Density-dependence vs. density-independence - linking reproductive allocation to population abundance and vegetation greenness

1. Recent studies have shown that optimal reproductive allocation depends on both climatic conditions and population density. We tested this hypothesis using six years of demographic data from eight reindeer (Rangifer tarandus) populations coupled with data on population abundance and vegetation greenness [measured using the Enhanced Vegetation Index (EVI)]. 2. Female spring body mass positively affected summer body mass gain, and lactating females were unable to compensate for harsh winters as efficiently as barren ones. Female spring body mass was highly sensitive to changes in population abundance and vegetation greenness and less dependent on previous autumn body mass and reproductive status. Lactating females were larger than barren females in the spring. Moreover, female autumn body mass was positively related to female autumn body mass and reproductive success and was not very sensitive to changes in vegetation greenness and population abundance. 3. Offspring autumn body mass was positively related to both maternal spring and autumn body mass, and as predicted from theory, offspring were more sensitive to changes in vegetation greenness and population abundance than adult females. A lagged cost of reproduction was present as larger females who were barren, the previous year produced larger offspring than equally sized females that successfully reproduced the previous year. 4. Reproductive success was negatively related to female autumn body mass and positively related to female spring body mass. Moreover, females who successfully reproduced the previous year experienced the highest reproductive success. The fact that negative density-dependence was only present for females that had successfully reproduced the previous year further support the hypothesis that reproduction is costly. 5. This study shows that female reindeer buffer their reproductive allocation according to expected winter conditions and that their buffering abilities were limited by population abundance and a lagged cost of reproduction and enhanced by vegetation greenness.     

Observational evidence of risk-sensitive reproductive allocation in a long-lived mammal

Organisms should adopt a risk-sensitive reproductive allocation when summer reproductive allocation competes with survival in the coming winter. This trade off is shown through autumn female body mass, which acts as an insurance against unpredictable winter environmental conditions. We tested this hypothesis on female reindeer in a population that has experienced a time period of dramatic increase in abundance. Environmental conditions during winter were fairly stable (with the exception of 1 year). We conclude that increased population abundance (perhaps in interaction with winter environmental conditions) could have represented a worsening of winter environmental conditions as both autumn offspring and spring female body mass decreased during the course of the study. Moreover, we found that the cost of reproduction was related to environmental conditions as: (1) autumn body mass was larger for barren than for lactating females, and this difference was temporally highly variable; (2) lactating females produced smaller offspring than barren ones in the following year; and (3) reproductive output (offspring size) decreased over time. We also found evidence of quality effects as lactating females had a higher reproductive success in the following year. In sum, a worsening of winter conditions lead to: (1) decreased reproductive output; (2) lowered autumn body mass for lactating females; and (3) increased body mass for barren females. Since females reduce their reproductive allocation as winter conditions becomes more severe, we conclude that reindeer have adopted a risk-sensitive reproductive allocation.     

Population Densities,Vegetation Green-Up,and Plant Productivity: Impacts on Reproductive Success and Juvenile Body Mass in Reindeer

Global warming is expected to cause earlier springs and increased primary productivity in the Arctic. These changes may improve food availability for Arctic herbivores, but may also have negative effects by generating a mismatch between the surge of high quality food in the spring and the timing of reproduction. We analyzed a 10 year dataset of satellite derived measures of vegetation green-up, population densities, calf body masses and female reproductive success in 19 reindeer (Rangifer tarandus) populations in Northern Norway. An early onset of spring and high peak plant productivity had positive effects on calf autumn body masses and female reproductive success. In addition, body masses and reproductive success were both negatively related to population density. The quantity of food available, as determined by the onset of vegetation green-up and plant productivity over the summer were the main drivers of body mass growth and reproductive success. We found no evidence for an effect of the speed of spring green-up. Nor did we detect a negative mismatch between early springs and subsequent recruitment. Effects of global warming on plant productivity and onset of spring is likely to positively affect sub-Arctic reindeer.     

Effect of month and season of calving on the length of subsequent calving interval in Nili-Ravi buffaloes

Data pertaining to records of 1,274 calving intervals for 400 breeding buffaloes maintained at the Livestock Experiment Station, Qadirabad, District Sahiwal (Pakistan), were analyzed to investigate the magnitude of influence of month and season of calving on the length of subsequent calving interval. The longest average calving interval of 609.9 days was recorded for buffaloes calving in January, while the shortest average calving interval of 502.8 days was observed for those calving in June, the difference being highly significant (P < 0.01). When the data were split in accordance with season of calving, the calving intervals for buffaloes calving in winter, spring, summer and autumn averaged 569.1, 570.6, 506.6 and 515.7 days, respectively. The differences between intervals for winter and spring calvings and between intervals for summer and autumn calvings were non-significant. All other differences were highly significant (P < 0.01). Thus, in most of the buffaloes calving in winter or spring, the first post-partum oestrus and conception are delayed till the following autumn or winter, resulting in significantly longer calving intervals. In contrast, animals calving in summer or autumn exhibit post-partum heat and conception during autumn or winter, resulting in shorter calving intervals.     

Experimental evidence of cost of lactation in a low risk environment for a long-lived mammal

In a previous experiment we have documented that organisms adopt a risk-sensitive reproductive allocation when summer reproductive investment competes with survival in the coming winter ( Bårdsen et al. 2008 ). This tradeoff is present through autumn female body mass, which acts as an insurance against unpredictable winter environmental conditions. We tested this hypothesis experimentally on female reindeer experiencing stable and benign winter feeding conditions. Additional supplementary feeding and removal of newborns represented two sets of experimental manipulations. Females in the supplementary feeding group increased more in winter body mass relative to control females. This manipulation, however, did not have any effect on summer body mass development for neither females nor offspring, but we found a positive effect of feeding on offspring birth mass for smaller females. In contrast, offspring removal did have a positive effect on summer body mass development as females in this group were larger in the autumn relative to control females. In essence, we documented two immediate effects as: (1) supplementary feeding did have a positive effect on spring body mass for smaller females; and (2) offspring removal did increase the female summer somatic growth as this had a positive effect on female autumn body mass. Additionally, we tested for lagged effects, but we could not document any biologically significant effects of neither manipulation in the coming spring. The fact that we only found rather weak effects of both manipulations was as expected for risk sensitive individuals experiencing benign environmental conditions over many years.     

An individual reproduction model sensitive to milk yield and body condition in Holstein dairy cows

To simulate the consequences of management in dairy herds, the use of individual-based herd models is very useful and has become common. Reproduction is a key driver of milk production and herd dynamics, whose influence has been magnified by the decrease in reproductive performance over the last decades. Moreover, feeding management influences milk yield (MY) and body reserves, which in turn influence reproductive performance. Therefore, our objective was to build an up-to-date animal reproduction model sensitive to both MY and body condition score (BCS). A dynamic and stochastic individual reproduction model was built mainly from data of a single recent long-term experiment. This model covers the whole reproductive process and is composed of a succession of discrete stochastic events, mainly calving, ovulations, conception and embryonic loss. Each reproductive step is sensitive to MY or BCS levels or changes. The model takes into account recent evolutions of reproductive performance, particularly concerning calving-to-first ovulation interval, cyclicity (normal cycle length, prevalence of prolonged luteal phase), oestrus expression and pregnancy (conception, early and late embryonic loss). A sensitivity analysis of the model to MY and BCS at calving was performed. The simulated performance was compared with observed data from the database used to build the model and from the bibliography to validate the model. Despite comprising a whole series of reproductive steps, the model made it possible to simulate realistic global reproduction outputs. It was able to well simulate the overall reproductive performance observed in farms in terms of both success rate (recalving rate) and reproduction delays (calving interval). This model has the purpose to be integrated in herd simulation models to usefully test the impact of management strategies on herd reproductive performance, and thus on calving patterns and culling rates.     

Male-caused failure of female reproduction and its adaptive value in alpine marmots (Marmota marmota)

We studied reproductive performance of free-living alpine marmots (Marmotamarmota) for 14 years in the National Park of Berchtesgaden, Germany.Female reproduction was influenced by body condition and social factors.Reproduction depleted fat reserves, and only females emergingfrom hibernation with sufficient body mass were able to reproducesuccessfully. Marmots lived in social groups in territoriesdefended by a dominant male and female. Subordinate femalesnever reproduced, regardless of body mass. Territory takeoversby males impaired reproduction of dominant females, but onlyif the takeover occurred after the mating period. Reproductivefailures occurred despite clear signs of pregnancy such enlargednipples or late molt. Decreasing progesterone levels after themating period and the lack of evidence for direct infanticideby new territorial males suggest a block of pregnancy as a likelyexplanation for reproductive failures in groups with male takeoversduring gestation. Rendering female reproduction impossible increasedfuture reproductive success of new territory owners. Nonparous femalessaved the energetic cost of maternal investment and thus emergedwith higher body mass in the following spring. In line withthis, females failing to wean young had higher reproductivesuccess in the subsequent year.     

Life history patterns of a livebearing fish in contrasting environments

Summary The population dynamics and energy allocations of the Gila topminnow, a small livebearing fish, were studied in two contrasting environments, a spring run of constant characteristics and a fluctuating desert wash. Topminnows grew and matured in two basic patterns. First, many fish in both areas matured the year after their birth. Second, spring fish born early in the breeding season grew rapidly, bred within five months, and died by eight months of age. Although spring fish assimilated more energy, wash fish actually expended more calories for growth and reproduction, partly because of lower maintenance costs. Reproductive effort of long-lived spring fish varied with age between 3.1 and 6.5%; whereas efforts of short-lived spring and wash fish increased steadily with age to 5.2 and 9.8%, respectively. Although spring fish produced eggs of higher energy content, females in both areas varied their investment per offspring, apparently tracking seasonal changes in the availability of food for fry. When long-lived spring fish experienced food shortage, they allocated less energy to both growth and reproduction; in contrast, wash and short-lived spring fish under similar conditions reduced only their growth allocation. The reproductive mass in spring fish appeared to be limited by food availability, incompletely filled the abdominal space, and reflected no tradeoff between fecundity and investment per offspring. Reproduction by wash fish appeared to be limited by body space and was characterized by a tradeoff between fecundity and egg size.     

Egg investment in response to helper presence in cooperatively breeding Tibetan ground tits

Life‐history theory predicts a trade‐off between current and future reproduction to maximize lifetime fitness. In cooperatively breeding species, where offspring care is shared between breeders and helpers, helper presence may influence the female breeders’ egg investment, and consequently, survival and future reproductive success. For example, female breeders may reduce egg investment in response to helper presence if this reduction is compensated by helpers during provisioning. Alternatively, female breeders may increase egg investment in response to helper presence if helpers allow the breeders to raise more or higher quality offspring successfully. In the facultatively cooperative‐breeding Tibetan ground tit Pseudopodoces humilis, previous studies found that helpers improve total nestling provisioning rates and fledgling recruitment, but have no apparent effects on the number and body mass of fledglings produced, while breeders with helpers show reduced provisioning rates and higher survival. Here, we investigated whether some of these effects may be explained by female breeders reducing their investment in eggs in response to helper presence. In addition, we investigated whether egg investment is associated with the female breeder's future fitness. Our results showed that helper presence had no effect on the female breeders’ egg investment, and that egg investment was not associated with breeder survival and reproductive success. Our findings suggest that the responses of breeders to helping should be investigated throughout the breeding cycle, because the conclusions regarding the breeders’ adjustment of reproductive investment in response to being helped may depend on which stage of the breeding cycle is considered.     

Reproductive performance in female common hamsters

We monitored individual reproductive timing and output in a common hamster population in Vienna over a 3-year period. Animals were live-trapped, weighed, individually marked, and reproductive status was determined at capture. Costs of reproduction were investigated by measuring body condition shortly before hibernation and overwinter survival. Our results indicated that early emerging females had more litters and weaned more offspring per season. Body mass throughout the active season did not differ significantly between females with high and low reproductive output. High reproductive output seemed to affect the duration of the active season. Successful females had a longer postreproduction period before hibernation than less successful ones, probably serving to balance the costs of reproductive effort by extended preparation for hibernation. Also, females that had emerged early in spring and had high reproductive success were more likely to survive the subsequent winter. Hence, we found female common hamsters to vary strongly in maternal investment capacity and to tailor reproductive strategies accordingly.     

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.     

Maternal winter body mass and not spring phenology determine annual calf production in an Arctic herbivore

Warming of the Arctic has resulted in earlier snowmelt and green‐up of plants in spring, potentially disrupting the synchrony between plant phenology and breeding phenology in herbivores. A negative relationship between offspring survival in West Greenland caribou and the timing of vegetation emergence was the first finding of such a mismatch in Arctic mammals. However, other studies indicate that the energy for foetal growth and early lactation is predominantly drawn from stored energy reserves typical of ‘capital’ breeders, suggesting that conditions well before spring influence calf production more than the timing of spring onset. Here we use 20 years of observations of marked Svalbard reindeer to evaluate determinants of annual recruitment, as measured by the presence of a calf at foot in mid‐summer. Spring temperatures and the enhanced vegetation index were used as proxies for spring onset, while data on body mass and pregnancy rates in late winter allowed us to determine maternal condition and the reproductive status before spring. Pregnancy rate, offspring survival and annual recruitment were all strongly correlated with average late winter adult female body mass (r = 0.87; r = 0.83; r = 0.92, respectively). Contrary to the findings in West Greenland, neither early calf survival nor annual recruitment were correlated with the two measures of annual variation in spring phenology (r = – 0.07, p = 0.8 and r = – 0.15, p = 0.6, respectively). We also revisit the Greenland data and reveal that the pattern of covariance between early and late measures of fecundity, as well as between early measures of fecundity and offspring survival, correspond with the results from Svalbard. Our results emphasize that conditions affecting maternal body mass during winter explain close to all the variation in recruitment, questioning the importance of the role of a mismatch between plant phenology and calving date.     

Influences of the feeding ecology on body mass and possible implications for reproduction in the edible dormouse (<Emphasis Type="Italic">Glis glis</Emphasis>)

The edible dormouse (Glis glis) is a small rodent and an obligate hibernator. Dormice undergo strong fluctuations of reproductive output during years that seem to be timed to coincide with future food supply. This behaviour enables them to avoid producing young that will starve with a high probability due to food shortage, and to increase their lifetime reproductive success. Aims of this study were to elucidate the extent to which feeding ecology in the edible dormouse has an impact on body mass and the fatty acid (FA) pattern of the white adipose tissue (WAT) before and after hibernation, which in turn might influence reproductive status in spring. Dormice show strong seasonal fluctuations of the body mass, which is reduced by one third during hibernation. Body mass and its changes depend on autumnal food availability as well as on the dietary FA pattern. During the pre-hibernation fattening period, dormice eat lipid rich food with a high content of linoleic acid. During hibernation, linoleic acid content is slightly but significantly reduced and body mass loss during winter is negatively correlated with the pre-hibernation linoleic acid content in the WAT. No relation between reproductive status and body mass, body condition or the FAs pattern of the WAT could be detected. However, in a year of high reproduction, dormice commence the shift to seed eating earlier than in a year of low reproduction. These seeds could be either a predictor for future food supply in autumn, or represent a high-energy food compensating high energetic costs of sexual activity in male edible dormice.     

Tradeoff between offspring mass and subsequent reproduction in a highly iteroparous mammal

When resources are limited, current maternal investment should reduce subsequent reproductive success or survival. We used longitudinal data on marked mountain goats Oreamnos americanus to assess if offspring mass at weaning affected maternal survival and future reproduction. Offspring mass was positively correlated with survival of old mothers, suggesting that mothers produced lighter kids, and hence reduced reproductive effort, in their last reproduction. Offspring mass at weaning did not affect survival of young and prime‐aged mothers, but females that had weaned heavy offspring had a reduced probability of subsequent reproduction in years of low population density. Because offspring survival is correlated with weaning mass, mothers’ allocation to reproduction involves a tradeoff between current and future fitness returns. We demonstrate for the first time that allocation to current offspring mass in an iteroparous mammal reduces the probability of subsequent reproduction.     

Influences of weather on reproductive function in male Song sparrows, Melospiza melodia

The avian reproductive cycle is integrated and timed by a variety of environmental factors that include day length, availability of food, nest sites, presence of a mate, etc. However, reproduction can be delayed or disrupted by inclement weather and, until recently, the endocrine responses of avian species to storms were entirely unknown. This communication describes changes in endocrine state in free-living male Song sparrows, Melospiza melodia, during gonadal recrudescence after a severe winter, and in response to storms in early spring and summer. Both the severe winter weather and an early spring snow storm delayed testicular development, and depressed circulating levels of testosterone. The sparrows did not appear to be stressed, however, since body mass and fat deposits were higher than in birds sampled during the previous spring after a less severe winter.
A second storm occurred in late May and early June when Song sparrows were feeding young. Curiously, plasma levels of testosterone were not affected, but the sparrows did appear to be stressed since there was a significant decline in body mass, and a marked increase in circulating levels of corticosterone. These data suggest that the effects of inclement weather on reproductive function can vary in relation to the stage in the reproductive cycle when the storm strikes, and that the endocrine mechanisms underlying acclimatization to severe meteorological conditions are also different.     

Seasonal control over allocation to reproduction in a tussock-forming and a rhizomatous species of Eriophorum in central Alaska

Summary The evergreen tussock-forming Eriophorum vaginatum revealed consistently earlier (c. 1 moth) phenology and greater biomass per tiller than the summergreen rhizomatous E. scheuchzeri in all four components measured (vegetative and reproductive shoots and stems) under the same climatic regime in central Alaska over one growing season. Greatest allocation to vegetative shoot growth occurred in mid-summer in both species. The tussock growth form of E. vaginatum raised shoot meristems 25–30 cm above the soil surface, where temperatures were warmer, permitting shoot growth to begin earlier in spring and continue longer in autumn than in E. scheuchzeri. Consequently, E. vaginatum was able to allocate reserves to reproductive tillers primarily in autumn and early spring, times when minimal reserves were required for vegetative growth. By contrast, the rhizomatous E. scheuchzeri had a more constrained growing season, and allocation to reproduction coincided with allocation to vegetative growth. For this reason, reserves were drawn down more fully in mid-summer in E. scheuchzeri than in E. vaginatum. The more conservative use of nutrient stores in E. vaginatum may relate to its great longevity, reduced allocation to reproduction (including low seedling recruitment), and relatively stable habitats. The mid-seasonal pulse of allocation to reproduction in E. scheuchzeri appears viable only in relatively fertile disturbed sites, where the soil nutrient supply is sufficient to support simultaneous allocation to vegetative growth and reproduction.     

Reproductive biology of Philodryas patagoniensis (Snakes: Dipsadidae) in south Brazil: Female reproductive cycle

In this study, we describe the female reproductive cycle of Philodryas patagoniensis in south Brazil, which was described through morpho‐anatomical and histological analyses. The peak of secondary vitellogenesis occurred during winter–spring (July–December), ovulation in spring (October–December), mating and fertilization in spring–summer (October–February), oviposition in spring–autumn (October–May) and births from late spring to autumn (December–July). The diameter of vitellogenic follicles/eggs was larger in winter–spring than in other seasons. The diameter of the shell glands was also larger in winter–spring. In spite of the clear reproductive peak, gonads only showed reduced activity in the autumn. Therefore, at the individual level, females have a discontinuous cyclical reproduction; in the populational level, the reproductive cycle is seasonal semisynchronous. We support the hypothesis that P. patagoniensis have the ability to produce multiple clutches with long‐term stored sperm. Sexual dimorphism in body size was evident, and females are significantly larger and heavier than males. Larger females were able to produce follicles and eggs in larger amount and size. The maternal body size was positively related to the reproductive effort and fecundity. To conclude, we deliberated about the proximal and distal causes that influence the reproductive traits and patterns of P. patagoniensis.     

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.     

Twelve fundamental life histories evolving through allocation‐dependent fecundity and survival

An organism's life history is closely interlinked with its allocation of energy between growth and reproduction at different life stages. Theoretical models have established that diminishing returns from reproductive investment promote strategies with simultaneous investment into growth and reproduction (indeterminate growth) over strategies with distinct phases of growth and reproduction (determinate growth). We extend this traditional, binary classification by showing that allocation‐dependent fecundity and mortality rates allow for a large diversity of optimal allocation schedules. By analyzing a model of organisms that allocate energy between growth and reproduction, we find twelve types of optimal allocation schedules, differing qualitatively in how reproductive allocation increases with body mass. These twelve optimal allocation schedules include types with different combinations of continuous and discontinuous increase in reproduction allocation, in which phases of continuous increase can be decelerating or accelerating. We furthermore investigate how this variation influences growth curves and the expected maximum life span and body size. Our study thus reveals new links between eco‐physiological constraints and life‐history evolution and underscores how allocation‐dependent fitness components may underlie biological diversity.     

Determinants and consequences of age of primiparity in bighorn ewes

Because variation in age of first reproduction can have major effects on individual fitness and population dynamics, it is important to understand what maintains that variability. Although early primiparity is assumed to be costly, it is sometimes associated with high lifetime reproductive success. We used a long‐term study on bighorn sheep Ovis canadensis to determine what variables affect age at first reproduction, investigate the impact of primiparity on body resources and quantify the reproductive performance of primiparous ewes. We then examined the consequences of delayed primiparity on adult body mass, longevity and lifetime reproductive success. Environmental conditions during early development, body mass as a yearling, genotype and maternal effects affected age of primiparity. Primiparous ewes lost more mass in winter and gained less mass in summer than multiparous ewes. Small yearling ewes that postponed reproduction attained similar adult mass than heavy yearling ewes who reproduced at a younger age. Early primiparity did not reduce longevity and was positively associated with lifetime reproductive success. Starting to reproduce as soon as possible appears to maximize fitness of females. When early life conditions are unfavorable, however, delayed primiparity allows greater body growth and likely maximizes survival. The combination of a conservative reproductive strategy and maternal effects on age of primiparity may partly delay population recovery following density‐dependent declines.