Reproductive performance in grey seals: age-related improvement and senescence in a capital breeder.

1. Three hypotheses have been advanced to account for age-related improvement in performance: the selection hypothesis predicts improved due to the loss of lower quality phenotypes, the constraint hypothesis predicts individuals improve function, and the restraint hypothesis predicts younger individuals forego or reduce effort because of mortality risks. A decline in age-related performance (i.e. senescence) is predicted by mutation accumulation, antagonistic pleiotropy and disposable soma (wear and tear) hypotheses. 2. Using five measures of performance - birth rate, maternal and pup birth mass, pup weaning mass, weaning success and lactation length - we tested these hypotheses concerning age-related change in reproduction in 279 female grey seals (Halichoerus grypus), ages 4-42 years, over a 23-year period between 1983 and 2005 on Sable Island, Nova Scotia. These females produced 2071 pups. 3. Although body mass of primiparous females increased with age (4-7 years) birth mass of their pups did not, but pup weaning mass did. Second- and third-parity females of the same age as primiparous females gave birth to and weaned heavier pups. However, parity and age were dropped from models when maternal body mass was included. 4. The proportion of females giving birth varied significantly with maternal age, increasing in young females and then declining late in life. Weaning success rate also increased rapidly to about 8 years and subsequently declined in females > 32 years. 5. Generalized additive models indicated nonlinear changes in 3 day body mass (i.e. approximately birth mass) and weaning mass of pups as a function of maternal age, after accounting statistically for the effects of maternal body mass. Mixed-effects, repeated-measures models fitted to longitudinal data further supported the conclusion that pup birth mass and weaning mass vary nonlinearly with maternal age and indicated nonlinear changes in lactation duration. 6. We found some support for the constraint hypothesis, but our findings were not consistent with the selection hypothesis or the restraint hypothesis as the basis for improvement in reproductive performance. 7. Senescence was evident in multiple female and offspring traits, indicating the degeneration in function of several physiological systems as predicted by the disposable soma hypothesis.

Stomach temperature telemetry reveals temporal patterns of foraging success in a free-ranging marine mammal.

1. We studied feeding frequency in free-ranging grey seals using stomach temperature telemetry to test if previously reported sex differences in the diving, movement and diet were reflected in the temporal pattern of foraging success. 2. Data were retrieved from 21 of 32 grey seals from 1999 to 2001, totalling 343 days and 555 feeding events, with individual record length varying from 2 to 40 days (mean: 16.33 +/- 2.67 days/seal). 3. Seals fed on 57.8 +/- 6.46% of days sampled and had an average of 1.7 +/- 0.26 meals per day, but individual variability was apparent in the temporal distribution of feeding as evidenced by high coefficients of variation (coefficient of variation = 69.0%). 4. Bout analysis of non-feeding intervals of six grey seals suggests that feeding intervals of individuals were varied and probably reflect differences in prey availability. Grey seals tended to have many single feeding events with long periods separating each event, as would be expected for a large carnivore with a batch-reactor digestive system. 5. We found significant sex differences in the temporal distribution of feeding. The number of feeding events per day was greater in males (2.2 +/- 0.4 vs. 1.0 +/- 0.2), as was time associated with feeding per day (56.6 +/- 5.8 min vs. 43.9 +/- 9.4 min). 6. The number of feeding events varied with time of day with the least number occurring during dawn. Feeding event size differed significantly by time of day, with greater meal sizes during the dawn and the smallest meals during the night. 7. The length of time between meals increased with the size of the previous meal, and was significantly less in males (541.4 +/- 63.5 min) than in females (1092.6 +/- 169.9 min). 8. These results provide new insight into the basis of sex differences in diving and diet in this large size-dimorphic marine predator.

The rate of fertilization in male mating tactics of the polygynous grey seal.

Studies using molecular markers have shown that some grey seal males may be gaining success through exhibiting alternative mating tactics. We estimated the probability of fertilization success of grey seal males exhibiting the primary tactic of female defence and one alternative tactic of mating with departing females on Sable Island, Nova Scotia, Canada, during the breeding seasons of 1997-2002. Although the fertilization rate of the primary tactic (27-43%) was greater than that of the alternative tactic (10-12%), these low rates indicate the potential fitness value of alternative mating tactics in this size-dimorphic pinniped species.

Variation in the mitochondrial control region in the Juan Fernández fur seal (Arctocephalus philippii).

The Juan Fernandez fur seal (Arctocephalus philippii was allegedly extremely abundant, numbering as many as 4 million prior to sealing which continued from the late 17th to the late 19th century. By the end of the sealing era the species was thought to be extinct until they were rediscovered at Alejandro Selkirk Island in 1965. Historic records would suggest that the species underwent a substantial population bottleneck as a result of commercial sealing, and from population genetic theory we predicted that the genetic variability in the species would be low. We compared the mtDNA control region sequence from 28 Juan Fernandez fur seals from two islands in the Juan Fernandez Archipelago (Chile). Contrary to expectation, we found that variation in the Juan Fernandez fur seals is not greatly reduced in comparison to other pinniped taxa, especially given the apparent severity of the bottleneck they underwent. We also determined minor, but significantly different haplotype frequencies among the populations on the two islands (Alejandro Selkirk and Robinson Crusoe Islands), but no difference in their levels of variability. Such differences may have arisen stochastically via a recent founder event from Alejandro Selkirk to Robinson Crusoe Island or subsequent genetic drift.

The energetics of male reproduction in an aquatically mating pinniped, the harbour seal.

The energy expenditure of breeding male harbour seals, Phoca vitulina, on Sable Island, Nova Scotia, was investigated by measuring changes in body mass, body composition, and water flux using isotope dilution. Seals lost 0.47% +/- 0.04% (n = 34) of their initial mass per day during the breeding season (4 wk), and fat, water, and protein accounted for 64.3% +/- 4.8%, 27.8% +/- 3.3%, and 6.9% +/- 1.4% of this mass loss, respectively (n = 31). Total energy expenditure was estimated as 33.3 +/- 1.9 MJ d(-1), or 3.9 +/- 0.2 W kg(-1) (n = 17), similar to rates measured in terrestrially mating pinniped species. However, unlike terrestrially mating pinnipeds, male harbour seals did not fast during the breeding season, and energy intake from foraging accounted for 61.8% +/- 4.0% of the total energy expended. Males derived most of their expended energy from food intake early in the breeding season. However, as oestrus females became increasingly available, reduced rates of food intake in males were coupled with increased rates of total energy expenditure. Larger males expended significantly more energy from body stores and more total energy than smaller males. Male harbour seals appeared to balance the energetic costs of reproduction against the constraints of small body size by foraging during deep-diving trips before the appearance of oestrus females and by opportunistic feeding throughout the breeding season while at sea. We suggest that size dimorphism may be less pronounced in aquatically mating pinnipeds partly because the temporal and spatial separation of foraging and reproduction is less distinct than it is for terrestrially breeding pinnipeds.

DNA fingerprinting evidence of nonfilial nursing in grey seals.

We tested the hypothesis that kin selection may play a role in fostering behaviour in grey seals. Fostering frequency varied among three colonies, ranging from 3% to 28%. Band-sharing coefficients (S) of DNA fingerprints, from two multilocus probes, were used to predict relatedness (r). Mean r did not differ between foster mother-pup pairs and the expected r = 0 for presumed unrelated female-pup pairs. Likewise, mean r between fostered and filial pups compared to r between presumed unrelated pups within the same beaches did not differ. Mean S values of presumed unrelated pups on different beaches within the two smallest colonies were indistinguishable, indicating that there is not increased variation in relatedness in small colonies. These results suggest that kin selection does not play a significant role in the maintenance of grey seal fostering behaviour.

Prenatal and postnatal transfer of fatty acids from mother to pup in the hooded seal.

Unlike most mammals, hooded seal (Cystophora cristata) pups are born with a substantial layer of adipose tissue. Subsequently, during the brief lactation period of only 4 days, fasting mothers mobilize enormous amounts of lipid from blubber and secrete milk (60% fat) at rates of 10 kg.day-1. Pups gain 7 kg.day-1 due primarily to the deposition of fat in blubber. We measured blubber content and fatty acid composition of blubber and milk in hooded seal mother-pup pairs at birth and over the 4-day lactation period to examine the nature and source of fetal lipids, the incorporation of maternal blubber fatty acids into milk lipid, and patterns of fatty acid deposition in suckling young. The fatty acid composition of the blubber of the newborn was notably different from that of its mother. Fetal deposition was likely due to a combination of both fetal synthesis and direct placental transfer of maternal circulating fatty acids. The blubber of the newborn was characterized by high levels (> 90% of total fatty acids) of saturated and monounsaturated fatty acids of primarily endogenous origin. In particular, the fetus appeared to have high delta-9 desaturase activity as evidenced by the large amounts of 14:1n-5 (4.2%) and 16:1n-7 (37.0%) in newborn blubber compared to maternal blubber (0.2% and 14.1%, respectively). Nevertheless, essential and long-chain polyunsaturated fatty acids of the n-3 and n-6 families, which could only have originated by direct transfer from the mother, comprised > 7% of pup blubber fatty acids and indicated greater rates of placental transfer than found in humans. In hooded seal mothers, rapid lipid transfer during the brief lactation period appeared to be facilitated by direct incorporation of mobilized fatty acids into milk. Although some differences in proportions of specific fatty acids were found between milk and maternal blubber, most of these differences declined over the course of lactation. However, selective mobilization of 20:5n-3 from maternal blubber into milk was apparent throughout lactation and resulted in elevated levels in pup blubber at weaning compared to maternal blubber. Ingested fatty acids were deposited directly and without modification into the blubber of pups, and by 4 days the fatty acid composition of pup blubber was virtually identical to that of the milk consumed.

Effects of suckling and the postsuckling fast on weights of the body and internal organs of harp and hooded seal pups.

The weights of harp seal pups quadruple during 13 days of suckling while hooded seal pups double in weight in a lactation period of just 4 days. Pups of both species then fast for a month or longer. As a first measure of tissue responses to this 'feast and famine' pattern, we weighted the body, sculp (blubber and attached skin), core (carcass including viscera) and major internal organs of seal pups at birth, at the end of suckling, and at the end of the fast. When expressed as a percentage of body weight, the weights of the internal organs of newborn harp and hooded seals were within the range reported for newborn land mammals. During suckling, harp and hooded seals gained 2.3 and 6.5 kg/day body weight, respectively, but a large part (64-73%) of this gain was blubber and skin rather than core. Even though pups were ingesting great quantities of fat, their digestive organs (stomach, small and large intestines, pancreas) were neither particularly large at birth nor did these organs gain in weight or length unusually rapidly. Most organs increased in weight in proportion to the increase in core weight, but the liver and spleen increased proportionately more than the core, and the stomach, heart and kidneys increased proportionately less. At the end of suckling, sculp accounted for more than half of the body weight in both species. The subsequent 4-week fast resulted in weight loss from both the sculp and core, and the liver and spleen decreased in weight by about 70%. The net effect of sequential suckling and fasting was particularly striking in the hooded seal pup, which has a lighter core, heart, liver and spleen at 1 month postpartum than at birth. These data illustrate a remarkable cycle of nutrient deposition and depletion which is undoubtedly central to the survival of young seals in the harsh pack-ice environment.

Cyclic dermatitis associated with Fusarium sp infection in pinnipeds.

Dermatitis associated with Fusarium sp infection developed in 3 California sea lions (Zalophus californianus) and 3 gray seals (Halichoerus grypus) at the National Zoological Park in Washington DC. The lesions were papular or nodular and were distributed mainly on the face, trunk, and flippers. One sea lion died 6 weeks after extensive cutaneous involvement. The lesions regressed after 1 mild exacerabtion in the other 2 sea lions. In the gray seals, the skin condition appeared to worsen during the summer and to regress during the winter, despite oral and topical treatment with miconazole and thiabendazole. Fusarium sp was repeatedly isolated from biopsy specimens of lesions. Hyperplasia of epidermal and follicular epithelium was associated with acute and chronic inflammation and fungal hyphae. The species of the fungus in 1 of the gray seals was determined to be F solani, a type occasionally associated with keratitis and opportunistic infections in human beings. Initial excessive chlorination and high fluctuating pool temperatures attributed to a faulty water treatment system were considered as factors in promoting fungal growth.

What happens between an external stimulus and an overt response? A study of covert behavior.

Peripheral components of feedthrough loops were psychophysiologically measured from the brain, both forelimbs, the tongue and the eyes during simple and choice reaction time tasks using linguistic and non-linguistic stimuli. Closing a microswitch with the little finger was the overt response. Covert electromyographic (EMG) responses were computer identified in the following average temporal order: generally, the earliest covert reactions were in the tongue, brain, eyes, and passive arm-hand region. Next were complex EMG events in the active limb. These covert reactions may function in feedthrough loops to generate and transmit codes during internal information processing. The passive arm-hand responses occurred significantly earlier than the onset of the covert EMG burst for closing the microswitch; perhaps there is an inhibitory response "commanding" the passive arm not to respond, before the other (active) limb can overtly respond. Mean response patterns to linguistic and non-linguistic stimuli were almost identical. Reaction time to the onset of the EMG burst for switch closing was from 40 to 95 milliseconds earlier than the usual overt reaction time measure (that to switch closing), suggesting that reaction time studies might be improved by using the onset of EMG increase as the more sensitive and precise measure.