Female body mass at arrival

Twenty-four adult females were caught upon arrival at the breeding grounds (Table 2) with an average body mass of 1464 ± 110 g. Small sample sizes precluded testing for year effects.

Arrival time and start of egg-laying

All local breeding geese arrived on BBI within 10 to 16 days of the arrival of the first geese (Fig. 3). The first egg was laid 1–4 days after arrival of the first geese in 1991–1994 and 8 days after arrival in 1995 (Fig. 3). Hatching was synchronised; usually all nests on BBI hatched within one week. In 1995, for instance, parents and goslings in 15 of 16 nests left the nest within a 3-day period (20–22 July). Thus it is likely that birds with larger clutches had started egg-laying some days earlier than those with a small clutch.

Table 1.

Nests of Brent Geese placed on a weighing platform on BBI. Clutch size was determined on the first day of the weighing period. The period (day/month) is from the day the weighing scale was dug in under the nest until the day the female left the nest. N²⁴: The number of 24 hours periods in which uninterrupted registrations were obtained. Success: the clutch hatched (+), or the eggs were predated or the female left the nest prematurely (-). Overall success rate was 19/23 = 83%.

Changes in body mass during incubation

The general pattern of female body mass change during incubation is shown in Fig. 4 for the six females with the best (least interrupted) data in 1993 and 1995. Three distinct periods can be distinguished: Period 1 (days 1–8 of incubation), when female body mass was essentially constant or even increasing slightly; Period 2 (days 8–21), when body mass decreased in a regular and linear fashion; Period 3 (last 3 days of incubation), when body mass decreased rapidly. For 15 females we were able to record body mass at the end of all three periods (Table 1). Average body mass for these birds was 1269 ± 67 g (range 1157–1386) at the end of period 1, 1176 ± 70 g (1077–1321) at the end of period 2 and 1066 ± 106 g (951–1304) at the end of period 3, when birds left the nest after hatching. There was no effect of year (ANOVA, F_3,11 = 1.18, P = 0.36) or clutch size (F_4,10 = 0.84, P = 0.53) on the body mass at the end of period 1.

Table 2.

Catch date and body mass of adult female Brent Geese caught at arrival on the breeding grounds.

Figure 3.

Arrival of breeding birds at BBI in 1991 and 1993–95. The number of Brent Geese present is expressed as a percentage of the total BBI breeding population. Arrows indicate the date of the first egg-laying.

Female recess time during incubation

All females left the nest daily to feed in the territory around the nest. As far as we could observe, females spent almost all recess time feeding: 90% of the time in 1990 (Spaans et al. 1993). Males defended the territory against conspecifics and kept watch over the nest during the absence of the female.

The average daily recess frequency for all balance-females (Table 1) is plotted against the day of incubation in Fig. 5A. During the first 21 days of incubation (period 1 and 2 combined) there was no clear trend and the average recess frequency was 13.1 ± 4 times per 24 h (number of days with 24 h non-stop registration of a female was 197). During period 3 the frequency decreased to 8.4 ± 5.5 times per day (n = 36).

Figure 4.

Average body mass during incubation of 3 females (nest numbers 303, 304 and 316) in 1993 and 3 females (501, 503 and 504) in 1995. The three periods during incubation are indicated (see text).

Average recess duration showed the same picture as the recess frequency: little variation in the first 21 days and shorter recesses during the last 3 days of incubation (Fig. 5B). The average duration of nest-recess in periods 1 and 2 was 15.1 ± 4.1 min (n = 197) and in period 3 was 9.9 ± 6.2 min (n = 36).

Average total daily recess time in periods 1 and 2 was 195 ± 70 min day^-1 (n = 197) and during period 3 was 87 ± 75.4 min day^-1 (n = 36) (Fig. 5C). Over the total incubation period females were off the nest on average 178 ± 81 min day^-1 (n = 233). Mean nest attendance was therefore (1440–178)/1440 = 87.6%

Recess time and body mass loss

Average daily body mass loss of the 15 females in period 2 was significantly negatively related to the average daily feeding time; birds feeding for longer lost mass more slowly (Fig. 6). The average recess time per day for these females during period 2 was 208 ± 59 min (range 129–293) and they lost on average 7.0 ± 3.0 g day^-1 (1.6–10.8) in this period. The intercept for zero recess time, extrapolating from these data, is 14.4 g body mass loss per day.

Figure 5.

Average daily recess frequency ± SE (A), average recess duration ± SE (B) and average daily recess time ± SE (C) per day of incubation of all females on a balance in all four years.

Risk of egg predation

Predation of an egg by avian predators occurred only during female recess periods when males strayed too far from the nest giving gulls the opportunity to remove the nests' down cover and take an egg. Such predation of single eggs occurred frequently. The average probability of a nest surviving one day without any egg predation was 0.979 ± 0.0053 (data from all 5 years, totalling 749 nest days from 61 nests, including nests on a balance). The probability of a clutch surviving the full 24-day incubation period without any egg predation was thus 0.97924 = 0.60. This means that on average 40% of the nests suffered from predation of one or more eggs.

Figure 6.

Average daily body mass loss during period 2 as a function of average daily feeding time for 15 females (y = -0.035× + 14.4; F_1,13 = 12.73, R² = 0.49, P = 0.0034).

Assuming that there is a linear relationship between time off the nest and predation risk, we can make a crude estimate of the predation risk per time unit based on the average daily clutch survival and the average daily recess time during periods 1 and 2. The 195 min. recess time resulted in a clutch survival of 0.979. Thus the survival per hour is 0.979^60/195 = 0.9935. The daily recess time (as shown in Fig. 6) can then be converted to daily probability of clutch survival to determine the relationship between body mass loss and predation risk. Plotting the clutch survival over the first 21 days (period 1 and 2) of the incubation (= daily survival to the power of 21) against daily body mass loss shows that the more birds relied on their stores (evidenced by their higher daily mass losses), the higher their clutch survival was (Fig. 7).

Figure 7.

The probability of the full clutch surviving the whole incubation period as a function of female body mass loss per day.

Stores at arrival

Carcass analysis of birds collected in winter and spring in NW Europe (Korte 1988) indicates that females have less than 10 g fat left at a body mass of 1025 g, the mass that we treat as representing lean body mass for Taimyr geese. Geese on arrival weighed on average 1464 g (Table 2) and at hatching weighed 1066 g. Because this latter value is the lowest body mass measured during the annual cycle (Ebbinge & Spaans 1995), and very close to the lean mass, we treat 1066 g as representing the average body mass of female Brent Geese without stores. The amount of stores (fat and protein) females had upon arrival can be estimated as 1464–1066 = 398 g. The highest fuelling rate for female Brent Geese, measured on spring staging sites, lies in the order of 15 g day^-1 (Ebbinge 1989). Therefore it would take 27 days of intensively feeding in the temperate zone (daylight period in spring: about 16 hours) to accumulate such an amount of stores.

Between arrival and clutch completion

The period between arrival and the start of egglaying was just a few days (Fig. 3). Since most of the tundra was still snow-covered in mid-June and the vegetation just starting to grow, our impression was that it could be hard for the geese to meet their daily demands during this period, let alone to replenish their stores. In Lesser Snow Geese Caerulescens caerulescens for instance, the pre-laying period is longer and can be energetically beneficial (Ganter & Cooke 1996). It is known that White-fronted Geese Anser albifrons can feed on perennial subterranean plant organs during this period, a highly nutritious food source (Fox & Madsen 1981, Budeau et al. 1991). To the best of our knowledge such feeding behaviour has never been observed in Brent Geese (Spilling et al. 1994). Thus it seems likely that Brent Geese have to derive most of the energy needed for egg-laying from their flown-in stores.

We measured body mass at arrival but were unable to measure pre-laying mass. However, using clutch-size and body mass of the 15 balance-females we can estimate their pre-laying body mass. The average clutch size was 3.8 ± 1.3 eggs (n = 15) (Table 1) and the average weight of an egg just after clutch completion was 79.5 g (n = 94, Spaans et al. 1993), so the total average clutch weight was 3.8 × 79.5 = 302 g. Adding this to the average body mass at the end of period 1 (1269 g), we end up with a minimum expected pre-laying body mass of 1269 + 302 = 1571 g. The average body mass of females caught at arrival (excluding two birds <1300 g that were probably incapable of breeding) was 1483 ± 95 g (n = 22, Table 2). The fact that predicted mass is higher (by 88 g) than measured mass at arrival might mean that body stores contain less water than eggs or that females are able to replenish their stores to some extent between arrival and clutch completion. In Light-bellied Brent Geese Branta b. hrota Ankney (1984) found that weight loss as a result of egg laying was also less than the clutch weight (a factor of 0.74). He concluded that at most 71% of the protein in a clutch would be derived from stores (Ankney 1984) and therefore 29% from locally ingested nutrients.

Energy expenditure of incubating females

We have only measured mass but this should be translated into energy. Energetic equivalents of body mass loss during starvation have been obtained for several species of birds (see Table 3). We assume that the measured energetic equivalent of 24 kJ g^-1 body mass loss found in domestic goose can be applied to incubating Brent Geese. The estimate of the daily energetic cost (without feeding) for our incubating Brent Geese becomes 14.4 g daily mass loss (extrapolated from feeding time = 0, Fig. 6) × 24 kJ g^-1 = 346 kJ.

The most detailed measurements of the energetic expenditure of incubating waterfowl (without feeding) concern the Common Eider Somateria mollissima borealis work done by Gabrielsen et al. (1991). They measured the metabolic rate of incubating birds, and found this to be 10% lower than the conventional resting metabolic rate (RMR) determined separately with birds caught on the nest. According to the extensive analysis of Parker & Holm (1990), daily energetic yield from body stores was 490 kJ; this is only 0.75 the RMR measured for birds at this site. RMR has been measured in the Brent Goose in three different studies (collated by Miller & McA. Eadie 2006). For comparison with our estimate from body mass loss in period 2 of incubation we can compute the RMR expected for the mean mass halfway through this period (1223 g). Computation from 6 birds given by Miller & McA. Eadie (2006) (disregarding one outlier) and correcting for body mass by the 0.71 exponent derived by these authors for geese and ducks yields an expected RMR of 452 kJ day^-1. The value we estimated for our incubating females was 346 kJ. Apparently our Brent Geese can manage daily energy expenditure at values close to the ‘economising’ Eiders of 0.75 RMR.

Table 3.

Energetic equivalents of body mass loss during starvation

Dependence on stores during the incubation period

It seems remarkable that female body mass was stable or even increased during the first week of incubation (Fig. 4). Our impression was that there was no more or better food during this period than later on in the season and the females were not feeding longer than during period 2 (Fig. 5C). Milne (1976) suggested that the fact that the female Eiders he studied became dehydrated during laying and early incubation was caused by the water demands of egg production. The latter could also have been the case in our situation: females recovering in period 1 by replenishing the loss of water associated with egg-laying.

During period 2, from days 8–21 of incubation, body mass decreased linearly (Fig. 4). Daily feeding time of the 15 balance-females during this period was on average 208 min resulting in a limited body mass loss of 7.0 g day^-1. Forty-nine percent of the variance in mass loss was explained by the feeding time (Fig. 6). We suspect that quality differences in the food, caused by vegetation differences between the territories (Spaans et al. 1993, Spilling et al. 1994), can explain another part of the variance in mass loss, as may food quality/quantity differences between years as a result of different weather conditions (Eichholz & Sedinger 1999).

The steep decrease in body mass during period 3 can partly be explained by the reduced feeding of the females in this period; many females did not leave the nest at all during the last few days of incubation. However, the average daily body mass loss of 37 g ((1176-1066)/3) is quite large for a fasting bird of this size (Afton & Paulus 1993) and exceeds by far the estimate of the daily mass loss required to balance the cost of incubation in period 2 (Fig. 6). This mass loss suggests that females rely mainly on protein in this period. Although protein yields 18.0 kJ g^-1 (Pond 1981), the loss of concomitant intracellular water reduces the caloric density of protein tissue to 4–8 kJ g^-1 (Cherel et al. 1988). If a female had no fat left and had to metabolise only protein, the daily body mass loss would be between 346/8 = 43 g and 346/4 = 87 g (assuming the costs are 346 kJ day^-1). Given the loss of 37 g day^-1 that we measured, it is likely that females partly rely on their protein stores in this stage; depletion of most of their available fat could be the main reason for this.

Extrapolation of the regression line in Fig. 6 to feeding time = 0 yields a daily body mass loss of 14.4 g for period 2 of incubation. Since our Brent Geese lost on average 7.0 g daily during period 2, they managed to cover about half of their costs from their stores. To extend these budget estimates to the entire incubation period we assume that period 1 will be comparable to period 2, since the daily recess time (and presumably food intake) is similar (Fig. 5C). Due to the reduced feeding time during period 3, females will depend more heavily on their body stores in these last days of incubation. Taking the reduced feeding time as point of departure, and assuming costs to the female are the same as in period 2, we have computed that only 30% of the costs can be collected by feeding. Overall, we estimate that (21/24 × 0.49) + (3/24 × 0.7) = 52% must be drawn from the body, i.e. the female Brent Goose depends on her body stores for slightly more than one-half of her energy expenditure during the entire incubation period.

Is the intake rate required during nest absence a reasonable figure to balance the budget? For period 2 females were absent from the nest for 208 min each day, and in this time they had to collect at least the equivalent of (14.4–7.0) × 24 = 178 kJ (the act of feeding will add additional costs not estimated here). The rate of collection of at least 178/208 × 60 = 51 kJ metabolizable energy per hour seems feasible: during spring fattening in the Wadden Sea Prop & Deerenberg (1991) found an average hourly metabolizable intake rate of 85 kJ.

Consequences of leaving the nest during incubation

The nest attendance of 87.6% is comparable with values found for other Brent subspecies, which vary from 81.7 to 91.9% and are the lowest of all goose species studied (Afton & Paulus 1993, Eichholz & Sedinger 1999). Females leaving the nest risk losing eggs to predators, and the probability of egg loss in our study increased with the time spent feeding (Figs 6 and 7). Overall, 40% of the nests we studied suffered egg predation.

If there is little food, however, there is little point in attempting to feed. In contrast to our results, Madsen et al. (1989) and Spaans et al. (1993) found that Brent Geese spent an increasing amount of time off the nest as the incubation period progressed. This may have been caused not only by the birds' declining stores but also by an absence or scarcity of food early in incubation. In general, the availability of food will improve over time as snowmelt progresses and plant production increases. Consequently, Brent Geese breeding in colder conditions (in cold years or at higher latitudes) will depend even more on their body stores, particularly during the first part of incubation (Eichholz & Sedinger 1999).

Females arriving in the breeding area in very good condition (Table 2) face a trade-off between laying a larger clutch or saving stores to reduce feeding during incubation. Our balance-females with large clutches (5 or 6 eggs, Table 1) started incubation with comparable stores to the females with smaller clutches (1271 vs. 1266 g respectively). It seems that females choose the larger clutch option rather than saving stores to reduce feeding. From the predation point of view this is understandable. An investment in an extra egg roughly means 3 g stores per day less available to metabolise. This increased the predation risk by about 10% (Fig. 7). In other words the probability that this egg would survive the incubation period, despite the extra recess time, was about 90%.

This study shows the ‘position’ of Dark-bellied Brent Geese on the continuous scale between the extremes of ‘capital’ and ‘income’ breeders (Klaassen 2003). During incubation geese draw heavily upon stores that remain after migration, and the more a bird has to forage away from the nest the greater the risk of nest predation. The body condition at departure from spring staging areas 5000 km away is therefore an important determinant of the breeding success of Taimyr Brent Geese. Birds must retain sufficient stores to produce a clutch, and after that the remaining stores cover about half the costs during incubation. Females arriving too light can only lay a small clutch and will have to spend a more time feeding during incubation, with an increased predation risk to the clutch.

The geese we studied are those that arrived in the breeding area in June; these could well be only those birds that have sufficient stores to start breeding. Later in the season thousands of non-breeding (adult) Brent Geese show up in our area, potentially being late or light birds that did not attempt to breed. The average goose in our sample may not necessarily be the average goose in the greater population.

Due to the short summer season at the high latitudes of Taimyr Peninsula (our study site was at 74°N) nesting must start as soon as possible after arrival. The long flight with limited refuelling possibilities between Europe and Taimyr will be one reason why Brent Geese cannot arrive with sufficient stores to incubate without leaving the nest. White-fronted Geese, in contrast, breed in the same area in Taimyr but manage to incubate continuously (Spaans et al. 1999), as their final spring fattening areas in central Russia are much closer (Mooij et al. 1999). Moreover their costs during incubation are comparatively lower due to the larger size of this species (Miller & McA. Eadie 2006).