An organism's evolutionary success is determined by its lifetime reproductive output. Producing and caring for offspring may decrease energy available for subsequent reproductive opportunities, and reduce longevity. Thus, organisms balance current reproduction against future survival and reproduction (Williams 1966). This trade-off is known as reproductive cost and is hypothesized to be an important factor shaping life-history strategy for many species (Roff 1992; Stearns 1992). Diverse factors such as age, age at first reproduction, previous breeding experience, population density, and environmental conditions may affect the occurrence and size of reproductive costs (e.g. Clutton-Brock 1984; Weimerskirch 1990; Reiter & LeBoeuf 1991; Stearns 1992; Viallefont, Cooke & Lebreton 1995; Pistorius et al. 2004; Tavecchia et al. 2005; Beauplet et al. 2006).
In species for which the age at first reproduction and reproductive effort vary among individuals, it is essential to study animals of known age to gain insights into reproductive costs. Long-term studies are especially valuable to demonstrate how reproductive costs vary with changing ecological circumstances (Festa-Bianchet 1989). The Erebus Bay population of Weddell seals Leptonychotes weddellii (Lesson) is a model system for investigating costs of reproduction in a long-lived mammal inhabiting a variable environment. This population of seals has been the subject of an ongoing mark–resight research programme since 1969 (Stirling 1969; Siniff et al. 1977; Testa & Siniff 1987; Cameron & Siniff 2004) and contains a large number and proportion of animals of known age for whom reproductive histories are known. Further, the population, which is located at approximately 77°S in McMurdo Sound in the Ross Sea region of Antarctica, is the southernmost breeding mammal population in the world and data from this population provide researchers with a thorough, long-term data set for a long-lived marine mammal. Weddell seals are intermittent breeders, and some individuals may breed annually for many consecutive years, while others may remain nonbreeders for several years in between breeding years (Testa 1987; Hadley et al. unpublished data). Nonbreeding has been shown to have both positive and negative consequences for survival rate in various species (Orell et al. 1994; Harris & Wanless 1995). The variation in breeding propensity displayed by Weddell seals makes the species an excellent subject for learning about life-history decisions and reproductive costs in long-lived animals.
In this study, we evaluated both costs to survival and costs to future reproduction for female Weddell seals in Erebus Bay, Antarctica. Contrasting predictions have been made regarding reproductive costs for long-lived species in variable environments. Life-history theory predicts that costs to survival should be strongly selected against in species with long reproductive life spans. Reproductive output for long-lived species is determined by the outcomes of numerous breeding attempts throughout life, whereas species with short life spans may benefit from maximal investment in one reproductive bout. Therefore, surviving to future reproductive opportunities is crucial for maximizing lifetime reproductive output in long-lived species (Williams 1966; Goodman 1974; Charlesworth 1980) and individuals should be less prone to trade their own survival for that of their offspring because any reduction in adult survival would greatly lower lifetime reproductive success (‘prudent parent’ reproductive strategy; Drent & Daan 1980; Cam et al. 1998). However, numerous studies of long-lived seabirds have demonstrated that large variation in breeding conditions favours flexibility of reproductive effort (i.e. occasional investment in reproduction at a cost to survival, or ‘flexible-strategy hypothesis’) (Reid 1987; Jacobsen, Erikstad & Sæther 1995; Erikstad et al. 1997, 1998; Golet, Irons & Estes 1998). Despite the lower reproductive costs to survival generally predicted for long-lived species, the variability of the polar environment may require that seals occasionally invest in reproduction at a cost to survival (the flexible-strategy hypothesis). Therefore, we expected that both types of costs would be apparent.
Life-history strategy and lifetime reproductive output are also influenced by the manner in which reproductive costs vary during an individual's lifetime. Numerous studies have demonstrated that younger animals conceive, implant, or give birth later, and have lower natality rates than do older animals (Sæther & Haagenrud 1983; Lunn, Boyd & Croxall 1994). Furthermore, first-year survival of offspring has been shown to increase with increasing maternal age for southern elephant seals Mirounga leonina (McMahon & Bradshaw 2004). For Weddell seals, we therefore predicted that costs to both survival and reproduction would vary with age, with young seals exhibiting larger costs.
Animals breeding for the first time are also thought to experience higher reproductive costs than are experienced breeders, regardless of age (Weimerskirch 1990; Viallefont et al. 1995). However, separating the effects of age and breeding experience may be difficult in practice. Many investigators lack detailed information about individual reproductive histories or age of animals in their study population (Barbraud & Weimerskirch 2005), whereas others may not have adequate sample sizes or variation in their data sets to examine animals of equal age with varying levels of experience, or animals of various ages with equivalent experience. Our data set included seals with and without breeding experience for every age from 4 to 14, and we were thus able to investigate separately the effects of age and breeding experience. Several studies have found higher reproductive costs for inexperienced breeders while controlling for age (Lunn et al. 1994; Viallefont et al. 1995), and we therefore predicted higher reproductive costs for inexperienced seals in our study.
In accordance with Pistorius et al.'s (2004) findings for southern elephant seals, we predicted that age of first reproduction would not affect reproductive costs. However, based on variation in age at first reproduction for Weddell seals reported in a previous analysis (Hadley et al. 2006), we expected that substantial heterogeneity in individual quality was present in this population. Numerous life-history studies have demonstrated the importance of considering individual variation in quality when assessing reproductive costs (van Noordwijk & deJong 1986; Weladji et al. 2006). Therefore, we also proposed an alternative prediction that if reproductive costs did vary with age at first reproduction, highest costs would be experienced by those individuals that delayed primiparity. We hypothesized that such individuals were of lower quality and thus expected them to suffer higher costs of reproduction relative to high-quality seals of the same age that had begun reproduction at the mean age or even earlier (Curio 1983; Cam & Monnat 2000; Cam et al. 2002; Beauplet et al. 2006).
For some species, reproductive costs may only be present under scenarios of population density or resource scarcity that lower survival rates beyond some threshold (Tuomi, Hakala & Haukioja 1983; Festa-Bianchet 1989; Stearns 1992; Reznick, Nunney & Tessier 2000; Tavecchia et al. 2005). Therefore, we expected reproductive costs to both survival and reproduction of Weddell seals to vary annually due to changing environmental conditions. The sensitivity of marine ecosystems, and especially upper trophic level predators, to climate change has been noted in numerous recent studies (e.g. Croxall, Trathan & Murphy 2002; Beauplet et al. 2005; Jenouvrier et al. 2005; McMahon & Burton 2005). During El-Niño Southern Oscillation (ENSO) events, lower pressure is evident in the Southern Ocean, leading to cooler sea surface temperatures (SSTs) and greater sea-ice extent (SIE) (Kwok & Comiso 2002). In the Ross Sea, phytoplankton blooms occurred later and were less extensive following winters with high maximum sea-ice extent (Arrigo & van Dijken 2004). Summer sea-ice extent determines the amount of open water available for phytoplankton blooms and therefore may determine foraging success of Weddell seals during the summer. Because of this relationship with marine primary productivity, annual measures of ENSO strength, SST, or seasonal measures of sea-ice extent in the Ross Sea region may explain annual variability in the magnitude of reproductive costs experienced by female Weddell seals in Erebus Bay. We expected that heavy sea-ice years (high ENSO index, low SST, and high sea-ice extent) would lead to decreased foraging success for female Weddell seals and would therefore be correlated with increased reproductive costs. Based on the principles of the prudent parent hypothesis (that long-lived species should incur costs to reproduction before they incur costs to their own survival) (Drent & Daan 1980; we predicted that climate and sea-ice fluctuations would induce greater variability in costs to reproductive probabilities than in survival costs.