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), gestation, parturition, lactation, post-lactational parental care, and maternal recovery. We point out that comparing the relative allocation of energy for these events across mammals is difficult because of life history variability (e.g., litter size, birth 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 sexual selection, 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 mammal 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 pregnancy 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 rodents 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 dogs, chipmunks) than to the heteromyids. As the authors conclude, "The comparison Mating of A. leucurus with D. merriami [kangaroo 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 copulation. 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, ejaculation 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