable to that observed in temperate resident passerines wintering at similar latitudes. Specifically, they increased body mass (13%), fat mass (246%), hematocrit (23%), pectoralis muscle thickness (8%), and Msum (27%). We also found remarkable cold tolerance in these birds, with individuals reaching Msum in helox at temperatures equivalent to less than 2907C in air. However, in contrast with resident temperate passerines, lean mass decreased by 12%, and there was no clear increase in maintenance costs (BMR). Our results show that the flexibility of traits underlying thermal acclimatization in a cold-adapted northern species is comparable to that of temperate resident species living at lower latitudes and is therefore not limited by life in near-constant cold

Snow Buntings Maintain Winter-Level Cold Endurance While Migrating to the High Arctic

Arctic breeding songbirds migrate early in the spring and can face winter environments requiring cold endurance throughout their journey. One such species, the snow bunting (Plectrophenax nivalis), is known for its significant thermogenic capacity. Empirical studies suggest that buntings can indeed maintain winter cold acclimatization into the migratory and breeding phenotypes when kept captive on their wintering grounds. This capacity could be advantageous not only for migrating in a cold environment, but also for facing unpredictable Arctic weather on arrival and during preparation for breeding. However, migration also typically leads to declines in the sizes of several body components linked to metabolic performance. As such, buntings could also experience some loss of cold endurance as they migrate. Here, we aimed to determine whether free-living snow buntings maintain a cold acclimatized phenotype during spring migration. Using a multi-year dataset, we compared body composition (body mass, fat stores, and pectoralis muscle thickness), oxygen carrying capacity (hematocrit) and metabolic performance (thermogenic capacity – Msum and maintenance energy expenditure – BMR) of birds captured on their wintering grounds (January–February, Rimouski, QC, 48°N) and during pre-breeding (April–May) in the Arctic (Alert, NU, 82°). Our results show that body mass, fat stores and Msum were similar between the two stages, while hematocrit and pectoralis muscle thickness were lower in pre-breeding birds than in wintering individuals. These results suggest that although tissue degradation during migration may affect flight muscle size, buntings are able to maintain cold endurance (i.e., Msum) up to their Arctic breeding grounds. However, BMR was higher during pre-breeding than during winter, suggesting higher maintenance costs in the Arctic