Energetics of pregnancy, lactation and neonatal development in ringed seals (Phoca hispida)

9 1995 ElsevierScience B.V. All rights reserved Whales, seals, fish and man A.S. Blix, L. WallCeand ~. Ulltang,editors

319

Energetics of pregnancy, lactation and neonatal development in ringed seals (Phoca hispida) Christian Lydersen Norwegian Polar Institute, Tromsr Norway Abstract. Ringed seal fetuses grow according to the equation: (fetal mass) 1/3 (g) = 0.075 (days) - 1.23 (r = 0.997), for the 241 days of active gestation. The energy content of newborn ringed seals (N = 3, mass =4.55 kg, fat = 4.75%, protein = 21.8%) and placentas (N= 3, mass =0.347 kg, fat = 1.88%, protein = 16.38%) are 26.3 MJ and 1.3 MJ, respectively. Metabolic requirements for the growing fetus for the whole gestation period are estimated to be 113.4 MJ. Ringed seal pups are nursed for approximately 39 days and grow at a daily rate of 0.35 kg. Their average metabolic rate is 3.8 times the predicted basal metabolic rate based on body size. The pups drink an average of 1379 ml of milk daily, with a caloric density of 17.32 kJ/g. Net milk energy output for the average female ringed seal over the whole lactation period is thus 931.5 MJ. Total net costs of pregnancy and lactation are thus 1072.5 MJ. Ringed seal neonates are somewhat more energetically costly to their mothers compared to other phocids (per mass unit) because of their unusual degree of activity. While most young phocids spend the majority of their time immobile, nursing ringed seal pups spend more than 50% of their time in the water. As a result they become skilled divers at an extremely early age, and are able to dive for 12 min and to depths of 90 m. Ringed seal pups keep their fetal whitecoat longer than any other phocid pups, and they occupy a high number of breathing holes compared to other age groups of the same species. All of these factors are considered to be evolutionary adaptations for predator avoidance, mainly from polar bears.

Key words: lactation, reproductive energies, diving, behavior, ringed seal pups

Introduction

The ringed seal (Phoca hispida) is the most numerous seal in the northern hemisphere. It has a circumpolar distribution and its total population size is estimated to be between 5-7 million individuals [1]. During the spring breeding and pupping season, ringed seals show a great affinity for ice, where stable land-fast ice seems to be the preferred habitat. The seals are able to maintain breathing holes in ice that is several metres thick and can thus, in principle, be found throughout the whole Arctic marine environment, including the north pole. Ringed seals are the smallest of the northern phocids. They have evolved under strong predation pressure from surface predators, mainly polar bears (Ursus maritimus), but also arctic foxes (Alopex lagopus) and birds such as ravens (Corvus corax) and glaucous gulls (Larus hyperboreus) [2-6]. The high levels of predation pressure have resulted in antipredator adaptations such as giving birth in snow-covered lairs, use of multiple lairs and breathing holes as possible escape routes in case of attack, and a generally

Address for correspondence: Norwegian Polar Institute, P.O. Box 399, N-9001 Tromsr Norway.

320 "nervous" haul-out behaviour. When hauled out, ringed seals normally raise their heads and scan the area every 10-15 s. Additionally, they position themselves at the breathing hole in such a way that the wind is coming from behind [7]. They are thus able to see predators approaching from the front, and smell predators coming from behind. Because of all these anti-predator adaptations, ringed seals are difficult to capture compared to other seal species, and most of the important events during the spring pupping and breeding season occur under the ice, or in snow-covered lairs. A recent report estimated the ringed seal population to be about 200,000 individuals in the region of Svalbard. This number is thought to represent the carrying capacity for this area [8]. Based on studies of ice conditions, and knowledge of densities of ringed seals in different types of ice [9,10], the annual pup production in Svalbard is estimated to be about 20,000 [11]. Thus, the ringed seal is the most abundant mammal in Svalbard. Energy invested in reproduction represents a major component of the annual energy budget of most mammalian species. During the last decade, a series of studies have documented the various components of energetic investment by female ringed seals, such that a reasonably complete analysis of reproductive energetics by females of this species is now possible. This is the subject of the present paper. The primary emphasis of this review is on information gathered from Svalbard during The Norwegian Marine Mammal Research Programme. In the Svalbard area, female ringed seals reach sexual maturity at 3-5 years of age [12]. Peak pupping for ringed seals in this area is the first week of April. Based on cross-sectional studies of ringed seals from the Canadian western Arctic, where ovaries and uterine cornuas were examined, it was estimated that ringed seal females have a delayed implantation of 89 days and an active gestation period of 241 days [13]. Another cross-sectional study of ringed seals from both Svalbard and the Canadian Arctic, that examined ovaries and mammary glands, concluded that ringed seals have an average lactation period of 39 days [14]. If we define 1 April as the nominal birth date in the Svalbard area, and extrapolate the data reported above to the Svalbard population, the average dates for ovulation, weaning and implantation would be 6 May, 9 May and 3 August, respectively (Fig. 1). Seventeen fetuses have been collected from ringed seals in Svalbard (Lydersen, unpublished data). Using collection date as a measure of age, these fetuses grow according to the equation: (fetal mass) 1/3 (g)= 0.075 ( d a y s ) - 1.23 (r = 0.997). Three newborn pups and placentas have also been collected from the same area. The mean mass of the pups was 4.55 _+0.30 kg, and the mean mass of the placentas was 0.347 _+0.140 kg. The total energy contents of a newborn pup and a placenta of average mass based on slaughter house chemical analyses were 26.3 MJ and 1.3 MJ, respectively (Lydersen, unpublished data). In addition to production of fetal and placental tissues, the cost of pregnancy also includes energy to maintain the metabolic requirements of the growing fetus. This cost can be estimated using a relationship derived for terrestrial mammals: QG = 18.4BM 1.2, where QG is the heat of gestation in MJ and BM is the body mass in kg of the newborn pup [15]. According to this

321

Implantation August 3 Fig. 1. Reproductive events in an annual cycle for adult ringed seal females from Svalbard.

relationship the energy required to cover the metabolic requirements of a growing ringed seal pup would be 113.4 MJ. Ringed seals are normally born in a lair that is dug out by the female in the snow covering a breathing hole [16]. Each female has several lairs and breathing holes, and can thus move between these structures if attacked by predators. It is thought that mothers actively move the pups if they are attacked while the pup is relatively young. Newborns do not have an insulating layer of subcutaneous blubber, but can survive brief immersions in ice-cold water through the use of relatively large stores of brown adipose tissue [17]. As lactation progresses pups deposit blubber and they start entering the water voluntarily. Based on VHF recordings of pup activity, nursing ringed seal pups spend up to 64% of their time in the water [18]. Pups of other phocid species that are born bearing lanugo, such as grey (Halichoeurs grypus) and harp (Phoca groenlandica) seals, usually stay on the ice or on shore until the nursing period is over [ 19,20] before they start to explore the aquatic environment. In order to obtain more detailed information on ringed seal pup diving behaviour, microprocessor controlled time-depth recorders (TDRs) (Mk5- Wildlife Computers) were used to collect more than 1,000 h of activity. This sample includes over 7,500 dives from three nursing ringed seal pups [21 ]. The pups were spending an average of 50.3% of this time in the water and 49.7% hauled out on the ice. When the pups were in the water, 20.5% of the time was spent actively diving, while the remaining 79.5% was spent at the surface. The pups used in this experiment inhabited three different geographical areas, and comparisons with sea maps for the respective areas showed that the pups were diving to the bottom in all three cases. The deepest recorded dive was 89 m. The longest recorded dives for the three pups were 5.8, 7.5 and 12.0 min re-

322 spectively. Based on information on body composition and oxygen stores for adult ringed seals [22], the aerobic dive limit (ADL) for a 20 kg ringed seal would be about 3.3 min. Thus, the aerobic dive limit was exceeded by all three pups. However, dives of duration longer than the ADL were exceptional; only 3.7% of all recorded dives exceeded this limit. Pups tended to spend more time in the water and more time actively diving with increasing age. They also increased the number of long dives as they became more competent in the water [21 ]. Two different longitudinal studies, one using tritiated and one using doubly labelled water, were conducted in order to measure growth, water flux and CO2 production, and to estimate milk intake and change in body composition of nursing ringed seal pups [23,24]. During these studies, pups were captured and their stomachs were evacuated of milk. They were then weighed and injected with a known volume of known concentration of labelled water. Then, after the injected isotopes were thought to be at equilibrium with the animal's body water pool, a blood sample was taken before the animal was released. The general procedure for all such experiments should be a serial blood sampling regime performed on some injected individuals to enable determination of equilibrium time for the size and species of animal involved. One should also know approximately the biological half-life of the oxygen isotope, since the most reliable results are obtained when animals are recaptured between one and two half-lives of the oxygen isotope [25]. For ringed seal pups with body masses of 20 kg or less, the injected tritium was in equilibrium with the rest of the body water pool within 30 min after intramuscular injections of the isotope [23]. This short interval reflects the relatively small size and high metabolism of the animals that were crawling around on the ice for most of the equilibration period. These factors are also reflected in the short biological half-life of tritium, of only 130 _+ 17 h in these pups [23]. For later experiments, generally the equilibration blood sample was taken after a waiting period of 1 h post injection after intravenous administration of isotopes, and recapture for terminating experiment or re-injecting isotopes was attempted about 1 week after initial injection. The average daily mass gains of the pups in the two isotope studies were 0.39 _ 0.10 kg and 0.35 _+0.08 kg, respectively. The daily water fluxes in the pups in the same two experiments were 62.9 +_21.5 ml/kg and 52 __.0 ml/kg. The fact that the former value is somewhat higher (although not significantly, P = 0.58, MannWhitney U-test) is expected since the pups in that study were smaller and if all other conditions were similar should thus have a higher mass specific metabolism. In order to calculate the proportion of the total water flux that results from metabolism versus external sources, a second isotope experiment was conducted using doubly labelled water [24]. CO2 production was measured to be 0.85 _+0.16 ml/g per h, corresponding to a field metabolic rate (FMR) of 0.55 +_0.10 MJ/kg per day or 3.8 _ 0.6 times the predicted basal metabolic rate (BMR) based on body size [26]. Using these measurements, metabolic water production was calculated and subtracted from the total water influx. This gave an estimate of water intake from external sources. It is assumed that all water entering the pups was from the milk. None of the pups in the doubly labelled water experiment was observed drinking water or eating snow. In

323 addition, the very small intraspecific variation in water flux, and the credible values for milk intake produced when using the measured water fluxes, suggest that any other intake of water could be neglected. Only one longitudinal record of ringed seal milk is available [23]. The average water content in the milk over an 18-day period was 48.6 +_5.3%. The average values for protein and fat were 9 . 9 _ 2.4% and 38.1 _+2.9%, respectively. The fat content increased from 36.4 to 41.5% during this period. Using these average values, the pups drank 1,379 ml milk daily of a caloric density of 17.32 kJ/g. During an average lactation period of 39 days, pups would thus drink 53.8 1 of milk or take in 931.5 MJ of energy. The body composition of the pups changed dramatically during the nursing period. New-born tinged seals consisted of 4.75% fat and 70.1% water [23]. As the pups grew, the fat content increased and the water content decreased (Fig. 2). Close to weaning, at a body mass of 21 kg, the fat and water content were 41% and 42%, respectively [24]. Nursing ringed seal pups used in the doubly labelled water study were equipped with Mk5 TDRs. Activity budgets, based on information collected with the TDRs, were constructed and used in conjunction with the FMR measurements in an attempt to calculate FMR for the different activities of the pups (Table 1). The three types of activities that can be separated from the TDR readings are hauled out on the ice (saltwater switch dry), actively diving (saltwater switch wet, and pressure transducer recording depths deeper than 1 m) and staying in the water at the surface (saltwater switch wet, and pressure transducer recording depths shallower than 1 m). When solving three equations with three unknowns, where the fractions of time spent in the three different activities for each pup were matched against the total energy con-

60

r/3

5O

,~

4o

"D'----------. o o

3O

9

Water

D

Fat

r r

9 Protein

r

20 I

10

!

14

16

9

!

9

18 Body

!

20

9

i

22

m a s s (kg)

Fig. 2. Variation in body composition in nursing ringed seal pups of different body masses from Sval-

bard spring 1992. (Water: y=43.60 + 2.39x-0.117x2, fat: y= 38.71 - 3.35x +0.164x2, protein: y = 4.39 + 1.93x - 0.070x2, r = 0.86 in all cases). From Lydersen et al. [24].

324 Table 1. Activity budgets and daily energy consumption for nursing ringed seal pups from Svalbard, spring 1992

Animal no.

Duration of experiment (days)

Mean body mass (kg)

Fraction of day hauled out (%)

Fraction of day at surface (%)

Fraction of day diving (%)

Energy consumption (kJ/day)

E 2034 E 2021 E 2056

10 11 10

19.15 18.60 18.05

46 60 50

38 32 42

16 8 8

10,499 8,727 10,032

sumption for each individual, FMRs for hauling out, actively diving, and staying in the water at the surface are calculated to be 1.34, 5.88 and 6.44 times BMR, respectively [24]. The former value seems very low for a growing pup and could be a sampling artifact. However, based on observations, ringed seal pups are very inactive when hauled out, and if they spend a lot of time sleeping, like nursing pups of other phocid species [ 19,20], this dramatically reduces their metabolic rate [27]. Information on activity of ringed seal mothers during the nursing period is scarce. In one study that employed acoustic telemetry on a single female that had an almost weaned pup (22 kg at first capture), it was found that the mother spent 55% of the recorded time in the water [28]. Another female equipped with a Mk5 TDR that had a younger pup (13 kg at first capture) spent 82% of a 17-day recording period in the water (Lydersen, unpublished data). Longitudinal mass loss data from nursing ringed seal mothers have been recorded from two individuals, one monitored over a 17-day period and one over an l 1-day period (Lydersen, unpublished data). They lost 0.62 kg/day and 0.68 kg/day, respectively. If we assume that all of this mass loss is fat, an average daily mass loss of 0.65 kg corresponds to an energy loss of 25.6 MJ. The daily milk energy output of an average female was calculated to be 23.9 MJ. Thus the mass loss of the mothers barely covers the expenses of the milk production. Assuming an average FMR for the mothers of twice BMR and a body mass of 70 kg, an energy equivalent of 14.2 MJ is needed to cover a mother's metabolism. Combining these figures, a daily deficit of 12.5 MJ is found. This has to be covered through eating. This energy value is a minimum estimate since the mass loss of the mothers probably does not consist of 100% fat, and the FMR of twice BMR is probably conservative. Stomach content analyses from ringed seals in the Svalbard area have shown that ringed seals eat mainly arctic cod (Boreogadus saida) and the amphipod Parathemisto libellula [29-31]. Bomb calorimetric measurements of specimens of these food types collected in August, show a caloric density of 3.8 kJ/g and 5.8 kJ/g for P. libellula and arctic cod, respectively. Using these values, ringed seal females would have to eat 2.2 kg of arctic cod or 3.3 kg of P. libellula daily during the nursing period in order to balance their energy budgets. These values are also minimal since the assimilation of energy from the food is not 100%. If we add up the energetic costs of pregnancy and lactation, the average net energy output for each ringed seal female to produce a weaned pup, is 1072.5 MJ (Table 2). Using the same values

325 Table 2. Minimum estimates of net energy required for a ringed seal female to produce a weaned pup MJ Energy content of newborn Energy content of placenta Heat of gestation Milk energy output Total

26.3 1.3 113.4 931.5 1,072.5

for the main prey items, this corresponds to a minimum of 185 kg of arctic cod or 282 kg of P. libellula. Generally, the most efficient energy transfers during lactation in phocid seals are found in species where the nursing period is short and the pups are inactive. Within phocids, ringed seals have the longest nursing period, and with the growth rate recorded for Svalbard, they use about 14 days to double their newborn mass. The corresponding figures for hooded (Cystophora cristata), harp and grey seals are 4, 6 and 9 days, respectively. In addition, newborns of these three species are 5, 2 and 4 times heavier than ringed seals at birth. However, the pups of these other species are very inactive during the nursing period compared to ringed seal pups. As was shown earlier, ringed seal neonates spend about 50% of their time in the water. Predation pressure is probably the major factor that has led to the observed differences in neonatal development and overall lactation strategies. By being active, and diving at an extreme early age, ringed seal pups develop diving skills that help them escape predators. The lactational strategy observed in the other species, where the pups stay helpless on the ice platform during the whole lactation period and thereafter start to explore the water, would be catastrophic in an area where polar bears are constantly hunting. The behaviour of ringed seal pups is of course in conflict with a maximum efficiency of energy retention, and the metabolic overhead paid by tinged seal mothers is the highest among phocid seals. Ringed seal pups store only about 36% of the energy they receive via milk as body tissue. The corresponding figures for harp and grey seal pups are 66% (Lydersen et al., unpublished data) and 75% [32], respectively. However, reproductive success is not measured as who produces the fattest pup but as the number of surviving offspring, and in an environment with constant threat of predation from the surface, learning to dive as fast as possible is a key to survival. Another feature of ringed seal behaviour during lactation that probably resulted from predation pressure is the relatively high number (8.5 _+3.5) of breathing holes used by the females and their pups, compared to the average of 3.5 found for other ringed seals [33]. In addition, the ringed seal pups keep their white lanugo for a very long time (up to 2 months in some cases) compared to pups of other species. At this stage the insulatory properties of the lanugo are of little value, but since vision is important to hunting polar bears [34], cryptic coloration will reduce the pup's chances of being detected when it is hauled out outside lairs.

326

Acknowledgements This study was funded by the Norwegian Fisheries Research Council (NFFR), Department of Fisheries and Oceans, Canada and the Fritjof Nansen Foundation for the Advancement of Science. I would like to thank K. Kovacs for comments on the manuscript.

References 1. Stirling I, Calvert W. Ringed seal. FAO Fish Ser 1979;5:66-69. 2. Smith TG. Predation of ringed seal pups (Phoca hispida) by the arctic fox (Alopex lagopus). Can J Zool 1976;54:1610-1616. 3. Smith TG. Polar bear predation of ringed and bearded seals in the land-fast sea ice habitat. Can J Zool 1980;58:2001-2009. 4. Gjertz I, Lydersen C. Polar bear predation on ringed seals in the fast-ice of Hornsund, Svalbard. Polar Res 1986;4:65-68. 5. Lydersen C, Gjertz I. Studies of the ringed seal (Phoca hispida) in its breeding habitat in Kongsfjorden, Svalbard. Polar Res 1986;4:57-63. 6. Lydersen C, Smith TG. Avian predation on ringed seal Phoca hispida pups. Polar Biol 1989;9:489--490. 7. Kingsley MCS, Stirling I. Haul-out behavior of ringed and bearded seals in relation to defence against surface predators. Can J Zool 1991 ;69:1857-1861. 8. JCdestr K, Ugland KI. S~barhetsanalyse for ringsel og grCnlandsel i Barentshavet nord. Det Norske Veritas Industrier AS, 1994;Rapport no 93-3740. 9. Lydersen C, Jensen PM, Lydersen E. A survey of the Van Mijen fiord, Svalbard, as a breeding habitat for ringed seals, Phoca hispida. Holarct Ecol 1990;13:130-133. 10. Lydersen C, Ryg M. Evaluating breeding habitat and populations of ringed seals Phoca hispida in Svalbard fjords. Polar Rec 1991;27:223-228. 11. Smith, TG, Lydersen C. Availability of suitable land-fast ice and predation as factors limiting ringed seal populations, Phoca hispida, in Svalbard. Polar Res 1991;10:585-594. 12. Lydersen C, Gjertz I. Population parameters of ringed seals (Phoca hispida Schreber, 1775) in the Svalbard area. Can J Zool 1987;65:1021-1027. 13. Smith TG. The ringed seal, Phoca hispida, of the Canadian western Arctic. Can Bull Fish Aquat Sci 1987;216:1-81. 14. Hammill MO, Lydersen C, Ryg M, Smith TG. Lactation in the ringed seal (Phoca hispida). Can J Fish Aquat Sci 1991;48:2471-2476. 15. Brody S. Bioenergetics and Growth, with Special Reference to the Efficiency Complex in Domestic Animals. New York: Reinhold, 1945. 16. Smith TG, Stifling I. The breeding habitat of the ringed seal (Phoca hispida). The birth lair and associated structures. Can J Zool 1975;53:1297-1305. 17. Taugbr G. Ringed seal thermoregulation, energy balance and development in early life. Thesis, Institute of Zoophysiology, University of Oslo, Norway. 1982. Can Fish Aquat Sci Transl Ser 1984;5090. 18. Lydersen C, Hammill MO, Ryg MS. Differences in haul-out pattern in two nursing ringed seal (Phoca hispida) pups. Fauna Norv Ser A 1993;14:47-49. 19. Kovacs K. Maternal behaviour and early behavioural ontogeny of grey seals (Halichoerus grypus) on the Isle of May, UK. J Zool London 1987;213:697-715. 20. Kovacs K. Maternal behaviour and early behavioural ontogeny of harp seals (Phoca groenlandica). Anim Behav 1987;35:844--855.

327 21. Lydersen C, Hammill MO. Diving in ringed seal (Phoca hispida) pups during the nursing period. Can J Zool 1993;71:991-996. 22. Lydersen C, Ryg MS, Hammill MO, O'Brien PJ. Oxygen stores and aerobic dive limit of ringed seals (Phoca hispida). Can J Zool 1992;70:458--461. 23. Lydersen C, Hammill MO, Ryg MS. Water flux and mass gain during lactation in free-living ringed seal (Phoca hispida) pups. J Zool London 1992;228:361-369. 24. Lydersen C, Hammill MO. Activity, milk intake and energy consumption in free-living ringed seal (Phoca hispida) pups. J Comp Physiol 1993;163:433-438. 25. Nagy, KA. The doubly labeled water (3HH180) method: a guide to its use. Los Angeles, CA: UCLA Publication No 12-1417, 1983. 26. Kleiber M. The Fire of Life: an Introduction to Animal Energetics. Huntington, NY: Robert E. Krieber, 1975. 27. Worthy GAJ. Metabolism and growth of young harp and grey seals. Can J Zool 1987;65:13771382. 28. Lydersen C. Monitoring ringed seal (Phoca hispida) behaviour by means of acoustic telemetry. Can J Zool 1991;69:1178-1182. 29. Gjertz I, Lydersen C. The ringed seal (Phoca hispida) spring diet in northwestern Spitsbergen, Svalbard. Polar Res 1986;4:53-56. 30. Lydersen C, Gjertz I, Weslawski JM. Stomach contents of autumn-feeding marine vertebrates from Hornsund, Svalbard. Polar Rec 1989;153:107-114. 31. Weslawski JM, Ryg M, Smith TG, Oritsland NA. Diet of ringed seals (Phoca hispida) in a fjord of west Svalbard. Arctic 1994;47:109-114. 32. Lydersen C, Hammill MO, Kovacs KM. Milk intake, growth and energy consumption in pups of ice-breeding grey seals (Halichoerus grypus) from the Gulf of St. Lawrence, Canada. J Comp Physiol B (in press). 33. Hammill MO, Smith TG. Application of removal sampling to estimate the density of ringed seals (Phoca hispida) in Barrow Strait, Northwest Territories. Can J Fish Aquat Sci 1990;47:244-250. 34. Stifling I. Midsummer observations on the behaviour of wild polar bears (Ursus maritimus) Can J Zool 1974;52:1191-1198.