Early‐life conditions impact juvenile telomere length,but do not predict later life‐history strategies or fitness in a wild vertebrate

Environmental conditions experienced during early life may have long‐lasting effects on later‐life phenotypes and fitness. Individuals experiencing poor early‐life conditions may suffer subsequent fitness constraints. Alternatively, individuals may use a strategic “Predictive Adaptive Response” (PAR), whereby they respond—in terms of physiology or life‐history strategy—to the conditions experienced in early life to maximize later‐life fitness. Particularly, the Future Lifespan Expectation (FLE) PAR hypothesis predicts that when poor early‐life conditions negatively impact an individual''s physiological state, it will accelerate its reproductive schedule to maximize fitness during its shorter predicted life span. We aimed to measure the impact of early‐life conditions and resulting fitness across individual lifetimes to test predictions of the FLE hypothesis in a wild, long‐lived model species. Using a long‐term individual‐based dataset, we investigated how early‐life conditions are linked with subsequent fitness in an isolated population of the Seychelles warbler Acrocephalus sechellensis. How individuals experience early‐life environmental conditions may vary greatly, so we also tested whether telomere length—shorter telomers are a biomarker of an individual''s exposure to stress—can provide an effective measure of the individual‐specific impact of early‐life conditions. Specifically, under the FLE hypothesis, we would expect shorter telomeres to be associated with accelerated reproduction. Contrary to expectations, shorter juvenile telomere length was not associated with poor early‐life conditions, but instead with better conditions, probably as a result of faster juvenile growth. Furthermore, neither juvenile telomere length, nor other measures of early‐life conditions, were associated with age of first reproduction or the number of offspring produced during early life in either sex. We found no support for the FLE hypothesis. However, for males, poor early‐life body condition was associated with lower first‐year survival and reduced longevity, indicating that poor early‐life conditions pose subsequent fitness constraints. Our results also showed that using juvenile telomere length as a measure of early‐life conditions requires caution, as it is likely to not only reflect environmental stress but also other processes such as growth.     

High red deer density depresses body mass of roe deer fawns

Many previous studies have pointed out that, when resources are limited, the potential for competition should be high among sympatric species that display overlaps in habitat and nutritional niches. However, reliable evidence of competition between red deer (Cervus elaphus) and roe deer (Capreolus capreolus) has not been yet reported for life history traits directly measuring performance such as body mass, reproduction, or survival. From long-term monitoring of deer populations in the reserve of La Petite Pierre (France), we measured the sex-specific responses of roe deer fawn body mass to changes in red deer density after accounting for possible confounding effects of date of shooting, climatic conditions, and roe deer density. As expected under the hypothesis of competition, red deer density in a given year had a marked negative influence on body mass of roe deer fawns born the same year and the following year. Fawn mass of roe deer males and females responded in similar ways to changes in red deer density. Our study provides the first evidence of a negative response of roe deer performance to high red deer density.     

Variations in adult body mass in roe deer: the effects of population density at birth and of habitat quality

Body mass is a key determinant of fitness components in many organisms, and adult mass varies considerably among individuals within populations. These variations have several causes, involve temporal and spatial factors, and are not yet well understood. We use long-term data from 20 roe deer cohorts (1977-96) in a 2600 ha study area (Chizé, western France) with two habitats contrasting in quality (rich oak forest in the North versus poor beech forest in the South) to analyse the effects of both cohort and habitat quality on adult mass (i.e. median body mass between 4 and 10 years of age) of roe deer (Capreolus capreolus). Cohort strongly influenced the adult body mass of roe deer in both sexes: males born in 1994 were 5.2 kg heavier when aged between 4 and 10 years old than males born in 1986, while females born in 1995 were 4.7 kg heavier between 4 and 10 years old than females born in 1982. For a given cohort, adult males were, on average, 0.9 kg heavier in the rich oak forest than in the poor beech forest. A similar trend occurred for adult females (0.5 kg heavier in the oak forest). The effects of cohort and habitat were additive and accounted for ca. 40% of the variation observed in the adult mass of roe deer at Chizé (males: 41.2%; females: 40.2%). Population density during the spring of the birth accounted for about 35% of cohort variation, whereas rainfall in May-June had no effect. Such delayed effects of density at birth on adult body mass probably affect population dynamics, and might constitute a mechanism by which delayed density-dependence occurs in ungulate populations.     

Bigger teeth for longer life? Longevity and molar height in two roe deer populations

The role of tooth wear as a proximate cause of senescence in ruminants has recently been highlighted. There are two competing hypotheses to explain variation in tooth height and wear; the diet-quality hypothesis predicting increased wear in low-quality habitats, and the life-history hypothesis predicting molar height to be related to expected longevity. We compared tooth height and wear from roe deer of known age from two contrasting populations of roe deer (Capreolus capreolus) in France: Trois Fontaines (TF) with good habitat and shorter animal life expectancy and Chizé (CH) with poor habitat and longer animal life expectancy. There was no population difference in tooth wear, leading to rejection of the diet-quality hypothesis. However, despite their smaller body size, initial molar height for animals from CH was larger than for animals from TF. This provides the first evidence that variation in longevity between populations can lead to differences in molar height within a species.     

European Roe Deer Increase Vigilance When Faced with Immediate Predation Risk by Eurasian Lynx

Prey animals must balance antipredatory behaviour with foraging behaviour. According to the risk allocation hypothesis, prey increase antipredatory behaviour and reduce foraging activity during pulses of high risk, but with continuous risk, other activities must continue and antipredatory behaviour decreases despite the risk. We studied the impact of lynx presence on the vigilance behaviour of wild roe deer under conditions of (i) a pulsed elevated risk by experimentally spreading lynx urine as an olfactory cue, and (ii) continuous risk by comparing an area where lynx was eradicated 160 years ago to an area where lynx has been re‐introduced 30 years ago. Roe deer were extremely vigilant in response to the predator olfactory cue; however, roe deer vigilance did not differ measurably among areas with or without potential lynx presence. Deer were more vigilant before sunset than during the night at both study areas, probably due to long‐term adaptation of roe deer to human hunting during daytime. Vigilance decreased from August to September even though activity of lynx increases in autumn, which may be a result either of increased foraging due to decrease in food quality in autumn, or of changes in social organization of the deer. Our results suggested that the degree of vigilance depends on environmental cues. We found that roe deer respond to lynx urine despite a long absence of lynx in the ecosystem. Our results support the risk allocation hypothesis for responses to pulses of high risk but not for responses to continuous elevated levels of risk.     

Reproductive constraints,not environmental conditions,shape the ontogeny of sex‐specific mass–size allometry in roe deer

In polygynous mammals, sex‐specific patterns of body growth are linked to divergent selection pressures on male and female body size, resulting in sexual dimorphism (SD). For males, reproductive success is generally linked to body size, hence, males should prioritise early growth. For females, reproductive success is linked to resource availability, so they may adopt a more conservative growth tactic. Using longitudinal monitoring of known‐age animals in two contrasting populations and an allometric approach to disentangle the relative contribution of structural size and physiological condition to SD, we addressed these issues in the weakly polygynous roe deer. Despite very different environmental conditions, we found remarkably similar patterns in the two populations in the mass–size allometric relationship at each life history stage, suggesting that relative allocation to structural size and physiological condition is highly constrained. SD in structural size (indexed by hind foot length) involved sex‐specific growth trajectories governed by a single mass–size allometric relationship during the juvenile stage, such that males were both bigger and heavier than females. In contrast, SD in physiological condition (indexed by the allometric relationship between body mass and hind foot length, expressed as body mass for a given body size) developed markedly during the sub‐adult stage in relation to sex differences in the timing of first reproduction. Among adults, males were heavier for a given size than females, suggesting that, relative to females, males express a capital breeder tactic, accumulating fat reserves to offset reproductive costs. By the senescent stage, SD in physiological condition had disappeared, with both sexes governed by a single allometric relationship, suggesting more rapid senescence in males than females. Individuals born into poor cohorts were generally lighter for a given size, indicating growth priority for skeletal size over physiological condition in both sexes. However, sex differences in cohort effects among sub‐adults resulted in lower size‐specific SD in poor cohorts, indicating that body condition of sub‐adult females is buffered against environmental harshness. We conclude that sex‐differences in reproductive tactics impose constraints on the ontogeny of SD in roe deer, leading to sex‐specific trajectories in structural size and physiological condition.     

Cohort effects in red squirrels: the influence of density, food abundance and temperature on future survival and reproductive success

1. Environmental conditions experienced early in life may have long-lasting effects on individual performance, thereby creating 'silver-spoon effects'. 2. We used 15 years of data from a North American red squirrel (Tamiasciurus hudsonicus Erxleben) population to investigate influences of food availability, density and spring temperature experienced early in life on reproduction and survival of female squirrels during adulthood. 3. We found that spring temperature and food availability did not affect female survival after 1 year of age, whereas higher squirrel densities led to lower survival, thereby affecting longevity and lifetime fitness. 4. In addition, both food availability experienced between birth and weaning, and spring temperature in the year of birth, had long-lasting positive effects on female reproductive success. These results emphasize the critical effect environmental conditions during the early life stages can have on the lifetime performance of small mammals. 5. These long-term effects of early food and temperature were apparent only once we controlled for conditions experienced during adulthood. This suggests that silver-spoon effects can be masked when conditions experienced early in life are correlated to some environmental conditions experienced later in life. 6. The general importance of silver-spoon effects for adult demographic performance might therefore be underestimated, and taking adult environment into account appears to be necessary when studying long-term cohort effects.     

Mismatch Between Birth Date and Vegetation Phenology Slows the Demography of Roe Deer

Marked impacts of climate change on biodiversity have frequently been demonstrated, including temperature-related shifts in phenology and life-history traits. One potential major impact of climate change is the modification of synchronization between the phenology of different trophic levels. High phenotypic plasticity in laying date has allowed many bird species to track the increasingly early springs resulting from recent environmental change, but although changes in the timing of reproduction have been well studied in birds, these questions have only recently been addressed in mammals. To track peak resource availability, large herbivores like roe deer, with a widespread distribution across Europe, should also modify their life-history schedule in response to changes in vegetation phenology over time. In this study, we analysed the influence of climate change on the timing of roe deer births and the consequences for population demography and individual fitness. Our study provides a rare quantification of the demographic costs associated with the failure of a species to modify its phenology in response to a changing world. Given these fitness costs, the lack of response of roe deer birth dates to match the increasingly earlier onset of spring is in stark contrast with the marked phenotypic responses to climate change reported in many other mammals. We suggest that the lack of phenotypic plasticity in birth timing in roe deer is linked to its inability to track environmental cues of variation in resource availability for the timing of parturition.     

The cost of growing large: costs of post‐weaning growth on body mass senescence in a wild mammal

Individual body mass often positively correlates with survival and reproductive success, whereas fitness costs of growing large are rarely detected in vertebrates in the wild. Evidence that adult body mass progressively declines with increasing age is accumulating across mammalian populations. Growing fast to a large body can increase the cellular damage accumulated throughout life, leading body growth in early life to be negatively associated with the rate of body mass senescence. Moreover, the onset of mass senescence may strongly depend on both sex‐specific reproductive tactics and environmental conditions. Assessing the timing and the rate of body mass decline with increasing age thus offers an opportunity to look for costs of having grown fast, especially after a poor start during early life, in both sexes and in different environments. Using a unique dataset including 30 years of longitudinal data on age‐specific body mass collected in two roe deer Capreolus capreolus populations subjected to contrasted environmental conditions, we looked for potential costs of high post‐weaning growth rate in terms of steeper rate of body mass senescence. Our analyses of body mass senescence accounted for the potential variation in the onset of senescence and allowed explicit comparisons of this variable between sexes and populations. Higher growth rates late in the growing period (after weaning) were associated with a steeper rate of body mass senescence, regardless of early mass (gained before weaning), but at different extents depending on sex and environmental conditions. Body mass senescence occurred earlier in males than in females, especially in the population facing limiting resources. In the wild, although heavy individuals generally survive better than small ones, the costs of growing large late in the growing period only became apparent late in life through mass senescence.     

Impact of environmental diversity of hunting complexes in the Lublin region on ontogenetic quality indicators in roe deer (<Emphasis Type="Italic">Capreolus capreolus</Emphasis>)

Populations of game are not confined to single ecosystems but function within higher-order units, e.g. ecological landscape. The basis for the establishment of the hunting complexes was the assumption that the existing game hunting grounds, i.e. the basic units implementing game management, are too small and do not cover the natural areas inhabited by game populations. Roe deer are flexible species and easily adapt to various site conditions, so they inhabit many different habitats, from large forest complexes, through small in-field tree stands and shrubs, to treeless grounds and field monocultures. The aim of the study was to determine a possible impact of environmental conditions prevailing in the hunting complexes of the Regional Directorate of State Forests (RDLP in Lublin) on the ontogenetic quality of roe deer. The study was conducted on 518 European roe deer (Capreolus capreolus) aged from 4 to 7 years (379 bucks and 139 does) harvested within hunting seasons 2010/2011–2013/2014. The results have shown that animals originating from areas with greater forest cover and denser stands are characterised by lower values of the mean ontogenetic quality parameters (carcase weight, kidney fat index, chest girth, weight of antlers) in comparison with animals from typical agricultural areas with fragmented forest complexes. These results indicate that, even in the case of such a eurytopic species as the roe deer, the ontogenetic quality differs between individual hunting complexes. The study has proved that strategies for hunting management of the roe deer should take into account the impact of the landscape structure, which provides a rationale behind creation of hunting complexes.     

Experimental induction of luteal cyclicity in roe deer (Capreolus capreolus).

Concentrations of progesterone and luteinizing hormone in plasma were analysed for two consecutive years in samples from nonpregnant female roe deer. Three animals were treated with monthly prostaglandin injections (325 micrograms cloprostenol) from October 1989 to April 1990 and from October 1990 to March 1991, and three were kept as controls. In control animals, a small increase in progesterone concentrations in July 1990 occurred at the same time as the commencement of the rut in other husbanded roe deer. In prostaglandin-treated animals, progesterone concentration was high at the time of the rut and remained so until late February 1990. After the next rut (August 1990), progesterone concentration remained high until March 1991. Between October and February-March, injections of prostaglandins induced dramatic, but temporary (lasting 72 h), decreases in plasma progesterone concentrations, indicating luteal regression and subsequent ovulation. We infer that roe deer can ovulate repeatedly and should therefore not be regarded as an obligate monoestrous species.     

Habitat use under predation risk: hunting, roads and human dwellings influence the spatial behaviour of roe deer

Wildlife populations are subjected to increasing pressure linked to human activities, which introduce multiple stressors. Recently, in addition to direct effects, it has been shown that indirect (non-lethal) effects of predation risk are predominant in many populations. Predation risk is often structured in space and time, generating a heterogeneous “landscape of fear” within which animals can minimize risks by modifying their habitat use. Furthermore, for ungulates, resource quality seems to be positively correlated with human-related sources of risk. We studied the trade-off between access to resources of high-quality and risk-taking by contrasting habitat use of roe deer during daytime with that during nighttime for 94 roe deer in a hunted population. Our first hypothesis was that roe deer should avoid human disturbance by modifying their habitat use during daytime compared to nighttime. Our results supported this, as roe deer mainly used open fields during nighttime, but used more forested habitats during daytime, when human disturbance is higher. Moreover, we found that diel patterns in habitat use were influenced by hunting disturbance. Indeed, the roe deer decreased their use of high-crops during daytime, an important source of cover and food, during the hunting season. The proximity of roads and dwellings also affected habitat use, since roe deer used open fields during daytime to a greater extent when the distance to these sources of disturbance was higher. Hence, our results suggest that roe deer resolve the trade-off between the acquisition of high-quality resources and risk avoidance by modifying their habitat use between day and night.     

Effects of cohort,sex, and birth date on body development of roe deer (Capreolus capreolus) fawns

We investigated the effects of the year of birth (cohort effect), sex and birth date on the variations observed in birth weight and postnatal growth rate in 209 newborn fawns marked during eight consecutive fawning seasons from a highly productive roe deer population under good nutritional conditions. Roe deer exhibited a fast body development with a birth weight of 1628 g and a postnatal growth rate of 139 g/day constant over the first 20 days of their life. As previously reported for dimorphic and polygynous ungulates, there was a marked cohort effect on the rate of body development. This variability was partly explained by climatic conditions during late gestation. When fewer than 5 days with rainfall over 5 mm occurred in April, fawns were heavier. High temperatures during April and during the winter could also be involved in fast body development of roe deer fawns. Sex of fawn did not affect roe deer growth pattern. This was expected on the basis of low sexual dimorphism in size and low polygyny level characteristic of roe deer. Lastly, the date of birth did not affect the body development of roe deer fawns. High constancy of mean birth dates and high synchrony of births observed in this population could account for this result.     

Comparing life expectancy of three deer species between captive and wild populations

Life in zoological gardens provides a number of benefits to captive animals, resulting in an artificial reduction of the “struggle for life” compared to their free-ranging counterparts. These advantages should result in a higher chance of surviving from 1 year to the next, and thus in longer average life expectancies for captive animals, given that the biological requirements of the species are adequately met. Here, we compare the life expectancy of captive and free-ranging populations of three deer species (reindeer Rangifer tarandus, red deer Cervus elaphus, and roe deer Capreolus capreolus). Whereas captive reindeer and red deer had life expectancies equal to or longer than free-ranging individuals, the life expectancy of captive roe deer was shorter than that of free-ranging animals. These results support the impression that roe deer are difficult to keep in zoos, whereas reindeer and red deer perform well under human care. We suggest that the mean life expectancy of captive populations relative to that of corresponding free-ranging populations is a reliable indicator to evaluate the husbandry success of a species in captivity.     

Seasonal variation of activity patterns in roe deer in a temperate forested area

We investigated the activity patterns of a European roe deer (Capreolus capreolus) population living in a forested Apennine area in central Italy, in order to shed light on the environmental and biological factors that were expected to account for the observed activity patterns on daily and yearly bases. Daily and seasonal activity patterns of 31 radio-collared roe deer were assessed through sessions of radio tracking for a total period of 18 consecutive months. Roe deer showed bimodal activity patterns throughout the year, with the two highest peaks of activity recorded at dawn and dusk. Activity patterns of males and females differed during the territorial period (from early spring to late summer), whereas they did not during the nonterritorial period. Most likely, behavioral thermoregulation can be held responsible for variation of daily activity patterns in different seasons. In winter, for instance, activity during the dawn period was significantly higher than in other seasons and daylight activity was significantly higher than at night. Nocturnal activity was highest in summer and lowest in winter. During the hunting season, moreover, roe deer showed lower activity levels than during the rest of the year. The prediction that roe deer would show lower activity levels during full moon nights, when the predation risk was assumed to be higher, was not confirmed by our data. Activity rhythms in roe deer were thus subjected to both endogenous and environmental factors, the latter working as exogenous synchronization cues. Accordingly, in changing environmental and ecological conditions, a circadian cycle of activity could be seen as the result of complex interactions among daily behavioral rhythm, digestive physiology, and external modifying factors.     

Species variation in the distribution of cholinesterases in the ovary of the plains viscacha, cat, ferret, rabbit, rat, guinea-pig and roe deer

Synopsis Sections of ovary from plains viscacha, cat, ferret, rabbit, rat, guinea-pig and roe deer have been histochemically processed to demonstrate acetylcholinesterase (AChE) and butyrylcholinesterase (BuChE) in nervous and non-nervous tissue. The effects of different reproductive states on enzyme activity were observed in some animals. AChE-containing nerves were sparse in rabbit and rat but plentiful in cat and roe deer. Nerves containing BuChE were not detectable in ferret or guinea-pig and were rare in cat. Species variations in the activity and type of enzyme were also found in non-neuronal tissues. Some blood vessels in the ovaries of guinea-pig and viscacha contained AChE. No other species showed a reaction for AChE in non-neuronal stromal tissue but BuChE was present at this site in all animals except rat. Granulosa cells reacted for AChE only in cat and rabbit while luteal cells were reactive in cat, rabbit and roe deer. Some BuChE activity was present in granulosa and or luteal cells in all species except roe deer. In rat, BuChE activity in luteal cells increased during oregnaney and the early phase of pseudopregnancy. The difficulty of assigning a function to ovarian cholinesterases is discussed.     

Vole fluctuations,red fox responses,predation on fawns,and roe deer dynamics in a temperate latitude

The alternative prey hypothesis predicts that predators respond both functionally and numerically (with a time lag) to fluctuations in the main prey abundance, which affects the survival of alternative prey. This pattern was found in northern Europe in the community formed by voles (Microtidae), red foxes (Vulpes vulpes) and roe deer (Capreolus capreolus). We studied the same predator—prey community in a temperate latitude where, according to the predation hypothesis, only the functional response of predators to changes in main prey availability should occur. In the years 1997–2007, in western Poland, we estimated the index of common vole (Microtus arvalis) abundance (burrow counts), the density of foxes (spotlight counts), the young production in foxes (young/adult ratio), the index of fox predation on fawns (prey remains near dens) as well as the reproduction index (fawn/female ratio) and density of roe deer (total counts). The vole abundance fluctuated considerably, the young production in foxes did not correlate with the main prey availability, but the density of foxes showed direct numerical response. The index of fox predation on fawns decreased with the vole abundance and negatively affected the fawn/female ratio in roe deer. Thus, the relationships between voles and foxes were not fully consistent with the predation hypothesis. The direct numerical response of foxes should tend to stabilize this predator—prey community. It is suggested, however, that responses showed by vole-eating predators in temperate latitudes may sometimes affect their alternative prey, including animals with unfavourable conservation status.     

Dispersal is not female biased in a resource-defence mating ungulate, the European roe deer

Dispersal is frequently more prevalent in one sex compared to the other. Greenwood proposed that patterns of sex-biased dispersal among birds and mammals are linked to their mating strategies. For species where males defend resources rather than females, he predicted female-biased dispersal, because males should remain at their birth site where they are familiar with the distribution of the resources that they must defend. Greenwood's hypothesis has been extensively supported among birds, where most species exhibit a resource-defence mating strategy. However, almost no equivalent information is available for mammals as males generally defend mates in this group. An exception is the European roe deer, a resource-defence mating ungulate. We thus tested Greenwood's hypothesis on this atypical mammalian model, looking for female-biased dispersal using sex-specific inter-individual genetic distances. We conclusively show that gene flow is not higher among females compared to males in the studied roe deer population, and hence that dispersal is not female-biased, suggesting that male mating strategy is not the primary selective force driving the evolution of dispersal in roe deer. We discuss the role of female mate choice and intra-sexual competition as possible alternative selective pressures involved.     

Early survival in roe deer: causes and consequences of cohort variation in two contrasted populations

Time- and sex-specific summer survival of roe deer fawns was estimated using capture-mark-recapture methods in two enclosed populations living in contrasting conditions. The population of Trois Fontaines (eastern France) was roughly constant in size throughout the study period, while in Chizé (western France), the population experienced frequent summer droughts and numbers decreased continuously during the study. Early survival of fawns was low and highly variable over the years at both Chizé and Trois Fontaines, and demonstrated marked variations between cohorts that need to be taken into account when modelling roe deer population dynamics. In Trois Fontaines, fawn survival was positively correlated with early body growth and total rainfall in May and June. In Chizé, fawn survival decreased with increasing density and tended to increase with increasing rainfall in May and June and adult female body mass. These factors explained more than 75% of the variability in early survival observed in both populations. Variation between cohorts had different consequences for the two populations. At Trois Fontaines, cohort variation was limited to a numerical effect on early survival. However at Chizé, cohort variation was long-lasting and affected the phenotypic quality of survivors at later ages, and thereby future survival and breeding abilities (both numerical and quality effects). Male and female fawns had similar survival over their first summer in both populations. This result contrasts with the lower survival of young males often observed in ungulates. Two ultimate causes can be proposed to account for the low and variable survival of roe deer fawns over the first summer: the high energy expenditures incurred by does during each breeding attempt and/or the low absolute body size of newborn roe deer fawns. Received: 28 April 1997 / Accepted: 14 July 1997     

Global climate change and phenotypic variation among red deer cohorts.

The variability of two fitness-related phenotypic traits (body weight and a mandibular skeletal ratio) was analysed among cohorts and age-classes of red deer in Norway. Phenotypic variation among cohorts was pronounced for calves, yearlings and reproductively mature adults. Fluctuations in cohort-specific mean body weights and skeletal ratios of adults correlated with global climatic variation in winter conditions influenced by the North Atlantic Oscillation while cohorts were in utero. Red deer born following warm winters were smaller than those born after cold winters, and this inter-cohort variability persisted into adulthood. Phenotypic variation among cohorts of red deer influenced by climate change may pose consequences for fitness of cohorts since body size and condition contribute to reproductive success and survival in male and female red deer. In particular, the recent trend of increasingly warm winters in northern Europe and Scandinavia may lead to reduced body size and fecundity of red deer, and perhaps other ungulates, in those areas.