Regulation of food provisioning in the Antarctic petrel; the importance of parental body condition and chick body mass

Authors

  • Torkild Tveraa,

    1. Norwegian Institute for Nature Research (NINA), Department of Arctic Ecology, Storgata 25, N-9005 Tromsø, Norway, and Biology Department, Faculty of Mathematical and Natural Sciences, University of Tromsø, N-9037 Tromsø, Norway;
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  • Bernt-Erik Sether,

    1. Department of Zoology, Norwegian University of Science and Technology, N-7034 Trondheim, Norway, and Norwegian Institute for Nature Research, Tungasletta 2, N-7005 Trondheim, Norway; and
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  • Ronny Aanes,

    1. Norwegian Institute for Nature Research, Tungasletta 2, N-7005 Trondheim, Norway
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  • Kjell Einar Erikstad

    1. Norwegian Institute for Nature Research (NINA), Department of Arctic Ecology, Storgata 25, N-9005 Tromsø, Norway, and Biology Department, Faculty of Mathematical and Natural Sciences, University of Tromsø, N-9037 Tromsø, Norway;
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Abstract

1. Two hypotheses may explain how long-lived seabirds regulate the food provisioning to their chick. The fixed level of investment hypothesis states that the parents provide food for their chick according to an intrinsic rhythm, independent of their chick's need. The flexible investment hypothesis states that the parents adjust their food provisioning both according to their chick's and their own need.

2. We tested how the Antarctic petrels adjust the food-provisioning according to their own body condition or to their chick's need. First, we selected parents in poor and good body condition. Then we gave all parents randomly a chick of different body mass, but of the same age. We then measured the chicks daily until they were fed for the first time after swapping.

3. Parents in good body condition at hatching were more likely to produce a chick that was still alive 9 days after hatching than parents in poor body condition. Chick body mass at day 9 and at the end of the guarding period was positively related to the mean body condition of the parents at hatching.

4. The meal size provided by parents in good body condition was larger than that provided by parents in poor body condition. Parents in good body condition delivered more food to small than to large chicks, whereas no such relationship was found among parents in poor body condition.

5. Our results suggest that the Antarctic petrel parents adjust the amount of food delivered to their chick according to both the chick's need and their own body condition, and that the ability to respond to the chick's need is dependent upon their own body condition.

Introduction

Life-history theory predicts that parental effort is regulated so that the costs and benefits of current reproduction are balanced to maximize lifetime reproductive success (Stearns 1992; Roff 1992). At every point in the breeding cycle, the parents must therefore decide how much energy should be used on reproduction and how much should be used in self maintenance. In long-lived species, even a small reduction in adult survival may have a large negative impact on lifetime reproductive success (Charlesworth 1980; Wooller, Bradley & Croxall 1992). It is therefore suggested that Procellariiformes have evolved a fixed level of parental investment independent of their chick's need (Ricklefs 1987, 1992; Hamer & Hill 1993, 1994; Lorentsen 1996; but see Bolton 1995a,b), presumably to minimize the costs of current reproduction (Srther, Andersen & Pedersen 1993). However, recent studies of other long-lived birds show that they may have a flexible investment dependent upon their chick's need (Johnsen, Erikstad & Srther 1994; Bertram, Welham & Ydenberg 1996; Cook & Hamer 1997; Erikstad et al. 1997).

The costs of current reproduction may be assessed through monitoring of parental body condition (Drent & Daan 1980; Chastel, Weimerskirch & Jouventin 1995a,b; Weimerskirch 1995; McNamara & Houston 1996). Accordingly, theoretical work has suggested that that parents in poor body condition should be restrictive in putting effort into their offspring, i.e. have a fixed level of investment in their chick. On the other hand, parents in good body condition should be expected to adjust their effort to their chick's need, i.e. have a flexible investment in their chick (McNamara & Houston 1996, Erikstad et al. 1998). This is because parents in good body condition can put more resources into their offspring before their body masses deplete to the threshold body condition where further investment is too costly for future maintenance (Chaurand & Weimerskirch 1994a; Weimerskirch et al. 1994). Accordingly, Chastel et al. (1995b) demonstrated that the annual breeding frequency is positively correlated to the parents’ body condition in the blue petrel Halobaena caerulea (Gmelin). Parental body condition may also reflect a parent's prospects of successfully raising chicks within a certain season (Lorentsen 1996; Srther et al. 1997). For instance, Srther et al. (1997) found a large annual variation in breeding success of the Antarctic petrel Thalassoica antarctica (Gmelin), and the within year variations were positively related to the parents’ body condition. However, Procellariiformes have a special breeding strategy. They exploit sparsely and patchily distributed prey, and the parents deliver large meals to the chick independently of each other. The chick's status at one feed may therefore not reflect its need at the next feed (Ricklefs 1992). Any adjustment of food provisioning to the chick's need may therefore not have evolved (Ricklefs 1992).

In the present study, we test experimentally how parental body condition may affect reproductive decisions in the Antarctic petrel. To evaluate the impact of variation in parental body condition, we selected parents in poor and good body condition at hatching and then randomly provided them with chicks of different body masses, but of the same age. By this design, we examined whether the parents delivered food to their chick according to own body condition or according to the chick's need. In general, we expected parents in good body condition to deliver more food to their chicks than parents in poor body condition as previously shown for the Antarctic petrel (Lorentsen 1996; Srther et al. 1997). If Antarctic petrels have a fixed investment in their chick, we expected no effect of chick body mass on the amount of food delivered. On the other hand, if Antarctic petrels have a flexible investment in their chick dependent upon the parental body condition and chick body mass, we expected that both the parental body condition and the body mass of the chick would significantly affect the amount of food delivered to the chick. Moreover, we expected that parents in good body condition would have a better ability to respond to the chick's need than parents in poor body condition.

Materials and methods

The study was carried out at Svarthamaren (71°53′S, 5°10′E), Dronning Maud Land, in continental Antarctica, from 27 December 1996–3 February 1997. At Svarthamaren ≈250 000 pairs of Antarctic petrels breed at high densities, allowing easy access to breeding birds (Røv, Lorentsen & Bangjord 1994). The incubation is shared by both parents, with one parent always incubating, while its mate spends the time at the sea foraging (Lorentsen & Røv 1995). The single chick is fed by both parents for ≈47 days (van Franeker 1994). The average feeding frequency per parent is once every 3·9 days (Srther et al. 1993), such that the chick is on average fed every other day. The size of the meals delivered by a parent ranges from 80 to 250 g and the mean meal size in 1992 was 148 g, SD = 32·0 g (Lorentsen 1996).

In order to obtain the hatching body condition of a sample of adults, we recorded the hatching date in 208 nests (Sample 1) and individually marked both parents with a steel ring. Morphological measurements recorded included skull length, bill depth (±0·05 mm) and wing length (±0·5 mm). These nests were visited daily, and breeding failure and the number of days the parents guarded their chick were recorded. The hatching body mass of the parent on the nest was measured and defined as their body mass at hatching, whereas the hatching body mass of the bird at sea was defined as their body mass at their first arrival to the colony after hatching (i.e. 1–7 days post-hatch).

In order to determine the sex of the study birds, we used the discriminant function presented by Lorentsen & Røv (1994), which is based upon the morphological characters measured.

To control for body size, we regressed body mass upon the first principal component (PC1) from a principal component analysis. The PC1 explained 12·7 (d_f. = 1, 207, P < 0·001) and 8·3 (d_f. = 1, 207, P < 0·001) percent of the variance in male and female hatching body mass, respectively. The residuals from these regressions were defined as the individuals’ hatching body condition.

We analysed variation in mass increments by analysis of covariance (PROC GLM, SAS Institute 1990). We entered ‘group of adult’ as a factor and ‘chick body mass prior to feeding’ as a covariate. The mass increments were skewed to the right. Square root transformation normalized this variable. All means are given as means ± 1 SE unless otherwise stated. Statistical tests are two-tailed, and P < 0·05 is considered as statistically significant.

Experimental design

All study parents hatched their egg between 6 and 16 January, with the mean hatching date at 12·4 ± 0·1 January. On 26 January when all parents had left their chick unattended, 177 pairs from Sample 1 (see above) still had a chick. Lorentsen (1996) has shown that the average body condition of the pair at hatching best explained the parents’ ability to deliver food to their chick. We therefore averaged the hatching body condition of the 177 pairs, and selected the 50 pairs with the poorest body condition (poor body condition) and the 50 pairs with the best body condition (good body condition). The 77 remaining pairs with an intermediate body condition were excluded. One day later, we gave the parents in poor and good body condition a foster chick of the same age from Sample 2 (see above). Consequently, all parents received a foster chick of similar age, but of different body mass. Owing to overnight loss, only 47 nests remained in the poor body condition group and 49 in the good body condition group. The variation in body mass among the 16-day-old foster chicks was large ( = 380 g, SD = 77·4, n = 96), ranging from 159 to 540 g, but there was no difference in the average body mass of foster chicks given to parents in poor and good body condition (372 ± 11·7, n = 47 vs. 388 ± 10·5, n = 49, t = 1·04, P = 0·30). Nor did the average hatching date of parents in poor (12·7 ± 0·22, n = 50, 1 = 1 January) and good body condition (12·3 ± 0·26, n = 50) differ significantly (t = 1·00, P = 0·32).

The body mass of the parents’ own chick was measured (±0·5 g) on the ninth day after hatching and at the end of the guarding period (7–15 days post-hatch).

The body masses of the foster chicks were measured daily from the time of swapping until the chicks were fed for the first time by their foster parents. The mass increase due to this first feed is hereafter referred to as the foster chick's mass increment. At this point, none of the parents had any knowledge about their chick's nutritional status.

In our analyses, we could not correct for the possible effect of double meals delivered to the chick, i.e. that both parents had fed the chick. However, the parents forage independently of each other, and the number of meals delivered per day is apparently not related to the body condition of the parents at hatching in this species (Lorentsen 1996).

Results

Parental body condition vs. chick survival and body mass

Parents in good body condition were more likely to produce chicks that survived until day 9 than parents in poor body condition (mean body condition of the pair: Wald-χ2 = 5·5, Δd_f. = 1, P = 0·02). Female body condition also contributed to the survival of chicks until day 9 (Wald-χ2 = 7·9, Δd_f. = 1, P < 0·001), whereas male body condition did not (Wald-χ2 = 0·24, Δd_f. = 1, P = 0·63). The chick body mass at day 9 was not related to the male hatching body condition, but was positively related to the hatching body condition of the female and the average hatching body condition of the pair (Table 1). The average body condition of the pair best predicted the chick's body mass at day 9 and at the end of the guarding period (Table 1, Fig. 1, see also Lorentsen 1996).

Table 1.  The relationship between parental body condition at hatching and the body mass of the original chick on day 9 post-hatch and at the end of the guarding period
 Parental hatching body condition
Dependent variableSexrd_f.P
Chick body mass on day 9
 Male0·111,192 0·11
 Female0·221,192<0·001
 Pair0·251,192<0·001
Chick body mass at end of the guarding period
 Male0·241,181<0·001
 Female0·241,181<0·001
 Pair0·361,181<0·001
Figure 1.

The relationship between the body mass of their original chick at the end of the guarding period and the average body condition (body mass corrected for body size) of the pair at hatching.

The mean body mass of chicks at day 9 was significantly lower in parents in poor (175 ± 7·3 g, n = 50) than in parents in good body condition (196 ± 6·3 g, n = 50, t = 2·16, P < 0·05). Thus, parents in good body condition were able to provide more food to their chicks than parents in poor body condition.

Mass increment

The time between swapping and the chick's first feed varied from one to several days. Accordingly, parents spending a long time foraging may return with larger meals than those returning after only a short stay at sea. We therefore corrected for the possible effect of feeding frequency on mass increment by entering the days elapsed from swapping and until the mass increase as a covariate. However, this factor was found to be insignificant (F = 1·70, d_f. = 1, 87, P = 0·20) and was subsequently removed from the analysis.

In general, parents delivered larger meals to small rather than to large chicks (F = 9·96, d_f. = 1, 88, P < 0·01). The mean meal size of parents in poor body condition was smaller than that of parents in good body condition (Fig. 2). Furthermore, the parents in poor body condition did not respond to an undernourished chick to the same extent as parents in good body condition (adult group vs. chick body mass interaction: F = 6·17, d_f. = 1, 88, P = 0·02).

Figure 2.

The average mass increment (±1 SE) of chicks of parents in the poor and the good body condition groups (see text for further explanations). The figures denote sample sizes.

Because of the significant interaction between chick body mass and adult group, we performed simple regressions within each group of adults. This analysis revealed that only parents in good body condition responded to their chick's need (Fig. 3; parents in poor body condition: r2 = 0·01, n = 43, P = 0·59; parents in good body condition: r2 = 0·21, n = 47, P < 0·01).

Figure 3.

The relationship between foster chick body mass prior to their first feed and their subsequent mass increment of (a) parents in poor body condition and (b) parents in good body condition.

Discussion

The main findings in this study may be summarized as follows: (i) Parents in good body condition at hatching were more likely to produce a chick that was still alive 9 days after hatching than parents in poor body condition. Their chicks were also heavier at day 9 and when left unattended (Table 1, Fig. 1). (ii) Parents in good body condition delivered larger meals to their chick than those in poor body condition (Fig. 2). (iii) Small chicks had larger mass increments than large chicks. However, this relationship was only significant for chicks with parents in good body condition (Fig. 3).

The finding that parents in good body condition deliver more food to their chick than those in poor body condition is in accordance with other studies of the Antarctic petrel in the same colony (Lorentsen 1996; Srther et al. 1997) and other seabird studies (Weimerskirch et al. 1994; Chaurand & Weimerskirch 1994b; Erikstad et al. 1997), suggesting that parental body condition may explain some of the variation in growth rates of chicks.

The results from this study show that Antarctic petrels in good body condition have a flexible investment and regulate their effort according to their chick's need (Fig. 3). This is in contrast to other studies of the Antarctic petrel in the same colony (Srther et al. 1993; Andersen, Srther & Pedersen 1993, 1995; Lorentsen 1996) and to studies of other Procellariiformes (Ricklefs 1987, 1992; Hamer & Hill 1993, 1994; but see Bolton 1995a,b). Two factors may explain this aberration. First, as shown by Erikstad et al. (1998), parents should not respond to the chick's demand when the breeding conditions are poor. Only when the breeding conditions reach some upper threshold should the parents be willing to respond to the chick's need. Second, our study suggests that only parents in good body condition can respond to the chick's need (Fig. 2). Similarly, Erikstad et al. (1997) cross-fostered 20-day-old puffin chicks Fratercula arctica (L.) and found that light chicks grew faster than heavier chicks after swapping. Moreover, parents in good body condition delivered more food to their chicks than those in poor body condition.

Parents in good body condition are better able to provide food for their chick than those in poor body condition. This may be explained by the fact that parents in good body condition are more efficient feeders than those in poor body condition (e.g. Reid 1988) and/or that parents in good body condition may have more resources stored than parents in poor body condition. This may allow them to give a larger proportion of the food load to the chick without causing their body mass to drop below some threshold at which costs for future reproductive output may be incurred (Chaurand & Weimerskirch 1994a; Tveraa, Lorentsen & Srther 1997). However, Tveraa et al. (1997) found no relationship between body condition and foraging success of Antarctic petrel females during the incubation period.

The finding that the Antarctic petrel already at the first delivery of food after swapping gave larger meals to small than to large foster chicks may be caused by two different mechanisms. First, heavy chicks may have less ability to swallow food than light chicks as heavy chicks may already be overfed which reduce their capacity to accept food from the parents (cf. Ricklefs 1992; Hamer & Hill 1994). Secondly, these results may suggests that the Antarctic petrel is able to both assess the nutritional status of their chick and to respond to it immediately. Such a mechanism may be important among Procellariiformes that feed their chick independently of each other at long (several days) intervals (e.g. Warham 1956; Richdale 1963). Two strategies may be used to respond to an undernourished chick. First, a parent may increase the foraging frequency and return to the nest after only a short stay at sea. However, as pointed out by Ricklefs (1987, 1992), the chick's need when one of the parents next returns to the colony may be poorly correlated to the chick's status at the previous feed as both parents feed the chick with large meals independently of each other. Second, a parent may respond directly to an undernourished chick by giving a larger proportion of its catch to the chick. This will minimize the chick's immediate probability of starvation.

It has been suggested that Procellariiformes cannot, or do not, respond to hunger calls from their chick, or that hunger calls may merely facilitate transfer of food (e.g. Ricklefs 1987, 1992). Alternatively, the chick's begging may be an important factor signalling the chick's nutritional needs in the Antarctic petrel and may regulate the amount of food given to the chick. Harris (1983) showed that the feeding rate of the puffin could be manipulated by playing recordings of chick's hunger calls. To what extent Antarctic petrel parents respond to their chick's need is apparently limited by the parents’ body condition. Studies which reveal the relationship between the chick's hunger call, the parents’ body condition and the amount of food delivered to the chick are needed to investigate such a possibility further.

In conclusion, this study has revealed that Antarctic petrels have a flexible investment in their chicks. However, the parents vary considerably in their ability to provide food to their chick. A chick's chance of survival is positively related to the parent's body condition. Parents in good body condition produce heavier chicks than those in poor body condition (Fig. 1) and may deliver lager meals (Fig. 2). Large chicks can sustain longer fasting periods than small chicks (e.g. Ricklefs & Schew 1994) allowing the parents of large chicks to spend more time searching for food than the parents of small chicks. This may in turn increase the parents’ probability of successfully finding food (cf. Tveraa et al. 1997; Tveraa et al. 1998). We therefore propose that both the chick's body mass and the parental body condition may be important factors which outweigh some of the negative effects of variation in food availability on chick growth and survival in this species (see also Srther et al. 1997). Moreover, parents in good body condition can apparently respond to their chick's need (Fig. 3) and give more food to an undernourished chick than parents in poor body condition. This will in turn increase the chick's probability of survival and recruitment to the population in the future. Parents in poor body condition do not, however, respond to their chick's need, probably because they maximize their own chances of surviving and reproducing in the future (Erikstad et al. 1998).

Acknowledgements

This is publication no. 148 from the Norwegian Antarctic Research Expedition (NARE) 96/97. The study was financed by the Research Council of Norway. We thank the Norwegian Polar Institute for logistical support during the expedition. Special thanks to Per Fauchald for enthusiastic and helpful comments on the paper and to Rob Barrett for improving the English. Keith Hamer and an anonymous referee are also acknowledged for helpful comments on the manuscript.

Received 26 September 1997; revision received 16 December 1997

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