Changes in body composition during breeding: Reproductive strategies of three species of seabirds under poor environmental conditions

Seabirds differ dramatically in life history traits and breeding strategies. For example, gulls have short incubation shifts (several hours) and high metabolic rates, auks have medium-length incubation shifts (12-24h) and high metabolic rates, and petrels have long incubation shifts (days) and low metabolic rates. How these different strategies affect the dynamics of body components is poorly known. We compared body, organ and lipid mass changes among three different seabirds (gull: black-legged kittiwake Rissa tridactyla; auk: thick-billed murre Uria lomvia; petrel: northern fulmar Fulmarus glacialis) at Prince Leopold Island, Nunavut, Canada during 2002 (a year with low reproductive success and poor chick growth across all three species). This study is among the first to compare mass and lipid dynamics among different species foraging in the same food web and at similar trophic levels during the same breeding season (same environmental conditions). In fulmars and murres, most of decreases in body mass reflected decreases in lipid mass while in kittiwakes the increase in body mass reflected an increase in lean mass, especially the muscle. The species with the longest fasting endurance (incubation shift length) had the highest percent body lipids during incubation (fulmars: 13.3%, murres: 7.3%, kittiwakes: 6.9%), the highest variability in body lipids, tended to regulate body mass primarily through lipid stores and tended to regulate exercise and digestive organs separately. In contrast, in the species with the highest metabolic rate, all organ systems were adjusted similarly and in relation to body mass, and in a similar manner between incubation (stress due to heavy ice conditions) and chick-rearing (lower stress due to ice-free conditions). In high metabolic rate species, we suggest that organ size varies in response to environmental stress. We conclude that the organ dynamics of seabirds are set by a combination of key life history traits (like incubation shift and metabolic rate) and environmental conditions.     

Variation in ice conditions has strong effects on the breeding of marine birds at Prince Leopold Island, Nunavut

The maximum extent of sea ice in the northern hemisphere has been contracting for several decades, with implications for all ice-associated biota. To determine how variation in ice conditions affects reproduction in marine birds, we studied the effects of ice conditions on breeding of four species of seabirds over four years at Prince Leopold Island, Nunavut, a colony close to the limits of ice conditions where breeding is feasible. In 2000 and 2003, open water was present close to the colony in June, when the birds began to lay eggs. In 2001 and 2002, the ice edge in June was >200 km to the east of the colony, forcing birds to commute long distances to open water to feed. Egg-laying by thick-billed murres, black-legged kittiwakes and glaucous gulls was delayed and eggs and clutches were smaller in 2001 and 2002. However, northern fulmars laid at the same time in all years, although their incubation shifts were longer in 2001 and 2002 than in 2003. Open water was present close to the colony by the time of hatching in all years. Despite this, nestling survival of northern fulmars, body condition and nestling growth of thick-billed murres and body condition and nestling survival of black-legged kittiwakes were lower in 2001 and 2002 than in –2000 and 2003. All these indicators suggest that feeding conditions in the years of late ice break-up continued to be worse than usual even after open water was available at the colony. Our study suggests that current trends towards earlier ice break-up in the Arctic may be beneficial for marine birds at Prince Leopold Island, at least in the short-term.     

Populations and trends of Canadian Arctic seabirds

Canada’s eastern Arctic (Nunavut and Arctic Quebec—Nunavik, N of 60°) supports large numbers of seabirds in summer. Seabird breeding habitat in this region includes steep, rocky coasts and low-lying coasts backed by lowland sedge-meadow tundra. The former areas support colonial cliff- and scree-nesting seabirds, such as murres and fulmars; the latter inland or coastal seabirds, such as terns, gulls and jaegers. The region supports some 4 million breeding seabirds, of which the most numerous are thick-billed murres (Uria lomvia; 75%), black guillemots (Cepphus grylle; 9%), northern fulmars (Fulmarus glacialis; 8%) and black-legged kittiwakes (Rissa tridactyla; 6%). The majority of Arctic seabirds breed in a small number of very large colonies (>10,000 birds), but there are also substantial numbers of non-colonial or small-colony breeding populations that are scattered more widely (e.g. terns, guillemots). Population trends among Canadian Arctic seabirds over the past few decades have been variable, with no strongly negative trends except for the rare ivory gull (Pagophila eburnea): this contrasts with nearby Greenland, where several species have shown steep declines. Although current seabird trends raise only small cause for concern, climate amelioration may enable increased development activities in the north, potentially posing threats to some seabirds on their breeding grounds.     

Variable sea‐ice conditions influence trophic dynamics in an Arctic community of marine top predators

Sea‐ice coverage is a key abiotic driver of annual environmental conditions in Arctic marine ecosystems and could be a major factor affecting seabird trophic dynamics. Using stable isotope ratios of carbon (δ¹³C) and nitrogen (δ¹⁵N) in eggs of thick‐billed murres (Uria lomvia), northern fulmars (Fulmarus glacialis), glaucous gulls (Larus hyperboreus), and black‐legged kittiwakes (Rissa tridactyla), we investigated the trophic ecology of prebreeding seabirds nesting at Prince Leopold Island, Nunavut, and its relationship with sea‐ice conditions. The seabird community of Prince Leopold Island had a broader isotopic niche during lower sea‐ice conditions, thus having a more divergent diet, while the opposite was observed during years with more extensive sea‐ice conditions. Species' trophic position was influenced by sea ice; in years of lower sea‐ice concentration, gulls and kittiwakes foraged at higher trophic levels while the opposite was observed for murres and fulmars. For murres and fulmars over a longer time series, there was no evidence of the effect of sea‐ice concentration on species' isotopic niche. Results suggest a high degree of adaptation in populations of high Arctic species that cope with harsh and unpredictable conditions. Such different responses of the community isotopic niche also show that the effect of variable sea‐ice conditions, despite being subtle at the species level, might have larger implications when considering the trophic ecology of the larger seabird community. Species‐specific responses in foraging patterns, in particular trophic position in relation to sea ice, are critical to understanding effects of ecosystem change predicted for a changing climate.     

Body condition of shorebirds upon arrival at their Siberian breeding grounds

Arctic breeding shorebirds carry substantial body stores on their long-distance migrations from their non-breeding grounds. Upon arrival at the breeding area the remains of these stores can be used for egg formation, insurance against poor feeding conditions or rebuilding organs. We quantified body condition (body mass, total body water, lean body mass and fat mass estimated using the deuterium dilution method) in seven shorebird species caught upon arrival in the Siberian Arctic. Arrival condition was compared with incubation condition in a subset of species. After correction for structural size, body mass was significantly lower at arrival than during incubation in most of the species (but 3–18% above lean mass). Fat index (fat mass/lean mass) varied between 5.1 and 13.2%. Fat stores were estimated to enable survival for 0.6 days for the smallest and 2.5 days for the largest species. We discuss possible functions of arrival stores: insurance, egg-formation or rebuilding organs. G. H. Visser: Deceased.     

Raising young reduces body condition and fat stores in black-legged kittiwakes

We conducted a manipulative experiment to investigate how raising chicks affects the body condition (body mass scaled by body size) and body composition (percent fat vs. lean mass) of black-legged kittiwakes (Rissa tridactyla). For 4 consecutive years (1991–1994) we removed eggs from randomly selected nests and then compared adults raising chicks with adults that had their eggs removed. At the end of the chick-rearing period, adults raising chicks were significantly lighter for their size than adults that had their eggs removed. Adults raising chicks also had a significantly lower percent body fat (by 28%) than adults from manipulated nests. The difference in percent body fat between the two groups was apparent at all levels of condition, suggesting that adults that are raising chicks apportion their reserves differently than adults that are working only to meet their own metabolic needs. End-of-season body condition of adults from manipulated and unmanipulated nests varied significantly among 5 years of study, and appeared to reflect differences in local foraging conditions. In all years, females were in worse condition than males at the end of the breeding season. This sex-specific condition difference did not, however, appear to indicate a greater short-term reproductive cost among females. Females were lighter for their size than males in both the manipulated and unmanipulated groups. Our results suggest that adult kittiwakes compromise their body condition and body composition during chick rearing to increase the likelihood of successfully fledging young, even though such adjustments may decrease their own post-reproductive survival probabilities. Prior to estimating the body composition of the experimental birds, we evaluated the usefulness of several noninvasive techniques for predicting fat mass in kittiwakes. We used cross-validation techniques to compare multiple regression models that included total body electrical conductivity (TOBEC), total body water (TBW), and morphometric measurements as independent variables. The most parsimonious model for predicting fat mass was based on TOBEC and mass measurements. TBW and morphometrics were of little utility in predicting fat mass in kittiwakes. Previous studies that have evaluated the usefulness of TOBEC as a predictor of fat mass have shown mixed results. We suggest that the size of the experimental subject relative to the size of the TOBEC measurement chamber may affect the accuracy of this technique. Received: 30 November 1998 / Accepted: 29 April 1999     

Adipokinetic hormone inhibits the formation of energy stores and egg production in the cricket Gryllus bimaculatus

Adipokinetic hormones (AKHs) mobilise lipids, carbohydrates and/or proline from insect fat body stores. In addition, AKHs inhibit lipid and protein synthesis in the fat body. In the current study, 100 pmol homologous Grybi-AKH was injected twice daily into adult female crickets, Gryllus bimaculatus, starting on the day of adult emergence. The effects of the injected AKH on the formation of energy reserves in the fat body and on egg production were measured on day 4 after adult emergence. In comparison to water-injected control animals, lipid and protein content in the fat body of the AKH-injected crickets was significantly reduced, suggesting an inhibitory effect of AKH on the formation of lipid reserves and protein stores. The content of glycogen and free carbohydrate in the fat body was significantly higher in the AKH-injected animals. The most pronounced effect of the AKH-injections was a significant reduction of ovary mass, due to the retarded maturation of the oocytes and the significantly lower number of terminal oocytes produced. It is concluded that AKH inhibits egg production indirectly by interference with the formation of energy stores in the fat body that are mobilised to fuel egg production.     

Relative contribution of lipid sources to eggs of lesser scaup

Studies of how birds mobilize nutrients to eggs have traditionally considered a continuum of possible allocation strategies ranging from income breeding (rely on food sources found on the breeding grounds) to capital breeding (rely on body reserves stored prior to the breeding season). For capital breeding, stored body reserves can be acquired either on or away from the breeding grounds, but it has been difficult to quantify the relative contribution of each, precluding identification of key habitats for acquiring nutrients for clutch formation. During 2006–2009, we explored the importance of spring‐staging habitats versus breeding‐area habitats for egg‐lipid formation in female lesser scaup Aythya affinis using stable carbon (δ¹³C) isotope analyses. Although δ¹³C values for abdominal lipid reserves brought to the breeding grounds overlapped those of local amphipods, we were able to quantify the importance of local plant carbohydrates (seeds of emergent wetland plants) to the production of eggs. We compared the importance of local wetland seeds (overall δ¹³C: ?29.1 ± 0.9‰ SD) to combined lipid stores and lipids from local amphipods (overall δ¹³C: ?23.8 ± 2.2‰). Local seeds and stored body lipids contributed equally to egg lipid formation across years but we found evidence of annual variation in their relative importance. Wetland seeds contributed 39% (SE = 10%) to egg lipid production, and the importance of this source varied by year (90% CI = 47–75% in 2006, 13–42% in 2007, 29–65% in 2008, and 7–30% in 2009). In contrast to earlier studies that suggest lesser scaup predominantly employ a capital breeding strategy, our results suggest that in some years females may attain half of their energy for clutch formation from foods on the breeding grounds.     

Body condition changes of sand martins (Riparia riparia) during breeding, and a comparison with fledgling condition

The body condition of adult sand martins during the breeding season and a sample of fledglings was investigated by carcass analysis and by examination of live birds in the field. Fat scoring of live individuals was a reliable predictor of an individual's lipid content in most instances. Body mass changes during breeding were related to changes in the size of birds' lipid reserves, pectoral muscle mass, body water, and to development of the reproductive system. In both males and females, reserve lipid declined between the onset of breeding and nestling rearing. Pre-breeding males had significantly greater pectoral muscle masses than did nestling rearing females. The potential significance of protein in pectoral muscles as an energy reserve during breeding was small compared with lipid reserves. By comparing potential energy reserves in body lipid and protein with daily energy expenditure, it was calculated that neither incubating nor nestling rearing adults could survive a day of normal activity without feeding. The selective premium on adults optimizing their use of time and energy for self-maintenance behaviour during breeding is therefore likely to be great.     

Amphibian lipid levels at metamorphosis correlate to post-metamorphic terrestrial survival

In organisms that have complex life cycles, factors in the larval environment may affect both larval and adult traits. For amphibians, the postmetamorphic transition from the aquatic environment to terrestrial habitat may be a period of high juvenile mortality. We hypothesized that lipid stores at metamorphosis may affect an animal’s success during this critical transition period. We examined variation in total lipid levels among years and sites in recently metamorphosed individuals of two pond-breeding salamander species, the marbled salamander (Ambystoma opacum) and the mole salamander (A. talpoideum), with limited data for one anuran species (southern leopard frog, Rana sphenocephala). Lipid levels were allometrically related to body size and ranged from 1.9 to 23.8% of body dry mass. The two salamander species differed in lipid allocation patterns, with A. opacum apportioning a higher percentage of total lipid reserves into fat bodies than A. talpoideum. Species differences in lipid allocation patterns may primarily reflect that large metamorphs will mature as one-year olds, and, regardless of species, will alter lipid compartmentalization accordingly. We used mark–recapture data obtained at drift fences encircling breeding ponds for 13 A. opacum cohorts to estimate the proportion of postmetamorphic individuals that survived to breed (age 1–4) and the mean age at first reproduction. Regression models indicated that size-corrected lipid level at metamorphosis (i.e., lipid residuals), and to a lesser extent rainfall following metamorphosis, was positively related to adult survival. Snout-vent length at metamorphosis was negatively related to age at first reproduction. We suggest that lipid stores at metamorphosis are vital to juvenile survival in the months following the transition from aquatic to terrestrial habitat, and that a trade-off shaped by postmetamorphic selection in the terrestrial habitat exists between allocation to energy stores versus structural growth in the larval environment.     

No Evidence of Metabolic Depression in Western Alaskan Juvenile Steller Sea Lions (Eumetopias jubatus)

Steller sea lion (Eumetopias jubatus) populations have undergone precipitous declines through their western Alaskan range over the last four decades with the leading hypothesis to explain this decline centering around changing prey quality, quantity, or availability for this species (i.e., nutritional stress hypothesis). Under chronic conditions of reduced food intake sea lions would conserve energy by limiting energy expenditures through lowering of metabolic rate known as metabolic depression. To examine the potential for nutritional stress, resting metabolic rate (RMR) and body composition were measured in free-ranging juvenile Steller sea lions (N = 91) at three distinct geographical locations (Southeast Alaska, Prince William Sound, Central Aleutian Islands) using open-flow respirometry and deuterium isotope dilution, respectively. Average sea lion RMR ranged from 6.7 to 36.2 MJ d⁻¹ and was influenced by body mass, total body lipid, and to a lesser extent, ambient air temperature and age. Sea lion pups captured in the Aleutian Islands (region of decline) had significantly greater body mass and total body lipid stores when compared to pups from Prince William Sound (region of decline) and Southeast Alaska (stable region). Along with evidence of robust body condition in Aleutian Island pups, no definitive differences were detected in RMR between sea lions sampled between eastern and western populations that could not be accounted for by higher percent total body lipid content, suggesting that that at the time of this study, Steller sea lions were not experiencing metabolic depression in the locations studied.     

The use of energy stores in the puerulus of the spiny lobster Jasus edwardsii across the continental shelf of New Zealand

Nektonic pueruli of the spiny lobster, Jasus edwardsii, were caught from two locations about 20 km apart across the continental shelf on the south east of the North Island, New Zealand. The pueruli were assayed for total protein, glucose, glycogen, and lipid content. Only the lipid content differed between pueruli caught onshore and offshore (mean difference=3.1 mg or 3.4% of dry mass). The average difference in lipid content measured over this distance was used to calculate the rate of energy consumption and timing for pueruli to actively swim from the continental shelf to shore. These results confirmed previous theoretical estimates and indirect measures. Furthermore, the rate of energy consumption would allow all of the pueruli caught offshore to swim to shore based on their total measured lipids. However, some individuals with low energy stores may be energetically compromised at arrival which may affect their subsequent moulting and survival. The results of this study indicate that lipid is the primary format for energy storage of the nektonic puerulus of the spiny lobster and that these lipid reserves have sufficient energetic capacity to allow the puerulus to actively swim the distance across the shelf to settle on the coast.     

Producing extra eggs does not deplete macronutrient reserves in European Starlings Sturnus vulgaris

Recent studies have suggested that the size of avian clutches may be determined in part by the costs of egg production, which are thought to involve the depletion of endogenous nutrient reserves. I tested the hypothesis that producing extra eggs would deplete protein and lipid reserves in a passerine species, the European Starling Sturnus vulgaris . The first three eggs of clutches were removed on the days they were laid to induce females to lay extra eggs. Females responded to this manipulation by laying, on average, 1.3 eggs more than controls. However, based on the distribution of clutch sizes, it appears that some females responded to the removal of three eggs by producing more than one extra egg, whereas others responded by laying no extra eggs or by deserting. In unmanipulated females, the lean dry mass of the flight muscles and total body lipid were found to decline throughout breeding, an observation which is often interpreted as evidence that egg production depletes endogenous reserves. However, females experimentally induced to produce an extra egg did not have reduced stores of protein or lipid at clutch completion. No effect was observed in starlings even though this study had substantial (80%) power to detect a change in protein reserves of the same magnitude as that observed in a previous study of gulls. The decrease in flight muscle mass that has frequently been observed during breeding in passerines may not be due simply to mobilization of endogenous protein reserves.     

Prey Patch Patterns Predict Habitat Use by Top Marine Predators with Diverse Foraging Strategies

Spatial coherence between predators and prey has rarely been observed in pelagic marine ecosystems. We used measures of the environment, prey abundance, prey quality, and prey distribution to explain the observed distributions of three co-occurring predator species breeding on islands in the southeastern Bering Sea: black-legged kittiwakes (Rissa tridactyla), thick-billed murres (Uria lomvia), and northern fur seals (Callorhinus ursinus). Predictions of statistical models were tested using movement patterns obtained from satellite-tracked individual animals. With the most commonly used measures to quantify prey distributions - areal biomass, density, and numerical abundance - we were unable to find a spatial relationship between predators and their prey. We instead found that habitat use by all three predators was predicted most strongly by prey patch characteristics such as depth and local density within spatial aggregations. Additional prey patch characteristics and physical habitat also contributed significantly to characterizing predator patterns. Our results indicate that the small-scale prey patch characteristics are critical to how predators perceive the quality of their food supply and the mechanisms they use to exploit it, regardless of time of day, sampling year, or source colony. The three focal predator species had different constraints and employed different foraging strategies – a shallow diver that makes trips of moderate distance (kittiwakes), a deep diver that makes trip of short distances (murres), and a deep diver that makes extensive trips (fur seals). However, all three were similarly linked by patchiness of prey rather than by the distribution of overall biomass. This supports the hypothesis that patchiness may be critical for understanding predator-prey relationships in pelagic marine systems more generally.     

Examining the potential for nutritional stress in young Steller sea lions: physiological effects of prey composition

The effects of high- and low-lipid prey on the body mass, body condition, and metabolic rates of young captive Steller sea lions (Eumetopias jubatus) were examined to better understand how changes in prey composition might impact the physiology and health of wild sea lions and contribute to their population decline. Results of three feeding experiments suggest that prey lipid content did not significantly affect body mass or relative body condition (lipid mass as a percent of total mass) when sea lions could consume sufficient prey to meet their energy needs. However, when energy intake was insufficient to meet daily requirements, sea lions lost more lipid mass (9.16±1.80 kg±SE) consuming low-lipid prey compared with eating high-lipid prey (6.52±1.65 kg). Similarly, the sea lions lost 2.7±0.9 kg of lipid mass while consuming oil-supplemented pollock at maintenance energy levels but gained 5.2±2.7 kg lipid mass while consuming identical energetic levels of herring. Contrary to expectations, there was a 9.7±1.8% increase in metabolism during mass loss on submaintenance diets. Relative body condition decreased only 3.7±3.8% during periods of imposed nutritional stress, despite a 10.4±4.8% decrease in body mass. These findings raise questions regarding the efficacy of measures of relative body condition to detect such changes in nutritional status among wild animals. The results of these three experiments suggest that prey composition can have additional effects on sea lion energy stores beyond the direct effects of insufficient energy intake.     

A comparison of techniques for classifying behavior from accelerometers for two species of seabird

The behavior of many wild animals remains a mystery, as it is difficult to quantify behavior of species that cannot be easily followed throughout their daily or seasonal movements. Accelerometers can solve some of these mysteries, as they collect activity data at a high temporal resolution (<1 s), can be relatively small (<1 g) so they minimally disrupt behavior, and are increasingly capable of recording data for long periods. Nonetheless, there is a need for increased validation of methods to classify animal behavior from accelerometers to promote widespread adoption of this technology in ecology. We assessed the accuracy of six different behavioral assignment methods for two species of seabird, thick‐billed murres (Uria lomvia) and black‐legged kittiwakes (Rissa tridactyla). We identified three behaviors using tri‐axial accelerometers: standing, swimming, and flying, after classifying diving using a pressure sensor for murres. We evaluated six classification methods relative to independent classifications from concurrent GPS tracking data. We used four variables for classification: depth, wing beat frequency, pitch, and dynamic acceleration. Average accuracy for all methods was >98% for murres, and 89% and 93% for kittiwakes during incubation and chick rearing, respectively. Variable selection showed that classification accuracy did not improve with more than two (kittiwakes) or three (murres) variables. We conclude that simple methods of behavioral classification can be as accurate for classifying basic behaviors as more complex approaches, and that identifying suitable accelerometer metrics is more important than using a particular classification method when the objective is to develop a daily activity or energy budget. Highly accurate daily activity budgets can be generated from accelerometer data using multiple methods and a small number of accelerometer metrics; therefore, identifying a suitable behavioral classification method should not be a barrier to using accelerometers in studies of seabird behavior and ecology.     

Nutrient reserve dynamics and energetics during long-term fasting in the king penguin (Aptenodytes patagonicus)

Males of king penguins (Aptenodytes patagonicus) naturally fast during one month at the beginning of their breeding cycle in the sub-Antarctic islands. Previous qualitative data have shown that this species adapts to prolonged fasting by mobilizing fat stores and minimizing protein loss and that this strategy ends with a progressive increase in protein utilization. In the present study, the quantification of nutrient utilization from body composition of captive birds indicates that, during the phase of protein conservation, 93% of the energy produced derives from the oxidation of fat stores, body protein accounting for the remainder (7%). Tissue composition analysis shows that integument (feathers, skin and subdermal fat) is the main lipid source (65% of the fat loss) during this period, and that pectoral muscles provide the majority of body protein (57% of the total loss). If the fast is prolonged until a body mass below 10 kg is reached, there is a progressive four-fold increase (from 1 68 to 6.50 gN/24h) in nitrogen excretion, together with a progressive exhaustion of fat stores. This shift in fuel metabolism is not a direct consequence of total lipid depletion, because 22% of the initial fat content still remains when proteins are no longer spared. During this later metabolic phase, protein is not only provided by pectoral muscles (71% of the loss), but also by hindlimb muscles (13%), and there remains only 2% of the initial amount of lipid in the integument at the end of the fast. Total energy expenditure is close to the fasting basal metabolic rate during the phase of protein conservation (2.52 W/kg), but it increases by 33% (3.36 W/kg) during the phase of protein wasting. This difference is probably due to a rise in locomotor activity, that is interpreted as reflecting a stimulation of food foraging behaviour before the lethal depletion of nutrient reserves.     

Seasonal cycles in total chemical composition of two Lake Baikal benthic-pelagic sculpins (Cottocomephorus, Cottoidei)

Annual cycles in chemical composition of the body, liver, gonads, red and white muscles were determined for two medium fat sculpins, Cottocomephorus grewingki and C. inermis , endemic to Lake Baikal. Their total lipid content ranged from 3 to 9% during the year. The content of defatted dry substance was 14–17%, similar to the protein content of the other Baikalian cottoid fishes. The prespawning period was characterized by a positive lipid and protein balance in both species. In C. grewingki the liver performed largely a metabolic function, whereas in C. inermis it served also as a storage site for lipid reserves. During spawning, total body lipids of females of both species showed a two- to threefold decrease. Males of C. grewingki guarding nests deplete greatly their total body lipids, which decrease seven- to ninefold by the time of larval hatching in comparison with the prespawning period, and constitute 1–2%. After spawning, lipid reserves of C. grewingki were quickly restored to the initial level (from about 3 to 9%) and maintained during the long sexual maturation period. In C. inermis total body lipids increased only twofold in comparison to those observed during the spawning period.     

Breeding and moulting fasts in macaroni penguins: Do birds exhaust their fat reserves?

• 1.1. Plasma concentrations of urea, uric acid and total lipid were compared in pre- and late-fast breeding and moulting macaroni penguins (Eudyptes chrysolophus) to test the hypothesis that birds exhaust their lipid reserves and initiate marked protein utilisation towards the end of natural fasts.
• 2.2. Male and female macaroni penguins fasted for a minimum of 29–32 days and 20 days during the breeding and moult fasts, and the difference in body weight over the sample period (reflecting body weight loss) was 31–34% and 41–47%, respectively.
• 3.3. There was no significant increase in plasma urea or uric acid at the end of either fast, nor any decrease in plasma lipid concentrations compared to pre-fast birds.
• 4.4. These results suggest that macaroni penguins continue to rely mainly on lipid reserves during the later stages of natural fasts. This is consistent with post-fast body composition data for other small penguin species.

     

Long-term fasting and re-feeding in penguins

Spontaneous fasting during reproduction (sometimes with a full stomach) and moult is a major characteristic of the annual cycle of penguins. Long-term fasting (up to four months in male emperor penguins) is anticipated by the accumulation of fat (incubation fast) and of fat and protein (moult fast). During most of the incubation fast, birds rely almost entirely on lipids as an energy source, body proteins being spared. However, below a critical (but non-total) fat store depletion, marked behavioural, metabolic, and endocrine changes occur. Spontaneous locomotor activity increases and the egg is transitorily left unincubated for increasingly long periods, until its definitive abandon and the bird departs to re-feed at sea. These changes are thought to be activated by an endogenous re-feeding signal triggered before lethal energy depletion. An increase in body protein catabolism in the face of a reduction in lipid availability and utilisation, and an increase in circulating corticosterone vs. a decrease in plasma prolactin, are likely to be major metabolic and hormonal components of this signal. The survival and rapid restoration of energy stores in birds having departed to re-feed at a stage of near total lipid depletion demonstrates the effectiveness of the re-feeding signal. Penguins, and possibly other seabirds, are therefore appropriate animal models for understanding the long-term interactions between body energy reserves and fasting, breeding and feeding physiology and behaviour.