Migration increases mitochondrial oxidative capacity without increasing reactive oxygen species emission in a songbird.

Birds remodel their flight muscle metabolism prior to migration to meet the physiological demands of migratory flight, including increases in both oxidative capacity and defence against reactive oxygen species. The degree of plasticity mediated by changes in these mitochondrial properties is poorly understood but may be explained by two non-mutually exclusive hypotheses: variation in mitochondrial quantity or individual mitochondrial function. We tested these hypotheses using yellow-rumped warblers (Setophaga coronata), a Nearctic songbird which biannually migrates two to five thousand kilometres. We predicted higher flight muscle mitochondrial abundance and substrate oxidative capacity and decreased reactive oxygen species emission in migratory warblers captured during autumn migration compared to a short-day photoperiod-induced non-migratory phenotype. We assessed mitochondrial abundance via citrate synthase activity and assessed isolated mitochondrial function using high-resolution fluororespirometry. We found 60% higher tissue citrate synthase activity in the migratory phenotype, indicating higher mitochondrial abundance. We also found 70% higher state 3 respiration (expressed per unit citrate synthase) in mitochondria from migratory warblers when oxidizing palmitoyl-carnitine, but similar H2O2 emission rates between phenotypes. By contrast, non-phosphorylating respiration was higher and H2O2 emission rates were lower in the migratory phenotype. However, flux through electron transport system complexes I-IV, II-IV and IV were similar between phenotypes. In support of our hypotheses, these data suggest that flight muscle mitochondrial abundance and function are seasonally remodeled in migratory songbirds to increase tissue oxidative capacity without increasing reactive oxygen species formation.

Experimental evidence that EPA and DHA are dietary requirements in a migratory shorebird, but they do not affect muscle oxidative capacity.

Dietary n-3 long chain polyunsaturated fatty acids (LCPUFAs) are hypothesized to be natural doping agents in migratory shorebirds, enabling prolonged flight by increasing membrane fluidity and oxidative capacity of the flight muscles. Animals can obtain n-3 LCPUFAs from the diet or by conversion of dietary α-linolenic acid, 18:3 n-3. However, the capacity to meet n-3 LCPUFA requirements from 18:3 n-3 varies among species. Direct tests of muscle oxidative enhancement and fatty acid conversion capacity are lacking in marine shorebirds that evolved eating diets rich in n-3 LCPUFAs. We tested whether the presence and type of dietary fatty acids influence the fatty acid composition and flight muscle oxidative capacity in western sandpipers (Calidris mauri). Sandpipers were fed diets low in n-3 PUFAs, high in 18:3 n-3, or high in n-3 LCPUFAs. Dietary fatty acid composition was reflected in multiple tissues, and low intake of n-3 LCPUFAs decreased the abundance of these fatty acids in all tissues, even with a high intake of 18:3 n-3. This suggests that 18:3 n-3 cannot replace n-3 LCPUFAs, and dietary n-3 LCPUFAs are required for sandpipers. Flight muscle indicators of enzymatic oxidative capacity and regulators of lipid metabolism did not change. However, the n-3 LCPUFA diet was associated with increased FAT/CD36 mRNA expression, potentially benefitting fatty acid transport during flight. Our study suggests that flight muscle lipid oxidation is not strongly influenced by n-3 PUFA intake. The type of dietary n-3 PUFA strongly influences the abundance of n-3 LCPUFAs in the body and could still impact whole-animal performance.

Migratory songbirds exhibit seasonal modulation of the oxygen cascade.

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.

The effects of training, acute exercise and dietary fatty acid composition on muscle lipid oxidative capacity in European starlings.

Migratory birds undergo seasonal changes to muscle biochemistry. Nonetheless, it is unclear to what extent these changes are attributable to the exercise of flight itself versus endogenous changes. Using starlings (Sturnus vulgaris) flying in a wind tunnel, we tested the effects of exercise training, a single bout of flight and dietary lipid composition on pectoralis muscle oxidative enzymes and lipid transporters. Starlings were either unexercised or trained over 2 weeks to fly in a wind tunnel and sampled either immediately following a long flight at the end of this training or after 2 days recovery from this flight. Additionally, they were divided into dietary groups that differed in dietary fatty acid composition (high polyunsaturates versus high monounsaturates) and amount of dietary antioxidant. Trained starlings had elevated (19%) carnitine palmitoyl transferase and elevated (11%) hydroxyacyl-CoA dehydrogenase in pectoralis muscle compared with unexercised controls, but training alone had little effect on lipid transporters. Immediately following a long wind-tunnel flight, starling pectoralis had upregulated lipid transporter mRNA (heart-type fatty acid binding protein, H-FABP, 4.7-fold; fatty acid translocase, 1.9-fold; plasma membrane fatty acid binding protein, 1.6-fold), and upregulated H-FABP protein (68%). Dietary fatty acid composition and the amount of dietary antioxidants had no effect on muscle catabolic enzymes or lipid transporter expression. Our results demonstrate that birds undergo rapid upregulation of catabolic capacity that largely becomes available during flight itself, with minor effects due to training. These effects likely combine with endogenous seasonal changes to create the migratory phenotype observed in the wild.

Short-term mercury exposure disrupts muscular and hepatic lipid metabolism in a migrant songbird.

Methylmercury (MeHg) is a global pollutant that can cause metabolic disruptions in animals and thereby potentially compromise the energetic capacity of birds for long-distance migration, but its effects on avian lipid metabolism pathways that support endurance flight and stopover refueling have never been studied. We tested the effects of short-term (14-d), environmentally relevant (0.5 ppm) dietary MeHg exposure on lipid metabolism markers in the pectoralis and livers of yellow-rumped warblers (Setophaga coronata) that were found in a previous study to have poorer flight endurance in a wind tunnel than untreated conspecifics. Compared to controls, MeHg-exposed birds displayed lower muscle aerobic and fatty acid oxidation capacity, but similar muscle glycolytic capacity, fatty acid transporter expression, and PPAR expression. Livers of exposed birds indicated elevated energy costs, lower fatty acid uptake capacity, and lower PPAR-γ expression. The lower muscle oxidative enzyme capacity of exposed birds likely contributed to their weaker endurance in the prior study, while the metabolic changes observed in the liver have potential to inhibit lipogenesis and stopover refueling. Our findings provide concerning evidence that fatty acid catabolism, synthesis, and storage pathways in birds can be dysregulated by only brief exposure to MeHg, with potentially significant consequences for migratory performance.

Experimental ghrelin administration affects migratory behaviour in a songbird.

Twice a year, billions of birds take on drastic physiological and behavioural changes to migrate between breeding and wintering areas. On migration, most passerine birds regularly stop over along the way to rest and refuel. Endogenous energy stores are not only the indispensable fuel to complete long distance flights, but are also important peripheral signals that once integrated in the brain modulate crucial behavioural decisions, such as the decision to resume migration after a stopover. A network of hormones signals metabolic fuel availability to the brain in vertebrates, including the recently discovered gut-hormone ghrelin. Here, we show that ghrelin takes part in the control of migratory behaviour during spring migration in a wild migratory passerine. We manipulated blood concentrations of ghrelin of 53 yellow-rumped warblers (Setophaga coronata coronata) caught during stopover and automatically radio-tracked their migratory behaviour following release. We found that injections of acylated and unacylated ghrelin rapidly induced movements away from the release site, indicating that the ghrelin system acts centrally to mediate stopover departure decisions. The effects of the hormone manipulation declined within 8 h following release, and did not affect the overall rate of migration. These results provide experimental evidence for a pivotal role of ghrelin in the modulation of behavioural decisions during migration. In addition, this study offers insights into the regulatory functions of metabolic hormones in the dialogue between gut and brain in birds.

Reversal of the adipostat control of torpor during migration in hummingbirds.

Many small endotherms use torpor to reduce metabolic rate and manage daily energy balance. However, the physiological 'rules' that govern torpor use are unclear. We tracked torpor use and body composition in ruby-throated hummingbirds (Archilochus colubris), a long-distance migrant, throughout the summer using respirometry and quantitative magnetic resonance. During the mid-summer, birds entered torpor at consistently low fat stores (~5% of body mass), and torpor duration was negatively related to evening fat load. Remarkably, this energy emergency strategy was abandoned in the late summer when birds accumulated fat for migration. During the migration period, birds were more likely to enter torpor on nights when they had higher fat stores, and fat gain was positively correlated with the amount of torpor used. These findings demonstrate the versatility of torpor throughout the annual cycle and suggest a fundamental change in physiological feedback between adiposity and torpor during migration. Moreover, this study highlights the underappreciated importance of facultative heterothermy in migratory ecology.

Torpor is an energy-saving strategy used by warm-blooded animals, including birds and small mammals. Similar to hibernation, although shorter in duration, torpor is a state of minimal activity, low body temperatures and reduced metabolism that helps animals conserve energy in unfavorable conditions. Some animals use torpor to survive times when food is not readily available. Hummingbirds, for example, eat nectar all day long to meet their high energy needs, but must build fat reserves to see them through their overnight fast. If they go to sleep with too little fat, they can descend into torpor to stretch out that limited energy supply and survive until morning. Many hummingbirds migrate to areas with warmer weather, where food remains available, for the winter months. The ruby-throated hummingbird (Archilochus colubris), for example, travels over 5,000 kilometers in its fall migration. Like most long-distance migrants, ruby-throated hummingbirds increase their fat stores before departing, using these stores to fuel their journey. It is thought that this bird may use torpor as a way to accelerate fat build up before its annual migration. However, it remained unclear whether hummingbirds switched from using torpor strictly in energy emergencies, to using it as strategy to prepare for migration. To shed light on this question, Eberts, Guglielmo and Welch investigated when, why and how hummingbirds save energy using torpor during the summer, and whether there are seasonal shifts in their use of torpor coinciding with migration. Eberts, Guglielmo and Welch hypothesized that a bird would initiate daily torpor if its energy stores fall below a critical level during the night, but that they may abandon this threshold (triggering torpor at higher fat levels) in late summer as a way to spare energy and gain fat before their annual migration. To test their hypotheses, Eberts, Guglielmo and Welch tracked body composition, food intake, energy expenditure and torpor use throughout summer in a group of captive ruby-throated hummingbirds. In the middle of the summer, the birds entered torpor and remained torpid for longer when they went to sleep with low fat stores. In late summer, however, the same birds were more likely to enter torpor at consistent times and when they had higher fat stores. Eberts, Guglielmo and Welch also observed that the more time birds spent in torpor, the more fat they gained. This suggests that in late summer, hummingbirds switch from using torpor as a survival strategy to using it to maximize energy savings before migration. These results clearly define the physiological rules governing torpor use in hummingbirds. They also support the long-standing assumption that torpor helps migratory species save energy and accumulate fat stores before long-haul flights.

Extraordinarily rapid proliferation of cultured muscle satellite cells from migratory birds.

Migratory birds experience bouts of muscle growth and depletion as they prepare for, and undertake prolonged flight. Our studies of migratory bird muscle physiology in vitro led to the discovery that sanderling (Calidris alba) muscle satellite cells proliferate more rapidly than other normal cell lines. Here we determined the proliferation rate of muscle satellite cells isolated from five migratory species (sanderling; ruff, Calidris pugnax; western sandpiper, Calidris mauri; yellow-rumped warbler, Setophaga coronata; Swainson's thrush, Catharus ustulatus) from two families (shorebirds and songbirds) and with different migratory strategies. Ruff and sanderling satellite cells exhibited rapid proliferation, with population doubling times of 9.3 ± 1.3 and 11.4 ± 2 h, whereas the remaining species' cell doubling times were greater than or equal to 24 h. The results indicate that the rapid proliferation of satellite cells is not associated with total migration distance but may be related to flight bout duration and interact with lifespan.

Using breath δ13C analysis to determine the effects of dietary carbohydrate and protein on glucose and leucine oxidation at rest in the yellow-rumped warbler (Setophaga coronata).

Fat is the major fuel for migratory flight of birds, but protein is also catabolized. Flight range could be reduced if protein is used too quickly from muscles and organs, and it is important to understand factors that influence protein catabolism. Previous correlative studies suggested high protein diets may increase protein use in flight, although a wind tunnel study with yellow-rumped warblers (Setophaga coronata) did not support this relationship. We tested the hypothesis that diet composition affects nutrient oxidation in resting, fasted yellow-rumped warblers. For method development, we gavaged or subcutaneously injected warblers with 13C labelled glucose or leucine, and measured δ13C of breath CO2 in real time using infrared laser spectrometry. Regardless of route of administration, leucine had greater instantaneous and cumulative oxidation than glucose. Compared to subcutaneous injection, gavaged birds reached maximum oxidation rate faster for leucine and glucose, respectively, had a higher maximum oxidation rate, and reached final cumulative oxidation approximately faster for leucine or glucose, respectively, indicating immediate oxidation of the substrates by the digestive system. Warblers (N = 10 each) were fed isocaloric 60% carbohydrate or 60% protein diets for minimum 2 weeks, and subcutaneously injected with 13C labelled glucose or leucine. Diet composition had little effect on oxidation kinetics except that warblers fed high-carbohydrate reached final cumulative oxidation of leucine more quickly than those fed high-protein. The findings do not support the hypothesis that high protein diets increase the oxidation of protein during negative energy states in migratory birds, and provide methodology that could be applied to test it in flight.

Nutritional consequences of breeding away from riparian habitats in Bank Swallows: new evidence from multiple endogenous markers.

The Bank Swallow (Riparia riparia), a threatened species in Canada, breeds primarily in banks at lakeshores and rivers and in artificial (typically inland) aggregate mining pits. Inland pits may be ecological traps for this species, but relative dietary trade-offs between these two nesting habitats have not been investigated. The availability of aquatic emergent insects at lakeshores may have associated nutritional benefits for growing nestlings due to increased omega-3 fatty acids (FAs) in prey. We compared the diets of juvenile swallows from lakeshore and inland pit sites using assays of stable isotope values (δ13C, δ15N, δ2H) of feathers, faecal DNA metabarcoding and blood plasma FAs. Colony proximity to Lake Erie influenced the use of aquatic versus terrestrial insects by Bank Swallow adults and juveniles. Feather δ2H was particularly useful as a tracer of aquatic emergent versus terrestrial prey, and inland juveniles had feathers enriched in 2H, reflective of diets composed of fewer aquatic emergent insects. DNA metabarcoding of juvenile and adult faecal material indicated that lakeshore birds consumed more aquatic-emergent chironomids than inland birds. Lakeshore juveniles had elevated plasma omega-3 eicosapentaenoic acid levels compared with inland pit-breeding birds. We discuss the need to consider 'nutritional landscapes' and the importance of this concept in conservation of declining species and populations.

Inferring spatial patterns of mercury exposure in migratory boreal songbirds: Combining feather mercury and stable isotope (δ2H) measurements.

Migratory songbirds breeding in the Canadian Boreal forest are exposed to mercury (Hg), a potent neurotoxin that impairs avian health, however, the degree of exposure depends on many factors. As breeding grounds are geographically remote and vast, the measurement of Hg in individual birds is impractical particularly at large spatial scales. Here, we present a Canada-wide dataset of nearly 2000 migratory songbirds that were used to assess summer Hg exposure of 15 songbird species sampled during fall migration. We measured Hg concentrations in tail feathers and related those to dietary guild, geographic capture location, age, sex and probable breeding ground locations using feather δ2H. Overall mean (±SE) feather Hg concentration was 1.49 ± 0.03 µg/g (N = 1946): however, a clear geographic gradient in feather Hg concentrations emerged being highest in East and lowest in West. Dietary guild was the next strongest predictor of feather Hg with insectivorous songbirds in Eastern Canada at particular risk due to Hg exposure on summer breeding grounds. This broad-scale assessment of Hg exposure in migratory songbirds in Canada can be used to guide future studies on finer-scale determinants of Hg exposure in birds.

Species-specific metabolic responses of songbird, shorebird, and murine cultured myotubes to n-3 polyunsaturated fatty acids.

Migratory birds may benefit from diets rich in polyunsaturated fatty acids (PUFAs) that could improve exercise performance. Previous investigations suggest that different types of birds may respond differently to PUFA. We established muscle myocyte cell culture models from muscle satellite cells of a migratory passerine songbird (yellow-rumped warbler, Setophaga coronata coronata) and a nonpasserine shorebird (sanderling, Calidris alba). We differentiated and treated avian myotubes and immortalized murine C2C12 myotubes with n-3 PUFA docosahexaenoic acid (DHA) and eicosapentaenoic acid (EPA), and with monounsaturated oleic acid (OA) to compare effects on aerobic performance, metabolic enzyme activities, key fatty acid (FA) transporters, and expression of peroxisome proliferator-activated receptors (PPARs). Sanderling and C2C12 myotubes increased expression of PPARs with n-3 PUFA treatments, whereas expression was unchanged in yellow-rumped warblers. Both sanderlings and yellow-rumped warblers increased expression of fatty acid transporters, whereas C2C12 cells decreased expression following n-3 PUFA treatments. Only yellow-rumped warbler myotubes increased expression of some metabolic enzymes, whereas the sanderling and C2C12 cells were unchanged. PUFA supplementation in C2C12 myotubes increased mitochondrial respiratory chain efficiency, whereas sanderlings increased proton leak-associated respiration and maximal respiration (measurements were not made in warblers). This research indicates that songbirds and shorebirds respond differently to n-3 PUFA and provides support for the hypothesis that n-3 PUFA increase the aerobic capacity of migrant shorebird muscle, which may improve overall endurance flight performance.

Stopover refuelling, movement and departure decisions in the white-throated sparrow: The influence of intrinsic and extrinsic factors during spring migration.

Differential migration timing between sex or age classes is an example of how migratory movement strategies can differ among subgroups within a population. However, in songbirds, evidence for intrinsic differences in en route migratory behaviour is often mixed, suggesting that the local environmental context may play a role in accentuating or diminishing patterns. We evaluated how multiple intrinsic and extrinsic variables influenced refuelling rates, local movement behaviour and departure decisions in the white-throated sparrow Zonotrichia albicollis during spring migration. This species exhibits a unique genetically based plumage dimorphism, providing a unique class of individual in which to evaluate patterns and processes of differential migration, in addition to sex, age and migration distance. At a migratory stopover site, plasma metabolite analysis was used to quantify individual variation in stopover refuelling rate. In after second year adults, automated and manual radio telemetry was used to quantify daily activity timing, daily movement distances, stopover duration and departure time. Arrival timing to the stopover site was determined using capture data. Non-breeding and previous breeding/natal latitude were determined using analysis of hydrogen isotopes in claws and feathers. Males arrived at the stopover site 11 days on average before females, but no difference in migration timing was observed between plumage morph or age classes. After second year, adults with more southern previous breeding latitudes arrived at stopover earlier, whereas second year birds making their first return migration arrived at stopover in an inverse relationship to non-breeding latitude. Stopover refuelling rate did not differ between ages, sexes or plumage morphs, and daily departure probability of adults was higher under warmer temperatures and favourable tailwinds. White-striped morphs moved greater distances during stopover, initiated daily activity earlier in the morning and departed for migration earlier in the evening than tan-striped morphs. Our results show that while individual phenotype can influence some aspects of local stopover-scale movement behaviour, evidence for differential stopover behaviour was weak. Differential migration timing is unlikely to result from intrinsic differences in en route refuelling rate and departure decisions, especially because the latter is strongly influenced by meteorological conditions.

Measuring power input, power output and energy conversion efficiency in un-instrumented flying birds.

Cost of flight at various speeds is a crucial determinant of flight behaviour in birds. Aerodynamic models, predicting that mechanical power (Pmech) varies with flight speed in a U-shaped manner, have been used together with an energy conversion factor (efficiency) to estimate metabolic power (Pmet). Despite few empirical studies, efficiency has been assumed constant across flight speeds at 23%. Ideally, efficiency should be estimated from measurements of both Pmech and Pmet in un-instrumented flight. Until recently, progress has been hampered by methodological constraints. The main aim of this study was to evaluate recently developed techniques and estimate flight efficiency across flight speeds. We used the 13C-labelled sodium bicarbonate method (NaBi) and particle image velocimetry (PIV) to measure Pmet and Pmech in blackcaps flying in a wind tunnel. We also cross-validated measurements made by NaBi with quantitative magnetic resonance (QMR) body composition analysis in yellow-rumped warblers. We found that Pmet estimated by NaBi was ∼12% lower than corresponding values estimated by QMR. Pmet varied in a U-shaped manner across flight speeds in blackcaps, but the pattern was not statistically significant. Pmech could only be reliably measured for two intermediate speeds and estimated efficiency ranged between 14% and 22% (combining the two speeds for raw and weight/lift-specific power, with and without correction for the ∼12% difference between NaBi and QMR), which were close to the currently used default value. We conclude that NaBi and PIV are viable techniques, allowing researchers to address some of the outstanding questions regarding bird flight energetics.

Turbulent Wake-Flow Characteristics in the Near Wake of Freely Flying Raptors: A Comparative Analysis Between an Owl and a Hawk.

Owl flight has been studied over multiple decades associated with bio-inspiration for silent flight. However, their aerodynamics has been less researched. The aerodynamic noise generated during flight depends on the turbulent state of the flow. In order to document the turbulent characteristics of the owl during flapping flight, we measured the wake flow behind a freely flying great horned owl (Bubo virginianus). For comparison purposes, we chose to fly a similar-sized raptor a Harris's hawk (Parabuteo unicinctus): one is nocturnal and the other is a diurnal bird of prey. Here, we focus on the wake turbulent aspects and their impact on the birds' flight performances. The birds were trained to fly inside a large-scale wind tunnel in a perch-to-perch flight mode. The near wake of the freely flying birds was characterized using a long duration time-resolved particle image velocimetry system. The velocity fields in the near wake were acquired simultaneously with the birds' motion during flight which was sampled using multiple high-speed cameras. The turbulent momentum fluxes, turbulent kinetic energy production, and dissipation profiles are examined in the wake and compared. The near wake of the owl exhibited significantly higher turbulent activity than the hawk in all cases, though both birds are similar in size and followed similar flight behavior. It is suggested that owls modulate the turbulence activity of the near wake in the vicinity of the wing, resulting in rapid decay before radiating into the far-field; thus, suppressing the aerodynamic noise at the far wake.

Temporal patterns of foraging by silver-haired bats during migratory stopover revealed by isotopic analyses (δ13C) of breath CO2.

The extent to which migratory bats forage at stopover sites or while in migratory flight is poorly understood. Endogenous fat stores have lower δ13C values relative to the dietary substrates from which they were synthesized, and so, the fed versus fasted state of bats should be discernable by comparing their breath δ13C at capture to that after a known period of fasting. We captured silver-haired bats (Lasionycteris noctivagans) at a stopover site at Long Point, Ontario, Canada, during spring and fall migration. We collected breath samples at capture and after fasting in captivity for 12 h, providing a fasted-state δ13C value corresponding to metabolism of fat stores. We also collected and weighed fecal pellets produced while in captivity. Breath δ13C values at capture were positively correlated with mass of feces produced. During spring migration, δ13C values of breath CO2 at capture were low and similar to fasting values, but increased with date consistent with increased foraging at stopover and reliance on exogenous dietary nutrients as the season progressed. The opposite temporal pattern was found during fall migration. Our findings suggest that bats forage during migratory stopover when environmental conditions permit despite potential time trade-offs between feeding and travel, and the energy savings resulting from torpor during roosting. This study provides insight into the eco-physiology of bat migration and shows the importance of foraging habitat for migratory bats.

The Value of Experimental Approaches in Migration Biology.

The past several decades have ushered in a golden age in the study of migration biology, leading to a wealth of descriptive articles that characterize various aspects of migration and its implications for individuals, populations, and ecosystems. However, relatively few studies have adopted an experimental approach to the study of migration, and fewer still have combined lab and field experiments to glean insights into the mechanisms underlying variation in migration behavior and success. Understanding the proximate and ultimate causes of migration timing, energy allocation and optimization, migration success, and fitness is important to aid the conservation and management of wildlife populations by establishing appropriate protections or managing environmental conditions that influence migration. With recent technological advances and miniaturization of animal-borne electronic tracking devices, as well as ground-, water-, and space-based telemetry infrastructure, researchers have the tools necessary to experimentally test hypotheses central to the mechanics of migrations and individual variation therein. By pairing physiological measurements, molecular analyses, and other approaches within an experimental framework, there is the potential to understand not only how animal migrations function but also what differentiates successful migrations from failed migrations and the associated fitness implications. Experimental approaches to migration biology are particularly important, as they will help us to better comprehend and hopefully predict animal responses to environmental and anthropogenic changes by isolating confounding variables that challenge inferences from observations.

Fatty acid profiles of the European migratory common noctule bat (Nyctalus noctula).

In animals, fatty acids (FA) are essential as structural components in membranes and for energy storage in adipocytes. Here, we studied the relative proportions of FA in a mammal with extreme changes in metabolic rates. Common noctule bats (Nyctalus noctula) switch from energetically demanding long-distance migration at high metabolic rates to regular torpor with extremely low metabolic rates. We found that composition of FA categories differed between adipose tissue types (white adipose tissue (WAT) vs brown adipose tissue (BAT)) and muscle tissue types (skeletal vs heart), but not between sexes. We found oleic acid to be the most abundant FA in all studied tissues. Concentrations of polyunsaturated FA (PUFA) were not always higher in muscular tissue compared with adipocyte tissue, even though high concentrations of PUFA are considered beneficial for low body temperatures in torpor. In all tissues, we observed a high content in monounsaturated fatty acids (MUFA), possibly to compensate for a low PUFA content in the diet. Ratios of ω6/ω3 were lower in the heart than in skeletal muscles of common noctules. Three FA (palmitic, oleic, and linoleic acid) accounted for about 70% of the FA in adipose tissue, which is similar to proportions observed in migrating birds, yet migrating birds generally have a higher PUFA content in muscle and adipose tissues than bats. Bats seem to contrast with other mammals in having a high MUFA content in all tissues. We conclude that FA profiles of bats differ largely from those of most cursorial mammals and instead are-with the exception of MUFA-similar to those of migrating birds.

Western diet consumption through early life induces microvesicular hepatic steatosis in association with an altered metabolome in low birth weight Guinea pigs.

Uteroplacental insufficiency-induced low birth weight (LBW) and postnatal high saturated fat/high sucrose-fructose diet (Western Diet, WD) consumption have been independently associated with the development of hepatic steatosis, while their additive effect on fatty acid, acylcarnitine and amino acid profiles in early adulthood have not been widely reported. We employed LBW, generated via uterine artery ablation, and normal birth weight (NBW) male guinea pigs fed either a WD or control diet (CD) from weaning to postnatal day 150 (early adulthood). Hepatic steatosis was absent in CD-fed offspring, while NBW/WD offspring displayed macrovesicular steatosis and LBW/WD offspring exhibited microvesicular steatosis, both occurring in a lean phenotype. Life-long consumption of the WD, irrespective of birth weight, was associated with an increase in hepatic medium- and long-chain saturated fatty acids, monounsaturated fatty acids, acylcarnitines, reduced oxidative phosphorylation complex III activity and polyunsaturated fatty acids, and molecular evidence of disrupted hepatic insulin signaling. In NBW/WD, hepatic C15:1 and C16:1n-6 fatty acids in phospholipids, C16, C18 and C18:1 acylcarnitines, concentrations of aspartate, phenylalanine, tyrosine and tryptophan and expression of carnitine palmitoyltransferase 1 alpha (CPT1α) and uncoupling protein 2 (UCP2) genes were elevated compared to LBW/WD livers. Our results suggest that LBW and life-long WD combined are influential in promoting hepatic microvesicular steatosis in conjunction with a specific mitochondrial gene expression and metabolomic profile in early adulthood.