AMER. ZOOL., 28:863-875 (1988)

Energy Allocation in Mammalian Reproduction'

JOHN L. GITTLEMAN Department of Zoology and Graduate Programs in Ecology and Ethology, University of Tennessee, Knoxville, Tennessee 37916

AND

STEVEN D. THOMPSON Department of Zoological Research, National Zoological Park, Smithsonian Institution, Washington D.C. 20008

SYNOPSIS. On behavioral, hormonal, and physiological grounds, mammalian reproduc- tion can be compartmentalized into the following continuous sequence of events: mating (courtship, estrous), , parturition, lactation, post-lactational , and maternal recovery. We point out that comparing the relative allocation of energy for these events across is difficult because of life history variability (e.g., litter size, weight), allometry, phylogeny, and individual variation. We review the empirical and theoretical literature on each of these events with respect to: different methodologies in measuring energy use; broad patterns of energy consumption across diverse mammalian taxa; and, identification of particular reproductive characteristics {e.g., birthing, parental care) which may be costly but have yet to receive energetic measurements. Although most studies have considered gestation and lactation the critical reproductive events for energy expenditure, variation in these events is substantial and almost certainly is a function of relative allocation of time to gestation vs. lactation as well as the presumed energetic costs of mating, birthing and parental care. In addition, repeated observations show that behav- ioral compensation is an extremely important strategy for minimizing energy requirements during reproduction. From this review, we argue that more complete analyses will come from (1) incorporating energetic measurements in studies of mammalian behavior and (2) including mechanisms of behavioral compensation into physiological studies.

INTRODUCTION ing from a current reproductive event Energy use during mammalian repro- (Trivers, 1972). Parental investment has duction has received considerable atten- typically been assessed via either behav- tion in recent years (see Harvey, 1986; ioral parameters, such as suckling fre- Loudon and Racey, 1987), particularly in quency or duration (e.g., Ortiz et ai, 1984; association with studies of , Costa and Gentry, 1986), or net produc- sex allocation, and parental investment. tion {e.g., litter mass at birth or weaning). Studies usually fall into one of two broadly In contrast, physiologists have studied defined categories: those concerned pri- energetic costs of reproduction by moni- marily with evolutionary (=fitness) conse- toring caloric intake, net production, met- quences (e.g., Clutton-Brock et al., 1982; abolic rate, and/or daily energy expendi- Ortiz et ai, 1984) or those interested in the ture (DEE) during specific reproductive energetic (=physiological) costs associated events (usually gestation or lactation), in with varying reproductive patterns {e.g., an attempt to understand the energetic Smith and McManus, 1975; Glazier, 1985è; consequences of variation in parameters Mattingly and McClure, 1985). Evolu- such as body size, litter size, and fecundity tionary biologists and behavioral ecologists {e.g.. Glazier, 1985a, b; Mattingly and have been primarily concerned with paren- McClure, 1985). One aim of this paper is tal investment, defined as costs to an indi- to emphasize the importance of both vidual's future reproductive success result- behavioral and physiological techniques for the study of energy use during reproduc- tion. We hope to show that (1) precise mea- surements of energetic constraints and ' From the Symposium on Energetics and Animal Behavior presented at the Annual Meeting of the consequences of reproductive behaviors American Society of Zoologists, 27-30 December must be incorporated into studies of mam- 1986, at Nashville, Tennessee. malian behavior and (2) behavioral flexi- 863 864 J. L. GiTTLEMAN AND S. D. THOMPSON

bility {e.g., in duration and/or frequency) nal recovery from reproduction (Elwood may dramatically alter the relative ener- and Broom, 1978). getic costs of specific reproductive events Second, most mammalian reproductive (see also Goldstein, 1988). Although we events and various energetic constituents primarily address problems related to are correlated with body size (see Eisen- mammalian reproduction, we believe a berg, 1981; Calder, 1984; Millar, 1984; general merging of energetics and behav- Schmidt-Nielson, 1984; Gittleman, 1986). ioral perspectives, encompassing multiple Resting metabolism (Kleiber, 1961), exis- measures of costs, will foster more com- tence metabolism (Kendeigh, 1969), birth plete analyses of the costs of reproduction and weaning masses (Millar, 1977), birth in most organisms (see also Bronson, 1979; weight (Leitch et ai, 1959), and gestation Calow, 1981, 1984; Altmann, 1983, 1986; length (Kihlström, 1972; Eisenberg, 1981), Knapton, 1984; Bennett, 1986; Costa and among others, demonstrate an exponential Gentry, 1986; Halliday, 1987). relationship to body size where the expo- nent of these relationships is < 1.0. In con- PROBLEMS AND PERSPECTIVES IN THE trast, functions describing capacity terms, COSTS OF MAMMALIAN REPRODUCTION for example digestive capacity (Kleiber, On behavioral (Eisenberg, 1981), hor- 1961) and storage capacity (Calder, 1984), monal (Rosenblatt and Siegel, 1983) and bear a nearly linear relationship to body physiological (Millar, 1977) grounds, mass. These allometric relationships affect mammalian reproduction can be compart- the relative ability of mammals differing in mentalized into the following continuous size to respond to periods of energy depri- sequence of reproductive events: mating vation or abundance. All else being equal, (courtship, estrous period), gestation, a larger can store proportionally parturition, lactation (suckling period), more energy and, likewise, draw upon pro- post-lactational parental care, and post-lac- portionally more reserves than a small tational/post-parental care maternal mammal (Lindstedt and Boy ce, 1985); as recovery. Most energetic studies have extreme examples, some large mammals focused on either caloric consumption or such as lactating gray seals (Davies, 1949), maternal metabolic rate, in conjunction rutting red deer (Mitchell et al., 1976), and with changes in maternal (during gesta- many lactating seals (Bartholomew, 1952; tion) and offspring mass, during only one Bowen et al., 1985) exclusively depend on reproductive event (usually gestation or an ability to fast through reproductive lactation). Although an evolutionary per- events. Many large mammals store energy spective requires that relative values of for carryover from one reproductive event these measures be used in comparisons of to another, usually from to lac- energetic costs of mammalian reproduc- tation, which may confound the relative tion, both within and between species, cost of each. This carryover is a particu- recent detailed studies show that, for sev- larly difficult problem when pregnancy and eral reasons, comparative statements are lactation events are studied separately. difficult to make. Third, comparative studies have repeat- First, even though mammalian repro- edly shown that phylogeny is an important ductive events appear discrete, intrinsic component to life history evolution (see variability in parameters such as birth Stearns, 1983; Harvey and Clutton-Brock, weight, litter size, weaning age, weaning 1985; Gittleman, 1986, 1988a). Life his- weight, and inter-birth interval, both within tory factors are often coupled with ener- and across species, often confound com- getic constraints (see McNab, 1980; Lind- parisons of energy expended during re- stedt and Calder, 1981; Calder, 1984), and production. For example, larger litters de- it follows that phylogeny may play an mand greater energy expenditures during important role in setting energetic costs, lactation (Millar, 1978; Mattingly and even at lower taxonomic (familial, generic) McClure, 1982; Glazier, 1985¿) and, in levels. For example, Kenagy and Barthol- some small mammals, produce slow mater- omew's (1985) study of reproductive pat- ENERGETICS AND MAMMALIAN REPRODUCTION 865 terns in five coexisting desert shows ular reproductive characteristics {e.g., male that, although the diurnal antelope ground ejaculate; parturition; paternal care) which squirrel {Ammospermophilus leucurus) is sym- may be costly but have yet to receive ener- patric with four nocturnal heteromyids, its getic study. timing of reproduction and reproductive effort are more similar to marmotine squir- ENERGETICS OF MAMMALIAN rels (ground squirrels, marmots, prairie REPRODUCTIVE EVENTS , chipmunks) than to the heteromyids. As the authors conclude, "The comparison Mating of A. leucurus with D. merriami [ Mating behavior includes interactions rat] illustrates the importance of consid- between a male and female in a situation ering whole suites of functional, reproduc- that leads to . These interac- tive, and life history traits when one exam- tions include investigatory behavior (mate ines adaptation to a particular environment. searching), mounting, lordosis, intromis- It also shows that the fixity of a series of sion, and any observable characters in the genotype can be a barrier postcopulatory interactions. Although each ("phylogenetic constraint") to the evolu- of these behaviors has been extensively tion of a major change in life history." analyzed from hormonal, neural, evolu- Fourth, experimental studies make it tionary, and genetic approaches (Beach, apparent that within single populations 1965; Diakow, 1974), energetic studies are individuals vary considerably in the quality still lacking. This is ironic considering that and quantity of maternal care, energy uti- some of the earliest studies in ethology used lization, and ability to produce milk, all of energetic terms. For example, a classic par- which will tilt the balance of energy costs adigm in studies of mating tested for the (Bronson and Rissman, 1986; Thompson number of ejaculates before an individual and Nicoll, 1986). In domestic rats, for reached "exhaustion" {e.g.. Beach and Jor- example, we know that such variation dan, 1956; Tiefer, 1969), with the pre- relates to heredity, neonatal development, sumption that a male's energetic capacity prior maternal experiences (age), and psy- was practically "unlimited." chological state {e.g., Denenberg ei al, Apparently only one study has directly 1962; Morton etal, 1963). Although indi- measured energy consumption during the vidual differences provide case studies for mammalian mating period. Kenagy (1987), examining adaptive allocation of energy in working with golden-mantled ground fitness terms, i.e., life-time reproductive squirrels {Spermophilus saturatus), found that success (see Charnov, 1982; Clutton-Brock, energy expenditure (kj/day; measured 1985; Stewart, 1986), small sample sizes using doubly labeled water) in males is and high variability should demand cau- 2.5 X BMR and in females 2.0 x BMR, tion, even when extrapolating between the difference mainly due to greater body closely related species. mass in males. The total energy expendi- In addition to the above difficulties, few ture during mating is only slightly greater studies have directly measured energy costs than periods outside of reproduction. in mammalian reproduction and the meth- Many behavioral studies have suggested ods vary greatly from study to study that the energetic costs of mating are sig- (Randolph et al, 1977; Millar, 1978; nificant. Males of larger species tend to McClure and Randolph, 1980; Glazier, show significant increases in activity levels 1985a, b; Costa and Gentry, 1986; Kunz (frequency and duration), decline in feed- and Nagy, 1987). Thus, our discussion of ing, and loss of as much as 20% body weight the relative energetic costs of reproductive during mating (McCullough, 1969). In male events will focus on: (1) different meth- red deer the proportion of daytime spent odologies in measuring energy use, (2) grazing fell from 44% outside of the breed- broad patterns of energy consumption, ing season to less than 5% during the rut across diverse taxa, for specific reproduc- (Glutton-Brock et al, 1982); similar pat- tive events, and (3) identification of partic- terns are observed in other ungulates 866 J. L. GiTTLEMAN AND S. D. THOMPSON

(Struhsaker, 1967; McCullough, 1969). In reduced numbers of in successive general, females do not appear to incur ejaculates (Dewsbury and Sawrey, 1984), large energetic demands while mating. often for periods of up to a week, and lim- Nevertheless, some energetic costs are sug- itations of other hormonal substances crit- 9 gested because stress induced situations, ical to successful mating; in , when such where food resources decline, cor- weight loss is in the range of 25% normal relate with decreases in length of breeding body weight, sperm production ceases season, breeding success, and estrous (Frisch, 1984). Furthermore, repetitive cycling (see Sadleir, 1969). It should be copulation for pregnancy initiation, female pointed out that a primary problem in choice and control, and risks of searching assessing energy usage during mating for a mate all entail presumed energetic costs events is the brief time-frame in which they and limit male reproductive capacity (see occur. Thus, it is especially difficult to sep- Dewsbury, 1982). Specific energetic mea- arate the costs of mating per se from other surements, yet to be completed, may pro- daily activities. vide critical constraints on copulatory abil- With respect to mate access and repro- ities and, interestingly, may suggest causal ductive success (RS), some indirect mea- explanations for alternative breeding strat- sures indicate the importance of metabolic egies in males (see Gibson and Guinness, rate. In European rabbits there is a positive 1980). correlation between resting metabolic rate Finally, perhaps the most extreme exam- (RMR) and social status among groups of ple of the evolutionary and energetic costs males organized in a stable hierarchy; the of mating are in the , where post- costs of body maintenance appear to be mating mortality occurs in males of several higher for high-ranking males with species of Antechinus. Such mortality is increased values of RS (Bell, 1983, 1986). partly caused by gastrointestinal ulcération However, subordinant tree-shrews {Tupaia and suppression of the immune system glis) and deer mice {Peromyscus maniculatus) brought on by stress. But there also appears have lower rates of metabolism than dom- to be an energetic reason. Using doubly inants (Farr and Andrews, 1978a, b; Fuchs labeled water, Nagy et al. (1978) showed and Kleinknecht, 1986). Certainly, there that there is no substantial increase in daily are several other interrelated variables energy expenditure during the mating sea- which influence higher RS in dominant son. However, since the resting metabolic males {e.g., access to better breeding areas; rate may increase in males by 17% at the earlier start to breeding: see Rutberg, time of mating (Cheal et al., 1976), there 1986); nevertheless, these high metabolic may be a reduction in energy spent on other rates in dominants and subordinates of dif- activities. There is indirect evidence that ferent species may reflect alternative ener- energy used in mating may substitute for getic constraints rather than contradictory a reduction in feeding (Lee and Cockburn, data. Thus, in Tupaia and Peromyscus sub- 1985). ordinates may have high RMRs due to stress from continual testing of the hierarchy whereas in rabbits subordinates may be Gestation more passive. Total energy investment during preg- It is often assumed that most of the ener- nancy involves many components includ- getic costs of mating in males is associated ing net production of fetal, uterine, pla- with searching for prospective mates and cental, and mammary tissue, production male-male conflicts. Although sperm are costs ("the work of growth" [Brody, 1945]), vastly smaller and the cost of testicular and increased maintenance costs associ- growth is negligible, numerous studies now ated with these new tissues {i.e., the metab- indicate that ejaculate cost in terms of some olism of added mass). Direct measurement behavioral and physiological measures is of each of these components is difficult and significant (Dewsbury, 1982). Sperm pro- generally has been restricted to laboratory duction is generally limited in terms of: or domesticated species {e.g., McC. Gra- ENERGETICS AND MAMMALIAN REPRODUCTION 867

ham, 1964; Myrcha et al, 1969; Studier et white rats, for example, there was little or al, 1973; Havera, 1979; Oftedal, 1985). no difference in food consumption between Neonatal mass (birth weight) is often pregnant and non-reproductive females employed as an indirect measure of uterine (Slonaker, 1925; Wang, 1925); however, and placental tissue masses and conse- activity (=wheel running) was 57-96% quently may estimate the energetic cost of lower in the pregnant individuals. Thus, at I pregnancy (Millar, 1977, 1981; Oftedal, least some species may shift allocation of 1985; Kunz, 1987; Kurta and Kunz, 1987). energy from activity to gestation by reduc- Caloric consumption studies reveal consid- ing the frequency and/or duration of cer- erable variation in net production of fetal tain behaviors (Racey, 1981, 1982); with- and placental tissues. Production efficiency out integration of behavioral and energetic ranges from about 10-15%, with domestic data, this tactic can result in an underes- mammals clustering at the high end and timation of the total energy allocated to wild mammals tending towards the low end gestation. A combination of caloric con- of the range (Myrcha et al, 1969; Studier sumption, respirometry, and time budgets et al, 1973; Oftedal, 1985); placental and of behavior, before and during gestation uterine proliferations account for about (reproduction) is a requisite for assessment 20% of the net caloric investment during of the allocation of energy to maintenance, gestation (Oftedal, 1985). Howover, al- "the work of growth" (Brody, 1945), and though the relative size of neonate(s) may net production during gestation. Respi- serve as a useful first approximation of rometry may be particularly important energy consumption during gestation, sig- because some species, especially those with nificant changes in maintenance require- low basal metabolic rates (Nicoll and ments, due to increased mass and/or Thompson, 1987; but see Nagy and Mont- increased specific metabolic rates, cannot gomery, 1980), show increased resting be detected solely through examination of metabolic rates during gestation, presum- net production; these may involve signifi- ably as a result of costs associated with cant energetic expenditures during gesta- growth of the fetus. However, this tion (Partridge et al, 1986; Thompson and increased metabolism is not due to a dif- Nicoll, 1986; Nicoll and Thompson, 1987). ferentially high rate of metabolism in fetal Studies of the energetic costs of gesta- tissue (Kleiber, 1961). tion have focused on caloric intake, some- For pregnant rodents, increase in mean times augmented with respirometry {e.g., daily caloric intake over non-reproductive Randolph et al, 1977). Measurement of rates ranges from 18-25% {e.g., Kaczmar- caloric intake by itself can produce mis- ski, 1966; Migula, 1969; Myrcha et al, leading estimates of reproductive costs. 1969; Mattingly and McClure, 1982) and Digestive efficiencies do change slightly at least one of these species may store during gestation and lactation, although energy as fat for use during lactation {i.e., the low magnitude of these changes usually Sigmodon hispidus: Randolph et al., 1977; leads to dismissal of their importance {e.g., see also Mattingly and McClure, 1985). Oftedal, 1985; but see Mattingly and For most rodents, stored fat is not impor- McClure, 1982). Of greater significance, tant for gestation. White-footed mice however, is the potential for compensa- {Peromyscus) with food availability 80-90% tion, via reallocation of energy from some of ad lib had no effect on body weight or nonreproductive level of activity or ther- fat content, but nevertheless fecundity sig- moregulatory (maintenance) expenditure. nificantly decreased (Merson and Kirkpat- It is difficult to compare caloric intake rick, 1981); similar effects of reduced data between species (or individuals) with- fecundity associated with lowered food out knowledge of (1) ambient tempera- reserves are found in other small mammals tures during measurement, (2) limits of (see Kenagy and Bartholomew, 1985). Fat thermoneutrality (or natural nest temper- storage may be of importance to bats, how- atures), and (3) variation in activity levels ever, because of their unavoidably high before and after reproduction. In some activity levels and obvious flight costs. For 868 J. L. GiTTLEMAN AND S. D. THOMPSON example, in some species {e.g., big brown ponent of the daily energy budget of a bat, Eptesicus fuscus) the fraction of body female mammal and, in the least, may influ- fat increases by as much as 68% in one week ence the ability of a female to expend during mid-pregnancy (Stack, 1985) and if energy during early lactation. storage is unavailable foetal growth rates and pregnancy rates often decline (Racey, Lactation 1973; Kurta, 1986). Although the causal Milk production represents the single mechanisms of these results are not known, most influential and unique feature of it appears from more extensive data on mammalian reproduction (Maynard Smith, other species that smaller mammals may 1977; Pond, 1977; Daly, 1979). The com- be more "hard-wired" to gestation length plexity of energy transfer and energy use itself rather than storage. After controlling during lactation has motivated a wide array for body size, birth weight, litter size, and of physiological and behavioral studies. In body temperature (Racey, 1981), increases addition to measuring caloric intake, in ingestion rates correlate most closely with labeled water, analysis of milk composition gestation length {e.g., Millar, 1977, 1978; and production/consumption have been McClure, 1987). widely employed to estimate the energy In contrast to rodents, larger mammals requirements for lactation (Oftedal, 1985; (ungulates) buffer the costs of gestation by Gittleman and Oftedal, 1987; Kunz and laying down fat reserves prior to concep- Nagy, 1987); respirometry has been used tion (see Frisch, 1984); if storage is not to a lesser extent {e.g., Thompson and adequate, pregnancy rates decline (peary Nicoll, 1986). Measurements of the caloric caribou: Thomas, 1982; barren ground content of milk have been combined with caribou: Dauphine, 1976; wild and domes- either behavioral indices of suckling rates tic reindeer: Klein and White, 1978). Well- (frequency and duration) or changes in mass fed pregnant ewes with heavy fat reserves of suckling young and mother (Ortiz et al., had only about half the foraging intake of 1984; Gittleman and Oftedal, 1987). How- lean ewes (Reid, 1961). Ingestion rates dur- ever, analyses of milk production do not ing gestation are generally not as high as assess metabolic costs of milk production during lactation (see Fleming et al., 1981), or maternal maintenance {e.g., increased thus the inference being that milk produc- rates of maternal metabolism) and will tend tion is more costly; indeed, because ges- to underestimate overall costs of lactation tation costs are less (particularly per day), (also see discussion in Oftedal, 1985). this may explain why, rather than have Lactation is generally considered the flexible lactation periods, in some taxa ges- most expensive aspect of reproduction for tation is extended during harsh ecological a female mammal {e.g., Hanwell and Peaker, conditions {e.g., hystricomorphs: Short, 1977; Millar, 1977, 1978; Randolph et al., 1985) or gestation varies in relation to 1977; Oftedal, 1985). Mean caloric intake dominance status {e.g., anthropoid pri- during lactation ranges from 66-188% mates: Altmann, 1986). greater than for non-reproductives {e.g., Although the birthing period is brief rel- McC. Graham, 1964; Kaczmarski, 1966; ative to other reproductive events, behav- Migula, 1969; Stebbins, 1977; Randolph ioral, hormonal, and energetic changes et al. 1977; Millar, 1978; Mattingly and indicate some costs. Peak rates of energy McClure, 1982; Sadleir, 1982; Glazier, use by pregnant mammals typically occur 1985«, b). These levels may vary directly within the few days preceding parturition. with litter size {e.g., Smith and McManus, In domestic cattle, heat loss increases sig- 1975; Millar, 1978; Sadleir, 1982) and may nificantly (200-300 kcal/day) during labor be over 200% in digestively inefficient and parturition due to some combination species {e.g., the folivorous "carnivore," the of increased fetal activity and the onset of red panda, Ailurus fulgens: Gittleman, fetal thermorégulation (Brockway et al., 1988è; see also Studier, 1979). Peak levels 1963; Oftedal, 1985). Thus, energetic costs of energy use may approach 2.5-5 times of parturition may be an important com- those of non-reproductive females (see ref- ENERGETICS AND MAMMALIAN REPRODUCTION 869 erences above). However, despite high nancy and lactation (Racey and Speakman, energy expenditures during lactation, net 1987). production ranges from about 15-45% (see The daily rates of energy transfer are Smith and McManus, 1975; Mattingly and most spectacular in some marine mammals McClure, 1982; Glazier, 1985è; Oftedal, where females lactate intensively for rela- 1985) which is similar to, or even slightly tively brief periods (four weeks or less), fast higher than, gestation. from food and water during lactation, pro- Behavioral changes parallel caloric intake duce energy-rich milk with high fat con- results. Numerous studies, particularly of tent, and wean their pups abruptly (see larger species, show that feeding bout Fedak and Anderson, 1982; Bonner, 1984; lengths may increase by as much as 30%; Ortiz et al, 1984; Costa et al, 1986; Costa frequency of feeding, and increased food and Gentry, 1986). Prior to weaning, the selection are associated with the onset of sole source of nutrients for the developing lactation (see CIutton-Brock et al., 1982; pup is mother's milk. Thus, the total Dunbar, 1984; Duncan«;/a/., 1984; Berger, amount of milk and metabolic energy 1986). However, as previously mentioned, expended by a female during the entire fat deposition prior to breeding or during lactation period can be calculated by gestation may supplement energy needs extrapolating the daily milk (via pup water during lactation (see also Pond, 1984; Ver- flux and milk composition) and metabolic non and Flint, 1984; McCIure, 1987) and expenditure rates. Costa et al (1986) show may affect litter size, sex ratio, offspring that, in seals {Mirounga angusti- size and brain size at weaning {e.g., McC. rostris), the high energy cost of lactation is Graham, 1964; Widdowson, 1981; reflected by females losing approximately McCIure, 1987). 42% of their body mass and expending Lactation also imposes significant 4,330 mj even though lactation only lasts demands to water balance, particularly for 26.5 days. Further metabolic savings are mammals from xeric habitats {e.g., Soholt, achieved by minimizing activity levels: 1977). The water in milk may be partly females spend considerable amounts of recycled via the young (Friedman and time asleep and remain within a few meters Bruno, 1976): in rats, if micturation is pre- of the parturition site for the entire lac- vented by urethral ligation, the transfer of tation period. Such energy saving mecha- water from mother to pups is greatly nisms, especially the lowered dependence reduced, and the mother's water intake on food energy intake to oflFset lactation increases. As would be predicted, when a costs, may be a critical strategy allowing lactating female is deprived of water intake for the elephant seal's remarkable return {e.g., during hibernation), the degree of in population numbers (see Costa et al, water recycling is higher {e.g., black bears, 1986). Unfortunately, there are no mea- Ursus americanus: Oftedal, in preparation). surements of the energetic costs of gesta- As in gestation, there is evidence that tion in marine mammals. some species divert energy from activity or Three caveats need to be made with the maintenance to reproduction by reducing general presumption that lactation is time allocations. In bats, even though the expensive. First, milk composition, milk total energy expenditure during lactation quantity, and consequently maternal may increase by 20-40% (see Anthony and energy output vary during the lactation Kunz, 1977; Kunz, 1987), females may shift period (Oftedal, 1980, 1984) and this may energy expenditure from maintenance drastically affect perceptions of efficiency metabolism, via relaxation of homeo- and investment (Glazier, 1985è). Thus, data thermy, to lactation, thus avoiding or min- from studies not controlling for lactation imizing increased food consumption. In stage are difficult to evaluate. Second, brown long-eared bats {Plecotus auritus) the because significant increases occur during rate of increase in both absolute energy lactation in various behaviors {e.g., activity expenditure and expenditure relative to cycle, nest building, huddling, aggression, basal metabolism were similar during preg- licking: see Ewer, 1973; Leuthold, 1977; 870 J. L. GiTTLEMAN AND S. D. THOMPSON

Galef, 1981; Glutton-Brock et al, 1982; Transporting an weighing 1.5 kg Ostermeyer, 1983; Gittleman, 1988è) and when six months old will increase the in anatomical weight {e.g., mammary tissue, energy cost of locomotion to a 15 kg male gut, heart: see Williamson, 1980; Sampson by 10% for the interval of carrying while and Jansen, 1984), it is difficuh to tease eliminating the added cost of locomotion apart the relative energetic costs of lacta- to the infant. Energy cost to such a male tion (milk production) versus these other carrier will involve an increased metabolic factors. Future studies should include mea- cost of 5.6% of his energy expenditure dur- surements of energy use in various aspects ing a 12 hr day if an infant is carried over of lactation, not only those associated with an all day route and 2.8% for a half day milk production. Third, considerable vari- route. Alternatively, many female mam- ation in lactation costs may be associated mals show significant weight loss during with intra-Iitter variation. Recent empiri- lactation and often display maternal weight cal data and theoretical models show that at weaning that is lower than that before in some species mothers differentially invest mating. The cost of reattaining that initial in males and females (see, e.g., Maynard body mass may be significant, and yet it is Smith, 1980; CIutton-Brock and Albon, altogether unstudied. 1982; Lee and Moss, 1986), with increased investment in the sex which has the more variable reproductive success (in most mammals, males) and is influenced by SYNTHESIS parental investment. As Glutton-Brock et Several implications derive from this dis- al. (1984) illustrate in red deer (Cervus ela- cussion for future studies of mammalian phus), indicators of a female's energetic reproduction. First, most studies have con- capacity (body weight, dominance) appear sidered gestation and lactation as the most to be good predictors of differential invest- important reproductive events with respect ment. Physiologists should, therefore, to energy expenditures. In this perspec- incorporate this evolutionary approach in tive, about 20% of the energy is allocated estimating costs of lactation. to gestation, 80% to lactation {e.g., Oftedal, 1985; see Table 1). However, the variation in this allocation should be substantial and Post-lactational parental care almost certainly is a function of the relative Despite an explosion of studies exam- allocation of time to gestation vs. lactation; ining the ecological and evolutionary fea- thus, as reflected by the predominance of tures of parental care in mammals (see, e.g., question marks in Table 1, the use of one Eisenberg, 1981; Gubernick and Klopfer, variable {e.g., gestation length) as an index 1981; Elwood, 1983; Taub, 1984; Gittle- of energetic cost (or parental investment) man, 1985), no study has directly measured is likely to lead to erroneous explanations the metabolic costs of parental care, either of reproductive strategies, sexual selec- in a male or female. This is a glaring omis- tion, and sex allocation. Second, behav- sion given repeated observations showing ioral compensation is potentially the most the presumed costly increase in food pro- important tactic for minimizing additional visioning, den site defense, infant carrying energy requirements during reproduction. behavior, and teaching duties. Take, for The complexity of this strategy is such that example, the energetic costs of carrying an attention need be given to changes in infant by a male , a common fea- maternal time/energy budgets from mat- ture in monogamous species (see Hamil- ing through weaning; without this infor- ton, 1984; Altmann, 1986). Increases in mation, the costs of reproduction may be energy costs of transporting a mass are seriously underestimated. Related to this directly proportional to the relative mass are potential problems of presumed ener- of the transported object and the lean body getic costs of behavior; every attempt mass of the carrier (Taylor et al., 1980). should be made to determine that, for ENERGETICS AND MAMMALIAN REPRODUCTION 871

TABLE 1. Relative energy allocation for mammalian reproduction.

Reproductive event % increase % total costs Efficiency Mate access ? ? Mating and courtship ? ? ? Gestation 20-30 20 10-15% Lactation 35-149 80 15-45% Parental care/recovery ?

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