Pinniped Life History (marine mammals)

The life history of an individual is the pattern of allocation of resources to maintenance, growth, and reproduction throughout its lifetime. Life history analysis attempts to explain the scheduling of the allocation process throughout an organism’s life. It assumes implicitly that it is appropriate to classify individuals by age because this is a major component of the independent variable representing time that is used to examine variation in resource allocation. However, we know that other properties of an individual, such as its body condition or foraging skill, are also important variables that affect reproduction and, ultimately, fitness.

Most life history studies involving pinnipeds have assumed that age is the main force in pinniped life histories when, in fact, age per se may have relatively little to do with influencing fitness. It is a paradox of life history studies that they are, by definition, time-based approaches to examining variation in the fitness between individuals when time itself probably has less biological importance than other factors. One such factor in pinnipeds is body size, long recognized as a determinant of sexual maturity in pinnipeds. Age at sexual maturity in pinnipeds can be expressed as a decreasing function of growth rate. Expressed at the level of populations, this is interpreted to mean that individuals within pinniped populations that are at a level well below the environmental carrying capacity would experience higher growth rates and would, therefore, become sexually mature at an earlier age (Bengtson and Laws, 1985). This was an implicit acknowledgment that age was not the operant factor in pinniped life histories and was at best secondary to the size of the energy reserves of an individual. Nevertheless, despite the considerably greater difficulties that exist with measuring age in pinnipeds than there are with measuring body size (e.g., mass or some other suite of morphometries), age has continued to be used as the primary independent variable in life history studies.

I. Characteristics of Pinniped Life Histories

Pinniped life histories are characterized by three main features: (1) by mammalian standards, pinnipeds have high annual survival rates, giving potential longevities in the order of 2-4 decades; (2) the average age at sexual maturity is delayed by 2-6 years depending on the species (Table I): and (3) each adult female normally produces a maximum of one offspring per reproductive cycle. Variations on this theme at the level of individuals and species can provide insight into the evolution of life histories in pinnipeds.

Pinniped life histories are assumed to have evolved to maximize the genetic fitness of individuals. This occurs in pinnipeds within the constraints of a semiaquatic existence and has most probably led to the relatively narrow range of life histories we observe within the taxon. All pinnipeds rely to some degree on ice or land for reproduction, particularly the processes of birth and lactation. Many interacting variables have led to the evolution of pinniped life histories, including the joint and sometimes conflicting needs to avoid predation, to forage with maximum efficiency, and to choose a mate of high quality.

TABLE I

Demographic Parameters Used to Describe Life Histories of Pinnipeds”

“Rates are expressed per year. Data for fur seals are summaries from tables in Wickens and York (1997); otherwise the original sources are given. Data for male mass were not included if no demographic data were available.

• Sexually and socially mature individuals.
• Pregnancy and birth rate are assumed to be equivalent.
• Juvenile survival rates fall within the same range.
• Juvenile survival >1 year old ~0.70.
• Survival in first year.

Values for juvenile males aged 4 months-2 years are 0.20-0.50: those for males aged 2-5 years are 0.75-0.90. ”Probably negatively biased because of the inclusion of juveniles.

By mammalian standards, pinnipeds are animals with a large body size. However, in terms of their demography and their investment in reproduction, pinnipeds do not appear to differ greatly from other mammals after body size has been taken into consideration. There are also no obvious relationships between body size and life history variables at the species level within the pinnipeds (Table I), although, as we shall see, this is not the case for variation between individuals within species.

Large body size has a cost in that relatively large amounts of resources are invested in tissue growth and maintenance and it takes a relatively long time to reach a body size capable of supporting reproduction. There is also a need to produce precocial young that can defend themselves against predation from an early age or that can forage independently of their mothers within days to weeks of birth. This necessitates greater investment in individual offspring and limits the number of young that can be produced at a single reproductive attempt. It also means that the rate of reproduction (number of young born per unit time) is relatively low. The combination of high investment in growth, causing a delay in sexual maturity, and low reproductive rates, even when sexually mature, means that pinnipeds must have relatively high longevities (low rates of mortality). Without this combination of demographic variables individuals could not, on average, replace themselves during their lifetimes.

II. Methods for Examining Life Histories

Life histories are represented most concisely by demographic models based on empirical measurements of survival and fecundity rates. Demographic variables for pinnipeds are summarized in Table I. Amongst the 36 species of pinnipeds, some form of demographic information is available for most species, but as seen from Table I, there are very few for which there could be said to be complete information, and, in almost all of these, information is mainly available for females. Very little is known about the life histories of male pinnipeds. It is also perhaps a little misleading to represent these demographic variables in terms of species, as many vary as much between different populations of the same species as they do between the species themselves. Averaging across populations also has the disadvantage that it obscures the variation in life histories between individuals. Therefore, while life histories may, in practice, often be examined at the level of populations using demographic parameters, it is an important tenet of life history analysis that it is based on the demography of individuals. This distinguishes life history analysis from the study of population dynamics, which normally deals with individuals as if they are all identical.

The most complete information about life histories for any population of pinnipeds comes from Weddell seals (Leptony-chotes weddellii) at McMurdo Sound, Antarctic (Hastings et al, 1998), and northern elephant seals (Mirounga angu-stirostris) from Ano Neuvo or the Farallon Islands, California (Reiter and Le Boeuf, 1981; Sydeman et al, 1991). These studies were based on the long-term mark-recapture of individuals. Similar studies have been carried out on Antarctic fur seals (Arctocephalus gazella) (Boyd et al, 1995) and gray seals (Hali-choerus grijpus) (Pomeroy et al, 1999). Mark-recapture is probably the only way to examine life histories in pinnipeds to provide the quality of data necessary to understand the complex interactions between factors that influence fitness. However, such studies can only be undertaken in special circumstances where there is particularly easy access to the study population. In most cases, information about population life histories has been derived from cross-sectional samples of populations based on one-off or sequential culls that were often part of a commercial harvest (Fowler, 1990; Bowen et al, 1981). Although some of the disadvantages of this method may be offset by the advantages of a large sample size, it has the potential to lead to misinterpretation of the pattern of life history. Some of these problems are discussed.

III. Constraints on Life Histories

Pinniped life histories have evolved under a combination of factors that are broadly based around the need for animals to balance their energy budgets. These include the constraints involved with (1) being homeothermic in water that is 25 times more conductive than air and (2) the high temporal and spatial variability in the distribution of resources within the marine environment. Phylogeny may also be seen as a constraint in that the ancestors of pinnipeds may not have possessed an ideal range of characteristics (physiological, anatomical, social, or distributional) for exploiting the marine environment. Therefore, current pinniped life histories may be constrained by difficulties with inherent mechanisms.

An example of such a constraint is the apparent necessity for a terrestrial (or pagophilic) phase during the reproductive cycle. This may be a consequence of the occupancy by ancestral pinnipeds mainly of temperate and polar marine habitats in which small neotates may have difficulty with thermoregulating in cold water, thereby necessitating terrestrial living for young neonates. Pinnipeds may have been locked into this form of reproductive cycle from an early stage in their evolution.

The constraint of the terrestrial phase in reproduction has brought with it other social and life history consequences. The necessity for mothers to find suitable terrestrial habitat (including ice) for parturition has more or less isolated, both spatially and temporally, the reproductive process from the feeding grounds. Species that exploit distant, unpredictable food sources require larger body mass than those that exploit food that is present at relatively close range to the pupping location. This is because there will be a critical duration over which a pup can be left without feeding and with low risk of starvation. If modiers cannot forage profitably during lactation within this critical duration, it is necessary for mothers to carry with them at parturition most of the food reserves required to raise their pup to independence (Boyd, 1998).

The extreme seasonality of food availability in higher latitudes has also led to extreme seasonality of reproduction, resulting in spatially and temporally synchronized reproduction. It is possible that both sexes have used this to affect greater mate choice, which has produced polygynous, highly competitive mating systems. These combined factors have led, in most species, to an annual cycle of reproduction.

IV. Costs vs Benefits of Reproduction

Even though individuals may have the option to reproduce annually, longitudinal studies show that they do not always exercise this option. Even when individuals do reproduce, they may adjust the amount of resources they supply to their offspring. The reasons for this are centered on the decisions that individuals must make during their life times in order to maximize their fitness, often measured in terms of number of offspring produced across their whole lifetime and not just one reproductive cycle.

There are obvious fitness gains from reproduction, but there are also costs involved. For example, in Antarctic fur seals (Arctocephalus gazella), reproduction in any year carries with it a 40% greater chance of dying in the following year. It also carries a similar cost in terms of reduced probability of breeding in the following year (Boyd et al., 1995). In northern elephant seals (Mirounga angustirostris), mothers that reproduce for the first time at age 3 incur greater costs, in terms of reduced survival, than those that breed first at age 4 (Reiter and Le Boeuf, 1991). Female gray seals (Halichoerus grypus) that expend more on their offspring in 1 year also have reduced reproductive success in the following year (Pomeroy et al., 1999). Thus, female pinnipeds must find a solution of how best to allocate energy between growth/maintenance and reproduction that optimizes the balance between fitness costs and benefits of reproduction. Those individuals that achieve the optimum balance will have greatest lifetime fitness. How pinnipeds make investment decisions in order to optimize this balance is unknown. In reality, few individuals may actually achieve the optimum, especially in variable environments, but natural selection favors those individuals that make investment decisions that approach the optimum most closely.

V. Age at First Reproduction

All pinnipeds experience a delay of several years in the time taken to reach sexual maturity (Table I). Several studies have shown that the age at first reproduction is not constant. In harp seals (Pagophilus groenlandicus) it is negatively related to population size (Bowen et al., 1981), implying that the age at which individuals mature is density dependent [although see Trites and York (1993)]. Further evidence for a shift in age at sexual maturity with population size exists for crabeater seals (Lo-bodon carcinophaga) (Bengtson and Laws, 1985). The speed with which the change occurs shows that this is not an effect mediated by natural selection for individuals with different life history patterns, rather it is almost certainly driven by changes in the growth rates of individuals as population density and, by implication, per capita food availability changes. Consequently, the mean age at sexual maturity in a population may simply be a reflection of the mean growth rate.

Among northern elephant seals, females tend to begin breeding at age 3 or 4. The fitness of individuals that begin to breed at age 4 is greater than those that begin at age 3 because there is a cost, in terms of reduced survivorship, for those that began breeding at age 3 (Reiter and Le Boeuf, 1991). In Antarctic fur seals there is a similar disadvantage to breeding at an earlier age (Lunn et al, 1994), although, for those individuals that survive, there is no subsequent effect on reproduction through the remainder of life.

These results suggest how age at sexual maturity can be determined by natural selection. In northern elephant seals and Antarctic fur seals there appears to be a trade-off between the fitness costs of breeding early in life and the fitness gains from early reproduction. Although, on average, individuals that begin breeding at age 3 have lower survival, it is possible that those that breed at age 3 and survive have increased fitness mainly because they have, on average, one more reproductive attempt than those that begin breeding at age 4. Animals may opt to take a greater risk by breeding first at age 3 but with the prospect of greater ultimate lifetime fitness. For the trade-off between breeding first at age 3 or age 4 to operate and be evolutionarily stable, both strategies must have equal median lifetime fitness.

VI. Variations in Measures of Fitness

Strictly speaking, fitness should be measured in terms of the number of grandchildren that are produced by an individual. However, no study of pinnipeds has been able to do this, so a variety of fitness indices are used. The simplest and least informative of these is fertility rate, followed by weaning rate, proportion of offspring surviving their first year, and proportion of offspring surviving to reproductive age. There are specific examples of each of these measures from studies of pinnipeds.

Fertility rates in pinnipeds are normally in excess of 0.8 (Table I) and, given other vital rates in pinniped demography, they normally have to be of this order for populations to have the potential to grow. Longitudinal studies of individual pinnipeds show that most females experience fallow reproductive cycles in their lifetimes (Lunn et al, 1994). It remains unclear if the observation of declining fertility with increasing age in cross-sectional samples of pinniped populations reflects senescence of individuals. The observation could equally be caused by greater survival rate, and therefore greater representation in older age classes, of individuals with intrinsically low reproductive rates.

Like age at sexual maturity, fertility is probably linked to the attainment of a critical minimum body condition at a specific stage of the reproductive cycle. In fact, physiologically, there may be virtually no difference between the process of puberty and the seasonal recrudescence of the reproductive system, so the two processes could be considered to be controlled by a common mechanism.

Fertility rates are influenced by previous experience of reproduction. In northern elephant seals, it appears that most females that miss a breeding attempt compensate for this by having a higher probability of weaning a pup in the following year, although, early in the reproductive life span, the opposite effect has been observed, i.e., individuals that miss a reproductive cycle have low success in the following year. Therefore, offspring quality may be affected by previous reproductive experience. Antarctic fur seals are significantly less likely to reproduce in a year following a reproductive attempt.

Weaning rates are affected by both age and previous experience of reproduction in northern elephant seals. It appears that although weaning rates increase initially with experience, these begin to decline later in life. This may represent a cumulative cost of reproduction that is manifest as senescence. However, it is still uncertain if this effect is an artifact of sampling caused by greater longevity in individuals that tend to skip reproduction more frequently or invest a smaller proportion of their energy reserves in their offspring.

In Weddell seals (Leptomjchotes weddellii) offspring survival to age 1 and reproductive age both increase with maternal age and experience and, for male offspring, in relation to maternal body length (Hastings and Testa, 1998). Again, this suggests that those individuals that were able to invest more resources in their offspring, by virtue of their larger size and greater experience (perhaps reflecting the occupancy of better habitat), had enhanced fitness.

VII. Comparing Males and Females

Because females are the limiting sex and because it is much more difficult to study reproductive success in males, more attention has been focused on female than on male pinnipeds. Nevertheless, males may invest large amounts of their energy reserves in reproduction. In general, males have shorter life expectancies than females (shown by lower annual survival rates in Table I), but it is not clear how this is influenced by the investment in reproductive effort. Investment theory would suggest that the shorter life expectancy of males is because of their preparedness to take greater risks with their survival. The potential gains from reproduction, in terms of offspring, in males that are successful competitors because they make a large investment are greater than for females that are restricted to producing a single offspring per season.

There is also confusion in the literature about when males become sexually mature. The age at physiological maturity in males is probably similar to that of females, but many authors make a distinction between physiological and social maturity, which is defined by the age at which individuals are capable of competing for matings. Recent genetic evidence (e.g., Amos et al., 1993) is casting doubt on some of the former interpretations of what social maturity actually means because the pattern of mating success in males often does not follow the pattern suggested by the observed social structure. In the near future, we may have to revise our views of the life history patterns of male pinnipeds.

VIII. Optimal Life Histories: Modeling the Way Forward

Life history analysis in pinnipeds is fraught with difficulties. Longitudinal studies in which individuals are studied throughout their lifetimes can only be carried out on a narrow range of accessible populations and they are expensive and logistically complex to maintain over the time periods (usually decades) required to achieve useful results. Cross-sectional studies are extremely limited in what they can tell us about the dynamics of life histories, and commercial harvests, the usual source of these data, are a thing of the past. We have to find a new way forward.

To date, almost all studies of pinniped the histories have been empirically based and, as pointed out in this description, they have highlighted the interactive nature of parameters such as longevity and reproductive rate. A modeling framework is required in order to allow these interactions to be investigated, to make better use of the data sets that already exist, and to identify critical gaps in the empirical data.

If a pinniped is to maximize its lifetime fitness F, then it must choose the optimal allocation of resources to reproduction through its lifetime. Thus, F = f + fz + fz ■. . f„ where fa is the fitness contribution from year a in the life of the pinniped, which lasts n years. We know that there are certain functional relationships between maternal size or condition and the probability that she will reproduce or survive. If we assume that the relationship between offspring condition and its ultimate fitness is asymptotic, then, up to a certain level, the more energy that a female delivers to her offspring the greater will be her fitness. If the energy delivered to an offspring (ea) is a proportion p of the energy available to the mother, then from what we know of the growth patterns and the energetic efficiencies of pinnipeds, it is possible to estimate the energy available for reproduction throughout the life span of an average individual. By setting rules that an individual will only reproduce if it has a sufficient excess of energy above that required for maintenance, we may be able to investigate the life history patterns in different environments as well as the effects of stochastic variability in food availability on life histories.

Many of the dynamic relationships described here should become explicit in the results of such an energy-based life history model. Similarly, such a model could help the interpretation of some of the cross-sectional population data in the context of dynamic life history processes. This type of approach seems to be essential if progress is to be made in pinniped life history analysis and for the full implications of life history analysis to be realized. Because the mechanism underlying population trajectories is the sum of individual life histories, understanding the environmental factors that affect life histories is fundamental to understanding population and species viabilities