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For most animals, the only way to obtain resources is by expending energy while foraging. The ability of individuals to adjust energy expenditure while foraging is likely to influence fitness (Drent & Daan 1980; Stephens & Krebs 1986) because foraging determines the intake of resources that are expended on fitness related activities. However, individuals face many fitness trade-offs, so they must differentially allocate time and energy between competing life-history traits such as reproduction, survival or growth (Stearns 1992). Thus, allocation links foraging and life-history traits and foraging effort should be treated as the result of allocation (Boggs 1992). This implies that foraging individuals should be able to adjust their energy expenditure according to allocation decisions. This is generally overlooked because most studies that focus on allocation processes only consider the input of resources obtained from foraging on life history, mainly reproduction through provisioning, whereas measures of energy expenditure and especially of resource storage are not examined. Conversely, studies on foraging consider patterns of resource intake, but generally do not address resource use or effort. It is typically assumed that foraging animals always maximize efficiency, or the ratio of energy gained over energy spent while foraging (Ydenberg et al. 1992). In addition, the patterns of energy intake and expenditure observed may be interpreted as having been optimized by natural selection (Ricklefs 1996), but the extent to which individuals are able to adjust energy expenditure according to allocation decisions is poorly studied. Therefore, being able to measure energy expenditure of foraging individuals when allocation decisions differ is of particular interest, but often logistically difficult. Indeed measures of reproductive effort should be dynamic and they should include measures of the energy allocated and individual variation in activity and foraging efficiency (Stearns 1992).
Pelagic seabirds are long-lived animals that rely on a food that is often located at long distances from the breeding grounds, implying a high cost of foraging to reach distant food resources (Ricklefs 1990; Weimerskirch 1999). On the other hand, they have to feed the chick as frequently as possible to enhance the probability of producing an offspring in good condition. Several species solve this conflict by using a specific strategy whereby parents alternate between short foraging trips where they feed the chicks and loose mass and long foraging trips where parents restore their body reserves (Chaurand & Weimerskirch 1994a). Short trips allow parents to increase feeding frequency but have a negative yield. This strategy has been shown to occur in many species of petrels and albatrosses (Weimerskirch 1999), and even in penguins (Clarke et al. 1998) that rely on distant resources. In some species, it has been shown by tracking that during short trips, birds forage close to the colony over coastal waters, and during long trips far from the colony, birds forage over pelagic waters (Weimerskirch et al. 1997). This system has been viewed as a typical example of time and energy constraints on foraging, related to allocation decisions (Weimerskirch 1999). However to be able to understand how foragers adjust foraging effort, it is necessary to measure not only the rate of food delivery to the offspring and self-feeding, but to simultaneously measure energy expenditure. This has not yet been done.
The aim of this study is to explore the connections between foraging and allocation of resources and to examine to what extent foraging effort can be treated as a result of allocation. Here we examine simultaneously the foraging efficiency (defined as the ratio of energy gained over energy spent while foraging), foraging success, energy expenditure and resource storage in relation to investment in reproduction. Specifically, we estimate energy gain and energetic efficiency in a small pelagic seabird, the blue petrel (Halobaena caerulea Gmelin), which uses a two-fold strategy. This was done by measuring the flow of energy to the chick, the amount of self-feeding by adults, and field metabolic rates of foraging adults.
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One of the major and unexpected result of this study is that energy expenditure of foraging blue petrels can differ extensively according to allocation decision of the adult. We clearly demonstrated that the metabolic cost of short foraging bouts is at least 1·5 times the energy expended during long bouts, and probably closer to 2·2. This result was unexpected because it is different from previous predictions on allocation, which assumed that foraging costs were similar between the two kinds of trips (e.g. Weimerskirch et al. 1997). The only study that has compared field metabolic rates during long and short foraging trips was carried out during two different periods, incubation (long trips) and brooding (short trips) in an albatross, and found only a 10% difference in foraging costs between long and short trips (Shaffer, Costa & Weimerskirch 2003). It is particularly surprising because one might expect that foraging in more distant areas would result in higher energy expenditure compared to foraging in nearby waters. Although foraging costs may not be so different between short and long foraging trips in other species during the chick-rearing period, at least in another species similar differences exist. This study was preceded by a pilot study in 1997 undertaken on thin-billed prions (Pachyptila belcheri Mathews). Despite the very low number of individuals successfully studied (n = 2 for both groups), we obtained the same pattern as in blue petrels: short foraging trips are more expensive compared to long foraging trips, 3062 vs. 2197 kJ day−1 kg−1, respectively.
The much higher foraging cost of shorts trips has several consequences in terms of breeding effort and allocation decisions. First, it means that individual blue petrels are able to adjust foraging effort according to the allocation decision. This is the first time this has been demonstrated. Obviously, it was more costly for blue petrels to forage during short trips than during long trips. A priori this would not be expected because during short trips, blue petrels forage close to the islands over the shelf area, whereas during the long trips, birds forage at least 1000 km from their colonies where swarms of Antarctic krill Euphausia superba, one of their main prey during long trips, occur (Cherel et al. 2002). This means that during short trips, birds probably have completely different ways of foraging compared to long trips. During long trips birds commute to Antarctic waters, perhaps by using favourable wind conditions to lower flight costs, to search in highly productive waters. During short trips, birds catch a limited amount of prey and expend much more energy to do so. Furness & Bryant (1996) have shown that costs of foraging of an other petrel species can vary considerably in relation to wind conditions. Blue petrels may either use a different flight behaviour, not using winds optimally or taking off and landing more frequently, which can result in higher energetic costs (Weimerskirch et al. 2000; Shaffer, Costa & Weimerskirch 2001). Alternatively, petrels may make more dives (Chastel & Bried 1996), which is a costly activity for flying birds (Bevan et al. 1995). The cost of foraging during short trips is 3·2 times the energy expenditure during resting (800 kJ day−1 kg−1, Brown 1988), and during long trips only 1·4–2·1 times resting metabolic rate.
Foraging animals have to adjust their breeding effort in relation to time and energy constraints (Ydenberg et al. 1992). However, there are few empirical studies that have examined the currencies associated with foraging behaviour and reproduction, especially for animals relying on distant resources. Blue petrels basically forage in Antarctic waters and breed on sub-Antarctic islands. When time away from the nest is less of a constraint, such as during incubation, adults basically forage for trips of 9–18 days. At this time the yield decreases with the duration of trips, but increases as the season progresses to the summer (Chaurand & Weimerskirch 1994b). In summer, blue petrels rearing chicks are faced with a trade-off between foraging close to the breeding grounds to maximize food delivery to the chick, and foraging further from the colony where efficiency is higher (Fig. 2). Our results show that birds can make a compromise by alternating between short and long trips. The currency during long trips is to maximize efficiency, whereas during short trips the currency is to maximize rate of energy delivery to the chick. For blue petrels, maximum efficiency is achieved when adult mass gain is highest and foraging costs lowest, for trips lasting 6 days. Although 6 days is the optimal duration of foraging trips, the most frequent trip durations were 7 days.
Very few provisioning studies distinguish between self-feeding and delivery but this is probably crucial because allocation of food between self-feeding and delivery has an important influence on foraging decisions (Ydenberg et al. 1992). Our study shows that self-feeding during long trips is crucial for the success of short trips because most of the energy used during short trips was probably derived from the energy stored during long trips (Fig. 2). Thus, blue petrels are probably using two completely different decisions rules to determine the effort while foraging because of this ability to store energy during long trips which can then be used to supplement the higher costs of conducing short trips. Moreover, all food acquired during short trips is delivered to the chick.
The decision rules to allocate energy towards the offspring or for self-feeding are probably under the control of the body condition of adult birds (Weimerskirch 1998, 1999). Decisions to initiate a long trip are related to the proximity of a mass threshold, and blue petrels are the only species that almost always alternate short and long trips. They do not perform successive short trips before a long trip to increase the energy flow to the chick as do all other species of petrels and albatrosses (Weimerskirch 1999). The low adult body mass attained at the end of short foraging trips (168 g) is close to the mass threshold attained at egg desertion (164 g, Chaurand & Weimerskirch 1994b), but is nevertheless higher than the critical body mass of 160 g (Ancel, Petter & Groscolas 1998) when they start to use protein extensively instead of fat reserves, i.e. when mortality risks are increased.
There were no important differences in the provisioning and costs between 1999 and 2000. The distribution of foraging trips and provisioning parameters were also similar to data obtained in 1989 (Chaurand & Weimerskirch 1994a) and 1998 (Cherel et al. 2002; Weimerskirch unpublished data). This suggests that the foraging strategies of blue petrels are not as flexible as those of other petrel species which can adjust to a larger degree their foraging and provisioning effort by modifying the succession and number of short and long trips, or the duration of trips (Granadeiro et al. 1998; Weimerskirch, Fradet & Cherel 1999; Duriez, Weimerskirch & Fritz 2000). This reduced flexibility is probably related to the long distance between the colony and the feeding grounds, and to the efficiency of foraging. The small body size of blue petrels also means that it has a smaller safety margin of stored energy (Weimerskirch 1999).