Testing the reproductive and somatic trade‐off in female Columbian ground squirrels

Energetic trade‐offs in resource allocation form the basis of life‐history theory, which predicts that reproductive allocation in a given season should negatively affect future reproduction or individual survival. We examined how allocation of resources differed between successful and unsuccessful breeding female Columbian ground squirrels to discern any effects of resource allocation on reproductive and somatic efforts. We compared the survival rates, subsequent reprodction, and mass gain of successful breeders (females that successfully weaned young) and unsuccessful breeders (females that failed to give birth or wean young) and investigated “carryover” effects to the next year. Starting capital was an important factor influencing whether successful reproduction was initiated or not, as females with the lowest spring emergence masses did not give birth to a litter in that year. Females that were successful and unsuccessful at breeding in one year, however, were equally likely to be successful breeders in the next year and at very similar litter sizes. Although successful and unsuccessful breeding females showed no difference in over winter survival, females that failed to wean a litter gained additional mass during the season when they failed. The next year, those females had increased energy “capital” in the spring, leading to larger litter sizes. Columbian ground squirrels appear to act as income breeders that also rely on stored capital to increase their propensity for future reproduction. Failed breeders in one year “prepare” for future reproduction by accumulating additional mass, which is “carried over” to the subsequent reproductive season.     

Best squirrels trade a long life for an early reproduction

Age at primiparity plays a crucial role in population dynamics and life-history evolution. Long-term data on female North American red squirrels were analysed to study the fitness consequences of delaying first reproduction. Early breeders were born earlier, had a higher breeding success and achieved a higher lifetime reproductive success than females who delayed their first reproduction, which suggests a higher quality of early breeders. However, early breeders had similar mass when tagged, and similar number of food caches available at one year of age as late breeders. Nevertheless, we found evidence of survival costs of early primiparity. Early breeders had a lower survival between one and two years of age than late breeders and a lower lifespan. Our study points out that two reproductive tactics co-occurred in this population: a tactic based on early maturity at the cost of a lower survival versus a tactic based on delayed maturity and long lifespan. High quality individuals express the most profitable tactic by breeding early whereas low quality individuals do the best of a bad job by delaying their first reproduction.     

The adaptive value of energy storage and capital breeding in seasonal environments

Timing of reproduction in a seasonal cycle is a life history trait with important fitness consequences. Capital breeders produce offspring from stored resources and, by decoupling feeding and reproduction, may bend the constraints caused by seasonality in food or predation. Income breeders, on the other hand, produce offspring from concurrent food intake, with the disadvantage of less flexibility, but with high efficiency and no inventory costs of carrying stores. Here, we assess relative profitability of capital and income breeding in herbivorous zooplankton inhabiting seasonal, high-latitude environments. We apply a state-dependent life history model where reproductive values are used to optimise energy allocation and diapause strategies over the year. Three environmental scenarios were modelled: an early, an intermediate, and a late feeding season. We found that capital breeding was most important in the early season. Capital breeding ranged from 7–9% of the eggs produced but, because of the high reproductive value of early eggs, capital breeding ranged from 9–30% when measured in terms of reproductive value. The main benefit of capital breeding was reproduction prior to the feeding season – when the reproductive value of an egg peaked. In addition, capital breeding was also used to increase egg production rates at times of income breeding. For individuals born late in the season the model predicted a two-year cycle instead of the typical annual life cycle. These individuals could then reap the benefits of early reproduction and capital breeding in their second year instead of income breeding late in the first year. We emphasize the importance of evaluating reproductive strategies such as capital and income breeding from a complete life cycle perspective. In particular, knowing the seasonality in offspring fitness is essential to appreciate evolutionary and population-level consequences of capital breeding.     

Long-term shifts in the cyclicity of outbreaks of a forest-defoliating insect

Optimisation of reproductive investment is crucial for Darwinian fitness, and detailed long-term studies are especially suited to unravel reproductive allocation strategies. Allocation strategies depend on the timing of resource acquisition, the timing of resource allocation, and trade-offs between different life-history traits. A distinction can be made between capital breeders that fuel reproduction with stored resources and income breeders that use recently acquired resources. In capital breeders, but not in income breeders, energy allocation may be decoupled from energy acquisition. Here, we tested the influence of extrinsic (weather conditions) and intrinsic (female characteristics) factors during energy storage, vitellogenesis and early gestation on reproductive investment, including litter mass, litter size, offspring mass and the litter size and offspring mass trade-off. We used data from a long-term study of the viviparous lizard, Lacerta (Zootoca) vivipara. In terms of extrinsic factors, rainfall during vitellogenesis was positively correlated with litter size and mass, but temperature did not affect reproductive investment. With respect to intrinsic factors, litter size and mass were positively correlated with current body size and postpartum body condition of the previous year, but negatively with parturition date of the previous year. Offspring mass was negatively correlated with litter size, and the strength of this trade-off decreased with the degree of individual variation in resource acquisition, which confirms theoretical predictions. The combined effects of past intrinsic factors and current weather conditions suggest that common lizards combine both recently acquired and stored resources to fuel reproduction. The effect of past energy store points out a trade-off between current and future reproduction.     

Increasing returns in the life history of Columbian ground squirrels

1. We examined positive associations and trade-offs of maternal and reproductive traits in a population of Columbian ground squirrels, Spermophilus columbianus .
2. Structural size, body condition, mother's personal allocation to body mass during reproduction, and timing of littering were estimated for live-trapped reproductive females that were observed during an 8-year period, and were compared to litter mass, litter size, and average pup mass using path analyses.
3. Mothers exhibited age-structured traits that influenced reproductive patterns. Yearling mothers were significantly smaller, bred later, and had smaller litters than older females. Mothers that gained more body mass during reproduction and older mothers in good body condition that were structurally large had larger litters.
4. Early seasonal timing of littering was an important positive influence on successful reproduction by older mothers only in early breeding seasons and in years when conditions for reproduction were good for all females.
5. The number of offspring that survived to 1 year of age was most strongly associated with litter mass and litter size; date of breeding was of secondary influence, with earlier litters exhibiting greater success.
6. In general, mothers that gained the most in body mass during reproduction were concurrently more successful in weaning large litters (perhaps due to better quality of foraging habitat).
7. In addition to expected reproductive trade-offs, reproduction by Columbian ground squirrels exhibited positive associations of life-history traits that may reflect evolutionary increasing returns.     

Lifetime selection on heritable life-history traits in a natural population of red squirrels

Abstract Despite their importance in evolutionary biology, heritability and the strength of natural selection have rarely been estimated in wild populations of iteroparous species or have usually been limited to one particular event during an organism's lifetime. Using an animal-model restricted maximum likelihood and phenotypic selection models, we estimated quantitative genetic parameters and the strength of lifetime selection on parturition date and litter size at birth in a natural population of North American red squirrels, Tamiasciurus hudsonicus. Litter size at birth and parturition date had low heritabilities ( h² = 0.15 and 0.16, respectively). We considered potential effects of temporal environmental covariances between phenotypes and fitness and of spatial environmental heterogeneity in estimates of selection. Selection favored early breeders and females that produced litter sizes close to the population average. Stabilizing selection on litter size at birth may occur because of a trade-off between number of offspring produced per litter and offspring survival or a trade-off between a female's fecundity and her future reproductive success and survival.     

Pre-breeding energy requirements: thyroid hormone, metabolism and the timing of reproduction in house sparrows Passer domesticus

We measured thyroid hormone (T3) levels and energy expenditure of pre-breeding house sparrows Passer domesticus in relation to the timing of breeding and reproductive success. The onset of reproduction was synchronised in two waves, separated by a three-week interval. On an annual basis, early breeders (birds that bred for the first time during the first wave) made significantly more breeding attempts, laid significantly more egg and raised 2.3 times more chicks to fledging than late breeders (birds that bred for the first time during the second wave). By the end of March, about one month before the first egg was laid in the population, plasma titres of testosterone in males and estradiol in females were still low and did not differ between early and late breeders. However, birds that subsequently bred early had higher titres of plasma triiodothyronine (T3) than birds that started to breed late. We show for the first time in a free-living bird population that Basal Metabolic Rate (BMR) is positively correlated with the plasma titre of T3. Differences in plasma T3 accounted for 48% of the inter-individual variation in BMR. Elevated T3 levels indicate that energy requirements increase prior to breeding. Although early breeding appears to be advantageous in terms of the number of offspring raised on an annual basis, the increased energy requirements prior to breeding are thought to delay the onset of reproduction in those birds that cannot afford the additional energy expenditure early in the season.     

Individual heterogeneity in life-history trade-offs with age at first reproduction in capital breeding elephant seals

Recruitment age plays a key role in life-history evolution. Because individuals allocate limited resources among competing life-history functions, theory predicts trade-offs between current reproduction and future growth, survival and/or reproduction. Reproductive costs tend to vary with recruitment age, but may also be overridden by fixed individual differences leading to persistent demographic heterogeneity and positive covariation among demographic traits at the population level. We tested for evidence of intra- and inter-generational trade-offs and individual heterogeneity relating to age at first reproduction using three decades of detailed individual life-history data of 6,439 capital breeding female southern elephant seals. Contrary to the predictions from trade-off hypotheses, we found that recruitment at an early age was associated with higher population level survival and subsequent breeding probabilities. Nonetheless, a survival cost of first reproduction was evident at the population level, as first-time breeders always had lower survival probabilities than prebreeders and experienced breeders of the same age. However, models accounting for hidden persistent demographic heterogeneity revealed that the trade-off between first reproduction and survival was only expressed in “low quality” individuals, comprising 35% of the population. The short-term somatic costs associated with breeding at an early age had no effect on the ability of females to allocate resources to offspring in the next breeding season. Our results provide strong evidence for individual heterogeneity in the life-history trajectories of female elephant seals. By explicitly modeling hidden persistent demographic heterogeneity we show that individual heterogeneity governs the expression of trade-offs with first reproduction in elephant seals.     

Maternal investment during pregnancy in wild meerkats

Maternal investment in offspring development is a major determinant of the survival and future reproductive success of both the mother and her young. Mothers might therefore be expected to adjust their investment according to ecological conditions in order to maximise their lifetime fitness. In cooperatively breeding species, where helpers assist breeders with offspring care, the size of the group may also influence maternal investment strategies because the costs of reproduction are shared between breeders and helpers. Here, we use longitudinal records of body mass and life history traits from a wild population of meerkats (Suricata suricatta) to explore the pattern of growth in pregnant females and investigate how the rate of growth varies with characteristics of the litter, environmental conditions, maternal traits and group size. Gestational growth was slight during the first half of pregnancy but was marked and linear from the midpoint of gestation until birth. The rate of gestational growth in the second half of pregnancy increased with litter size, maternal age and body mass, and was higher for litters conceived during the peak of the breeding season when it is hot and wet. Gestational growth rate was lower in larger groups, especially when litter size was small. These results suggest that there are ecological and physiological constraints on gestational growth in meerkats, and that females may also be able to strategically adjust their prenatal investment in offspring according to the likely fitness costs and benefits of a particular breeding attempt. Mothers in larger groups may benefit from reducing their investment because having more helpers might allow them to lower reproductive costs without decreasing breeding success.     

Climate change and micro-geographic variation in laying date

Climate change has been shown to affect the timing of reproduction, with earlier reproduction being associated with an increase in temperature. Changes in the timing of reproduction arise from changes in food availability as well as other factors, and differences in the timing of reproduction among sites may cause sites with early reproduction to contribute disproportionately to local recruitment. In this study, spatial variation in the laying date of barn swallows Hirundo rustica at 39 sites in a 45-km²study area during the period 1971–2004 was used to investigate micro-geographic patterns in the timing of breeding. I found that individuals breeding at sites with early reproduction had a disproportionately large reproductive success. Early sites were characterized by early plant phenology, as determined by the date of leafing of the broad-leaved elm Ulmus glabra and date of flowering of the snowdrop Galanthus nivalis during a single year. Such early sites showed greater advancement in laying date between 1971 and 2004 than the average site. Early sites were also generally occupied during more years by a larger number of breeders than were late sites. Breeders at early sites produced more fledglings, and breeders at such sites were characterized by a smaller adult body size and larger secondary sexual characters than individuals at the average site. These observations are consistent with the hypothesis that temporal changes in the timing of reproduction occur as a consequence of differential recruitment at phenologically early sites that produce disproportionately large numbers of offspring. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Territorial bequeathal by red squirrel mothers: A dynamic model

Female red squirrels (Tamiasciurus hudsonicus) sometimes bequeath their territory to their offspring. Late-breeding females are more likely to leave than are early-breeding females. Early-breeding females tend to lose weight during reproduction while late-breeding females do not. Early-born juveniles are more successful at winning territories than are those born late. I use dynamic programming to investigate the trade-offs involved in territorial bequeathal from the female's perspective as a function of breeding date, litter size and female body condition. The model predicts that two classes of females are more likely to bequeath: those in good condition early in the season, and those in poor condition at the season's end. Only versions of the model incorporating a function improving the female's ability to win a territory over the season mimicked the pattern of bequeathal observed in the field. A seasonal effect is likely an important factor in driving the pattern of strategies observed.     

Female red squirrels fit Williams' hypothesis of increasing reproductive effort with increasing age

Williams predicted that reproductive effort should increase as individuals age and their reproductive value declines. This simple prediction has proven difficult to test because conventional measures of energy expenditure on reproduction may not be a true reflection of reproductive effort. We investigated age-specific variation in female reproductive effort in a stable population of North American red squirrels where energy expenditure on reproduction is likely to reflect actual reproductive effort. We used seven measures of reproductive effort spanning conception to offspring weaning. We found that females completed growth by age 3 and that reproductive value decreased after this age likely because of reproductive and survival senescence. We therefore, predicted that reproductive effort would increase from age 3 onwards. The probability of breeding, litter mass at weaning, and likelihood of territory bequeathal were all lower for 1- and 2-year-old females than for females older than 3 years, the age at which growth is completed. That growing females are faced with additional energetic requirements might account for their lower allocation to reproduction as compared with older females. The probability of attempting a second reproduction within the same breeding season and the propensity to bequeath the territory to juveniles increased from 3 years of age onwards, indicating an increase in reproductive effort with age. We think this increase in reproductive effort is an adaptive response of females to declining reproductive values when ageing, thereby supporting Williams' prediction.     

Short-term versus long-term effects of food intake on reproductive output in a viviparous snake, Vipera aspis

Feeding rates influence reproductive output in many kinds of animals, but we need to understand the timescale of this influence before we can compare reproductive energy allocation to energy intake. A central issue is the extent to which reproduction is fuelled by long-term energy stores ("capital" breeding) versus recently-acquired resources ("income" breeding). Our data on free-living aspic vipers show that there is no simple answer to this question: reproductive frequency is determined by long-term energy stores, offspring size is influenced by maternal food intake immediately before ovulation, and litter size is influenced by both long-term stores and short-term energy acquisition. Thus, offspring size in free-living vipers reflects the mother's energy balance over the preceding year (via a trade-off between litter size and offspring size) as well as her energy balance in the current breeding season. Hence, different components of a given reproductive output (litter) are not only functionally linked, but also respond to different temporal scales of prey availability. A female's body size has little effect on her reproductive output. Attempts to quantify reproductive energy allocation must take into account the fact that different reproductive traits (such as offspring size versus number) may respond to energy availability over different timespans. Thus, although the aspic viper is a typical "capital breeder" in terms of its reliance on stored reserves for maternal "decisions" concerning reproductive frequency, it is to some degree a facultative "income breeder" with respect to the determination of offspring size and litter size.     

Capital or income breeding? A theoretical model of female reproductive strategies

Energy storage is an important component of life-history variation.A distinction is recognized between species that provision offspringusing energy gained concurrently (income breeders) and thosethat provision offspring using energy stores accumulated atan earlier time (capital breeders). Although this distinctionhas been recognized for some time, surprisingly little attentionhas been paid to the general adaptive value of the 2 strategies.Here, we present a simple, general framework for modeling femalereproductive strategies. We show that our framework can be applicableeither to annual breeders that aim to maximize the energy deliveredto their offspring before independence, or to species with shorterreproductive cycles that aim to maximize reproductive rate,given that their offspring must build up a given level of reservesbefore independence. For both scenarios, we show that the costsof accumulating capital can lead to pure income breeding, purecapital breeding, or a mixture of the 2 strategies. Our modelallows the effects of a variety of parameters to be assessed.Length of gestation, offspring metabolism, efficiency of energytransfer from mother to offspring, and the relative rates ofenergy gain by females with and without offspring are all importantfactors. The cost associated with accumulated capital is a particularlycritical determinant of the strategy adopted. More detailedapproaches to specific systems may provide a greater understandingof the factors promoting different maternal strategies for offspringprovisioning.     

Determinants of reproductive success in female Columbian ground squirrels

Summary We studied the reproductive success of female Columbian ground squirrels (Spermophilus columbianus) in southwestern Alberta for nine years. We defined reproductive success as the number of offspring surviving their first hibernation, classified as yearlings. The number of weaned juveniles explained one third of the variance in number of yearlings at emergence from their first hibernation the following spring, and much of the variance in individual reproductive success originated after weaning. Weight of adult females at emergence from hibernation was correlated with annual reproductive success. The mother's survival beyond weaning and the subsequent winter's snow accumulation had positive effects on annual reproductive success, whereas population density and summer temperature had negative effects. We found no effects on annual reproductive success of date of litter emergence, weight at emergence as a yearling, presence or absence of adult kin, distance from the natal site, location within the study area, winter temperature or summer precipitation. Age of first breeding did not affect lifetime reproductive success, which ranged from 0 to 19 yearlings produced over a lifetime. The greatest source of variation in lifetime reproductive success for females surviving to breeding age was offspring survival, followed by reproductive lifespan.     

Resource use for reproduction depends on spring arrival time and wintering area in an arctic breeding shorebird

Resources for egg production may come from body reserves stored before breeding (“capital breeders”) or from food acquired at the breeding site (“income breeders”). Arctic migrants were long thought to be capital breeders, because they often arrive at a time when local food availability is still limited. However, later evidence suggested that arctic breeding shorebirds are primarily income breeders, or that they use a mixed strategy depending on laying date. We explored the relationship between laying date and resource use for reproduction in the pectoral sandpiper Calidris melanotos breeding in the Alaskan arctic by contrasting carbon isotope (δ¹³C) values of the local diet and of maternal plasma, cellular blood, feather and claw with those of the eggs produced. Our results revealed that early breeding females utilize resources for egg production that were acquired recently at staging areas, whereas later breeding females mostly relied on nutrients derived from local food sources. These findings suggest that the resource allocation strategy used for reproduction differs among females, and varies depending on the timing of arrival and the start of reproduction. The arrival date at the breeding ground and laying date may critically depend on non‐breeding season events such as winter habitat choice, staging areas or migration routes. By comparing maternal feather δ¹³C, claw δ¹³C and feather δD, we examined whether non‐breeding season events influenced the use of resources for egg production through variation in capture date or clutch initiation date. Female pectoral sandpipers originating from moulting areas characterized by higher (more positive) δD signatures were caught earlier and started laying earlier, and they used stored resources for reproduction. Using regional maps of δD values for precipitation in the wintering sites in South America, we compared the spatial variation in the observed feather δD signatures. This analysis indicated that female pectoral sandpipers with higher δD signatures, presumably coming from more north‐easterly wintering sites in southern America, started laying earlier and used mostly stored resources for egg production, compared to females that wintered (or at least moulted) further south. Our results thus show that winter moulting habitat is linked to breeding resource allocation strategy in this high‐arctic breeding shorebird.     

The translocation and post release settlement of red squirrels Sciurus vulgaris to a previously uninhabited woodland

Red squirrels have undergone a 30% contraction of their range in the last 10 years in Ireland, a decline attributed to the introduced grey squirrel. Large regions in the west of Ireland are free of both species of squirrel, due to the isolation of forests there and their relatively recent planting. The potential of these forests as translocation sites for red squirrels was investigated to ascertain the possibility of increasing the range of red squirrels in Ireland. Nineteen red squirrels were moved into Derryclare wood, Co. Galway using a soft release into enclosures, and their subsequent survival and settlement in the wood was monitored, using trapping and radio-tracking. The successful release of 94.7% of squirrels from the enclosure, and 68.4% survival to the start of the following year’s breeding season were in excess of the target survival rates of 75 and 50%, respectively. Five of the females were found to be lactating in May 2006, and seven offspring captured in August 2006. A squirrel was observed in a follow-up visit in October 2007. Radio-tracked red squirrels tended to remain in the general vicinity of release, incorporating supplementary feeders as part of their home ranges. Squirrels also fed on the natural food available in the wood, with feeding signs readily observed in the wider woodland. The techniques used proved very successful in survival, retention and future reproduction of the translocated population. Timing of release may be an important consideration for future translocations with survival better in summer-released animals.     

Intraspecific variation in male mating strategies in an African ground squirrel (Xerus inauris)

Male mating strategies respond to female availability such that variation in resources that affect spatial distribution can also alter cost–benefit tradeoffs within a population. In arid‐adapted species, rainfall alters reproduction, behavior, morphology, and population density such that populations differing in resource availability may also differ in successful reproductive strategies. Here, we compare two populations of Cape ground squirrels (Xerus inauris), a sub‐Saharan species with year‐round breeding and intense mating competition. Unlike most mammals where males resort to aggressive interactions over females, male X. inauris are tolerant of one another, relying instead on other nonaggressive pre‐ and postcopulatory strategies to determine reproductive success. Our findings suggest that differences in resource availability affect female distribution, which ultimately leads to intraspecific variation in male reproductive tactics and sexual morphology. Sperm competition, assessed by reproductive morphometrics, was more pronounced in our high resource site where females were distributed evenly across the landscape, whereas dominance seemed to be an important determinant of success in our low resource site where females were more aggregated. Both sites had similar mating intensities, and most males did not sire any offspring. However, our low resource site had a higher variance in fertilization success with fewer males siring multiple offspring compared with our high resource site where more individuals were successful. Our results lend support to resource models where variations in female spatial distribution attributed to environmental resources ultimately impact male reproductive behaviors and morphology.     

Dispersal and recruitment during population growth in a colonial bird, the great cormorant Phalacrocorax carbo sinensis

While the factors influencing reproduction and survival in colonial populations are relatively well studied, factors involved in dispersal and settlement decisions are not well understood. The present study investigated exchanges of great cormorants Phalacrocorax carbo sinensis among six breeding colonies over a 13‐year period when the breeding population in Denmark increased from 2800 to 36 400 nests. We used a multistate capture‐recapture model that combined multisite resightings and recoveries to examine simultaneously recruitment, natal dispersal, breeding dispersal and annual survival of first‐year, immature and breeding great cormorants. Mean survival of first‐year birds (0.50±0.09, range=0.42–0.66 among colonies) was lower than survival of breeders (0.90±0.06, range=0.81–0.97). Mean survival of immature birds over the study period was 0.87±0.08. Dispersal from a colony increased with decreasing mean brood size in the colony in both first‐time and experienced breeders. The choice of the settlement colony in first‐time breeders was affected by conditions in the natal colony and in the colonies prospected during the pre‐breeding years. In particular, first‐time breeders recruited to colonies where they could expect better breeding success. Experienced breeders relied mainly on cues present early in the season and on their own breeding experience to choose a new breeding colony. Newly established colonies resulted mainly from the immigration of first‐time breeders originating from denser colonies. Dispersal was distance‐dependent and first‐time breeders dispersed longer distances than breeders. We suggest that the prospecting behaviour allows first‐time breeders to recruit in nearby as well as more distant potential breeding colonies. Dispersing breeders preferred to settle in neighbouring colonies likely to benefit from their experience with foraging areas. We discuss the importance of these movements for growth and expansion of the breeding population.     

Reproductive timing and reliance on hoarded capital resources by lactating red squirrels

Successful reproduction in a seasonal environment can be accomplished with resources that are stored before use (“capital resources”) or resources that are used immediately (“income resources”). Research examining capital versus income resource usage during reproduction has primarily focused on assigning species to positions along a capital–income gradient. Here, we examine the causes and reproductive consequences of among and within-year variation in hoarded capital versus income resource usage by female North American red squirrels (Tamiasciurus hudsonicus) during mid-lactation in a highly seasonal environment. Among years, the proportion of feeding events that were on capital resources (PROPCAP) averaged 39 % during the yearly median mid-lactation periods, but ranged widely between 2 and 100 %. In years with earlier parturition dates, females primarily used hoarded capital resources during mid-lactation, whereas in years with later parturition dates, females primarily used income resources during mid-lactation. Within years, PROPCAP during mid-lactation tended to be greater in early-breeding females than in late-breeding females. Rates of water flux in females during mid-lactation provided further evidence that late-breeding females used more water-rich income resources. The proportion of litters that were partially or completely lost, and the litter mass that lactating females supported, was not influenced by the large among-year differences in hoarded capital resource usage. Red squirrels appear to delay reproduction following years with low cone production to time peak reproductive demands to be late enough to be supported by income resources that only become available later in the season. In conclusion, our results offer a rare example of the capacity of a food-hoarding mammal to support reproduction exploiting a wide range of capital and income resources.