Camp. B;ochew. Ph,sio/. Vol. 82A. No. 4. pp. 885-889. 19x5 Printed in Great Britain

0300.9629185 $3.00 + 0.00 [c, 1985 Pergamon Press Ltd

ENERGY REQUIREMENTS FOR GESTATION AND

LACTATION IN A DELAYED IMPLANTER, THE

AMERICAN BADGER

HENRY J. HARLOW, BRIAN MILLER, THOMAS RYDER* and LISA RYDER

Department of Zoology and Physiology, University of Wyoming, Laramie, WY 82071, U.S.A. Telephone: (307) 76GJ207; *Wyoming Department of Game and Fish Cheyenne, WY 82002, U.S.A.

(Receioed 11 April 1985)

Abstract-l. Two adult female badgers were water-deprived and/or fasted during the last one-half to two-thirds of pregnancy while a third pregnant female received water ad libitum and was fed meat and dog food.

2. The litter size, birth weights, post partum energy consumption, growth rate, development of homeothermy, tooth eruption and date of weaning, as well as other developmental characteristics, were not significantly different between cubs born to the fed or fasted mothers.

3. The energy demands for gestation are apparently small and are accommodated by fat reserves during periods of food deprivation. However, the calculated energy for lactation is 16 times that of gestation, which is quadruple the expenditure for most mammals.

4. As a result of delayed implantation, the length of gestation and litter weights of badgers are considerably below those predicted from allometric equations.

5. The period of lactation is therefore extremely critical to the survival of both the cubs and lactating adults which require heavy fat stores and possibly torpor to ensure sufficient energy availability during prolonged winter food shbrtage.

INTRODUCTION

Although several investigators have attempted to

analyse food habits (Errington, 1937; Lampe, 1976; Jense and Linder, 1970) and energy requirements (Harlow, 1981a,b; Lampe, 1976) of badgers (Taxidea taxus) under field and laboratory conditions, little is known concerning the energy needs of badgers during gestation and postnatal growth. For example, do predictive allometric equations for gestation and lactation hold true for a mammal engaging in delayed implantation and delivery of altricial young? The cost of lactation is generally 2-4 times the energetic ex- penditure for gestation (Hytten and Thompson, 1968; Myrcha et al., 1969; Nelson and Evans, 1961). How- ever, studies comparing these variables in a delayed implanter such as the badger are not available. As a result of such altricial young, it is reasonable to predict that the cost for lactation in this animal is much higher than in spontaneous implanting mam- mals with more precocial young. In addition to this lack of knowledge on energy needs for gestation and lactation of delayed inplanters, it is not known to what extent food deprivation may influence fetal growth and postnatal development of these animals. It has long been supposed that pregnant mammals under conditions of food deprivation will either reabsorb embryos (Brodie, 1945) or produce young with reduced birth weights (Verme, 1965, 1977; Rob- inette et ul., 1955; Hesselton and Jackson, 1971) as well as developmental impairments that consequently produce higher neonatal mortality (Verme, 1977).

Because badgers are delayed implanters which normally experience extended periods of restricted food intake during winter, it is the purpose of this study to test the null hypotheses that: (1) birth

weights are not below allometrically predicted values with a consequent larger than predicted maternal investment in lactation and (2) food deprivation during gestation will not impair normal fetal and postnatal growth. To address these hypotheses, energy requirements of gestation and lactation were determined on cubs born to fed and fasted mothers.

MATERIALS AND METHODS

Three adult female badgers (Taxidea taxus) were trapped in late August just after the peak of the breeding season in SE Wyoming (42”OO’N 105”2O’W). These animals weighed an average of 9.5 kg. They were maintained in 1 x I rn’ stainless-steel cages to which were attached wooden nest boxes. Badgers were exposed to a light-dark cycle simulating a natural changing photoperiod and were fed ad libitum a combination of Purina dog chow and meat until March. Approximately 1 month prior to the expected date of parturition, one badger was deprived of food (DF) for 30 days but given water ad libirum, another was deprived of both food and water (DFW) for 20 days and the third was provided both food and water (C) ad libitum. Following parturition all fasted females were again given food and water ad libitum.

The cubs from the control mother (C), and the cubs from DF, were weighed daily. The postpartum time for devel- opment of such characteristics as eye opening, eruption of deciduous and permanent teeth, weaning and leaving the nest were noted. In addition the rectal temperature of cubs was measured using a YSI telethermometer. The cubs were removed from their mothers at 4 days of age and fed with a milk substitute (Esbilac) until 45 days of age, then switched to a combination of milk substitute and dog food (Purina Cycle 1 puppy chow). The heat of combustion of the milk substitute was 767cal/ml, and the dog food was 1.25 kcal/g wet wt as determined by bomb calorimetry using a Phillipson microbomb. The quantity of these substances

885

HENRY J. HARLOW et al. 886

IO 20 30 40 50 M) 70

TIME AFTER BIRTH (DAYS)

Fig. 1. Body weight gain (kg) for the first 70 days post- parturition of three badger cubs born to fed mothers, a cub born to a mother fasted for 30 days and 2 cubs born to a

mother fasted and deprived of water for 20 days.

consumed by each cub was carefully monitored and con- verted to kilocalories. Offspring from DFW were weighed at birth and allowed to remain with their mother. These cubs periodically were taken from their mother to examine developing characteristics and to be weighed. In a previous season, 2 cubs were born to a captive badger maintained on food and water ad M&urn. These cubs were hand-reared in a manner identical to that described above and periodically weighed from birth through the first 70 days of life. The postpartum time for development of such characteristics as previously described were also noted. A Student’s t-test was used for comparisons between the mean body weights and an F statistic was used for comparison of the sum-square error between regression lines of weight gain (Neter and Wasserman, 1974).

RESULTS

The DF mother lost 1.9 kg body mass (15% of total body mass in 30 days). She produced 2 cubs which weighed 86 and 93 g. Two cubs weighing 102 and 110 g were produced by the DFW mother. This mother lost 1.1 kg body mass (13% of total body mass in 20 days). The control mother produced two cubs weighing 89 and 92 g. In addition, in a previous season, a mother badger on ~~li~i~u~ food and water also produced 2 cubs weighing approximately the same (89 and 95 g) as this control litter. And the postnatal growth rates of these cubs were not significantly different from the growth rates of cubs from the fed mother in this study during the first 70 days of development (Fig. 1).

There did not appear to be a reduction in birth weight of badger neonates as a result of depriving the

mother of food and/or water during gestation com- pared to cubs from fed mothers. In addition there were no apparent differences in postnatal growth between cubs from fed and fasted mothers. Body weight increase of cubs from fasted mothers was not significantly different from the cubs of fed mothers during the first 70 days of development (Fig. 1). However, the young from the fed mother appeared to have a somewhat higher growth rate than the average rate of cubs from fasted mothers (Fig. 2). This occurred even though the hand-reared cubs from fed and fasted mothers had approximately the same daily caloric intake (Fig. 3). Solid food in the diet dra- matically increased the daily caloric consumption by hand-reared cubs (Fig. 3), however, this was followed by a reduction in growth rate (Fig. 2) for all cubs for approximately IO days, perhaps as as result of a lag time required for the gut digestive flora to change.

The rectal temperature of hand-reared pups from both fasted and fed mothers was 35°C at birth which fluctuated erratically between 31 and 35C for the first 2 weeks. At the age of 16 days, the fur had thickened and darkened and was associated with a fully developed homeothermic state with a stable body temperature of 36°C. There were no consistent differences in the rate of development as indicated by the post-parturition date for eruption of teeth, open- ing of eyes or the commencement of weaning between cubs from fasted and fed mothers. The average time of development for these and other traits for all cubs is reported in Fig. 4.

DISCUSSION

Food deprivation during gestation in badgers ap- parently does not impair normal fetal and postnatal growth. This is consistent with the badger’s winter

I6 2’0 3’0 40 50 $0 70

TIME AFTER BIRTH (DAYS)

Fig. 2. Growth rate (g/day) of a badger cub born to a fed mother and an average of 3 badger cubs born to fasted

mothers during 65 days post-parturition.

Gestation and lactation energy requirements 887

l

. YawiS FROU A FED MDTHER

. You16 FROM A FASTED YOTILR

i

r

SOLID FOOO fN THE InET

IO 20 30 40 50 60 TIME AFTER BIRTH (DAYS)

Fig. 3. Energy consumed (kcal/day) during the first 55 days post-parturition of a badger cub born to a fed mother and

a badger cub born to a mother fasted for 30 days.

habits. In northern latitudes it is exposed to long winters characterized by low temperatures and food scarcity (Lampe, 1976). In addition, the badger is not known to cache large quantities of food during winter but copes with extended intervals without food and water while restricted below ground (Harlow, 1981a). A potential compounding factor to food deprivation and cold exposure during the winter is the energy demands of gestation. Although ovulation and con- ception in the badger occurs in August when food is plentiful (Hamlett, 1932) and fat stores are being accumulated (Harlow, 1981a), implantation of blas- tocysts occurs in March and April when food is scarce (Long, 1972) and fat reserves are being de- pleted (Harlow, 1981a). If energy demands associated with environmental conditions are extensive, either in magnitude or duration, the developing embryo may be absorbed or the prenatal development may be impaired, resulting in fewer numbers of young per litter, reduced size of individuals at birth or an impaired growth rate of the young which could potentiate a higher postnatal mortality. For example, Verme (t962, 1963) reported that poor nutrition greatly influences fetal development of white-tailed deer, especially during the final stages of gestation. Fawns from poorly fed mothers weighed less than fawns from fed mothers and nearly all of them died. A similar relationship is evident in other animals such as pronghorns (Martinka, 1966), elk (Green, 1950) and bears (Rogers, 1976). However, the badger moth-

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,O ESTIMATED DAY3 3~ FROM IWLANTATION

:YES BEQINNW TO OfEN

HEAD STRIPE fORhUN

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ANINES ERUPTINO

rPREMOLARS ERlJfYlNQ

rOBSERVED OUT Of NESTING BOX

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WEANED fROY MILK TO SW0 FOOD

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Fig. 4. The course of development for badger cubs from fasted and fed mothers.

888 HENRY J. HARLOW et ul.

ers in these experimental conditions of food de- privation lost between 13 and 15% of their body mass during gestation but still gave birth to young of the same size and condition of health as young from a fed mother.

Two factors may be involved which allow for normal gestational development of badgers during food deprivation. First, the cost of gestation may indeed be small enough to present only a minimal additional energy demand on the mother. Second, the badger may store sufficient fat reserves to maintain fetal growth even under prolonged periods of im- paired food intake. When considering the first factor, the energy required for fetal tissue production can be calculated as an increase in maternal body mass because the fetus behaves metabolically as a part of the maternal organism rather than as an independent homeotherm (Kleiber, 1975). The average body mass of badger cubs at birth was 94.9 g. With an average caloric content for mammalian tissue of 1.4 Cal/g (Eisenberg, 1981) the energy content of a litter of 2 cubs would be 265.7 kcal. Golley (1960) reported that the growth efficiency of the weasel was 26.8%. If we assume that the growth efficiency of the badger is similar to weasels and that the growth efficiency of the fetus is similar to the adult, then the energy demand upon the mother to produce 2 cubs aver- aging 94.9 g each would be 991.4 kcal.

In a previous study, non-pregnant badgers, weigh- ing an average of 9.7 kg, metabolized a total of 373.6 kcal/day which was reduced to 213 kcal/day after 20 days without food (Harlow, 1981a). As- suming the decrease in metabolism and weight loss was linear, the total energy expenditure for the non-pregnant female during a 20-day fast can be estimated to be 52,317 kcal. The period between implantation and parturition of a badger is about 40 days (Personal communication, Wright, University of Montana, Missoula, 1984) with the greatest energy expenditure occurring during the last one-third of pregnancy (Moen, 1973). Therefore, if the above- mentioned female were pregnant and fasted during the last 20 days of gestation, the energy cost of gestation could be estimated at being less than a 2% increase in the metabolic requirements.

It is interesting that the allometric equation pre- dicting litter weight for a mammal (Y = 0.97 W” 92; Blueweiss et al., 1978) does not appear to apply to the badger. For example, a 9.5 kg badger would be expected to produce a litter weighing 1005 g but in fact produced a litter of 200 g. Indeed this may be a result of its short gestation length of only 40 days as contrasted to the predicted 119 days based upon body mass (Y = 11 I+““; Blueweiss ef al., 1978). In fact, simply to be monogamous implies the production of altricial young with low maternal investment at birth (Zeveloff and Boyce, 1980). However, it is possible that as a result of delayed implantation the badger has an unusually short gestation period resulting in even lower parental investment for gestation. Con- sequently food deprivation during pregnancy may have little effect on prenatal growth and devel- opment.

However, the energy cost of lactation has a greater consequence on the mother. Assuming that the cal- oric content of badger milk is similar to that of

Esbilac (767 Cal/ml) and that the energy required for milk production by the mother is 1.6 times the energy content in the milk (Crampton and Harris, 1969) then by extrapolating the data from Figs 2 and 3, it is apparent that the badger cubs demanded a meta- bolic expenditure of approximately 16,832 kcal prior to the initiation of weaning. The caloric requirements for nursing 2 cubs over this 40-day period is therefore about 16 times more demanding than gestation.

This is an extraordinarily high ratio compared to other mammals. The cost of lactation is generally 24 times that of gestation (Migula, 1969; Myrcha et ul.,

1969; Nelson and Evans, 1961). However, for a delayed implanter whose length of gestation and birth weights are tremendously below that predicted for instantaneous implanters it would be expected that the cost of lactation would be considerably greater. In order to make up for this altricial condi- tion, the badger cub would either have to have a high growth efficiency or place large demands upon the mother for milk. Growth efficiency of 45-day old cubs can be determined from the caloric equivalence of the tissue mass divided by the total calories consumed for 45 days (Figs 2 and 3). The average growth efficiency for the cubs was 27% which is not significantly greater than for other mammals (Golley, 1960; Kleiber, 1975). These altricial young must therefore put a large postnatal demand on the mother for very rapid tissue growth during the nursing period.

We conclude that the influence of food deprivation on the fitness of the mother and offspring does not appear during gestation but rather lactation. In order to insure its gentic investment in healthy neonates during winter cold and food scarcity, the mother must maintain ample energy reserves. Even though the badger loses considerable body fat during January and February, it still has about 20% of its body weight as fat reserves in March (Harlow, 198 la) to provide for energy demands during lactation. The badger also has the capacity to reduce its energy requirements by undergoing periodic torpor (Harlow, 1981a), the savings of which could potentially be spent to maintain lactation. As an alternative strategy to insure continuous milk production, the badger mother may periodically leave the natal den to search for food. The female fisher (Mavtes pennanti) often leaves its offspring in the den for several hours during which time it is believed that the cubs undergo torpor (Powell and Leonard, 1983). If badger cubs have the ability to become torporous, this would also reduce the demands upon the lactating female, thereby help- ing to insure survival through the critical late winter period.

Acknowledgements-We thank Mr Lawrence Atkinson for help in trapping female badgers, Stan Lindstedt for insight into allometric condsiderations and Larry Irwin for his helpful comments on the manuscript. This research was supported, in part, by a University of Wyoming Grant-in- Aid to the Senior author.

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