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- Materials and methods
Trivers (1972) defined parental investment as ‘any investment by the parent in an individual offspring that increases the offspring chances of surviving at the cost of the parent ability to invest in other offspring’. A central point in life history theory is that parental investment in current reproduction should be balanced by the costs in terms of residual reproductive value (Williams 1966; Stearns 1992). For many bird species, the nestling rearing phase is a critical period for decisions influencing this balance (Drent & Daan 1980). During this period, breeding birds must decide how to allocate the energy they gather between themselves and their offspring. In short-lived passerines, the probability of survival to future reproduction is low, so an increase of parental effort at the expense of their survival would be expected in response to an increment in chick demand (Linden & Møller 1989). In contrast, in long-lived species such as seabirds current reproductive investment is more likely to be regulated by the impact of reproductive effort on the future reproduction of the parents, and the adults should be restrictive in increasing effort (Drent & Daan 1980; Linden & Møller 1989). Nevertheless, in seabirds, the studies of experimentally increased reproductive effort have shown differing results, with costs of reproduction passed to offspring (intergenerational costs; Harris 1966; Jarvis 1974; Ricklefs 1987; Sæther, Andersen & Pedersen 1993; Mauck & Grubb 1995), absorbed by parents (intragenerational costs; Reid 1987; Weimerskirch, Chastel & Ackermann 1995), or shared (Jacobsen, Erikstad & Sæther 1995; Tveraa, Lorentsen & Sæther 1997; Weimerskirch, Prince & Zimmermann 2000).
There is much debate about how seabirds optimize the balance between current reproductive effort and future reproduction, and two main mechanisms have been proposed. The ‘fixed investment hypothesis’ posits that seabirds have a fixed level of investment in their current reproduction, independently of offspring requirements (Ricklefs 1987; Sæther, Andresen & Pedersen 1993; Mauck & Grubb 1995). The ‘flexible investment hypothesis’ suggests that long-lived birds have a flexible reproductive effort according with offspring demand and condition (Reid 1987; Johnsen, Erikstad & Sæther 1994; Jacobsen et al. 1995; Weimerskirch et al. 1997). These two mechanisms are not mutually exclusive, and energy allocation during reproduction should be dependent upon breeding condition: when food is easily available and parents are in good condition they can compensate to some extent to chick requirements, but they may be unable to do so when resources are less available (Erikstad et al. 1997; Erikstad et al. 1998; Weimerskirch et al. 2000; Weimerskirch, Zimmermann & Prince 2001). In this context, permanent monitoring of own body condition should be essential in reproductive decisions (Drent & Daan 1980), and parents could regulate the risk of an increase in mortality under the control of a mass threshold (Monaghan, Uttley & Burns 1992; Chaurand & Weimerskirch 1994; Olsson 1997). In fact, evidence is accumulating that adult body mass plays an important role in foraging behaviour, food provisioning and regulation of parental effort in seabirds (Monaghan et al. 1989; Chaurand & Weimerskirch 1994; Chastel, Weimerskirch & Jouventin 1995; Erikstad et al. 1997; Tveraa et al. 1997; Dearborn 2001; but see Wernham & Bryant 1998).
In addition to their body condition and food availability, females should optimize their breeding decisions in relation to the level of effort of the partner (Chase 1980; Houston & Davies 1985; Winkler 1987). In species with biparental care, a conflict between sexes over division of work probably occurs (Trivers 1972). The reduction of feeding effort by one partner should, in most cases, result in an increased effort by the other (Winkler 1987), as was supported by several studies in short-lived passerines (e.g. Wright & Cuthill 1989, 1990; Whittingham, Dunn & Robertson 1994; Markman, Yom-Tov & Wright 1995; Sanz, Kranenbarg & Tinbergen 2000). As far as we know, only two studies have tested the compensatory response in long-lived birds, showing that a decrease in the incubation effort by one partner produces a compensatory response by the other partner depending on its body condition (Tveraa et al. 1997; Dearborn 2001).
The best way to explore the relationship between current reproductive effort and the cost imposed on future reproduction may be by experimental manipulations of reproductive effort (Reznick 1985; Partridge & Harvey 1988). As a model, experimental modifications of brood size in birds have been studied (Linden & Møller 1989; Dijkstra et al. 1990; Stearns 1992). Despite a large number of brood size experiments to study the cost of reproduction in short-lived birds (Dijkstra et al. 1990; Murphy 2000), few have involved long-lived birds and results have been mixed (e.g. Golet, Irons & Estes 1998). Manipulation of brood size does not manipulate the reproductive effort directly (Lessells 1991; Lessells 1993), and assumes reproductive costs representing a linear function of brood size. However, some general models predict that the optimal response could yield a decrease, no response or even an increase in effort with increasing brood size (Winkler 1987; Tammaru & Hörak 1999). Brood size enlargements might have limited ability to detect reproductive costs, because the parents may reduce their parental effort adaptively (Tammaru & Hörak 1999). Thus, results of brood size manipulations should be compared with other studies that manipulate parental effort, such as handicap experiments, to understand better the breeding decisions involved.
The blue-footed booby (Sula nebouxii Mine-Edwards) is a potentially interesting species for examining sexual differences in the regulation of parental body condition during the breeding season. In this long-lived species (annual survival rate > 90%; Croxall & Rothery 1991), females are approximately 31% heavier than males during the breeding season (Nelson 1978) and recruit at an earlier age (Osorio-Beristain & Drummond 1993). In contrast with many seabirds with similar parental roles, female boobies feed chicks three times more than do males (Anderson & Ricklefs 1992; Guerra & Drummond 1995). Males forage inshore, close to the colony, and females make longer trips to offshore waters (Nelson 1978). In a recent study, female boobies with experimentally increased reproductive effort (shortened wing span) reduced their body condition and shared the cost with their offspring (Velando 2002). In addition to that experimental study, here we reported two experiments: the manipulation of the amount of effort by the male and a brood size manipulation. The main objective of this study was to investigate body condition regulation by examining: (1) how females respond to reduced effort by their partners; (2) whether males and females have a flexible or fixed body condition regulation in response to reproductive effort manipulation; and (3) whether parental effort is regulated by a body mass threshold comparing the adult body mass in three different experimental studies that increased reproductive effort in the same season.
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We showed that in blue-footed boobies the sexes reacted differentially to being handicapped. In handicapped males condition remained stable, while in handicapped females condition deteriorated (Fig. 4; Velando 2002). The mass loss of handicapped females could be an adaptive response to compensate for the increase in their flight costs (see Norberg 1981; Pennycuick 1989). In fact, some bird species lose mass abruptly at the onset of the nestling phase to increase their efficiency in transporting food to their chicks (Moreno 1989; Jones 1994). However, that is not the case for blue-footed boobies, which maintain stable their body mass throughout the reproductive cycle (Wingfield et al. 1999; Velando 2002). In addition, the reduction of female body mass as a response to a handicapped partner and brood enlargement suggest that low body mass of experimental females represents energy stress associated with parental investment (Golet & Irons 1999). Reduction in body condition may be interpreted as an increase in reproductive costs (Drent & Daan 1980), which may reduce their long-term physiological condition (as for the immune system, e.g. Alonso-Alvarez & Tella 2001) and thereby their residual reproductive value, through elevated mortality or reduced future reproductive success (Golet et al. 1998; Wernham & Bryant 1998). We did not test for survival or fecundity costs across years, but in birds brood size manipulations that have demonstrated effects on adult condition have also often shown effects on adult residual reproductive value (review in Golet et al. 1998). Handicapping experiments and brood enlargement experiment had a strong effect on chick mass, indicating a reduction of parental effort. Seabird species exhibit positive correlations between mass at fledging and subsequent survival and lifetime reproductive success (Perrins, Harris & Britton 1972; Jarvis 1974; Spear & Nur 1994; but see Harris & Rothery 1985).
sex differences in body mass regulation
The fact that males and females responded differentially in each of three different manipulations and their coincident pattern (Fig. 4) are fascinating findings. This different response suggests that costs or benefits of mass regulation differ between sexes (see Winkler 1987). Females compensated partially the reduced contribution of their partner. A compensatory response protects the chicks from detrimental effects of reduction in the amount of food delivered to the brood. In addition, females shared with the offspring the cost of being handicapped (Velando 2002), and also reduced their body mass in response to brood enlargement. This suggests that females can regulate their effort in relation to offspring needs, conveyed probably through the chick's begging behaviour (Drummond 2002). In our study, males did not reduce their body condition as a response to handicap manipulation or to compensate for their partner's lower parental care, although the power of our tests was low. We did not measure directly male reproductive effort, but offspring and female partners reduced their body mass in the male handicapping experiment, which seems to suggest that males reduced their contribution. Males also did not reduce their body condition as a response to brood enlargement but increased their body condition when the brood was reduced. Thus, these results as a whole suggest that males work at some physiological maximum or are unwilling to pay the cost in terms of future survival when the cost of reproduction is increased.
The differences in body mass regulation agree with the differential provisioning pattern by male and female blue-footed boobies, a species where females are larger than males. Thus, Guerra & Drummond (1995) showed that male food contribution increases gradually until chicks are 10 days old, after that remaining constant, while female food contribution increases continuously during chick growth (at least until chicks are 35 days old). Thus, females seem to have a flexible parental effort according to the chicks’ needs, whereas males have a fixed contribution after chicks are 10 days old. Like males, females probably have an upper limit but they could be working with a buffer of nutritional reserves. Several hypotheses can be proposed to explain this differential body mass regulation. (1) Long-lived seabirds can accumulate fat as energy reserves for self-maintenance (Cherel, Leloup & Le Maho 1988). Female blue-footed boobies are 31% heavier than males and females may have more stored fat than males. (2) Male may also deplete their reserves earlier due to previous investments in nest and territory defense (see Nelson 1978). (3) Moreover, in the blue-footed booby, it has been suggested that males and females differ in their foraging areas (Nelson 1978) and female boobies could be better foragers than males (Anderson & Ricklefs 1992) which could, in turn, influence the factors that govern energy allocation as occurs in wandering albatrosses, Diomedea exulans (Weimerskirch et al. 1997). (4) Another potential explanation is that future reproductive success differs between sexes, but there are no data on sex-specific fitness. (5) Lastly, in the blue-footed booby extra-pair copulations represent 13·3% of copulations by all females (Osorio-Beristain & Drummond 1998), and males may be careful in their parental effort decisions due to uncertainty of paternity. Despite the above explanations, the generality of differential response to manipulations between sexes remains to be explored, as already pointed out by Moreno et al. (1995).
clutch size and parental condition
Blue-footed boobies in this and most other populations rarely lay three eggs (Nelson 1978; A. Velando, unpublished data), despite their ability to brood experimental extra fledglings, as other Sulids (; Jarvis 1974). Nevertheless, offspring from enlarged broods have lower body mass that can affect their fitness (Lindström 1999). Mothers should lay the clutch size that maximizes the number of new recruits in the population (Lack 1966; Perrins & Moss 1975). In addition, each female can have her own optimal clutch size depending on her particular situation (individual optimization hypothesis; Perrins & Moss 1975; Pettifor, Perrins & McCleery 1988). In long-lived birds, females’ optimal decision should depend on their safety margin regarding their critical physiological condition. We found some evidence that the parental ability of boobies that naturally laid different number of eggs differed. Parents rearing unmanipulated broods had similar condition at the end of the experiment independently of their initial brood size, but males with two-egg clutches that were reduced to one nestling had better condition than those of natural broods with one or two nestlings (Fig. 3). This suggests that, at least, males with two-egg clutches were able to allocate more resources to reproduction than males with one-egg clutches.
In addition to their own quality, females should adjust their clutch size to the quality of their mate. In seabirds, there is some evidence that parents are able to exchange information about their current body condition (Tveraa et al. 1997). Whether females adjust clutch size to male quality remains an open question, but it should be taken into account in species with sex-specific optimal clutch size.
regulation of parental investment and body mass threshold
The present results suggest that reproduction is costly for adult blue-footed boobies. Results of experimental studies on reproductive costs of seabird species are summarized in Table 2. From 23 experiments reporting adult condition or survival the results are mixed, with 65% finding some cost in adults. Although experimental designs varied widely, general trends can be detected in these experiments. No experiment showed that the experimentally imposed cost is paid only by parents, and only one study did not find any cost in offspring or parents (Harris 1966). Thus, most of the studies showed that the cost is passed to offspring or shared. In the blue-footed booby male costs of reproduction were detected, in terms of body condition, when effort was experimentally reduced, whereas female costs were evident when effort was increased experimentally. Also, some studies detected parental costs but other failed to demonstrate reproductive costs in the same species (Table 2). The failure in detecting parental cost in some experiments might have resulted from a reduced parental effort due to their body condition regulation. The reduced condition of nestling resulted from experiments where the parental effort was increased provides clear evidence that parents are restricted in the amount of food that they can supply to the young. Therefore, the inability of some studies to detect parental costs should be not used as evidence that reproduction is cost-free (Golet et al. 1998; Wernham & Bryant 1998; Tammaru & Hörak 1999).
The results of Table 2 suggest that seabirds are restrictive in the increase of parental effort. In some cases, parents may compensate for the increase in chick demand, although this compensation seems to be limited. Thus, for instance, in the Antarctic petrel (Thalassoica antarctica) the ability of parents to adjust their effort is dependent on their own condition (Tveraa et al. 1998), and during incubation the parents deserted the egg when their body mass reached some critical lower threshold (Tveraa et al. 1997). A critical body mass level also probably regulates parental desertion during incubation and the reduction in parental effort during the chick stage in many seabirds (Monaghan et al. 1989; Monaghan et al. 1992; Chaurand & Weimerskirch 1994; Olsson 1997; Weimerskirch 1998).
In Isla Isabel, blue-footed bobbies deserted their nests but maintained their body mass during the El Niño event of 1992 (Wingfield et al. 1999). In our studies, we showed that female boobies decreased their own body mass until a certain common mass level. In the three experiments with increased costs, females reached very similar values of body mass (Fig. 4), whereas offspring suffered differentially between experiments (Figs 1 and 3; Velando 2002). This suggests that females are working with a buffer of nutritional reserves at this critical level, and that below this level, females preferentially allocated resources to the maintenance of their body condition at the expense of investment in current reproduction. Our study was conducted during a good breeding season; females can use their nutritional reserves without compromising their future survival due to the good food availability (e.g. Weimerskirch et al. 2000,2001) or alternatively, females can risk some of their future survival in order to produce young which would have better chances of survival (Erikstad et al. 1998).