Consequences of maternal size for reproductive expenditure and pupping success of grey seals at North Rona, Scotland


Patrick Pomeroy, Sea Mammal Research Unit, Gatty Marine Laboratory University of St. Andrews, St. Andrews, Fife KY16 8LB, UK. Fax: 01334 462632. E-mail:


1. The reproductive performance of individually marked mothers aged between 4 and 36 years breeding at the established grey seal colony of North Rona, Scotland was studied. Natality rate was between 0·805 and 0·975 for these females during 1979–95 and 57% of females produced 74% of the pups born. Mothers pupped successfully on N. Rona after absences of up to 5 years.

2. The average maternal postpartum mass (MPPM) of mothers was 190 ± 23 (SD) kg, larger than had been recorded from this colony previously. Although annual mean MPPM increased during the study, there were increases and decreases in individuals’ MPPM between years.

3. Pup mass at birth and pup growth rate were related to MPPM and date of parturition. No evidence of differential postpartum expenditure in the sexes was found. Relative pup birth mass decreased with MPPM but relative pup weaning mass remained constant over the range of MPPM.

4. Maternal mass expenditure during lactation averaged 39% of MPPM, and the consequences for MPPM in the year following either high or low relative expenditure were inversely related to relative expenditure in the first year. However, mothers increased their mass after skipping breeding in a year.

5. General Linear Models and REML analyses indicated that expenditures were significantly different between mothers when other variables and factors had been taken into account. In general, maternal expenditure was greater for animals of larger masses and duration of lactation, but corrected maternal expenditure of longer individuals was less than expected. Pup mass at weaning was influenced by mother's identity and year and there was evidence that individual mothers which were longer for their weight raised smaller pups.

6. The life history consequences of reproductive expenditure in any year appeared in subsequent breeding patterns. The cost of breeding for larger animals and larger expenditures was indicated by lower pupping success rates in years following births and skipped breeding years.


In most mammalian species, mothers bear all the direct costs associated with producing offspring, which include those for gestation, birth, lactation and parental care. In long-lived iteroparous animals, the success of any one reproductive event may be influenced by efforts in previous seasons (Clutton-Brock, Guinness & Albon 1983; Newton 1989). The extent to which the reproductive effort in any one season influences future reproductive success depends on the availability of resources, their variability and the animal's response to that variability. Population parameters may be influenced by intrinsic differences between individuals, such as age, condition, fecundity or individual quality, but these need to be considered along with extrinsic effects such as spatial or temporal variation in weather or food supply. While the dynamics of a population can be described by the changes in the average life table parameters, individual reproductive performances must be examined to understand how these demographic changes are brought about. Furthermore, accounting for the way that resources are allocated to reproduction over the course of female lifetimes offers insights into the factors which shape and constrain maternal reproductive strategies with their corresponding fitness consequences.

For a number of mammalian species, including some pinnipeds, there are demonstrable costs to producing young (Clutton-Brock, Guinness & Albon 1983; Huber et al. 1991; Reiter & Le Boeuf 1991; Sydeman et al. 1991; (but see also Sydeman & Nur 1994)). For example, a cost of pupping in any year for Weddell seals (Leptonychotes weddelli Lesson) was a reduction of 0·05 in the probability of pupping the following year (Testa 1987). Antarctic fur seals Arctocephalus gazella Peters showed a reduction in adult female survival as a result of pregnancy and there was an age-related decline in pregnancy rate above the age of 8 years (Boyd et al. 1995).

Some components of each reproductive episode are variable and depend critically on maternal state which is influenced by environmental factors such as food availability, or may reflect individual responses to circumstances, such as maternal control of expenditure. Studies have considered the effects of limited resource availability on maternal allocation of resources (e.g. Anderson & Fedak 1987a,b; Campagna et al. 1992; Iverson et al. 1993; Festa-Bianchet, Jorgensen & Wishart 1994; Fedak, Arnbom & Boyd 1996). Survival of offspring to the weaning stage has been related to maternal investment in a number of mammalian species (red deer Cervus elaphus L., Clutton-Brock, Albon, Guinness 1987a; Clutton-Brock 1991; Soay sheep Ovis aries L. Clutton-Brock et al. 1992; bighorn sheep Ovis canadensis L. Festa-Bianchet et al. 1994, Antarctic fur seals, Lunn, Boyd & Croxall 1994; Arnbom, Fedak & Boyd 1997). For example, factors affecting birth mass in mammals have been shown to include maternal age, parity, body condition and social status as well as date of birth and offspring sex (Guinness, Clutton-Brock & Albon 1978; Reiter, Panken & Le Boeuf 1981; Clutton-Brock, Albon & Guinness 1984; Boyd & McCann 1989; Michener 1989; Trites 1991). Different females may vary in condition from each other but the same female may vary in condition from one breeding season to the next and may vary her expenditure in response to her state at parturition from year to year. Her state in any one year may depend on her previous expenditure or foraging success. Furthermore, animals may vary in the extent of their adjustment in expenditure and there may be a systematic variation in adjustment of expenditure in relation to condition at parturition across animals of different sizes. Thus, in a longitudinal study of the type reported here, we may expect a complex pattern of variation in maternal expenditure both across animals and within animals over different years (Trillmich 1996). This aspect of maternal variation has been partially accounted for in previous longitudinal studies of pinnipeds by using age-specific cohorts of animals (e.g. Trillmich 1986; Testa 1987; Reiter & Le Boeuf 1991; Sydeman et al. 1991; Boyd et al. 1995). However, the effects of maternal body size and expenditure in one season on that in the next, both within and between individuals demands examination.

Maternal expenditure (the resources used to rear offspring) can be difficult to measure in species which have complex life histories, a long rearing period or large brood size. However, phocid seals have life history characteristics which make measurement of maternal postpartum reproductive performance relatively straightforward. Mothers face a simplified version of the major trade-off between their reproductive effort and its allocation between offspring because they produce a single pup at each episode. Grey seal mothers do not feed during lactation, so their mass and body composition at parturition set limits to what they may expend on their pups. This stored reserve can be viewed as an index of the individual's capacity to tolerate environmental variability. Because the size of stored reserves is positively related to the mother's postpartum mass, the absolute and relative measure of reserves expended should also be related to postpartum mass (Arnbom, Fedak & Boyd 1997). Thus in common with other mammals, variations in maternal condition at parturition may account for a significant portion of preweaning and possibly postweaning offspring mortality (Guinness et al. 1978; Clutton-Brock et al. 1983; Clutton-Brock et al. 1992; Bowen et al. 1994; Arnbom et al. 1997).

In the eastern Atlantic, female grey seals Halichoerus grypus Fabricius come ashore to pup in the autumn. Timing of reproduction is highly synchronous and occurs in large aggregations of animals on remote islands and coasts. Although individual seals show fidelity to breeding sites, females may pup each year or miss some years (Pomeroy et al. 1994; Twiss et al. 1994). Pups are weaned after about 18 days (Bonner 1972), but the breeding season may last from 5 to 10 weeks depending on site. Adult male grey seals are typically two or three times the mass of females, but the postpartum masses of breeding females may range from 120 to 250 kg.

Longitudinal mass change data from a population of known individual grey seals at North Rona, Scotland was collected to investigate the consequences of inter- and intra-individual variation in maternal body size on reproductive expenditure and pupping success. Maternal expenditure is affected by postpartum body size and the duration of lactation, while pup mass at weaning provided a measure of the resultant of maternal expenditure. This basic relationship may be modified by associated factors such as pup sex, birth date, maternal mass, age and length as well as the year. Specifically we examined (i) long-term variation in natality; (ii) maternal postpartum mass and reproductive expenditure, assessed by mass change during lactation; (iii) the relationships between factors contributing to maternal expenditure and its product, the weaned pup; (iv) the roles of previous maternal parity, size and expenditure in mothers’ subsequent success in rearing pups to weaning.


Study populations and site

The breeding colony of grey seals on North Rona, Scotland (59°06′N, 05°50′W) is concentrated on the flat, low-lying peninsula of Fianuis where around 95% of the colony's pups are born (Boyd & Laws 1962; Boyd, Lockie & Hewer 1962). Pup production peaked around the 8th October in each year and annual pup production varied between 1600 and 1100 during the study (Hiby et al. 1992; SMRU unpublished data). The numbers of pups born in different parts of Fianuis varies from year to year (Boyd & Campbell 1971; Anderson, Burton & Summers 1975; Summers et al. 1975), but most females are faithful to previous pupping sites (Pomeroy et al. 1994).

Capture and marking

All procedures involving capture and handling of animals were carried out under UK Home Office licence. Data on the study population were collected for the years 1979–81 1985–89 1993–95 (inclusive). In October 1985, 67 breeding females were captured, weighed and branded. Included in this total were 11 females that had been tagged (Jumbo rototags, Dalton, UK) during earlier studies (Fedak & Anderson 1982) and 10 females that bore cohort-specific brands applied to weaned pups in the 1960–68 period (Boyd & Campbell 1971). The marked population was increased by an additional 18 breeding females in 1987 and a further 6 breeding females in 1988. Not all mothers in the study were aged, but 48 females were aged between 4 and 36 years, according to either cohort brands or dentine and cementum layering in incisor teeth.

Females were anaesthetized using a pressurized dart to deliver a mass specific intramuscular dose of ketamine hydrochloride and valium during 1985–88 or zolazepam-tiletamine (‘Zoletil’, Virbac, UK) during 1988–95 and hot-iron branded with individual letter/number ciphers on each flank (Anderson & Fedak 1987b). An additional female was tagged but not branded as she bore a large recognizable scar on her side. Brands were applied to some animals that had been tagged previously, to make them more obvious. Subsequent catching effort concentrated on marked animals. Adults and pups were tagged in the rear hind flipper and marked temporarily with a water/alcohol soluble dye.

Brands have proved to be a reliable long-lasting way of identifying grey seals (Harwood, Anderson & Curry 1974). Throughout this study, brand condition at recapture or resighting was recorded where possible. We recorded brand condition in 39 (78 brands) of the females recaptured in 1986, a year after branding. Of these, brand condition for 26 females was classified as ‘good’ with both brands clear, brand condition for 13 females was classified as ‘poor’ (either one or both sides were unclear in some respect). There was no difference in the subsequent observed return rates for females with ‘good’ verses ‘poor’ brands (G-test of goodness-of-fit with Williams correction, Sokal & Rohlf 1981; Gadj = 0·00, P > 0·9).

Presence and natality of study animals

The breeding status and locations of individual seals within the colony were recorded each day. We collected detailed behavioural information including parturition and weaning dates for mothers by conducting observations from a hide overlooking the southern half of the Fianuis peninsula during the hours of daylight (≈8 h per day, Pomeroy et al. 1994). Regular surveys of all seals on the Fianuis peninsula were carried out at 4–5 day intervals, when fieldworkers scanned the entire colony without entering breeding groups. Seal immobilization (see below) provided regular opportunities to observe animals at close range throughout the colony.

Study females were classified as present only after they had been identified by 2 observers. Of the females marked at N. Rona, 91% returned in at least 1 year after marking. However, 55% of marked animals failed to reappear on N. Rona in at least one year while they were known to be alive (45/82). Some females were absent from N. Rona for two or more consecutive seasons before reappearing to pup subsequently (absent 2 consecutive years n = 17; absent 3 consecutive years n = 5; absent 5 years n = 1). Therefore, it was not possible to make assumptions about survival based solely on absence from the island. The number of study females returning to N. Rona declined during the study (Table 1). It was assumed that absences represented years where no pup was produced, this was corroborated by maternal postpartum mass change data (see results below).

Table 1.  Resighting data in subsequent years for grey seal mothers that were marked in 1985 on North Rona, according to whether they pupped early (on or before 8 October) or late (after 8 October) in 1985. The proportions of the original 1985 early and late pupping animals in those resighted in each year are also shown
  Early puppingLate pupping   
YearTotal number presentPresentAbsentPresentAbsentProportion of 1985 earlies in resightsProportion of 1985 earlies resightedProportion of 1985 lates resighted

Parturition dates of the 67 study females marked in 1985 ranged from 16 September to 21 October (mean 2 October ±10d). Thus, the study females tended to pup in the early to mid-season part of the breeding curve. To examine whether this influenced the probability of their being resighted in subsequent years we classed these 67 females as either ‘early’ or ‘late’ pupping females according to their 1985 birth dates and examined their appearance in subsequent seasons (Table 1). Early pupping females made up a similar proportion of the total sighted in each year and this was independent of the number of marked animals resighted. In addition, the resighting rate of early and late pupping animals was similar in each year. Therefore our observations on marked animals were representative of their return patterns to N. Rona.

The reproductive state of each returning female was assessed while she was ashore. Females which were seen to nurse, defend or maintain position by particular pups were classed as mothers of those pups. Pups were classed as weaned when the mother had left them. A female pupped successfully if her pup survived to weaning and had (i) a lactation period longer than 10 days; or (ii) had attained a mass of more than 30 kg by the end of the lactation period (Kovacs & Lavigne 1986). Pup mortality was estimated from counts of dead pups visible in the colony.

Mass of mothers and pups at birth and weaning

At each capture, study females were weighed to the nearest 1 kg using a load cell (Active Load and Pressure System Ltd, Reading, UK; Crane weigher, Todd Scales, Newmarket, Suffolk, UK) in a stretcher net suspended from a tripod. Load cells were checked regularly for calibration against a known mass. Pups were sexed and then weighed with a spring balance to the nearest 0·5 kg (Salter Industrial Measurements Ltd, West Bromich, UK) at each capture (Anderson & Fedak 1987a). In each year, mothers and their pups were weighed near the start and end of the lactation period. The analyses of maternal mass reported here are restricted to mothers that were weighed 4 days or less after giving birth. We use maternal postpartum mass (MPPM) to define a mother's condition at the start of a lactation period. Mean MPPM was estimated by extrapolation, using the product of average daily mass loss for that mother in that season and the number of days from parturition to first weighing to add to the first mass obtained for the mother. Maternal mass at weaning was estimated by subtracting the product of the number of days between last weighing and weaning date (range 0–7 days) and the daily mass loss rate.

Pup mass at birth was not measured directly in most cases as it was essential to avoid disturbance of mother-pup pairs early in lactation, but was estimated by extrapolation. Pup growth was assumed to follow a Gompertz curve. We assumed that there was no increase in pup mass in its first day and that growth rate in the last day the mother was present was half of the calculated growth rate over the measurement interval, although we are aware that in a few cases pups began feeding almost immediately after birth. Otherwise, growth rate (kg day−1) was assumed to be constant and could be estimated by the linear relationship between mass gain and time measured between weighings. If the first weighing of a pup was greater than 4 days after birth, we used the mean pup birth mass from this study to estimate mass gain during lactation.

Dates expressed as integers in the text have used 1 September as day 1.

Data analysis

Normally distributed data were presented as means and standard deviations within groups initially, and means with standard errors among groups (Sokal & Rohlf 1981). Our data included measurements of the same females in different years, with year to year variation in the exact composition of the females represented (Results I). Mass data were presented in a hierarchical way in Results II, such that in IIa, bivariate mass relationships treat all data as though they were independent. In section IIb, we used generalized linear models to examine the factors which may affect maternal expenditure and pup mass at weaning. Maternal standard length (nose–tail) was used as a condition-independent proxy for maternal body size. Trends within animals were examined using a general linear model with a fixed mother effect, i.e. allowing a separate intercept for each mother, fitted by the Minitab GLM procedure (Minitab Inc., Pennsylvania). This model makes no assumptions about the variation in individual mother effects. Trends across animals were first examined separately for each year, and then analysed together using a model incorporating trends within and between animals, and a random mother effect to allow for correlation arising from repeat observations on the same mother over time. For a single explanatory variable, the model can be written as

Yij = m + tj + bB xi + bW(xij– xi) + Mi + Zij

where: Yij is the response for the ith mother in the jth year; xij is the corresponding value of the explanatory variable; xi denotes the average value of x for the ith mother; m denotes an overall mean; tj is an effect for the jth year; bW is the slope of the within animal trend; bB is the slope of the trend between average values of Y and xi. The Mi denote random effects for mothers and the Zij are random residual effects – these are assumed to be independent and Normally distributed with zero mean and constant variances VM and VZ, respectively (e.g. Diggle et al. 1996). The model can be used to test the hypothesis of equality of slopes: H0: bW = bB. An extension of the model including three explanatory variables (MPPM, duration of lactation, maternal length) was fitted by the method of residual maximum likelihood (REML) using the statistical package Genstat (Genstat 5 Committee 1993).

In Results III logistic regression analysis was used to determine the importance of variables on the binary response of pupping success. Logistic models were fitted using an iterative maximum-likelihood technique and the generalized linear model procedure in Genstat 5. The difference between ‘deviance’ values of the model before and after a single term was included was used to test if inclusion of the term improved the fit of the model significantly. Deviance values are distributed approximately as χ2 with degrees of freedom equal to the difference in degrees of freedom between the models. Examination of relationships between more than two variables used the GLM procedure available in Minitab Version 10·5 (Minitab Inc. Pennsylvania). Except for specified cases, P-values quoted in regressions refer to the probability of coefficients differing from 0.


I. reproductive histories of female grey seals


We used data from all pupping histories to generate a minimum estimate for birth rate at N. Rona of 0·805 within the marked population (minimum number of pups produced/number of pupping opportunities for extant animals = 387/481). However, some study females have produced more pups at N. Rona than others (57% of females produced 74% of all pups). All females new to the study had pupped in the year they were marked. There were 12 definite cases when branded females returned to North Rona and remained ashore for between 1 and 54 days without pups or showing any sign of having given birth. We are sure that these females did not rear pups in these cases. Reasons for this may include miscarriage, stillbirths or simply not being pregnant on arrival at the rookery. If these were the only nonparous cases in the study the upper limit to our estimate of natality would be (469/481) = 0·975.

Pre-weaning pup mortality

Annual pup mortality over the season on the N. Rona breeding colony varied between 0·10 and 0·20 but also varied according to specific location and stage in the pupping season. The overall mean preweaning mortality rate of pups born to study females was 0·169 ± 0·239 (arcsin transformed proportion), but the proportion of pup mortalities which individual mothers experienced over their recorded pupping histories varied from 0 to 0·80.

Trends in prepartum time ashore and mother's parturition dates

Parous females were seen ashore for an average of 4·1 ± 3·6 days (n = 83, range 0–19 days) before parturition. There was no difference in the time spent ashore by mothers before the birth of male or female pups (t = 1·77, P > 0·05, d.f. = 78). There was no evidence that the number of days spent ashore before mothers gave birth was positively related to maternal postpartum mass (MPPM), maternal age or year (MPPM F[1,64] = 0·12, P > 0·5, r2 = 0·01; maternal age F[1,62] = 0·35, P > 0·9, r2 = 0·13; year F[6,73] = 2·07, P > 0·05, r2 = 0·15) but was inversely related to birth date (F[1,78] = 8·4, P < 0·01, r2 = 0·10).

We could show no relationship between parturition date and mothers’ age (F[1,59] = 1·09, P = 0·3, r2 = 0·02). Serial analysis of pupping dates for these marked mothers showed no consistent trends. Individual females tended to be relatively constant in the dates on which they pupped from year to year. Birth dates were later for mothers that pupped in the consecutive years, year t and year t+1 [partum date t +1 = 6·75 + 0·817(partum date t), F[1,119] = 306·7, P < 0·001, r2 = 0·72]. When parturition dates of each mother were compared to their first recorded parturition dates, irrespective of the pupping history of the mother, the mean day difference up to 10 years after the first parturition date recorded was in the range −3 to +4 days (Fig. 1). After a period of more than 10 years, the few parturition dates observed (n = 5 from 2 mothers) were all at least 6 days earlier than the first parturition date observed for each of those mothers.

Figure 1.

Change in parturition date of individual adult female grey seals with time since first record of parturition date was recorded at N. Rona. The mean (± SE) difference across animals between pupping date in year t, year t + s is plotted in days against the number of years s between recorded parturitions. The number of points for each year interval is indicated.

Ii. mass relationships for mothers and pups

(a) Univariate and bivariate descriptive mass relationships

The mean MPPM during the study was 190 ± 23 kg (n = 184, range 131–251 kg, Table 2). There was no evidence of a difference between mean MPPM for mothers of male and female pups (t = −1·05, P > 0·2, d.f. = 182). There was no difference in MPPM between years for mothers of male pups, but mothers of female pups were larger in 1993 than in 1979 (anova; male pups F[10,89] = 1·39, P > 0·1; female pups F[9,70] = 2·25, P < 0·05, Tukey test). Annual mean MPPM varied over the course of the study (Fig. 2), but interpretation of this was not straightforward because some individuals were measured in most years, while others were measured rarely. This aspect of the data is considered below. Large mothers tended to give birth early in the season (F[1,44] = 10·41, P < 0·01 r2 = 0·57).

Table 2.  Summary of mean mass, mass change and birth date statistics for grey seal mothers and pups during 1979–95 at North Rona, grouped according to the sex of the pup. The data presented are from reproductive episodes from which most birth and weaning information was available. Probability P of homogeneity of means for the two groups is shown for two sample t-tests with pooled variances
Pup mass at birth (kg)16·41·945715·82·09520·17
Mass gain of pup (kg)28·910·63425·49·9230·21
Pup growth rate (kg day−1)1·750·61541·610·65450·26
Pup mass at weaning (kg)45·011·143441·310·38230·21
Birth date38·37·165738·87·79520·71
MPPM (kg)185·321·3453185·022·75420·95
Maternal mass at weaning (kg)119·519·434122·417·8230·57
Maternal mass loss (kg)68·716·93464·917·1230·41
Maternal mass loss rate (kg day−1)3·780·93533·600·89420·34
Maternal length (m)1·680·082731·690·092350·96
Duration of lactation (days)17·44·723616·75·20270·54
Figure 2.

Mean (± SE) annual maternal postpartum mass (MPPM) (kg) of study female grey seals weighed in each year at N. Rona during the years of the study 1979–95. The number of points for each year is indicated.

Overall, the mean maternal mass at weaning was 117 ± 18 kg (n = 127, range 82–166 kg). There was no annual difference in maternal mass at weaning (anovaF[10,117] = 1·24, P > 0·2). Mothers of male and female pups did not differ in their masses at weaning (t = −1·14, P > 0·2, d.f. = 125). The mean ages at which mothers gave birth to male and female pups did not differ (t = −1·48, d.f. = 149, P > 0·14).

There were no differences between birth masses of male or female pups between years (males anovaF[6,25] = 1·55, P > 0·2; females anovaF[9,23] = 2·18, P > 0·05). At birth, there was no difference in mean mass of male and female pups (t = −1·19, P > 0·2, d.f. = 63, Table 2), nor were there differences in birth date or duration of lactation between sexes (Table 2).

Relative pup birth mass, expressed as a percentage of MPPM, was the same for male and female pups (arcsine transformation of percentage, Sokal & Rohlf 1981: males 8·90 ± 0·70%, n = 53, females 8·56 ± 0·63%, n = 42; t = −1·29, P > 0·2, d.f. = 93). Relative pup weaning mass, expressed as a percentage of MPPM, was the same for male and female pups (t = −1·06, P > 0·2, d.f. = 28) and averaged 21·32 ± 2·84% of MPPM. A regression of log-transformed pup birth mass (PBM) against log-transformed MPPM indicated that relative pup birth mass decreased with increasing MPPM (log PBM = 0·985 + 0·34 log MPPM, F[1,93] = 9·76, P < 0·01, r2 = 0·10; regression coefficient b significantly different from 1, t = 5·97, P < 0·001, d.f. = 95). However, a regression of log-transformed pup weaning mass (PWM) against log-transformed MPPM indicated that relative pup weaning mass remained constant over the size range of mothers encountered in the study (log PWM = −0·557 + 0·824 log MPPM, F[1,54] = 7·9, P < 0·01, r2 = 0·13; regression coefficient b not significantly different from 1, t = 0·60, P > 0·2, d.f. = 56).

Changes in mass. On average, maternal mass loss during lactation was 74·6 ± 20·3 kg (n = 127, range 8–131 kg) and average maternal mass loss rate was 3·85 ± 0·93 kg day−1 (n = 183, range 1·2–6·6 kg day−1). Mothers lost an average of 39·1 ± 0·6% (n = 122, range 4·8–47·5%) of MPPM during the lactation period. Total mass loss and the rate of maternal mass loss during lactation was the same for mothers of male and female pups (t = – 0·86, P > 0·35, d.f. = 125; t = 0·15, P > 0·8, d.f. = 181, respectively). Total mass loss and rate of mass loss for mothers during lactation did not differ between years (total mass loss anovaF[10,116] = 1·52, P > 0·1; rate of mass loss anovaF[10,172] = 0·63, P > 0·5).

The growth rate of pups was related to maternal mass loss rate (r2 = 0·492, n = 97). Overall, male and female pups grew at the same rate, 1·72 ± 0·57 kg day−1 (t = −1·15, P > 0·2, d.f. = 97). There were no differences in pup growth rate between the sexes within either the early or late groups (Table 3). However, male and female pups born in the early part of the season grew faster and reached larger masses at weaning than their counterparts born in the later half (Table 3). The birth masses of male pups were greater than those of female pups in the late half of the season, and early born female pups were larger than late-born female pups (Table 3).

Table 3.  Comparison of mean growth, mass and duration of lactation statistics for pups born at North Rona 1979–95, according to their sex and birth date category (early and late) in the breeding season
Mass statisticPups comparedPeriodmean ± SDd.f.Significance
Daily growth rate of pupAll pupsEarly:latee:1·90 ± 0·60
l: 1·48 ± 0·51
97P < 0·001***
 M:FAll seasonNS
 M:FEarly bornNS
 M:FLate bornNS
 MaleEarly:latee: 1·97 ± 0·53
l: 1·50 ± 0·61
52P < 0·01**
 FemaleEarly:latee: 1·82 ± 0·68
l: 1·44 ± 0·36
43P < 0·05*
Pup birth massAll pupsEarly:lateNS
 M:FAll seasonNS
 M:FEarly bornNS
 M:FLate bornM: 16·3 ± 1·9
F: 15·0 ± 2·0
42P < 0·05*
 FemaleEarly:latee: 16·4 ± 2·1
l: 15·0 ± 2·0
42P < 0·05
Pup mass at weaningAll pupsEarly:latee: 47·5 ± 8·8
l: 37·7 ± 10·0
54P < 0·001***
 M:FAll seasonNS
 M:FEarly bornNS
 M:FLate bornNS
 MaleEarly:latee: 48·8 ± 9·8
l: 39·5 ± 10·9
32P < 0·05*
 FemaleEarly:latee: 45·8 ± 7·2
l: 33·5 ± 6·5
20P < 0·001***
of lactation

Average gross mass transfer efficiency (pup mass gain × 100/maternal mass loss, arc-sin transformation) during lactation was 45·4 ± 1·4% (n = 93, range 17·5–89·0%). Mass transfer efficiency was not related to sex of pup or MPPM (pup sex t = −0·287, P > 0·7, d.f. = 91; MPPM anovaF[1,87] = 1·38, P > 0·2). However, a greater proportion of maternal mass loss (or expenditure) was converted to pup mass gain in the early part of the season than later (anovaF[1,87] = 7·66, P < 0·01).

Between-year mass changes of individual females. Inter-annual variation in MPPM of individual females during the period 1979–95 was significant (Fig. 3, overall range 131–251 kg, anova years F[2,164] = 3·21, P = 0·001; largest individual range 228–166 kg decrease in 3 years). In general, MPPMs of individuals tended to increase slowly with time.

Figure 3.

Sample of trajectories of maternal postpartum mass (MPPM)(kg) for individual study female grey seals at N. Rona. Each line connects masses of the same female in different years.

(b) Multivariate analyses of factors affecting maternal expenditure and weaning mass

Table 4 presents a summary of the results of the GLM and REML models which examine factors affecting the within and between mother variation in maternal expenditure. Table 5 presents the same analyses for pup mass at weaning.

Table 4.  Models of factors affecting maternal expenditure, estimated by mass loss (kg) in grey seals at North Rona. (a) Trends within mothers were examined using a general linear model with a fixed mother effect. A full GLM model rejected the terms pup sex, birth date, pup mass at birth, maternal length2 and the interactions birth date × pup sex, pup mass at birth × birth date, and pup mass at birth × MPPM. Non-significant terms shown in (a) are presented for comparison with results from analyses (b) and to allow comparison with Table 5. (b) A model incorporating trends within bW and between bB animals was developed for three explanatory variables (MPPM, duration of lactation, maternal length) by the method of residual maximum likelihood (REML) (a) GLM model, n = 121, 27.1% of variation within mothers was accounted for by trends
Term CoefficientSEFd.f.P% variance explained
  1. REML model variance components:

  2. within mothers Vz = 67.5 (SE = 13·9)

  3. between mothers Vm = 37.5 (SE = 16·5).

Constant 96·063·96    
Mother   2·15660·00572·9
MPPM  0·840·0454·2510·00027·9
Duration of lactation  2·070·0120·6710·00044·7
Maternal length −0·160·020·5210·4751·4
Year   0·88100·5554·5
(b) REML model CoefficientSEZP  
Duration of lactationbW
Maternal lengthbW
Table 5.  Models of factors affecting pup mass (kg) at weaning for grey weals at North Rona. (a) Trends within mothers were examined using a general linear model with a fixed mother effect. A full GLM model rejected the terms pup sex, birth date, pupmass at birth, maternal length2 and the interaction terms birth date × pup sex, pup mass at birth × birth date, pup mass at birth × MPPM, pup mass at birth × maternal length and duration of lactation × MPPM. Non-significant terms shown in (a) are presented for comparison with results from analyses (b) and to allow for comparison with Table 4. (b) A model incorporating trends within bW and between bB animals was developed for three explanatory variables (MPPM, duration of lactation, maternal length) by the method of residual maximum likelihood (REML) (a) GLM model, n = 119, 25·0% of variation within mothers was accounted for by trends
Term CoefficientSEFd.f.P% variance explained
  1. REML model variance components:

  2. within mothers Vz = 27·4 (SE = 17·9)

  3. between mothers Vm = 13·0 (SE = 6·4).

Constant 96·562·43    
Mother   2·35660·00275·0
MPPM −0·030·030·1810·6741·1
Duration of lactation  0·600·013·9310·05411·5
Maternal length −0·340·016·1810·0171·0
Year   5·22100·00048·9
(b) REML model CoefficientSEZP  
Duration of lactationbW
Maternal lengthbW

Maternal expenditure models. There were significant differences between mothers in their expenditures when maternal mass and duration of lactation had been taken into account (Table 4a). GLM and REML models indicated that within mothers, maternal expenditure increased with MPPM and duration of lactation (Table 4a,b). The terms maternal length, year, birth date, pup sex and mass at birth were not significant in determining maternal expenditure. However, there were no differences between slopes within and between animals (bB–bW) for MPPM and duration of lactation and both had strong positive effects on maternal expenditure (Table 4b, Fig. 4). No effect was detected for maternal length within mothers, but between mothers there was a significant decrease in maternal expenditure with increasing maternal length (Table 4b).

Figure 4.

Sample of trajectories of the relationship between maternal expenditure and maternal postpartum mass (MPPM)(kg) for individual study female grey seals at N. Rona. Each line connects data for the same female in different years.

Variation in pup mass at weaning. Masses of pups at weaning were significantly different according to the identity of their mother when maternal mass and duration of lactation had been taken into account (Table 5a). Individual effects accounted for 75% of the variation in weaning mass. No effect on pup mass at weaning was detected for MPPM within mothers, but between mothers there was good evidence that larger mothers produced larger pups at weaning (Table 5b). Pup masses at weaning also increased with duration of lactation, with a similar effect within and between mothers. The relationship between pup mass at weaning and maternal length was less clear (Table 5b). Between mothers, pup mass at weaning tended to decrease with maternal length, but no effect was detected within mothers and the difference between the within and between effects was not significant (Table 5b). Almost half the variation in pup mass at weaning was explained by the year in which the pup was born (Table 5a). This strong year effect was not apparent for maternal parameters.

Consecutive year effects. The effect of reproductive expenditure in one year on the following year's breeding was investigated by examining the relationship between MPPM and expenditure (estimated as mass loss during lactation) for mothers whose MPPM and expenditure was measured in the consecutive years t and t + 1. The difference in expenditure between years (ΔE) was related to the difference in MPPM (ΔMPPM) between years: ΔE = 1·563 + 1·079 ΔMPPM, anovaF[1,23] = 15·9, P = 0·001, r2 = 0·41. In general, females that increased MPPM between years expended more in the second season and females that weighed less in the second year had smaller expenditures in that year (Fig. 5). However, there were consistent differences in expenditure between year pairs. Mothers expended less in breeding in 1986 than would be predicted by their change in mass from 1985 to 1986, while in 1987 mothers expended more in breeding than would be predicted by their change in mass from 1986 to 1987. There was no evidence of a relationship between ΔE in successive years and MPPM in the first year (anovaF[1,23] = 2·98, P > 0·05). There were no differences in ΔE or ΔMPPM between mothers that gave birth to male or female pups in the first year (ΔE t = – 0·19, P > 0·8, d.f. = 23: ΔMPPM t = 0·16, P > 0·8, d.f. = 23).

Figure 5.

The relationship between change in maternal expenditure during lactation (assessed by mass change, kg) and the corresponding change in maternal postpartum mass (MPPM) between consecutive years for female grey seals at N. Rona. Symbols represent year pairs:diamond = 79–80; closed circle = 85–86; up triangle = 86–87; left triangle = 88–89; star = 93–94.

Mean maternal expenditure during lactation was 39% of MPPM (section IIa). When maternal expenditure in year t was smaller than this average, MPPM increased in the following year, but when expenditure was greater than average, MPPM was depressed in the subsequent year (Fig. 6).

Figure 6.

The relationship between change in maternal postpartum mass between consecutive years and relative maternal expenditure (arcsin transformation of percentages) in the first year of the comparison for female grey seals at N. Rona. Symbols represent year pairs as in Fig. 5.

Iii. comparison of successful and unsuccessful breeding episodes

Effects of maternal breeding state in one year on breeding state in the next year

We examined the breeding states of our study females in pairs of consecutive breeding seasons. Females which had been absent in one year were as likely to return to N. Rona the following year as females which had been present: preturn = 0·623; preturn = 0·668, respectively, Gadj = 2·74, 1 d.f., P > 0·05. When absences from N. Rona were classed as non-pupping years, parity in the first year had a significant effect on a female's likelihood of pupping the following year: females who pupped in year 1 were more likely to pup in year 2 than those which did not (Gadj = 5·73, P < 0·05). When we compared return rates of mothers which had pupped unsuccessfully in year t, females were as likely to be present as absent in year t + 1 (Gadj = 0·001, P > 0·9), but if they pupped in year t + 1 they had the same probability of pupping success as mothers pupping after a year's absence (Gadj = 0·01, P > 0·9) or mothers pupping the year after a successful breeding episode (Gadj = 0·24, P > 0·9).

Effects of maternal mass and expenditure on pupping success

A logistic regression model indicated that MPPM and maternal expenditure were significant predictors of pupping success after allowing for year effects (Table 6). For the purposes of between year comparisons, the distributions of MPPM and maternal expenditure were categorized into small (first quartile), medium (second and third quartiles) and large (fourth quartile) groups. In any year, the pupping successes of mothers with the smallest MPPM and expenditures were lower than those of the larger groups (Table 7a, Gadj = 8·7, P < 0·01; Gadj = 11·2, P < 0·001, respectively). Pupping success of mothers present in the year after a pupping event was the same for each MPPM and expenditure category in the first year (Gadj = 0·88, P > 0·5; Gadj = 0·1, P > 0·5, respectively). However, pupping success rates were lower in the second year than in the first for the animals in the medium and large MPPM and expenditure categories (Table 7b, Gadj = 13·3, P < 0·001; Gadj = 7·0, P < 0·01; Gadj = 10·1, P < 0·001, respectively). The effect of including animals which were absent from N. Rona but known to be alive in the year after pupping in the calculation of pupping success was considered (Table 7c). There was no change in subsequent pupping success for animals in the smallest MPPM category from the first year, while mothers with low expenditures in the first year had significantly lower success rates in year 2 (Table 7c, Gadj = 0·03, P > 0·5; Gadj = 7·71, P < 0·01, respectively).

Table 6.  Results of a multiple logistic regression analysis with pupping success of grey seals on N. Rona as the binary response and sex of pup, year MPPM (kg) and relative maternal expenditure (%). Degrees of freedom are given with the vaiable name. For models 3–6, b is the estimated linear slope coefficient on a logistic scale. The significance of each factor or variable was determined by the chi-square deviance corresponding to the trend. Total n = 192
ModelTerms included (d.f.)χ2 devianceb (SE)P
1year (10)12·3 0·27
2Sex (1)0·0 1·00
3MPPM (1)5·340·04 (0·02) 0·02
4Relative maternal expenditure (1)23·725·51 (7·08)<0·001
5Year, MPPM (1)3·930·04 (0·02) 0·047
6Year, relative maternal expenditure (1)22·1988·9 (55·3)<0·001

Variables associated with pupping success and failure

We examined quantitative variables which had been measured for mothers at N. Rona and might be linked with pupping success and failure. Pupping failure in any year was defined as any cases where mothers did not pup successfully, including failure to give birth, or preweaning pup mortality. Where mass measurements were available for cases when pupping failed, the birth masses of pups whose mothers were unsuccessful were lower than those for successful mothers (pup birth masssuccess = 16·3 ± 1·9, pup birth massfail = 14·4 ± 2·5, t = 2·90, P = 0·005, d.f. = 106). No difference was detected between MPPMs of successful and unsuccessful mothers (MPPMsuccess = 190·7 ± 22·5, MPPMfail = 172·3 ± 23·2; t = 2·20, P > 0·05, d.f. = 94). The ages of mothers in successful and unsuccessful pupping attempts were not different (t = 0·66, P > 0·5, n = 191), but failed puppings occurred later in the season than successful breeding attempts (birth datesuccess = 37·9 ± 7·1, birth datefail = 43·3 ± 8·9, t = −2·31, P = 0·023, n = 108).

Regular and irregular pupping females

We compared data for mothers with an unbroken series of three breeding episodes to mothers skipping the middle year of the same period. Three time periods were considered; 1985–87 1987–89 and 1993–95. Comparisons were made within these periods initially to exclude potential pooling biases (Table 8). ‘Regular’ mothers raised a pup to weaning over three consecutive seasons, ‘skipper’ mothers raised pups in years 1 and 3 but either failed in pupping or were absent from N. Rona in the middle year. In the 1985–87 period, the breeding statistics for regular and skipper mothers were the same. In the 1987–89 period, mothers that skipped a year were longer and younger than regular breeding mothers. Note that animals skipping a year in this triad would have missed 1988, when the phocid distemper epizootic (PDV) occurred in W. Europe. In the 1993–95 period regular breeders were older than mothers which skipped a season, but their pups gained less mass. When all year groups were combined, mothers that skipped a season pupped earlier, were younger, had longer lactation periods and slower growing pups than mothers which bred regularly (Table 8). The relationship between the change in MPPM and the change in birth date from the start to the end of the 3-years period (i.e. 1985–87) is shown in Fig. 7. There was no difference between regulars and skippers, but the general form of the relationship agreed with that observed for successive year changes: mothers who increased MPPM tended to have earlier birth dates and vice versa, irrespective of the time period considered. If many of the females were young and still growing at the start of the study, it is likely that most of the positive mass changes would tend to occur in the first time period with few in the latest period. However, there were individual mass increases in all periods considered, over a span of 10 years, suggesting that mass gains were not age-dependent. The absence of any age-related effect was indicated further by mass decreases associated with later birth dates in all time periods, not just the earliest (Fig. 7).

Table 8.  Comparison of breeding statistics for grey seal mothers , their pups at N. Roma according to whether they breed regularly (regs) over a 3-years period or skip (skip) the middle year. Significance test on each is Kruskal-Wallis test of ranks for groups. Thumbnail image of
Figure 7.

The relationship between change in maternal postpartum mass between consecutive years and change in parturition date over the same period for female grey seals at N. Rona.


This study has indicated the patterns of variability in maternal body size and reproductive expenditure which a sample of long-lived mammals showed over a 16-years period and related these to sequential breeding success. Maternal reproductive expenditure patterns in grey seals were influenced by maternal size and relative maternal expenditure had consequences for future pupping success. The reproductive strategies used by individual mothers within the population indicate the likely phenotypic constraints on parameters such as body size operating in this established breeding colony.

Pupping histories of individual females

Natality rate for study females at N. Rona was estimated to be between 0·805 and 0·975 during the period 1979–95. This is comparable to estimates for other phocid species (e.g. Testa 1987; Le Boeuf & Reiter 1988; Boyd et al. 1995) and for UK grey seals. Fecundity estimates for samples of grey seals shot around the UK in the 1970s ranged from 0·8 to 0·95 (Boyd 1985). The current model used to estimate annual grey seal pup production assumes that adult fecundity rate in the UK grey seal population is 0·95 (A.R. Hiby, personal communication). The lower limit estimate for our study animals assumes that: (i) females classed as nulliparous had not come ashore pregnant, then pupped and lost their pup before it had been seen; and (ii) absences from N. Rona indicated years where no pup was produced. There is no evidence to suggest that females pupped elsewhere and returned to N. Rona later. There have been only two sightings of marked animals which had pupped away from the colony where they were marked and neither animal was observed to return subsequently to the marking colony (Pomeroy et al. 1994; unpublished data). Evidence for non-breeding in these intervening years comes from the comparison of regular and irregular pupping mothers. Whereas regular pupping mothers had slightly lower MPPMs between years (−2·3 kg), mothers that skipped the middle year returned 13·9 kg heavier (Table 8).

In general, parous females on N. Rona were more likely to pup the following year than non-parous females. The corresponding fact that just over half of the study females produced 74% of the pups in the study provides substantial evidence for individual variation in female quality and success (Trillmich 1996).

Changes in maternal mass

Typical mothers expended an average of 46·5% of their mass on coming ashore before returning to sea. This was calculated by assuming that an average mother of 190 kg postpartum mass had a mass loss of 7·4 kg during the 4·1 days spent ashore before birth (1·8 kg day−1 mass loss for a non-lactating adult female, unpublished results), gave birth to a pup of 16·15 kg, with an associated placenta of 2·2 kg (calculated from Boyd 1990) and lost 74·6 kg during lactation. In comparison, female southern elephant seals lost 39·5% of their mass after coming ashore (Arnbom et al. 1997).

Mothers from this sample on N. Rona have become larger since Anderson & Fedak (1987b) recorded a median MPPM of 175·7 kg for mothers in their sample from N. Rona in the early 1980s. By 1995 the masses of mothers in this study (including some individuals which had been present in Anderson & Fedak's 1987 analysis) were larger and comparable in mass to grey seal mothers weighed at Sable Island by Iverson et al. (1993) and Boness, Bowen & Iverson (1995) (N. Rona 195·0 ± 4·5; Sable Is. 207·0 ± 13·3, 190·5 ± 7·8, respectively). In the eastern Atlantic grey seals have been thought to be smaller on average than their western Atlantic counterparts (Coulson & Hickling 1960; Coulson & Hickling 1960; Anderson & Fedak 1987a; Bowen, Stobo & Smith 1992; Iverson et al. 1993). Eastern Atlantic grey seals have been recorded in the literature as differing significantly from their western counterparts in virtually all reproductive parameters, notably in timing of reproduction (earlier), mean body masses of adults, mean growth rates of pups, mean mass at weaning (all less), breeding site topography and social organization (Boness & James 1979; Fedak & Anderson 1982; Anderson & Harwood 1985; Anderson & Fedak 1987a,b; Bowen et al. 1992; Iverson et al. 1993). The increase in mean MPPM of these mothers at N. Rona over the period of this study has been gradual (+20 kg over 15 years) and has occurred against a background of substantial individual variation. In general, postpartum masses of females increased asymptotically (Anderson & Fedak 1987a), but individuals displayed increases and decreases in MPPM between years (±30–40 kg between consecutive years for individuals). If growth and survival are correlated similarly between colonies it is possible that different MPPMs could be recorded from colonies with different age structures. However, environmental fluctuations such as food availability from one year to the next or occurrences of disease may bring about additional changes in MPPM with consistent trends between individuals. For example, in 1988, fewer branded animals returned to N. Rona and the mean MPPM of those that returned was less than in 1987 or 1989 (Fig. 2).

Grey seal maternal expenditure

The fact that few breeding episodes fell into either extreme of our expenditure classifications suggests that maternal size and expenditure are under relatively strong selective pressure. The advantages which large size confer are countered by costs. Our data suggest that costs are delayed, such that mothers have comparatively low pupping success rates in the year following relatively high expenditures (Table 7). Although maternal expenditure in one year and MPPM in the following year were negatively correlated in this study, there was little reduction in MPPM for mothers in the year following a larger than average expenditure (Fig. 6) but the subsequent pupping success of mothers with high relative expenditures was reduced more than for animals of average expenditures (Table 7). As the advantages to mothers of having a bigger mass appear to relate to size of offspring at weaning, it is worth considering why mothers do not continue to increase their mass, and therefore their potential total expenditures on pups (Le Boeuf & Reiter 1988; Arnbom et al. 1997). Larger females incur greater absolute maintenance costs because of metabolic overheads associated with servicing a larger body mass, but these greater costs must be borne throughout the year, not just for the brief period of breeding (Festa-Bianchet et al. 1996). In circumstances where food availability is a limiting factor, larger than average females may be disadvantaged in having to sustain a greater foraging requirement whereas average sized females can produce pups that are big enough without incurring additional survival risks. This situation may be expected as a density-dependent consequence of increased population size (Clutton-Brock et al. 1987a,b).

Table 7.  Pupping success for female grey seals at North Rona according to maternal postpartum mass (MPPM) and relative maternal expenditure (%) in the year during and the year following a pupping event. Mass and expenditure classes represent the first, second and third, fourth quartiles of their respective distributions in the first year. Pupping success for group (a) was calculated as the proportion of animals present on North Rona in year 1 that raised pups successfully. Pupping success for group (b) was calculated as the proportion of animals present on North Rona in year 2 that raised pups successfully. Pupping success for group (c) was calculated as the proportion of animals present on North Rona plus those absent but which were known to be alive that raised pups successfully (absentees in year 2 were assumed to have failed to wean a pup)
 MPPM (kg)Relative expenditure (%)
 <178 kg178–208 kg>208 kg<3535–44>44
(a) Pupping success in year 10·880·990·990·830·981·00
n, year 15090523512334
Mean ± SE expenditure % in year 134·0 ± 1·739·3 ± 0·940·5 ± 1·5   
(b) Pupping success in year 20·900·830·780·800·860·80
n, year 22052205425
Mean expenditure % in year 236·2 ± 2·441·1 ± 1·537·1 ± 2·3   
(c) Pupping success in year 20·860·540·610·240·620·44
n, year 221792317589

Efficiency of mass transfer

Maternal expenditure in the postpartum period comprises maternal metabolic demands, direct energy transfer to the pup, and losses to waste products. Efficiency of mass transfer in grey seals at N. Rona was 45%, which is comparable to 46·1% recorded by Fedak & Anderson (1982) for the same population and 40·2% for eastern Atlantic grey seals (Iverson et al. 1993). Baker, Barrette & Hammill (1995) recorded a mean mass transfer efficiency of 49·3% for ice-breeding grey seals in the St. Lawrence area, but noted that some mothers had fed during lactation. Estimates derived for other short lactation phocid species are similar: southern elephant seals Mirounga leonina L. 46% (Fedak et al. 1996; Arnbom et al. 1997), northern elephant seals Mirounga angustirostris L. 58% (Costa et al. 1986; Deutsch et al. 1994). Arnbom et al. (1997) suggest that the difference in efficiency between elephant seal species may be explained by different basal metabolic rates, using moult metabolism as evidence (Boyd, Arnbom & Fedak 1993). The efficiency of mass transfer for study females at N. Rona was greater at the start of the season which suggests that behaviour changes according to colony conditions (Boness et al. 1995).

Variation in pup mass at weaning

There were significant year effects on pup weaning mass within mothers even when pup and mother dependent variables were taken into account (Table 5). Several explanations for this may be considered. First, differences in mass transfer efficiencies may arise from environmental fluctuations during lactation, or from individual maternal variation in behaviour. Second, variation in energetic content of mothers could occur, possibly as a result of food availability in the preceding year. Third, disturbance could interfere with pup feeding so that mothers expend more reserves on locomotion and associated behaviours. Fourth, changes in the social structure of the breeding colony could have resulted in reduced efficiency of mass transfer in some years, according to a mother's position in the colony. Expenditures were higher and lower in some years than expected (Fig. 5). Individual differences in overall maternal expenditure may be related to differing reproductive overheads as much as direct expenditure in pups, so that a mother's behaviour on the colony would have important consequences for her offspring's growth and survival. It is likely that annual variation in environmental conditions during the lactation period may be important, as in other species (Albon, Clutton-Brock & Guinness 1987; Langvatn et al. 1996).

There was no evidence of differential maternal postpartum expenditure in the sexes (as assessed by mass change) in this study, once maternal factors had been taken into account. Pups born early in the season had larger mothers, greater rates of growth, mass at weaning and survival to weaning. However, weaning mass of pups was not explained simply by the mother's identity or MPPM and there was a strong year effect (Table 5). Earlier work on the same colony had found evidence of differential investment in pups (Anderson & Fedak 1987b). Although their data were taken from almost equal numbers of male and female pups, the male pups in Anderson & Fedak's (1987b) sample were born an average of 5 days earlier than the female pups, highlighting the need for sampling to avoid biases in studies of this type.

Pup mortality

Baker (1984) found that starvation was the main cause of grey seal pup mortality at the breeding colonies on the Monach Isles, N. Rona and Orkney. Desertion by mothers, failure to establish a mother–pup bond and failure to feed normally are the most likely reasons for pup starvation and are the factors which are likely to be influenced by maternal mass or condition. On N. Rona, pupping failure was associated with low maternal postpartum mass, younger females and birth dates occurring in the later part of the breeding season.

Post-weaning mass has been shown to affect juvenile survival in ungulate species (Guinness et al. 1978; Festa-Bianchet et al. 1996) but there are few data available to determine the effect of post-weaning mass on subsequent survival of phocid pups. Data on northern and southern elephant seal post-weaning survival have been equivocal and may suggest that pup survival above a certain threshold level is simply stochastic, but the most recent work on southern elephant seals indicates greater return rates for pups that were weaned larger (C. McMann, personal communication). When a pup has been weaned it must learn to forage in a patchy environment, using the stores supplied by its mother as a buffer until it can exploit resources successfully. At the same time a mother must replenish her own depleted reserves so that significant stresses such as reduced food availability following directly after breeding could produce maternal as well as offspring morbidity or mortality.

Factors affecting pupping success in grey seals

There was consistent evidence of substantial individual differences in reproductive performance between the female grey seals, both in maternal expenditure and its result, pup mass at weaning (Tables 4, 5). In any year female grey seals breeding on N. Rona had highest pupping success if they were large, pupped in the early part of the breeding season, and expended at least the average on raising their offspring. On average, mothers expended the same proportion of their total mass during lactation to produce pups whose size at weaning was directly proportional to the mother's postpartum mass. Although there were significant positive linear relationships overall between maternal expenditure and MPPM and pup mass at weaning and MPPM in this study, each was modified by other variables and factors. By following the same individuals over the course of the study, it was possible to differentiate between sources of variation in the data. The form of the variation seen in this study is illustrated by examining the relationship between maternal expenditure and MPPM within and between animals (Fig. 4). The overall relationship showed an increase in expenditure with MPPM, and the relationship between animals was not significantly different to that within individuals (Table 4). REML procedures also highlighted the subtler negative effects of maternal length between animals on both maternal expenditure and pup mass at weaning. Grey seals continue to increase in length (albeit slowly) with age. In our sample, longer animals were older (age = −50·1 + 0·41 × length; se of slope = 0·09; r2 = 0·28; n = 58; P < 0·001) and these longer animals expended less during lactation and weaned smaller pups (Table 4,5). Similar trends were found in southern elephant seals (Fedak et al. 1996). Data from the smallest female grey seals are difficult to collect because of the predisposition of these animals to desert their pups if disturbed but we have shown that smaller (and therefore on average, younger) grey seal females at North Rona were less successful in raising pups than larger ones. They had lower expenditures, produced smaller pups at weaning and tended to breed later in the season when pupping success rates are lower (Boness et al. 1995). Some or all of these trends are found in many other species of mammals which can result in fewer viable offspring among the youngest mothers (Albon et al. 1983; Bowen et al. 1994; Lunn et al. 1994; Boness et al. 1995; Arnbom et al. 1997). This effect may be enhanced by a lack of experience in young females.

Fitness costs of reproduction

The fitness costs of reproduction to females are typically considered as lowered future fertility or increased mortality of parous females (Clutton-Brock et al. 1983). Our data indicate that mothers skipped breeding years and that this phenomenon was related to relative expenditure. Multiparous female grey seals at N. Rona had similar pupping success rates in any given year irrespective of their body mass or relative expenditures in that year (Table 7a). However, the cost to mothers of average and larger MPPM and average or greater than average expenditures was in terms of reduced pupping success in the following year, which mothers with small MPPMs and proportionately small expenditures that returned did not appear to suffer (Table 7b). Mothers with small MPPMs had pupping success rates that were comparable to those of larger females in the year following a birth and most returned – this was explained by the fact that their first year expenditures were lower than average (34 ± 1·7%). Mothers with greater than average MPPMs expended relatively little more than mothers of average size (40·5 ± 1·5, 39·3 ± 0·9%, respectively) and had fewer absentees the following year, but this situation was reversed for expenditure categories (Table 7c). Unexpectedly, the highest proportion of absentee mothers occurred in the year following low maternal expenditures (Table 7c). However, this group of absentees comprised a few mothers that returned subsequently (generally the smaller individuals in the group) and animals that were never seen again (all sizes). Thus, relatively low expenditure in average or larger sized animals was an indication of their imminent loss to the N. Rona breeding colony.

Evidence for fitness costs of reproduction to female pinnipeds is limited. Otariid mothers may have lactation periods of over a year, and Galapagos fur seal mothers (Arctocephalus galapagoensis Heller) with pups from the previous season had reduced natality (Trillmich 1986). Antarctic fur seals of all ages were significantly less likely to pup in years following a birth than previously nonparous animals and natality of primiparae was lowered more than multiparae. There were also costs via reduced survivorship following pupping (Boyd et al. 1995). Amongst phocids, evidence for fitness costs of reproduction for northern elephant seals varied from site to site (Le Boeuf & Reiter 1988; Huber et al. 1991; Sydeman et al. 1991). None of these studies controlled for the effect of maternal size on expenditure or success, but there was strong evidence of the influence of maternal size rather than maternal age for southern elephant seals (Fedak et al. 1996; Arnbom et al. 1997) and in this study (Table 4,5). Otariids may suffer size-dependent consequences for pupping success because larger mothers would have higher metabolic overheads, but there are few data to test this.

Interpreting the relationships between age, size and reproductive expenditure requires comprehensive reproductive life history data. Some aspects of reproductive performance typically have a quadratic relationship in which performance increases and then declines with age (e.g. Clutton-Brock et al. 1992). Reproductive senescence has been proposed for northern fur seals Callorhinus ursinus Gray (Trites 1991). The only data which may indicate such an effect in phocids is for northern elephant seals (Sydeman et al. 1991). However, Trillmich (1996) pointed out that senescence need not be invoked if females within the population followed two strategies, the ‘live fast, die young’ option or the ‘long view’ option involving delayed reproduction, alternate breeding and non-breeding years and high survivorship. These strategies could explain the population parameters observed in fur seals (Trites 1991) and female grey seals may also employ similar strategies (Table 8). On N. Rona, the decrease in maternal expenditure with increasing maternal length between mothers is good evidence that the benefits of size are not unlimited. It is also true that maternal length and mass are not reliable indicators of age. However, it is unlikely that longer grey seal mothers simply have higher metabolic overheads, as both maternal expenditure and pup mass at weaning decreased with increasing maternal length across animals (Table 5). This poorer reproductive performance could arise in different ways: (i) individual quality – some females expend less on reproduction because they are poor mothers with the result that available resources go towards somatic growth; (ii) the age at which females recruit into the breeding population determines the likely limits to their potential size, with the youngest breeding primiparae unable to compensate for the effects of their earliest efforts. Females that have high expenditures in one year may simply skip breeding the following year, though the mechanism which allows this is unclear (Table 7).

Ultimately, mothers must make reproductive allocation decisions between current expenditure on producing a big pup and its inherent costs, both in depressed maternal survival probability and in subsequent decreased natality, associated with depletion of maternal reserves and their future reproductive potential (Clutton-Brock et al. 1983; Stewart 1986). Resolution of this conflict depends on the balance between the costs and benefits associated with the options. The benefits to offspring are more difficult to assess than effects on mothers. Grey seals have been described as moderately polygynous (e.g. Boness & James 1979; although see Amos et al. 1993, 1995) and breeding adult males are typically twice the mass of females when animals mate. Nevertheless, we have seen that there were no sex differences in pup masses at weaning in spite of the fact that males were born heavier. Arnould, Boyd & Socha (1996) found that Antarctic fur seal pups were allocating resources differently before they weaned, so that male pups had a greater lean body mass than female pups of the same mass. Early survival of males may be traded off against potential breeding success gains brought about through large body size in otariid species, but early resource allocation in grey seal pups has not been documented.


Maternal reproductive parameters of grey seals at N. Rona were influenced strongly by maternal body mass, length and duration of lactation. Substantial individual variation was found between mothers in the number of pups produced, pupping success and maternal mass change characteristics. In any year, a mother's pupping success was correlated with her size and relative expenditure on the pup. However, mothers experienced size- and expenditure-dependent costs of reproduction through lower pupping success and more absences from the colony in the year following a birth. There was evidence of a decline in reproductive performance with maternal length, but this could not be attributed directly to age. Substantial individual variation in maternal reproductive success among grey seals at North Rona can be attributed to variations in life-history patterns. Maternal body size at parturition has a profound influence on reproductive expenditure and pupping success in each breeding episode with consequences for subsequent breeding episodes which may be modified at each iteration by resource availability and predictability.


We would like to thank all those who assisted in fieldwork, particularly S. Twiss, P. Whitty, J. Lawson, J. Reilly, R. & J. Baker, B. McConnell, R. Harcourt, M. Jüssi, C. Blomquist, S. Licence, P. Allen, R. Gadbury, O. Kiely and S. Moss. The cooperation and assistance of Scottish Natural Heritage, H.M. Coastguard and the Northern Lighthouse Board are acknowledged gratefully. The work was carried out as part of the UK's NERC Research Programme and since 1993 has been supplemented by grants from the Royal Society and NERC to B. Amos. We thank S. Twiss, P. Hammond, J. Harwood and two anonymous referees for their help in refining the paper.

Received 4 August 1997;revisionreceived 2 June 1998