Food supply and individual quality influence seabird energy expenditure and reproductive success.

Breeding animals trade off maximizing energy output to increase their number of offspring with conserving energy to ensure their own survival, leading to an energetic ceiling influenced by external, environmental factors or by internal, physiological factors. We examined whether internal or external factors limited energy expenditure by supplementally feeding breeding black-legged kittiwakes varying in individual quality, based on earlier work that defined late breeders as low-quality and early breeders as high-quality individuals. We tested whether energy expenditure increased when food availability decreased in both low- and high-quality birds; we predicted this would only occur in high-quality individuals capable of sustaining high levels of energy expenditure. Here, we find that food-supplemented birds expended less energy than control birds because they spent more time at the colony. However, foraging trips of food-supplemented birds were only slightly shorter than control birds, implying that food-supplemented birds were limited by food availability at sea similarly to control birds. Late breeders expended less energy, suggesting that low-quality individuals may not intake the energy necessary for sustaining high-energy output. Food-supplemented birds had more offspring than control birds, but offspring number did not influence energy expenditure, supporting the idea that the birds reached an energy ceiling. Males and lighter birds expended more energy, possibly compensating for relatively higher energy intake. Chick-rearing birds were working near their maximum, with highest levels of expenditure for early-laying (high-quality) individuals foraging at sea. Due to fluctuating marine environments, kittiwakes may be forced to change their foraging behaviors to maintain the balance between reproduction and survival.

Accelerating animal energetics: high dive costs in a small seabird disrupt the dynamic body acceleration-energy expenditure relationship.

Accelerometry has been widely used to estimate energy expenditure in a broad array of terrestrial and aquatic species. However, a recent reappraisal of the method showed that relationships between dynamic body acceleration (DBA) and energy expenditure weaken as the proportion of non-mechanical costs increases. Aquatic air breathing species often exemplify this pattern, as buoyancy, thermoregulation and other physiological mechanisms disproportionately affect oxygen consumption during dives. Combining biologging with the doubly labelled water method, we simultaneously recorded daily energy expenditure (DEE) and triaxial acceleration in one of the world's smallest wing-propelled breath-hold divers, the dovekie (Alle alle). These data were used to estimate the activity-specific costs of flying and diving and to test whether overall dynamic body acceleration (ODBA) is a reliable predictor of DEE in this abundant seabird. Average DEE for chick-rearing dovekies was 604±119 kJ day-1 across both sampling years. Despite recording lower stroke frequencies for diving than for flying (in line with allometric predictions for auks), dive costs were estimated to surpass flight costs in our sample of birds (flying: 7.24× basal metabolic rate, BMR; diving: 9.37× BMR). As expected, ODBA was not an effective predictor of DEE in this species. However, accelerometer-derived time budgets did accurately estimate DEE in dovekies. This work represents an empirical example of how the apparent energetic costs of buoyancy and thermoregulation limit the effectiveness of ODBA as the sole predictor of overall energy expenditure in small shallow-diving endotherms.

Resting costs too: the relative importance of active and resting energy expenditure in a sub-arctic seabird.

Breeding is costly for many animals, including birds that must deliver food to a central place (i.e. nest). Measuring energy expenditure throughout the breeding season can provide valuable insight into physiological limitations by highlighting periods of high demand, and ultimately allows improvement of conservation strategies. However, quantifying energy expenditure in wildlife can be challenging, as existing methods do not measure both active (e.g. foraging) and resting energy costs across short and long time scales. Here, we developed a novel method for comparing active and resting costs in 66 pre-breeding and breeding seabirds (black-legged kittiwakes, Rissa tridactyla) by combining accelerometry and triiodothyronine (T3) as proxies for active and resting costs, respectively. Active energy costs were higher during incubation (P=0.0004) and chick rearing (P<0.0001) than during pre-laying, because of an increase in the time spent in flight of 11% (P=0.0005) and 15% (P<0.0001), respectively. Levels of T3, reflecting resting costs, peaked marginally during incubation with a mean (±s.d.) concentration of 4.71±1.97 pg ml-1 in comparison to 2.66±1.30 pg ml-1 during pre-laying (P=0.05) and 3.16±2.85 pg ml-1 during chick rearing (P=0.11). Thus, although chick rearing is often assumed to be the costliest breeding stage by multiple studies, our results suggest that incubation could be more costly as a result of high resting costs. We highlight the importance of accounting for both active and resting costs when assessing energy expenditure.

Altered Oxidative Status as a Cost of Reproduction in a Seabird with High Reproductive Costs.

AbstractLife history theory posits that reproduction is constrained by a cost of reproduction such that any increase in breeding effort should reduce subsequent survival. Oxidative stress refers to an imbalance between the prooxidant reactive oxygen species (ROS) and antioxidant defense. If not thwarted, ROS can cause damage to DNA, lipids, and proteins, potentially increasing the rate of senescence and decreasing cellular function. Reproduction is often associated with higher metabolic rates, which could increase production of ROS and lead to oxidative damage if the animal does not increase antioxidant protection. Thus, oxidative stress could be one mechanism creating a cost of reproduction. In this study we explored how reproduction may affect oxidative status differently between male and female thick-billed murres during early and late breeding seasons over three consecutive years. We manipulated breeding efforts by removing an egg from the nest of some individuals, which forced females to relay, and by handicapping other individuals by clipping wings. We measured total antioxidant capacity (TAC), uric acid (UA) concentration, and malondialdehyde (MDA; an index of lipid oxidative damage) concentration in blood plasma as well as activities of superoxide dismutase (SOD), glutathione peroxidase (GPx), and catalase (CAT) in red blood cells. Oxidative status was highly variable across years, and year was consistently the most important factor determining oxidative status; inconsistent results in previous field studies may be because reproductive oxidative stress occurs only in some years. Females had lower SOD and GPx and higher MDA and TAC than males immediately after egg laying, suggesting that the cost of egg laying required investment in cheaper nonenzymatic antioxidant defenses that had lower capacity for defending against lipid peroxidation. Delayed birds had lower UA and lower SOD, GPx, and CAT activity compared with control birds. In conclusion, when reproductive costs increase via higher energy costs or longer breeding seasons, the oxidative status of both male and female murres deteriorated as a result of reduced antioxidant defenses.

Seasonal variation of mercury contamination in Arctic seabirds: A pan-Arctic assessment.

Mercury (Hg) is a natural trace element found in high concentrations in top predators, including Arctic seabirds. Most current knowledge about Hg concentrations in Arctic seabirds relates to exposure during the summer breeding period when researchers can easily access seabirds at colonies. However, the few studies focused on winter have shown higher Hg concentrations during the non-breeding period than breeding period in several tissues. Hence, improving knowledge about Hg exposure during the non-breeding period is crucial to understanding the threats and risks encountered by these species year-round. We used feathers of nine migratory alcid species occurring at high latitudes to study bird Hg exposure during both the breeding and non-breeding periods. Overall, Hg concentrations during the non-breeding period were ~3 times higher than during the breeding period. In addition, spatial differences were apparent within and between the Atlantic and Pacific regions. While Hg concentrations during the non-breeding period were ~9 times and ~3 times higher than during the breeding period for the West and East Atlantic respectively, Hg concentrations in the Pacific during the non-breeding period were only ~1.7 times higher than during the breeding period. In addition, individual Hg concentrations during the non-breeding period for most of the seabird colonies were above 5 µg g-1 dry weight (dw), which is considered to be the threshold at which deleterious effects are observed, suggesting that some breeding populations might be vulnerable to non-breeding Hg exposure. Since wintering area locations, and migration routes may influence seasonal Hg concentrations, it is crucial to improve our knowledge about spatial ecotoxicology to fully understand the risks associated with Hg contamination in Arctic seabirds.

Muscle myonuclear domain, but not oxidative stress, decreases with age in a long-lived seabird with high activity costs.

In birds, many physiological parameters appear to remain constant with increasing age, showing no deterioration until 'catastrophic' mortality sets in. Given their high whole-organism metabolic rate and the importance of flight in foraging and predator avoidance, flight muscle deterioration and accumulated oxidative stress and tissue deterioration may be an important contributor to physiological senescence in wild birds. As a by-product of aerobic respiration, reactive oxygen species are produced and can cause structural damage within cells. The anti-oxidant system deters oxidative damage to macromolecules. We examined oxidative stress and muscle ultrastructure in thick-billed murres aged 8 to 37 years (N=50) in pectoralis muscle biopsies. When considered in general linear models with body mass, body size and sex, no oxidative stress parameter varied with age. In contrast, there was a decrease in myonuclear domain similar to that seen in human muscle aging. We conclude that for wild birds with very high flight activity levels, muscle ultrastructural changes may be an important contributor to demographic senescence. Such gradual, linear declines in muscle morphology may eventually contribute to 'catastrophic' failure in foraging or predator avoidance abilities, leading to demographic senescence.

Flight costs in volant vertebrates: A phylogenetically-controlled meta-analysis of birds and bats.

Flight costs play an important role in determining the behavior, ecology, and physiology of birds and bats. Mechanical flight costs can be estimated from aerodynamics. However, measured metabolic flight costs (oxygen consumption rate) are less accurately predicted by flight theory, either because of (1) variation in flight efficiency across species, (2) variation in how basal costs interact with flight costs or (3) methodological biases. To tease apart these three hypotheses, we conducted a phylogenetically-controlled meta-analysis based on data from birds and bats. Birds doing short flights in a lab had higher metabolic rates than those with sustained flapping flight. In turn, species that used sustained flapping flight had a higher metabolic rate than those that flew primarily via gliding. Models accounting for relatedness (phylogeny) explained the data better than those that did not, which is congruent with the idea that several different flight Bauplans have evolved within birds and bats. Focusing on species with sustained flapping flight, for which more data are currently available, we found that flight cost estimates were not affected by measurement methods in both birds and bats. However, efficiency increased with body mass and decreased with flight speed in both birds and bats. Basal metabolic rate was additive to flight metabolic rate in bats but not birds. We use these results to derive an equation for estimating metabolic flight costs of birds and bats that includes variation in whole animal efficiency with flight speed and body mass.

Light oiling of feathers increases flight energy expenditure in a migratory shorebird.

Flying birds depend on their feathers to undertake most activities, and maintain them in peak condition through periodic molt and frequent preening. Even small exposures to crude oil reduce the integrity of feathers, and could impair flight performance. We trained wild western sandpipers (Calidris mauri) to perform endurance flights in a wind tunnel, and used magnetic resonance body composition analysis to measure energy expenditure after birds were exposed to weathered MC252 crude oil from the Deepwater Horizon oil spill. The cost of transport was 0.26±0.04 kJ km-1 in controls, and increased by 22% when the trailing edges of the wing and tail were oiled (<20% of body surface; considered light oiling). Additional crude oil on breast and back feathers (∼30% total surface; moderate oiling) increased the cost of transport by 45% above controls. Oiling tended to decrease flight control, and only half of moderately oiled birds completed the flight test. We then flew birds at a range of speeds to estimate basic kinematic parameters. At low speeds, light and moderately oiled birds had larger wingbeat amplitudes than controls, while moderately oiled birds showed greater wingbeat frequencies across all speeds, and a shift in optimal flight speed towards higher wind speeds. We suggest these changes reflect poorer lift production and increased drag on the wings and body. Oiling will increase the difficulty and energy costs of locomotion for daily and seasonal activities such as foraging, predator evasion, territory defense, courtship, chick provisioning, commuting and long-distance migration. These sub-lethal effects must be considered in oil spill impact assessments.

Counting calories in cormorants: dynamic body acceleration predicts daily energy expenditure measured in pelagic cormorants.

The integral of the dynamic component of acceleration over time has been proposed as a measure of energy expenditure in wild animals. We tested that idea by attaching accelerometers to the tails of free-ranging pelagic cormorants (Phalacrocorax pelagicus) and simultaneously estimating energy expenditure using doubly labelled water. Two different formulations of dynamic body acceleration, [vectorial and overall DBA (VeDBA and ODBA)], correlated with mass-specific energy expenditure (both R(2)=0.91). VeDBA models combining and separately parameterizing flying, diving, activity on land and surface swimming were consistently considered more parsimonious than time budget models and showed less variability in model fit. Additionally, we observed evidence for the presence of hypometabolic processes (i.e. reduced heart rate and body temperature; shunting of blood away from non-essential organs) that suppressed metabolism in cormorants while diving, which was the most metabolically important activity. We concluded that a combination of VeDBA and physiological processes accurately measured energy expenditure for cormorants.

Windscapes shape seabird instantaneous energy costs but adult behavior buffers impact on offspring.

BACKGROUND: Windscapes affect energy costs for flying animals, but animals can adjust their behavior to accommodate wind-induced energy costs. Theory predicts that flying animals should decrease air speed to compensate for increased tailwind speed and increase air speed to compensate for increased crosswind speed. In addition, animals are expected to vary their foraging effort in time and space to maximize energy efficiency across variable windscapes. RESULTS: We examined the influence of wind on seabird (thick-billed murre Uria lomvia and black-legged kittiwake Rissa tridactyla) foraging behavior. Airspeed and mechanical flight costs (dynamic body acceleration and wing beat frequency) increased with headwind speed during commuting flights. As predicted, birds adjusted their airspeed to compensate for crosswinds and to reduce the effect of a headwind, but they could not completely compensate for the latter. As we were able to account for the effect of sampling frequency and wind speed, we accurately estimated commuting flight speed with no wind as 16.6 ms(?1) (murres) and 10.6 ms(?1) (kittiwakes). High winds decreased delivery rates of schooling fish (murres), energy (murres) and food (kittiwakes) but did not impact daily energy expenditure or chick growth rates. During high winds, murres switched from feeding their offspring with schooling fish, which required substantial above-water searching, to amphipods, which required less above-water searching. CONCLUSIONS: Adults buffered the adverse effect of high winds on chick growth rates by switching to other food sources during windy days or increasing food delivery rates when weather improved.

Age-related variation in energy expenditure in a long-lived bird within the envelope of an energy ceiling.

Energy expenditure in wild animals can be limited (i) intrinsically by physiological processes that constrain an animal's capacity to use energy, (ii) extrinsically by energy availability in the environment and/or (iii) strategically based on trade-offs between elevated metabolism and survival. Although these factors apply to all individuals within a population, some individuals expend more or less energy than other individuals. To examine the role of an energy ceiling in a species with a high and individually repeatable metabolic rate, we compared energy expenditure of thick-billed murres (Uria lomvia) with and without handicaps during a period of peak energy demand (chick-rearing, N = 16). We also compared energy expenditure of unencumbered birds (N = 260) across 8 years exhibiting contrasting environmental conditions and correlated energy expenditure with fitness (reproductive success and survival). Murres experienced an energy ceiling mediated through behavioural adjustments. Handicapped birds decreased time spent flying/diving and chick-provisioning rates such that overall daily energy expenditure remained unchanged across the two treatments. The energy ceiling did not reflect energy availability or trade-offs with fitness, as energy expenditure was similar across contrasting foraging conditions and was not associated with reduced survival or increased reproductive success. We found partial support for the trade-off hypothesis as older murres, where prospects for future reproduction would be relatively limited, did overcome an energy ceiling to invest more in offspring following handicapping by reducing their own energy reserves. The ceiling therefore appeared to operate at the level of intake (i.e. digestion) rather than expenditure (i.e. thermal constraint, oxidative stress). A meta-analysis comparing responses of breeding animals to handicapping suggests that our results are typical: animals either reduced investment in themselves or in their offspring to remain below an energy ceiling. Across species, whether a handicapped individual invested in its own energy stores or its offspring's growth was not explained by life history (future vs. current reproductive potential). Many breeding animals apparently experience an intrinsic energy ceiling, and increased energy costs lead to a decline in self-maintenance and/or offspring provisioning.

Thyroid hormones correlate with resting metabolic rate, not daily energy expenditure, in two charadriiform seabirds.

Thyroid hormones affect in vitro metabolic intensity, increase basal metabolic rate (BMR) in the lab, and are sometimes correlated with basal and/or resting metabolic rate (RMR) in a field environment. Given the difficulty of measuring metabolic rate in the field-and the likelihood that capture and long-term restraint necessary to measure metabolic rate in the field jeopardizes other measurements-we examined the possibility that circulating thyroid hormone levels were correlated with RMR in two free-ranging bird species with high levels of energy expenditure (the black-legged kittiwake, Rissa tridactyla, and thick-billed murre, Uria lomvia). Because BMR and daily energy expenditure (DEE) are purported to be linked, we also tested for a correlation between thyroid hormones and DEE. We examined the relationships between free and bound levels of the thyroid hormones thyroxine (T4) and triiodothyronine (T3) with DEE and with 4-hour long measurements of post-absorptive and thermoneutral resting metabolism (resting metabolic rate; RMR). RMR but not DEE increased with T3 in both species; both metabolic rates were independent of T4. T3 and T4 were not correlated with one another. DEE correlated with body mass in kittiwakes but not in murres, presumably owing to the larger coefficient of variation in body mass during chick rearing for the more sexually dimorphic kittiwakes. We suggest T3 provides a good proxy for resting metabolism but not DEE in these seabird species.

High flight costs, but low dive costs, in auks support the biomechanical hypothesis for flightlessness in penguins.

Flight is a key adaptive trait. Despite its advantages, flight has been lost in several groups of birds, notably among seabirds, where flightlessness has evolved independently in at least five lineages. One hypothesis for the loss of flight among seabirds is that animals moving between different media face tradeoffs between maximizing function in one medium relative to the other. In particular, biomechanical models of energy costs during flying and diving suggest that a wing designed for optimal diving performance should lead to enormous energy costs when flying in air. Costs of flying and diving have been measured in free-living animals that use their wings to fly or to propel their dives, but not both. Animals that both fly and dive might approach the functional boundary between flight and nonflight. We show that flight costs for thick-billed murres (Uria lomvia), which are wing-propelled divers, and pelagic cormorants (Phalacrocorax pelagicus) (foot-propelled divers), are the highest recorded for vertebrates. Dive costs are high for cormorants and low for murres, but the latter are still higher than for flightless wing-propelled diving birds (penguins). For murres, flight costs were higher than predicted from biomechanical modeling, and the oxygen consumption rate during dives decreased with depth at a faster rate than estimated biomechanical costs. These results strongly support the hypothesis that function constrains form in diving birds, and that optimizing wing shape and form for wing-propelled diving leads to such high flight costs that flying ceases to be an option in larger wing-propelled diving seabirds, including penguins.

Parents are a drag: long-lived birds share the cost of increased foraging effort with their offspring, but males pass on more of the costs than females.

Life history theory predicts that parents will balance benefits from investment in current offspring against benefits from future reproductive investments. Long-lived organisms are therefore less likely to increase parental effort when environmental conditions deteriorate. To investigate the effect of decreased foraging capacity on parental behaviour of long-lived monogamous seabirds, we experimentally increased energy costs for chick-rearing thick-billed murres (Uria lomvia). Handicapped birds had lighter chicks and lower provisioning rates, supporting the prediction that long-lived animals would pass some of the costs of impaired foraging ability on to their offspring. Nonetheless, handicapped birds spent less time underwater, had longer inter-dive surface intervals, had lower body mass, showed lower resighting probabilities in subsequent years and consumed fewer risky prey items. Corticosterone levels were similar between control and handicapped birds. Apparently, adults shared some of the costs of impaired foraging, but those costs were not measurable in all metrics. Handicapped males had higher plasma neutral lipid concentrations (higher energy mobilisation) and their chicks exhibited lower growth rates than handicapped females, suggesting different sex-specific investment strategies. Unlike other studies of auks, partners did not compensate for handicapping, despite good foraging conditions for unhandicapped birds. In conclusion, parental murres and their offspring shared the costs of experimentally increased foraging constraints, with females investing more than males.

High corticosterone, not high energy cost, correlates with reproductive success in the burrow-nesting ancient murrelet.

Theory and observations suggest that offspring abandonment in animals may occur when the costs to future reproductive output of current reproductive effort outweigh the fitness benefits of rearing the current brood. While hormonal cues (i.e. corticosterone) or energy reserves are believed to be involved, few studies have directly focused on the proximate cues influencing behaviours directly related to reproductive success. To address this information gap, we determined the incubation metabolic rates and corticosterone (CORT) levels of naturally fasting and freely incubating ancient murrelets (Synthliboramphus antiquus). Respiratory quotient (RQ) increased with date, suggesting that incubating ancient murrelets shifted from strictly lipid-based metabolism towards more protein-based metabolism as incubation progressed. Birds that hatched only one nestling had higher levels of circulating CORT than those which hatched two, suggesting that birds which laid only a single egg found incubation more stressful than those which laid two. However, CORT levels and incubation shift lengths were not correlated, suggesting that birds that undertook prolonged incubation shifts did so only when their energy stores were not jeopardized.

Accelerometry predicts daily energy expenditure in a bird with high activity levels.

Animal ecology is shaped by energy costs, yet it is difficult to measure fine-scale energy expenditure in the wild. Because metabolism is often closely correlated with mechanical work, accelerometers have the potential to provide detailed information on energy expenditure of wild animals over fine temporal scales. Nonetheless, accelerometry needs to be validated on wild animals, especially across different locomotory modes. We merged data collected on 20 thick-billed murres (Uria lomvia) from miniature accelerometers with measurements of daily energy expenditure over 24 h using doubly labelled water. Across three different locomotory modes (swimming, flying and movement on land), dynamic body acceleration was a good predictor of daily energy expenditure as measured independently by doubly labelled water (R(2) = 0.73). The most parsimonious model suggested that different equations were needed to predict energy expenditure from accelerometry for flying than for surface swimming or activity on land (R(2) = 0.81). Our results demonstrate that accelerometers can provide an accurate integrated measure of energy expenditure in wild animals using many different locomotory modes.

Individual specialization in diet by a generalist marine predator reflects specialization in foraging behaviour.

1. We studied chick diet in a known-age, sexed population of a long-lived seabird, the Brünnich's guillemot (Uria lomvia), over 15 years (N = 136; 1993-2007) and attached time-depth-temperature recorders to examine foraging behaviour in multiple years (N = 36; 2004-07). 2. Adults showed specialization in prey fed to offspring, described by multiple indices calculated over 15 years: 27% of diet diversity was attributable to among-individual variation (within-individual component of total niche width = 0.73); average similarity of an individual's diet to the overall diet was 65% (mean proportional similarity between individuals and population = 0.65); diet was significantly more specialized than expected for 70% of individuals (mean likelihood = 0.53). These indices suggest higher specialization than the average for an across-taxa comparison of 49 taxa. 3. Foraging behaviour varied along three axes: flight time, dive depth and dive shape. Individuals showed specialized individual foraging behaviour along each axis. These foraging strategies were reflected in the prey type delivered to their offspring and were maintained over scales of hours to years. 4. Specialization in foraging behaviour and diet was greater over short time spans (hours, days) than over long time spans (years). Regardless of sex or age, the main component of variation in foraging behaviour and chick diet was between individuals. 5. Plasma stable isotope values were similar across years, within a given individual, and variance was low relative to that expected from prey isotope values, suggesting adult diet specialized across years. Stable isotope values were similar among individuals that fed their nestlings similar prey items and there was no difference in trophic level between adults and chicks. We suggest that guillemots specialize on a single foraging strategy regardless of whether chick-provisioning and self-feeding. With little individual difference in body mass and physiology, specialization likely represents learning and memorizing optimal feeding locations and behaviours. 6. There was no difference in survival or reproductive success between specialists and generalists, suggesting these are largely equivalent strategies in terms of evolutionary fitness, presumably because different strategies were advantageous at different levels of prey abundance or predictability. The development of individual specialization may be an important precursor to diversification among seabirds.