This paper not to be cited without prior reference to the authors International Counci1 for the
Exploration of the Sea
CH 1982/N:] 5
Harine Haxr.ma1s Connnittee
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!HE ENERGY COSTS AND EFFICIENCY OF LACTATION IN GREY SEALS
Shei1a S Anderson and Michael A Fedak
Sea Mamma1 Research Unit, Natural Environment Research Counci1
c/o
British Antarctic Survey, Mading1eyRoad, Cambridge CB3 OETABSTRACT
Fema1e grey seals transfer 1arge amounts of energy rapid1y and efficient1y to their pups. Using information from seria1 weighings and from carcase' analysis we have ca1cu1ated the energy costs of reproduction and the efficiency of lactation for fema1e grey seals. Fema1es use over ]25.6 MJ/day for maintainance and milk production. Pups conSUI!le 7].2 HJ/day in milk and can convert 58.6 HJ/day into growth and stored fat. The gross
efficiency of.the transfer from mother to pup is about 577.. Over 807. of the fema1es' energy reserves are used to feed their pups. This massive transfer of resources in a short time per iod is thought to be an adaptation of an offshore aquatic feeder which has to return to land to give birth.
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Les femelies des phoques gris transferent beaucoup'd'€nergie, d'une facon rapide et efficace; aleurs jeunes. En uti1isant 1es donnees obtenues des pes~es en serie et de l'ana1yse des carcasses, nous avons calcule 1es depenses d'energie de 1a reproduction et l' efficacite de 1a 1actation chez les. feI!lelles des phoques gris. Les feme11es depensent plus de ]25.6 MJ/jour pour l'entretien et 1a
production de 1ait. Les jeunes consomment 7].2 HJ/jour en lait et ils ont 1a capacite de convertir 58.6 }U/jour en croissance et en graisse de reserve. L'efficacite brute du transfert de mere a'jeune est environ 57h. Plus de 80% des reserves d'energie des femelies sont utilisees.a nourrir 1eurs jeunes. On considere ce transfert enorme de ressources en peu de temps.comme l'adaptation necessaire d'un mannnifere marin qui est ob1ige de rentrer a 1a terre pour donner
naissance. ' .
INTRODUCTION
The grey seal (Ha1ichoerus grypus) is the most numerous seal species in British waters where the population isapproachin~85,000 and may still be increasing. Fishing and conservation interests both hold strong opinions on the management of this population, usually arguing for opposed policies. The resources consumed by the species are a subject of controversy, but it is difficult.to make field observations on food consumption of an aquatic mammal. A more profitable line of approach may be to measure the aniI!lals' energy
requirements. We report here on the energy costs experienced by female grey seals during the breeding season, a study which forms the first part of a wider investigation on energy flow through the grey seal population.
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fat reserves during the non-breeding period of the year while the foetus is developing. In the autumn British seals come ashore for 2-3 weeks to give birth and feed their pups. After this short period they mate and return to
the sea leaving their pups to live on stored fat, in the form of blubber, for 1-4 weeks until they enter the sea and learn to feed themselves.
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Lactation is therefore abrief period of intense energy demands for females: Iri grey seals the demands are met entirely from stored fat reserves. The
loss of weight of females can be used to measure the energy costs of lactation, which in this species represents the total investment in maternal care. By weighing females and their pups repeatedly throughout the lactatio~period we determined the daily weight loss of females and the weight gained by the pups. From measurements of the calorific density of the tissues lost and gained, we were able to calculate the amount of energy used by females for maintainance and milk production; and to estimate how much of the energy
received in the form of milk was used by the pups for maintainance, growth and blubber production.
METHODS
During October 1979 we measured weight changes in 14 pairs of mothers and pups at North Rona, Outer Hebrides, which lies 47 miles NVT of Cape Wrath, Scotland,~
and where there is a breeding colony of c2,500'female grey seals, (Summers, Burton &Anderson, 1975). We immobilized adult females using a mixture of ketamine hydroc'il1oride (Vetalar, .Parke -Dav{s"/Warner Lambert, _Usk -Road~.. ~'- .. Pontypooi, Gwent, NP4'8YH, UK) and xylazine (Rompün, Bäyer UK Ltd, Eastern Way, Bury St Edmunds, Suffolk, IP32 7AH, UK) in the approximate ratio of 5ketamine.to 1 xylazine by weight (Parry, Anderson and Fedak, '1980), but the pups' could be handled without being tranquillized. When a drugged female was tractable, it was weighed on a stretcher placed across two bathroom-type scales which were resting on tripod stands with adjustable
legs to allow for irregular terrain. After the weight was recorded, we placed the·animal on the ground, took standard body measurements and tagged it for . future identification; It was then released and allowed to recover. At the
same time .the pup was weighed in a sling. suspended from a hand-held spring balance and,after tagging, was released near its mother. The accuracy of weighing was ± 2kg for adults and ± 0.5kg for pups. This procedure was repeated near the end of the lactation period when we considered that the female was About to leave (ie if the mother began to hok very thin and/or was receptive
to bulls). Seven of the 14 pairs of animals were also weighed at the end of lactation and then about one week later in order to measure weight loss of
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unfed pups. Environmental conditions during the study period were recordedby taking weather readings twice daily~
RESULTS
Environmental conditions
The weather conditions faced by the animals during lactation varied little, with the exception of wind which occasionally reached force 10 on the Beaufort
scale. The average wind velocity during the study period was 8 m/s. The temperature averaged looe (range 30-140
) and relative humidity 95% (range
90-100%). Rain fell on 17 of the 27 days of the study, usually in brief showers. Weight changes
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rate observed in pups is the same as that reported e1sewhere (Boyd
&
Campbe11~1971; Coulson &Hickling~ 1960). There is no consistent change in the rate of weight 10ss or gain with the size of the female~ the date of birth or the e1apsed time of 1actation~ Pair (i) is an interesting exception; part way through lactation the mother's rate of weight 10ss increased about 30% whi1e her pup's growth rate near1y doub1ed. We have no explanation for this. From our sma11 samp1e size~ it appears that 1arge mothers did not fatten their pups more quick1y than sma11er mothers. The rate at which pups gained weight stayed constant throughout lactation and did not seem to depend on whether the pup was born ear1y or late in the breeding period. Since weight change was a linear function of time~ all the data cou1d be norma1ized by plotting weight change as a function of time. (Fig 2). The slope of the regression of female weight change against day of lactation~ which was constrained to go through
the origin~ was 3.60kg/day with a standard deviation of O.llkg. A simi1ar linear regression for pups gave an average weight increase of 1.64kg/day with standard deviation of 0.05kg.
Calculation of energy equivalents
Using an average lactat ion period of 18 days (Bonner~ 1972)~ the total average weightloss of fema1es wou1d be 65kg whi1e pup gain wou1d be 30kg. We can use
these data to estimate the energy exchange between females and pups by combining them with.information from carcase analysis of females and pups in .early and 1ate lactat ion (Sea Mamma1 Research Unit~ unpub1ished data).· ~he carcase analysis showed that most of the weightloss in females resulted from loss of fat stored in b1ubber and ~~sc1e and the average energy va1ue of this weight 10ss was 34.7 kJ/gm. By mu1tip1ying average weight 10ss by this energy va1ue we calcu1ate that fema1es use approximate1y 125.6 MJ/day to maintain themse1ves and produce milk. These measurements of energy utilization during lactation are remarkab1y sici1ar to estimates for Canadian harp seals (Phoca groen1andica) made by Stewart and Lavigne (in press)~ based on the carcase analysis of large numbers of females ear1y and late in lactation. The average.energy value of
the weight gained by the pups was 26.8 kJ/gc and 70% of the joules gained were in.the b1ubber (S}ffiU unpub1ished.data). From theweight gain in pups we can ca1culate that pups are storing on average 44~0 HJ/day, but they will be assimi1ating more to ac count fortheir dai1y metabolie requirements. We can estimate·this metabolie requirement from the weight 10ss of weaned pups which was 0~53kg/day (SD = 0.090, n =34). Thus, pups require about 14.6 MJ/day for dai1y metabolism, and pups being fed assimilate 58.6 MJ/day. There are no : figures available for the efficiency with which seal pups convert milk into
stored or metabolizab1e energy, but assuming sicilar estimates to those for deer and dairy cows of about 80% (}~en, 1973);then pups must be receiving about
1.2 }U/day in milk. Since grey seal milk has an averageca10rific density of 22.3 MJ/gm (L McConne11; pers. comm)~ this wou1d amount to near1y three kg .of milk per day.
Energetic efficiency of lactating fema1&a
Of the 125.6 HJ/day used by the female; we estimated that 71.2 }U/day appear as milk, and the remainder is used for maintenance requirements and activity~
This corresponds to a grass efficiency, as defined by Brody (1945), of 57%. Thus 57% of the energy in the mother's mobilized reserves,is avai1ab1e to the pupfor maintenance or growth. The'dai1y resting metabolism~ estimated from oxygen consumption on two 160kg non-1actating. grey seal fema1es,on land was on average 4~800kca1/day (20.1MJ/day) (S}ffiU unpub1ished data). Female grey seals therefore increase their dai1y energy use by a factor of six during
lactation. .
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The relatively high efficiency measured in the g~ey seal is prohably; in part, due tri the fact that the seal is producing milk from stored reserves while the goat, cowand rat are producing milk, at least in part,from food eaten during lactation. Thus, they incur the energy costs associated with ingestion and assimilation. These costs have been paid by the seal earlier in the year. There is a sma11 additional cast to be paid for first converting food energy to stored fat and thenmilk., In dairy cows this additional cast amounts to a 25-307. increase in ingested energy required (Flatt &Moe, 1971). These considerations must be kept in mind when comparing the energy costs of
1actation'in different animals. However, the six fold increase in the use and output of'energy in grey seals is much higher than that reported for other species (Randolph ~ al, 1977).
Female grey seals look very thin when they leave their pups, compared with their rotundness at the start of nursing. The 65kg of weight,which they lose, largely fat, represents about 2260MJ assuming a weight lossequiva1ent of 34.7kJ/gm. How does this amount compare to the total energy reservesbrought ashore? The average weight of females at the start of lactation was 179kg. The scu1p
(blubber-plus skin) makes up about 407. of the weight of immediately pre-partum fema1es (Mansfield, 1977), and about 10kg of this is skin and hair.' A further
10% of the remaining carcase is fat (Stewart &Lavigne, in press). Thus, a ~
fema1e of 170kg brings ashore about 68kg of stored fat. As the ca10rific density of fat is 9.45kca1/gm (39.5kJ/gm) (Paine, 1971) we can.estimate that an average fema1e brings ashore 2686 MJ stored as fat. On average fema1es are therefore using around 84% of their energy reserves during lactation. The remaining 16% may weIl be important for insulation when the seal re-enters the sea.
DISCUSSION
The postnatal care of grey sealoffspring is contributed solely by females and is intensive though short in duration. The lack of variation in the weight lass or gain of mother/pup pairs is independent of fema1e size and stage of lactation, indicating that raising a pup successfully incurs a fixed cast to the female. As we have shown, this cast is high iri energy terms and must make a relatively greater drain on small compared with large females. As yet we have no
information on the effect that high demand on an individual's body resources may have on future reproductive success of survival. Although we describe the
energy costs as high; the total costs of lactation may be similar to that of other animals: the significant point is that the grey seal female's energy ~ output is raised hy a factor of six during aperiod that she is dependent on her stored resources. The calculated milk yield of about 3kg is comparable to
that which can be derived from the equations of Hanwe11
&
Peaker (1977) foreutherian marnmals, but the energy value of the milk; according to their equations, would be only 14.6MJ/day. The much higher energy value of 71.k~/day calculated' for grey seals is achieved by the high fat content of the milk which is in
excess of 50% (Amoroso, Gaffin, et al, 1951). It seems certain that, in
energetic terms, lactation is the-most critical period of the annual cycle for the success of reproduction. The amount of stored energy available at the start of lactation ~ust represent a significant fraction of the seal's yearly energy budget. The condensation of parental investment into a short span is typical of northern phocid seal breeding systems. The most extreme example is the harp seal which has a nine-day suckling per iod during which the pups gain weight at the rate of 2.5kg/day (Stewart
&
Lavigne, 1980). The short lactation period can be seen as an adaptation of mammals which feed off-share but have ,to return to land or ice to give birth. At sea, phocid seals have few predators,•
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that reducing time spent ashore to a minimum has been advantageous.
However, there is a good energetic reason for minimizing the length of time spent suckling in a situation where the mother depends entirely on stored
energy reserves to produce milk. Since the female has to meet her own metabolie needs from these reserves, the faster lactation is completed the greater fraction of these reserves can be made available to the pup. In a sense, rapid lactation allows a reduced "overhead cost" to be realized.
ACKNOWLEDGEHENTB
We are grateful to Kathy Parry and Kees Zoon for assistance in the field and to John Harwood and David Lavigne for helpful comments on-the manuscript. This work was partly funded under EEC contract ENV 405-80-UK(B).
REFERENCES
Amoroso, E. C., Goffin, A., Halley, G., Matthews, D. J. (1951). Lactation in the grey seal. J. Physiol., 113:4-5 •
Bonner, W. N. (1972). The grey seal and common seal in European waters. Oceanogr. Mar. Biol. Ann. Rev. 10:461~507.
Boyd,.J. M. & Campbell , R. N. (1971). The grey seal (Halichoerus grypus) at North Rona, 1959-1968. J. ZooI., 164:469-512.
Brody, S. (1945). Bioenergetics and growth. Hafner, New York, p820-843. Coulson, J. C. &Hickling, G. (1960). Grey seals at the Farne Islands
1958-1959. Trans. Nat. Hist. Soc. Northumberland, Durham and Newcastle-upon-Tyne, N. S• 13 : 15I -I78 •
Flatt, W. P. &Moe, P. W. (1971). Partition of nutrients between lactation andbody weight gain in 'dairy cattle.· In Lactation, p341-347. I. R. Falconer (ed). Butterworths, London.
BanweIl, A. &Peaker, M. (1977). Physiological effects of lactation on the mother. Symp. zool. Soc. Lond. No 41:297-312 •
Mansfield, A. W. (1977). Growth and longevity of the grey seal, Halichoerus grypus in eastern Canada. ICES Marine Mammal Committee GM 1977/N:6. Moen, A. N. (1973). Wildlife Ecology: An Analytical Approach. W. H. Freeman,
San Francisco.
Paine, R. T. (1971). The measurement and application of the calorie to ecological problems. Ann. Rev. Ecol. Systematics. 2:145-164.
Parry, K., Anderson, S. S. &Fedak, M. A. (1981). Chemical immobilization of grey seals. J. Wildl. Manage. 45(4):986-990.
Randolph, P. A., Randolph, J. C., Mattingly, K. & Foster, ~f. }1. (1977). Energy
costs of reproduction in the cotton rat, Sigmodon hispidus.Ecology58(1):31-45 Stewart, R. E. A. &Lavigne, D. }f. (1980). Neonatal growth of northwest
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Stewart, R. E. A. &Lavigne, D. M. (in press). Pinniped bioenergetics.
!n:Perspectives in Vertebrate Science. Vol2. Lavigne, D. M., Ronald, K. and Stewart, R. E. A. (eds).
Stirling, I. &Archibald, W. R. (1977). Aspects of predation of seals by polar bears. J. Fish. Res. Bd. Can. 34: 1126-1129.
Summers, C. F., Burton, R. W. &Anderson, S. S. (1975). Grey seal (Halichoerus grypus) pup production at North Rona: a study of birth and survival
statistics collected in 1972. J. Zo01., Lond. 175:439-451.
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FEMALE WEIGHT
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Figure 1. Weight loss of laetating grey seals and eorresponding growth of their pups on North Rona. Eaeh mother/pup pair is indicated by a letter. The" estimated stage of laetation at the start of measurement of eaeh pair is
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Figure 2. Weight changes of grey seal mothers and pups. The data have been normalized so that starting weight and the time of the first weighing are equal to zero. Average rates of loss and ga in have been determined from the slope of the least squares regression line through the points forced through the origin. The average weight gain of females is 3.60 kg/day (Sn
