Ajustements phénotypiques en réponse aux contraintes associées à l'hiver, la migration et la reproduction chez le plectrophane des neiges

RÉSUMÉ : Les organismes sont confrontés à de multiples contraintes environnementales auxquelles ils peuvent répondre par des ajustements phénotypiques menant potentiellement à des compromis physiologiques. Contrairement aux espèces vivant uniquement en milieux tempérés, les mécanismes sous-jacents aux ajustements phénotypiques des espèces confrontées au froid la majeure partie de l'année sont encore mal compris. Ma thèse porte sur les ajustements phénotypiques du plectrophane des neiges (Plectrophenax nivalis), un passereau migrateur qui hiverne en zone tempérée (entre 40° et 60°N) et migre au printemps vers les régions arctiques pour se reproduire. Plus particulièrement, je me suis intéressée aux variations de composition corporelle (masse corporelle, lipidique et maigre, épaisseur des muscles pectoraux), de capacité de transport de l'oxygène (hématocrite) et de performance métabolique (coûts de maintenance physiologiques - BMR et de capacité thermogénique - Msum) au cours de l'hiver, de la migration et de la reproduction. Pour cela, j'ai effectué de 2013 à 2019, des mesures (1) sur des individus maintenus captifs en volière extérieure à Rimouski (QC, 48°N), (2) sur des individus capturés sur leur aire d'hivernage à Rimouski et (3) à l'extrême nord de leur aire de reproduction, à Alert au Nunavut (82°N). Dans le chapitre 1, j'ai étudié les ajustements phénotypiques hivernaux des plectrophanes maintenus captifs en zone tempérée. L'objectif était de déterminer si le patron d'ajustements de cette espèce associée au froid la majeure partie de sa vie se conformait à celui des espèces résidentes aux mêmes latitudes. Les augmentations de masse corporelle et lipidique, d'épaisseur des muscles pectoraux, d'hématocrite et de Msum observées entre l'été et l'hiver suggèrent que la flexibilité phénotypique des traits associés à l'acclimatation thermique chez les espèces nordiques est comparable à celle des passereaux résidents des zones tempérées et donc que ces ajustements ne sont pas contraints par la vie dans un environnement froid. Toutefois, le déclin de masse maigre et la stabilité du BMR observés au cours de l'hiver suggèrent que les plectrophanes peuvent aussi minimiser les coûts énergétiques de la vie en milieux froids. Au chapitre 2, j'ai analysé les patrons d'ajustements phénotypiques de plectrophanes maintenus captifs au cours des périodes correspondant à la migration et la reproduction et je les ai comparées au phénotype hivernal. L'objectif était de voir si et par quel mécanisme, les traits associés à l'acclimatation au froid hivernal pouvaient être transférés aux stades ultérieurs du cycle annuel. Les résultats montrent que, bien que la masse corporelle, la masse lipidique et le BMR augmentent pour la migration, les traits liés à l'endurance au froid ne changent pas en parallèle puisqu'ils sont déjà élevés à la sortie de l'hiver. Il s'agit de la première démonstration directe que des traits phénotypiques associés à l'acclimatation hivernale peuvent se transférer au phénotype migratoire et même se maintenir en période de reproduction. Au travers du chapitre 3, j'ai comparé le phénotype de plectrophanes capturés en milieu naturel en hiver à Rimouski et en pré-reproduction à Alert. L'objectif était de déterminer si l'endurance au froid et les traits associés pouvaient se maintenir à un niveau hivernal durant la migration et la pré-reproduction. Les résultats indiquent que malgré un déclin d'épaisseur des muscles et d'hématocrite, l'endurance au froid et les réserves énergétiques étaient maintenues. Ces résultats confirment l'hypothèse selon laquelle les espèces migratrices spécialistes du froid pourraient maintenir leur endurance au froid à un niveau hivernal jusqu'à la pré-reproduction. Enfin dans le Chapitre 4, j'ai examiné l'évolution du phénotype entre la période de pré-reproduction et d'approvisionnement des oisillons à Alert afin de déterminer comment la transition entre les stades de vie sur les aires de reproduction, en interaction avec les conditions thermiques printanières, pouvait influencer l'endurance au froid. Les résultats montrent que les plectrophanes maintiennent une capacité thermogénique élevée tant que les températures demeurent inférieures à 0-2°C, qu'ils se reproduisent activement ou non. Ces observations suggèrent donc que les plectrophanes subissent probablement un double coût physiologique à la fin du printemps, lorsque les activités de reproduction (c.-à-d., production et incubation des œufs) commencent alors que les températures sont encore inférieures à 0-2°C. De manière générale, cette étude démontre que les mécanismes d'acclimatation thermique établis jusqu'à maintenant ne sont pas tous généralisables aux espèces arctiques. Elle constitue donc un point de référence pour de futures recherches comparatives. -- Mot(s) clé(s) en français : Flexibilité phénotypique, Acclimatation au froid, Migration, Taux métabolique de base, Capacité thermogénique maximale, Composition corporelle, Effets reportés, Oiseaux arctiques. -- ABSTRACT : Organisms are confronted with multiple environmental constraints to which they can respond through phenotypic adjustments that can potentially lead to physiological trade-offs. Contrary to species living only in temperate environments, the mechanisms underlying the phenotypic adjustments of species confronted with cold temperatures during most of the year are still poorly understood. My thesis focuses on the phenotypic adjustments of snow bunting's (Plectrophenax nivalis), a migratory passerine that winters in temperate zones (between 40° and 60°N) and migrates in spring to Arctic regions to breed. More specifically, I was interested in the variations of body composition (body mass, lipid and lean mass, pectoral muscle thickness), oxygen transport capacity (hematocrit) and metabolic performance (physiological maintenance costs - BMR and thermogenic capacity - Msum) among the winter, migratory and reproductive stages. For this, I conducted measurements from 2013 to 2019 on individuals either (1) held captive in an outdoor aviary in Rimouski (QC, 48°N), (2) on wild individuals captured on their wintering grounds in Rimouski and (3) wild birds captured at the northernmost point of their breeding range in Alert, Nunavut (82°N). In Chapter 1, I studied the winter phenotypic adjustments of buntings held captive in the temperate zone. The objective was to determine if the pattern of adjustments for this cold-associated species conformed to that of resident species at the same latitudes. Increases in body and lipid mass, pectoral muscle thickness, hematocrit, and Msum observed between summer and winter suggest that the phenotypic flexibility of traits associated with thermal acclimation in northern species is comparable to that of temperate resident passerines and thus that these adjustments are not constrained by life in a cold environment. However, lean mass declined and BMR remained stable over the winter, suggesting that buntings may also minimize the energetic costs of living in cold environments. In Chapter 2, I analyzed the phenotypic adjustment patterns of captive buntings during periods corresponding to migration and reproduction and compared them to the winter phenotype. The objective was to see if, and by what mechanism, traits associated with winter cold acclimation could be transferred to later stages of the annual cycle. The results show that although body mass, lipid mass and BMR increase for migration, traits related to cold endurance do not change in parallel since they are already elevated at the end of winter. This is the first direct demonstration that phenotypic traits associated with winter acclimation can transfer to the migratory phenotype and even be maintained during the breeding season. Through Chapter 3, I compared the phenotype of free-living buntings caught during winter at Rimouski and during pre-breeding at Alert. The objective was to determine whether cold endurance and associated traits could be maintained at a winter level during migration and pre-breeding. Results indicate that despite a decline in muscle thickness and hematocrit between winter and pre-breeding, cold endurance and energy reserves were maintained. These results support the hypothesis that migratory cold specialist species could maintain their cold endurance at a winter level until pre-breeding. Finally, in Chapter 4, I examined the change in phenotype between the pre-breeding and chick provisioning periods at Alert to determine how the transition between life stages on the breeding grounds, in interaction with spring thermal conditions, could influence cold endurance. Results show that buntings maintain a high thermogenic capacity as long as temperatures remain below 0-2°C, whether or not they actively reproduce. These observations therefore suggest that buntings likely experience a double physiological cost in late spring, when reproductive activities (i.e., egg production and incubation) begin and air temperatures are still below 0-2°C. Overall, this study demonstrates that not all thermal acclimation mechanisms e tablished to date are generalizable to Arctic species. It therefore provides a reference point for future comparative research. -- Mot(s) clé(s) en anglais : Phenotypic flexibility, Cold acclimatization, Migration, Basal metabolic rate, Maximal thermogenic capacity, Metabolic performance, Pectoral muscles, Hematocrit, Arctic bird

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

Early life neonicotinoid exposure results in proximal benefits and ultimate carryover effects

Neonicotinoids are insecticides widely used as seed treatments that appear to have multiple negative effects on birds at a diversity of biological scales. Adult birds exposed to a low dose of imidacloprid, one of the most commonly used neonicotinoids, presented reduced fat stores, delayed migration and potentially altered orientation. However, little is known on the effect of imidacloprid on birds growth rate despite studies that have documented disruptive effects of low imidacloprid doses on thyroid gland communication. We performed a 2 × 2 factorial design experiment in Zebra finches, in which nestling birds were exposed to a very low dose (0.205 mg kg body mass - 1) of imidacloprid combined with food restriction during posthatch development. During the early developmental period, imidacloprid exposure resulted in an improvement of body condition index in treated nestlings relative to controls. Imidacloprid also led to compensatory growth in food restricted nestlings. This early life neonicotinoid exposure also carried over to adult age, with exposed birds showing higher lean mass and basal metabolic rate than controls at ages of 90–800 days. This study presents the first evidence that very low-dose neonicotinoid exposure during early life can permanently alter adult phenotype in birds

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

Limited heat tolerance in an Arctic passerine: Thermoregulatory implications for cold-specialized birds in a rapidly warming world

Arctic animals inhabit some of the coldest environments on the planet and have evolved physiological mechanisms for minimizing heat loss under extreme cold. However, the Arctic is warming faster than the global average and how well Arctic animals tolerate even moderately high air temperatures (Ta) is unknown. Using flow-through respirometry, we investigated the heat tolerance and evaporative cooling capacity of snow buntings (Plectrophenax nivalis; ≈31 g, N = 42), a cold specialist, Arctic songbird. We exposed buntings to increasing Ta and measured body temperature (Tb), resting metabolic rate (RMR), rates of evaporative water loss (EWL), and evaporative cooling efficiency (the ratio of evaporative heat loss to metabolic heat production). Buntings had an average (±SD) Tb of 41.3 ± 0.2°C at thermoneutral Ta and increased Tb to a maximum of 43.5 ± 0.3°C. Buntings started panting at Ta of 33.2 ± 1.7°C, with rapid increases in EWL starting at Ta = 34.6°C, meaning they experienced heat stress when air temperatures were well below their body temperature. Maximum rates of EWL were only 2.9× baseline rates at thermoneutral Ta, a markedly lower increase than seen in more heat-tolerant arid-zone species (e.g., ≥4.7× baseline rates). Heat-stressed buntings also had low evaporative cooling efficiencies, with 95% of individuals unable to evaporatively dissipate an amount of heat equivalent to their own metabolic heat production. Our results suggest that buntings’ well-developed cold tolerance may come at the cost of reduced heat tolerance. As the Arctic warms, and this and other species experience increased periods of heat stress, a limited capacity for evaporative cooling may force birds to increasingly rely on behavioral thermoregulation, such as minimizing activity, at the expense of diminished performance or reproductive investment

Spatial mapping of lichen metabolites using mass spectrometry: application to the crustose lichen Ophioparma ventosa

International audienc

Early life neonicotinoid exposure results in proximal benefits and ultimate carryover effects

Neonicotinoids are insecticides widely used as seed treatments that appear to have multiple negative effects on birds at a diversity of biological scales. Adult birds exposed to a low dose of imidacloprid, one of the most commonly used neonicotinoids, presented reduced fat stores, delayed migration and potentially altered orientation. However, little is known on the effect of imidacloprid on birds growth rate despite studies that have documented disruptive effects of low imidacloprid doses on thyroid gland communication. We performed a 2 × 2 factorial design experiment in Zebra finches, in which nestling birds were exposed to a very low dose (0.205 mg kg body mass - 1) of imidacloprid combined with food restriction during posthatch development. During the early developmental period, imidacloprid exposure resulted in an improvement of body condition index in treated nestlings relative to controls. Imidacloprid also led to compensatory growth in food restricted nestlings. This early life neonicotinoid exposure also carried over to adult age, with exposed birds showing higher lean mass and basal metabolic rate than controls at ages of 90–800 days. This study presents the first evidence that very low-dose neonicotinoid exposure during early life can permanently alter adult phenotype in birds

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