What is the appropriate timescale for measuring costs of reproduction in a `capital breeder' such as the aspic viper?

Before we can quantify the degree to which reproductive activities constitute a cost (i.e., depress an organism's probable future reproductive output), we need to determine the timescale over which such costs are paid. This is straightforward for species that acquire and expend resources simultaneously (income breeders), but more problematical for organisms that gather resources over a long period and then expend them in a brief reproductive phase (capital breeders). Most snakes are capital breeders; for example, female aspic vipers (Vipera aspis) in central western France exhibit a 2- to 3-year reproductive cycle, with females amassing energy reserves for one or more years prior to the year in which they become pregnant. We use long-term mark-recapture data on free-living vipers to quantify the appropriate timescale for studies of reproductive costs. Annual survival rates of female vipers varied significantly during their cycle, such that estimates of survival costs based only on years when the females were ‘reproductive’ (i.e., produced offspring) substantially underestimated the true costs of reproduction. High mortality in the year after reproducing was apparently linked to reproductive output; low energy reserves (poor body condition) after parturition were associated with low survival rates in the following year. Thus, measures of cost need to consider the timescale over which resources are gathered as well as that over which they are expended in reproductive activities. Also, the timescale of measurement needs to continue long enough into the post-reproductive period to detect delayed effects of reproductive ‘decisions’. This revised version was published online in July 2006 with corrections to the Cover Date.     

Senescence and costs of reproduction in the life history of a small precocial species

Species following a fast life history are expected to express fitness costs mainly as increased mortality, while slow‐lived species should suffer fertility costs. Because observational studies have limited power to disentangle intrinsic and extrinsic factors influencing senescence, we manipulated reproductive effort experimentally in the cavy (Cavia aperea) which produces extremely precocial young. We created two experimental groups: One was allowed continuous reproduction (CR) and the other intermittent reproduction (IR) by removing males at regular intervals. We predicted that the CR females should senesce (and die) earlier and produce either fewer and/or smaller, slower growing offspring per litter than those of the IR group. CR females had 16% more litters during three years than IR females. CR females increased mass and body condition more steeply and both remained higher until the experiment ended. Female survival showed no group difference. Reproductive senescence in litter size, litter mass, and reproductive effort (litter mass/maternal mass) began after about 600 days and was slightly stronger in CR than IR females. Litter size, litter mass, and offspring survival declined with maternal age and were influenced by seasonality. IR females decreased reproductive effort less during cold seasons and only at higher age than CR females. Nevertheless, offspring winter mortality was higher in IR females. Our results show small costs of reproduction despite high reproductive effort, suggesting that under ad libitum food conditions costs depend largely on internal regulation of allocation decisions.     

Seasonal variation of mortality,detectability, and body condition in a population of the adder (Vipera berus)

We analyzed seasonal variation in mortality rates in adult males and females of the European adder (Vipera berus), using data collected during a 13‐year capture–recapture study (2005–2017) in a large population. We concurrently obtained quantitative information on the seasonal variation in the detectability and body condition of adders. Our results show strong seasonality in body condition, encounter, and capture rates of adult adders, and these patterns differ markedly between sexes and between breeding and nonbreeding females. Seasonal variation in mortality rates was however virtually nonexistent in males and moderately low in both breeding and nonbreeding females. In addition, we found no evidence for among‐year differences in the seasonal mortality schedules of males and females. During periods of intensive basking, both males and pregnant females are highly visible for humans, but are not subject to strong natural mortality. This low susceptibility to predation is presumably induced by various factors, including the limitation of overt exposure to short periods of time and specific microhabitats, the dorsal coloration pattern that provides cryptic protection and possibly also an aposematic warning signal, and presumed seasonal differences in the foraging behavior and food requirements of natural predators. Our data provide some evidence that female adders, but not males, are relatively vulnerable to predation during the seasonal migrations between the hibernation and feeding habitats. Mortality in the females was not much elevated during their breeding years, but was notably highest in the spring of the ensuing nonbreeding year. After giving birth, reproductive females are extremely emaciated and have a weakened general condition. They then run the risk of dying from starvation either before, during, or after hibernation. The higher mortality after giving birth, that is sustained over a period of ca. 9 months, should be considered as an indirect and delayed survival cost of reproduction.     

Reproductive effort and costs of reproduction in female European ground squirrels

Reproductive effort, factors affecting reproductive output and costs of reproduction were studied in primiparous yearling compared to multiparous older female European ground squirrels (Spermophilus citellus). Yearling females weaned smaller litters than older ones. Litter size increased with posthibernation body mass at the expense of slightly lighter young for yearling but not for older mothers. In older females, on the other hand, emergence body mass influenced offspring mass, whereas litter size was affected by oestrus date. High reproductive effort entailed reproductive costs in terms of reduced subsequent fecundity but not subsequent survival for both yearling and older females. The production of large litters and long duration of lactation delayed subsequent oestrus, which, in turn, correlated negatively with litter size. During the second half of lactation, oestradiol levels were significantly elevated, indicating the initiation of follicular maturation processes. Oestradiol levels during that time correlated negatively with current, but positively with subsequent litter size. We therefore assume that inhibitory effects of lactation on gonadal development may mediate the negative relationship between reproductive effort and subsequent reproductive timing in adults. This effect is absent in yearlings because they are reproducing for the first time. Reproductive output in yearlings was influenced by interactions between structural growth and puberty. Received: 22 March 1999 / Accepted: 7 June 1999     

Fat is sexy for females but not males: the influence of body reserves on reproduction in snakes (Vipera aspis)

Reproduction is energetically expensive for both sexes, but the magnitude of expenditure and its relationship to reproductive success differ fundamentally between males and females. Males allocate relatively little to gamete production and, thus, can reproduce successfully with only minor energy investment. In contrast, females of many species experience high fecundity-independent costs of reproduction (such as migration to nesting sites), so they need to amass substantial energy reserves before initiating reproductive activity. Thus, we expect that the relationship between energy reserves and the intensity of reproductive behavior involves a threshold effect in females, but a gradual (or no) effect in males. We tested this prediction using captive vipers (Vipera aspis), dividing both males and females into groups of high versus low body condition. Snakes from each group were placed together and observed for reproductive behavior; sex-steroid levels were also measured. As predicted, females in below-average body condition had very low estradiol levels and did not show sexual receptivity, whereas males of all body condition indices had significant testosterone levels and displayed active courtship. Testosterone levels and courtship intensity increased gradually (i.e., no step function) with body condition in males, but high estradiol levels and sexual receptivity were seen only in females with body reserves above a critical threshold.     

Energy versus risk: costs of reproduction in free‐ranging pythons in tropical Australia

Abstract Data from a 12‐year field study have allowed us to quantify ‘costs of reproduction’ in a natural population of water pythons (Liasis fuscus) in tropical Australia. Both sexes of pythons cease feeding during the reproductive season. For males, this involves fasting for a 6 week period. Adult males lose weight rapidly over this period (approximately 17% of their body mass) but regain condition in the following months, and do not experience reduced survival. In contrast, reproductive adult females cease feeding for 3 months, lose an average of 44% of their body mass over this period, and experience increased mortality. A causal link between reproductive output and reduced female survival is supported by (i) a decrease in survival rates at female maturation; (ii) a correlation between survival rates and frequency of reproduction, in a comparison among different size classes of adult pythons; and (iii) a lowered survival rate for females that allocated more energy to reproduction. Hence, both sexes experience substantial energy costs of reproduction, but a relatively higher energy cost translates into a survival cost only in females. Such non‐linearities in the relationship between energy costs and survival costs may be widespread, and challenge the value of simple energy‐based measures of 'reproductive effort’.     

Determinants of reproductive success in female adders,Vipera berus

Summary Female lifetime reproductive success in a small population of individually-marked adders in southern Sweden was studied over a period of seven years. Reproductive characteristics varied little from year to year and were consistent through time in individual females. Most females mature at four years of age and reproduce every two years. The total number of offspring produced by a female depends on her adult body size (and thus, litter size) and longevity (and thus, number of litters per lifetime). Adult body size in females is influenced mainly by subadult growth rates. Offspring size depends on maternal body size and a tradeoff between offspring size and offspring number. Maternal age does not affect litter sizes and offspring sizes except through ontogenetic changes in maternal body size.Survival of females after parturition is low because of the high energy costs of reproduction, compounded by low feeding rates of gravid females because of their sedentary behaviour at this time. About one-half of females produce only a single litter during their lifetimes, although some females live to produce four or five litters. On a proximate basis, rates of energy accumulation for growth (in subadults) and reproduction (in adults) may be the most important determinants of fitness in female adders.     

Sexual abstinence and the cost of reproduction in adult male water snakes, Nerodia sipedon

Low frequency of reproduction among iteroparous organisms is most often observed among female ectothermic vertebrates and is thought to be a strategy used to defer reproductive costs. We assessed reproductive costs of male water snakes ( Nerodia sipedon ) to determine why half of adult males abstain from reproduction each year. There was no evidence of a short-term energetic cost of reproduction. Change in mass did not differ between reproductive and non-reproductive males during the one-month mating season or during the entire four-month activity season. Changes in mass of reproductive males were similar at two sites in which the spatial distribution of females differed. However, there were size-specific differences in growth and survival between reproductive and non-reproductive males. Among reproductive males growth rate decreased with body size at a lower rate than among non-reproductive males. Survival increased with body size for reproductive males, but decreased with body size among non-reproductive males. Most of the differential survival between reproductive and non-reproductive males did not occur during the mating season but rather during hibernation. Size-related differences between reproductive and non-reproductive males may reflect selection having eliminated low quality males from the larger size classes. Overall our results appear most consistent with there being high variance in male quality, such that the best males can bear the cost of reproducing and still grow and survive as well or better than low quality males that abstain from reproduction.     

Hormonal manipulation of offspring number: maternal effort and reproductive costs

We used exogenous gonadotropin hormones to physiologically enlarge litter size in the bank vole (Clethrionomys glareolus). This method allowed the study design to include possible production costs of reproduction and a trade-off between offspring number and body size at birth. Furthermore, progeny rearing and survival and postpartum survival of the females took place in outdoor enclosures to capture salient naturalistic effects that might be present during the fall and early winter. The aim of the study was to assess the effects of the manipulation on the growth and survival of the offspring and on the reproductive effort, survival, and future fecundity of the mothers. Mean offspring body size was smaller in enlarged litters compared to control litters at weaning, but the differences disappeared by the winter. Differences in litter sizes disappeared before weaning age due to higher mortality in enlarged litters. In addition to the effects of the litter size, offspring performance was probably also influenced by the ability of the mother to support the litter. Experimental females had higher reproductive effort at birth, and they also tended to have higher mortality during nursing. Combined effects of high reproductive effort at birth and high investment in nursing the litter entailed costs for the experimental females in terms of decreased probability of producing a second litter and a decreased body mass gain. Thus, enlarged litter size had both survival and fecundity costs for the mothers. Our results suggest that the evolution of litter size and reproductive effort is determined by reproductive costs for the mothers as well as by a trade-off between offspring number and quality.     

Sex, Reproductive Status, and Cost of Tail Autotomy via Decreased Running Speed in Lizards

Autotomy, voluntary shedding of body parts to permit escape, is a theoretically interesting defense because escape benefit is offset by numerous costs, including impaired future escape ability. Reduced sprint speed is a major escape cost in some lizards. We predicted that tail loss causes decreased speed in males and previtellogenic females, but not vitellogenic females already slowed by mass gain. In the striped plateau lizard, Sceloporus virgatus , adults of both sexes are subject to autotomy, and females undergo large increases in body condition (mass/length) during vitellogenesis. Time required for running 1 m was similar in intact autotomized males and previtellogenic females, but increased by nearly half after autotomy. Vitellogenic females were slower than other lizards when intact, but their speed was unaffected by autotomy. Following autotomy, speeds of all groups were similar. Thus, speed costs of autotomy vary with sex and reproductive condition: decreased running speed is not a cost of autotomy in vitellogenic females or presumably gravid females. Costs of autotomy are more complex than previously known. Speed and other costs might interact in unforseen ways, making it difficult to predict whether strategies to compensate for diminished escape ability differ with reproductive condition in females.     

The energy costs of sexual dimorphism in mole-rats are morphological not behavioural

Different reproductive strategies of males and females may lead to the evolution of differences in their energetic costs of reproduction, overall energetic requirements and physiological performances. Sexual dimorphism is often associated with costly behaviours (e.g. large males might have a competitive advantage in fighting, which is energetically expensive). However, few studies of mammals have directly compared the energy costs of reproductive activities between sexes. We compared the daily energy expenditure (DEE) and resting metabolic rate (RMR) of males and females of two species of mole-rat, Bathyergus janetta and Georychus capensis (the former is sexually dimorphic in body size and the latter is not) during a period of intense digging when males seek females. We hypothesized that large body size might be indicative of greater digging or fighting capabilities, and hence greater mass-independent DEE values in males of the sexually dimorphic species. In contrast to this prediction, although absolute values of DEE were greater in B. janetta males, mass-independent values were not. No differences were apparent between sexes in G. capensis. By comparison, although RMR values were greater in B. janetta than G. capensis, no differences were apparent between the sexes for either species. The energy cost of dimorphism is most likely to be the cost of maintenance of a large body size, and not the cost of behaviours performed when an individual is large.     

Relationship between reversed sexual dimorphism,breeding investment and foraging ecology in a pelagic seabird,the masked booby

Reversed sexual dimorphism (RSD) may be related to different roles in breeding investment and/or foraging, but little information is available on foraging ecology. We studied the foraging behaviour and parental investment by male and female masked boobies, a species with RSD, by combining studies of foraging ecology using miniaturised activity and GPS data loggers of nest attendance, with an experimental study where flight costs were increased. Males attended the chick more often than females, but females provided more food to the chick than males. Males and females foraged during similar periods of the day, had similar prey types and sizes, diving depths, durations of foraging trips, foraging zones and ranges. Females spent a smaller proportion of the foraging trip sitting on the water and had higher diving rate than males, suggesting higher foraging effort by females. In females, trip duration correlated with mass at departure, suggesting a flexible investment through control by body mass. The experimental study showed that handicapped females and female partners of handicapped males lost mass compared to control birds, whereas there was no difference for males. These results indicate that the larger female is the main provisioner of the chick in the pair, and regulates breeding effort in relation to its own body mass, whereas males have a fixed investment. The different breeding investment between the sexes is associated with contrasting foraging strategies, but no clear niche differentiation was observed. The larger size of the females may be advantageous for provisioning the chick with large quantities of energy and for flexible breeding effort, while the smaller male invests in territory defence and nest guarding, a crucial task when breeding at high densities. In masked boobies, division of labour appears to be maximal during chick rearing—the most energy-demanding period—and may be related to evolution of RSD.     

Annual cycle of energy and time expenditure in a golden-mantled ground squirrel population

Summary We have analyzed seasonal shifts of energy and time allocation in a population of golden-mantled ground squirrels (Spermophilus saturatus) by directly measuring total daily energy expenditure (DEE) with an isotopic technique (doubly labeled water=dlw), and by estimating components of total DEE through an integration of field behavioral observations with laboratory-measured rates of energy expenditure (oxygen consumption) associated with major behavioral and physiological states. Hibernation laster about 7 1/2 months, and the 4 1/2-month activity season consisted of mating, a 28-d gestation of 3–5 young, 5 1/2 weeks of postnatal growth building to a peak in lactation just before the young emerged above ground, an additional 2–3-week period of maternal care before dispersal, and finally restoration of body mass preceding hibernation. Although the hibernation season comprised nearly two-thirds of the year, it involved only 13–17% of annual energy expenditure, leaving about 85% of energy expenditure for the active season. Ground squirrels were actually present on the surface for only about 11% of the year's time, and the foraging time required to obtain the total annual energy supply amounted to only about 2% of the year's time. The squirrels fed mainly on herbs in the early season and hypogeous fungi later; both were used extensively during peak lactation when female energy expenditure and demand were maximal. Average daily foraging time increased steadily throughout the season to a maximum of 28% of aboveground time as availability of greens diminished and fungus predominated in the diet; time availability did not limit foraging since the animals sat on average for 65% of the daily surface time of about 7 h. Timing of reproduction is apparently optimized such that peak reproductive energy demands are matched with maximal food availability and moderate thermal conditions that minimize energy demand. Despite the greater body mass of males, the greatest total DEE (measured by dlw) of any squirrels at any time of year was that of females during peak lactation. For production of young and lactation through above-ground emergence of an average litter of 2.7, females required a total energy increase of 24% above annual nonreproductive metabolism. Yearling females all bred and performed similarly to older females, yet some costs were greater because the yearlings began and ended hibernation at smaller mass, compensated by giving birth later, and finally showed a greater absolute increase in body mass over the active season than older females. Annual metabolic energy expenditure of breeding males was about 18% greater than that of females, due to greater male body mass. Yet the annual energy intake requirement for both sexes was essentially identical (about 42MJ) due to the greater reproductive export by females in the form of newborn and milk. During the mating season males showed wide-ranging exploratory behavior and social interactions, including aggression, that involved considerable locomotory energy expenditures. Although we did not directly account for the energetics of these specific reproductive behaviors, they are critical to male reproductive success and on a daily basis they probably involved much greater energy expenditure than sperm production. Some yearling males avoided these costs by foregoing testicular development, yet they allocated four times as much energy to growth as older males, thereby increasing somatic condition for the future.     

Optimization of reproductive effort and foraging time in mammals: The influence of resource level and predation risk

Summary The trade-off between fitness benefits from foraging and associated costs in terms of predation risk is analysed by a simple model which takes into account the differential predation risk for reproducing and non-reproducing individuals. The currency that animals are assumed to maximize is their expected absolute fitness (probability of survival plus half of the expected litter size) after a potential reproductive period. Depending on resource levels and predation risk, this maximization can be achieved by (1) opting for individual survival and behaving as a strict time minimizer, (2) by reproducing at the maximal rate and behaving as a strict energy maximizer or (3) by submaximal reproductive effort and a behaviour intermediate between time minimization and energy maximization. Small changes in the availability of food or cover or in the density of predators can shift the optimum from one strategy to another. The shift is particularly abrupt, if predation pressure increases and the availability of resources remains high. This could explain the spatial and temporal variation in the reproductive effort and body weight observed in boreal small mammals with sustained, multiannual population fluctuations.     

Reproductive success and risk of predation in normal and melanistic colour morphs of the adder, Vipera berus

In a population of adders (Vipera berus) in Southwest Sweden, melanistic males were heavier than normal coloured males of the same length. Victory in male-male sexual combats was positively related to size. Higher risk of predation in the black morph was inferred from experiments showing a high predator attack rate on models of the black morph. Even the bright colour in newly moulted basking males of the normal morph gives cryptic protection. In females, melanism probably also affects body size and risk of predation by visually searching predators. The thermoregulatory influence of black colour, the reproductive success and the maintenance of two colour morphs in the population are discussed.     

The effects of size, age and a cost of early breeding on reproduction in female mountain hares

Both age and size may influence female reproductive performance in mammals, and successful early reproduction may lead to reduced success at later attempts. The effects of age, size and early reproduction on distribution of reproductive effort throughout a single breeding season was examined in female mountains hares Lepus timidus L. Hind foot length was used as an index of body size, because, unlike body weight, it did not fluctuate with reproductive status. Fifty-six female carcasses were collected from March to October 1984, and their litters were assigned to one of three chronologically equal'litter periods'(1–3) of equal length. Whereas number of ova shed was always independent of age, large females shed more ova than did smaller females in litter periods 1 and 2. Prenatal mortality of ova and embryos was highest during litter period 1, when it was independent of age and size. Although prenatal mortality remained high in first year females in litter period 2, there was an overall decline through to the final litter period when it was negligible. Total number of young produced through the season increased with skeletal size in old females (age > 1), but not significantly in first year females. It is concluded that large size, rather than age, favours early reproduction in mountain hares. Every additional offspring produced in litter periods 1 and 2 reduced that female's production in period 3. After correcting for this cost of early reproduction the number of young produced in the final litter period also increased with maternal size.     

Repeated matings offset costs of reproduction in female crickets

Summary Courtship food gifts can be a significant source of nutrition to females and costly for males to produce; hence, costs of reproduction should be reduced for multiple-mating females and increased for multiplemating males in a gift-giving species. We tested this hypothesis by experimentally manipulating mating opportunities of males and females of two cricket species,Gryllodes sigillatus, a gift-giving species andGryllus veletis, a non-gift-giving species. Females of both species consume the externally attached spermatophore after mating, but inG. sigillatus, the sperm-containing ampulla is accompanied by a large gelatinous spermatophylax. In both species, survival of mated females given limited access to males was reduced relative to virgin females, thus suggesting a cost of reproduction to females. However, females given unlimited mating opportunities lived as long as virgins and also produced significantly more offspring than limited-access females. These results suggest that benefits of repeated matings, particularly those arising through spermatophore consumption, offset costs of reproduction in females. Lack of a treatment by species interaction suggests that females of both species derive nutritional benefits through spermatophore consumption, and that any additional advantage to the consumption of the spermatophylax inG. sigillatus is offset by more frequent mating byG. veletis females. In contrast to females, varying mating opportunities had no effect on male survival, suggesting that mating effort is not very costly to males. Male survival increased linearly with body mass but only when males were food-deprived, suggesting that larger males possess greater initial energy reserves to sustain their longevity when food-stressed.     

Repeated matings and sperm depletion in the freshwater crayfish Austropotamobius italicus

1. In sexually reproducing organisms, the energetic costs of spermatogenesis can be considerable, and can limit the reproductive potential of the males. In species where males mate more than once during the reproductive season, the costs of sperm production are generally predicted to result in a decrease of ejaculate size and quality with successive fertilizations. 2. In this study we examined the variation in ejaculate size among successive fertilizations in a long‐lived freshwater crayfish species, Austropotamobius italicus. 3. Sexually active adult males of various sizes were allowed to mate repeatedly with different females on consecutive days. Trials for a given male ended when he copulated but did not release any sperm or refused to mate. 4. Males fertilized between 0 and 4 females, and most (42.5%) fertilized a single female. The overall number of females fertilized by a given male decreased with increasing male body size. Ejaculate size decreased markedly with consecutive fertilizations in a similar fashion among both large and small males, while simultaneously increasing with female body size. The total ejaculate size over successive fertilizations decreased with increasing male size. 5. Our study indicates that either sperm production or release involves non‐trivial costs in freshwater crayfish, and suggests that large/old males may face greater difficulties in gamete release than small/young ones, as shown by the lower number of females fertilized by large compared with small males, which may reflect the ongoing senescence of their reproductive performance.     

Reproductive allocation and the long-term costs of reproduction in Siparuna grandiflora, a dioecious neo-tropical shrub

1 Using a combination of observational and experimental approaches, both allocation of resources to reproduction (often called the direct cost of reproduction) and the subsequent long-term costs (the indirect, delayed or demographic cost) associated with reproductive allocation to male and female function in Siparuna grandiflora (Siparunaceae), a tropical dioecious shrub, were examined.
2 The objectives were to determine whether females allocate more biomass or nitrogen per reproductive episode than males, and whether there is a long-term cost of reproduction in terms of subsequent growth or reproduction for either sex. If there is no long-term cost of reproduction, then reproduction may be viewed as free in an evolutionary sense.
3 As is generally the case in dioecious species, females allocated more biomass and nitrogen to reproduction than males. Females also showed delayed costs of reproduction in terms of decreased growth and subsequent reproduction, whereas males did not.
4 The lack of measurable delayed costs in males suggests that with the evolution of dioecy, selection has reduced delayed costs of reproduction in S. grandiflora males. In contrast, females that were prevented from reproducing were able to re-allocate resources to growth, and produced more stem length on average than males. This re-allocation response may have evolved to reduce delayed costs of reproduction in females over time frames longer than that considered in the present study.