Polar Biology

, Volume 27, Issue 4, pp 253–256 | Cite as

Annual energy budget and food requirements of breeding wandering albatrosses (Diomedea exulans)

Short Note

Abstract

Energy budgets form an integral part of our understanding of animal energetics, particularly when presented in the context of reproduction. In this paper, I created a time-energy budget for a breeding pair of wandering albatrosses (Diomedea exulans) to estimate the annual breeding costs and food requirements of the population at Possession Island, Crozet Archipelago. For a breeding cycle that lasts 356 days on average, a pair uses 2,733 MJ to raise a single chick to fledging. This estimate is 1.21 times higher than previously calculated for wandering albatrosses breeding at Marion Island. Unlike the current analysis, the previous study assumed that foraging costs were constant across all stages of the breeding cycle. Recent evidence shows that foraging costs vary during breeding for wandering albatrosses at Crozet and this is probably true for all populations. Incubation costs have also been shown to be substantially lower than previously determined. Therefore, if a wandering albatross pair at Crozet uses a total of 2,733 MJ to breed, they would need to consume at least 1.7 kg bird−1 day−1 of fresh food, on average, to balance their own energy requirements and to provision a single chick for approximately 278 days. At this rate of food consumption, the breeding population at Crozet would consume approximately 340 tonnes of fresh food per breeding season.

Introduction

Pelagic seabirds (i.e. albatrosses and petrels) generally represent the extreme in avian breeding ecology because they exhibit prolonged breeding cycles, slow natal development, and low annual reproductive output (Lack 1968; Ricklefs 1990). These extreme life-history characteristics are thought to have evolved from a variety of reasons, such as the limitation of energy resources in the pelagic environment (Lack 1968; Ashmole 1971), or possibly physiological restraint exhibited by adults when breeding (reviewed in Hamer et al. 2002). Consequently, the level of energy used by parents for breeding activities and the associated food requirements to carry out these activities, have a significant impact on the success or failure of reproduction (e.g. Chastel et al. 1995; Tveraa et al. 1998; Weimerskirch 1999). The construction of time-energy budgets can therefore provide a useful tool for modeling the constraints that affect breeding performance in these birds, as well as many other organisms. Food consumption can also be estimated from energy-budget models (e.g. Furness 1978) and from direct measures of metabolism (Nagy et al. 1984; Gabrielsen et al. 1987; Nagy 1987). Overall, these estimates may be critical for evaluating how individuals or populations respond to variability in the supply and demand of energy resources (Nagy 1989), and they may provide information about the role that seabirds play as top predators in the marine environment.

The development of time-energy budgets depends on our ability to partition the cost of specific activities in relation to how animals function within their environment. Thus, as measurements of energy expenditure and related activity patterns are obtained, the accuracy of energy-budget models can be improved. As an example, Adams et al. (1986) previously estimated the breeding costs of wandering albatrosses (Diomedea exulans) to be 2,263 MJ per pair per year (discounting the costs of the pre-egg laying stage). This energy budget was based on foraging costs of adult albatrosses measured during the chick-rearing period only, and thus assumed that foraging costs were constant across all reproductive stages (i.e. incubation, chick-brooding, and chick-rearing). More recently, however, Shaffer et al. (2003) determined that foraging costs of wandering albatrosses were 10% higher during chick-brooding than during incubation. Other studies on wandering albatrosses (Salamolard and Weimerskirch 1993; Weimerskirch et al. 1997b; Weimerskirch and Lys 2000) have also shown that parents regulate energy flow to the nest throughout reproduction, suggesting that energy expenditures of adults vary between reproductive stages. Lastly, the energetic costs at the nest during incubation in wandering albatrosses were shown to be 1.8 times lower than previously measured (Shaffer et al. 2001b). Given these more recent observations in breeding effort and overall performance, I constructed a time-energy budget for wandering albatrosses to re-evaluate the annual breeding cost and food requirements of this species. The results of the new energy budget predict that annual breeding costs of wandering albatrosses are 21% higher and food requirements are nearly 50% greater than previously reported.

Materials and methods

Time-energy budgets were created for a pair of wandering albatrosses breeding on Possession Island (46°S, 52°E), Crozet Archipelago, southwestern Indian Ocean (hereafter called Crozet). Because wandering albatrosses are sexually size dimorphic (males are ~20% heavier; Tickell 1968; Shaffer et al. 2001c), time and energy of activities within each stage of breeding were totaled separately for each sex, and then combined for the pair. During breeding, wandering albatrosses undergo three stages, which can be defined as: (1) egg-incubation stage, (2) chick-brooding stage where either adult broods (and guards) a young chick at the nest, (3) chick-rearing stage where an older chick is left alone at the nest while both adults forage at sea (Tickell 1968). Foraging costs during the incubation and chick-brooding stages were obtained from Shaffer et al. (2001a, 2003) and egg-incubation costs were from Shaffer et al. (2001b). The cost of adults to brood a chick has not been measured directly, so I assumed that it was at least equivalent to the cost of incubation (Shaffer et al. 2001b). This assumption is reasonable because Bevan et al. (1995) observed no statistical difference in cost to adult black-browed albatrosses (Thalassarche melanophrys) when incubating an egg or brooding a chick. The foraging costs of adults rearing chicks have not been measured at Crozet. However, Weimerskirch and Lys (2000) determined that wandering albatrosses rearing chicks alternate between long trips like those performed during incubation, and short trips like those performed during chick-brooding. On average, males spend 59% of their time conducting short trips, whereas females spend 44% of their time conducting short trips, and time at the nest for either parent to provision a chick is less than 12 h (Weimerskirch and Lys 2000). Therefore, I estimated the energetic cost of the chick-rearing period by assuming that the cost per day of adults foraging on long or short trips was equivalent to those measured during incubation or brooding stages, multiplied by the percentage of time each adult spent conducting either type of foraging trip. These costs were then amortized over a 246-day period, which is the average duration of the chick-rearing stage (Tickell 1968). Details of total costs and durations for each stage are summarized in Table 1.
Table 1

Time-energy budgets of breeding wandering albatrosses on Possession Island, Crozet Archipelago. The time and cost of feeding a chick at the nest during the chick-rearing period was assumed to be negligible because adults remain at the nest for less than 1 day on average (Weimerskirch and Lys 2000). Daily energy expenditure (DEE) is presented in kilojoules (kJ) and total energy expenditure (TEE) is presented in megajoules (MJ). The body masses given are the average body masses of adult male and female wandering albatrosses (Shaffer et al. 2001a, 2003)

Reproductive stage and activity

Time/energy

Male (10.35 kg)

Female (8.25 kg)

Totals per pair

Incubation

On nest

Time (days)

39

39

78

DEE (kJ day−1)

1,749

1,394

3,143

TEE (MJ)

68.2

54.4

123

At sea

Time (days)

39

39

78

DEE (kJ day−1)

4,333

3,748

8,081

TEE (MJ)

169

146

315

Totals

Time (days)

78

78

156

TEE (MJ)

237

201

438

Chick-brooding

On nest

Time (days)

20

12

32

DEE (kJ day−1)

1,749

1,394

3,143

TEE (MJ)

35.0

16.7

51.7

At sea

Time (days)

12

20

32

DEE (kJ day−1)

4,844

4,127

8,971

TEE (MJ)

58.1

82.5

141

Totals

Time (days)

32

32

64

TEE (MJ)

93.0

99.0

192

Chick-rearing

At sea (short trips)

Time (days)

145

109

254

DEE (kJ day−1)

4,844

4,127

8,971

TEE (MJ)

702

450

1,152

At sea (long trips)

Time (days)

101

137

238

DEE (kJ day−1)

4,333

3,748

8,081

TEE (MJ)

438

513

951

Totals

Time (days)

246

246

492

TEE (MJ)

1,140

963

2,103

Totals for breeding

Time (days)

356

356

712

TEE (MJ)

1,470

1,263

2,733

Results and discussion

If both wandering albatross parents provision their chick until it fledges (~356 days post-laying; Tickell 1968), the combined total cost of breeding for the pair would be approximately 2,733 MJ (Table 1). This equates to average energy expenditures of 4,130 kJ day−1 for a 10.35-kg male and 3,548 kJ day−1 for an 8.25-kg female over the entire breeding cycle. The main difference in cost between male and female wandering albatrosses is attributed to sexual size dimorphism in this species and not to differences in parental effort (Shaffer et al. 2003). The annual breeding cost of 2,733 MJ for a wandering albatross couple is 1.21 times higher than previously estimated for wandering albatrosses breeding at Marion Island (46°S, 37°E), southwestern Indian Ocean (Adams et al. 1986). Several factors may explain the difference in breeding cost between the two estimates. Primarily, Adams et al. (1986) assumed that average energy expenditures of foraging adults were constant across incubation, chick-brooding, and chick-rearing, though it was only measured during chick-rearing. A recent study showed that foraging costs of breeding adults were more variable (10% higher during chick-brooding compared to incubation) between reproductive stages at Crozet (Shaffer et al. 2003). Furthermore, other studies that examined breeding performance of wandering albatrosses at Crozet show that parental effort and body condition vary throughout breeding (Salamolard and Weimerskirch 1993; Weimerskirch et al. 1997b; Weimerskirch and Lys 2000). Thus at Crozet and probably other breeding locations (e.g. Kerguelen, Macquarie, Marion, Auckland, and South Georgia Islands), foraging costs of wandering albatrosses are not constant throughout the breeding cycle. This conclusion is also supported by similar research on other seabird species (e.g. Obst et al. 1987; Bevan et al. 1995; Bech et al. 2002).

The cost of incubation for wandering albatrosses breeding at Crozet has also been shown to be significantly lower (1.8 times; Shaffer et al. 2001b) than measurements collected from adults at Marion Island (Brown and Adams 1984). The main difference in cost can be attributed to measurement technique (respirometry vs doubly labeled water) and the duration over which energy expenditures were measured (Shaffer et al. 2001b). Thus, for a 78-day incubation period, the combined total cost for both adults would be 123 MJ (Table 1) compared to an estimate of 201 MJ reported earlier by Adams et al. (1986).

The difference in total breeding costs of wandering albatrosses at Crozet and Marion Islands could also be attributed to intrinsic variation between populations. However, the breeding populations at Crozet and Marion Islands are probably quite similar because both islands occur at the same latitude and are closer to each other (~1,200 km) than they are to other islands. Furthermore, some immigration and emigration of albatrosses between each island has previously occurred (Weimerskirch et al. 1997a), and the foraging ranges of each population are well within that of the other (Weimerskirch et al. 1993, 1994). Therefore it seems unlikely that intrinsic differences could account for the discrepancies in breeding costs that I calculated compared to that reported earlier by Adams et al. (1986).

When evaluating the total energetic costs to adult wandering albatrosses during each stage in the breeding cycle, it is clear that chick-rearing is the most costly part of reproduction because it requires 246 days or 77% of the total duration of the breeding cycle (Fig. 1). However, even when the costs to adults are averaged over a daily basis [e.g. 2,103×10kJ÷(246 days×2 adults) from Table 1], energy demand is higher during the chick-rearing stage compared to that of the brooding and incubation stages (Fig. 1). One factor that may contribute to the high cost of chick-rearing is that wandering albatrosses provision their chicks throughout the Antarctic winter when food is thought to be less plentiful and weather conditions are more extreme (Salamolard and Weimerskirch 1993). Nevertheless, wandering albatross adults compensate for the high cost of chick-rearing by regulating energy flow between themselves and their chicks using two foraging modes (i.e. alternating between short and long foraging trips; Weimerskirch et al. 1997b). Furthermore, adults have a large “safety margin” of energy reserves due to their body size (Weimerskirch and Lys 2000), which can buffer the impact of high energy demand and presumed low food availability during chick-rearing.
Fig. 1

The average cost per day and proportion of the total cycle for each breeding stage in wandering albatrosses at Crozet. The average cost for each stage (gray bars) and all stages combined (black bar) includes both time at sea and time on the nest for a breeding pair (see Table 1 and text for details). The breeding cycle includes the incubation (Inc), chick-brooding (Brd), and chick-rearing (Chk) stages

If the total annual energy budget of breeding wandering albatrosses is 2,733 MJ per pair, then a couple would need to consume 809 kg of food to satisfy the energy requirements of all activities (i.e. 2,733×103 kJ÷3.38 kJ g−1, assuming metabolizable energy yield is 3.38 kJ g−1 fresh mass; Adams et al. 1986). Chicks receive an additional 180–195 kg of food during the chick-rearing period (Weimerskirch and Lys 2000), so total food consumption of a wandering albatross pair breeding on Crozet would be ~1,000 kg per breeding season. Considering that parents spend about 300 days at sea [356  days total−(39 days during incubation+12 to 20 days during brooding); see Table 1], the average daily food consumption of both adults over the entire breeding season would be about 3.4 kg day−1 per pair, or 1.7 kg day−1 per bird. This quantity of food slightly underestimates the rate of food consumption on single foraging trips as determined directly by stomach temperature sensors (2.1±1.0 kg day−1 per bird; Weimerskirch et al. 1994), but it seems more reasonable than a rate of 1.1 kg day−1 per bird determined by Adams et al. (1986).

Finally, one of the major benefits of developing a time-energy budget is the ability to not only estimate food consumption for a breeding pair (above), but also to extrapolate food consumption for a breeding population. Possession Island in the Crozet Archipelago has an annual breeding population of 340 wandering albatross pairs (Weimerskirch et al. 1997a). Therefore, if a breeding pair consumes 1,000 kg per season, the entire breeding population on Possession Island would consume approximately 340 tonnes of fresh food per breeding season.

Notes

Acknowledgements

I thank H. Weimerskirch, D.P. Costa, and two referees for providing comments on earlier drafts of the manuscript. Logistical and financial support came from the National Geographic Society (grant no. 6346-98), National Science Foundation (awards INT-9873760 and IBN-9972651), and the Office of Naval Research (award no. N00014-00-l-0880).

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Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  1. 1.Department of Ecology and Evolutionary BiologyUniversity of California Santa CruzSanta CruzUSA

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