Improving the success of reinforcement programs: effects of a two-week confinement in a field enclosure on the anti-predator behaviour of captive-bred European hamsters.

Captive breeding programs are an important pillar in biodiversity conservation, aiming to prevent the extinction of threatened species. However, the establishment of self-sustaining populations in the wild through the release of captive-bred animals is often hampered by a high mortality upon release. In this study, we investigated how a 2-week confinement period within a large field enclosure affected the anti-predator behaviour of 'naive' captive-bred hamsters and how potential modifications persisted over time. During three consecutive tests, hamsters were confronted with a moving predator model (a red fox mount, Vulpes vulpes) and their behaviour was filmed. After the initial round of confrontation with the predator model, one group of hamsters (field group) was released into a field enclosure protected from predators, while the other group (control) remained in their individual laboratory cages. After 2 weeks, hamsters from the field group were recaptured and individuals of both groups underwent a second confrontation test. A total of 1 month after their return from the field enclosure, field hamsters were subjected to a last confrontation test. Video analysis, investigating four behavioural variables, revealed that field hamsters significantly modified their behavioural response following the 2 weeks confinement in the enclosure, while this was not the case for control hamsters. In addition, most behavioural modifications in field hamsters persisted over 1 month, while others started to revert. We suggest that an appropriate pre-release period inside a field enclosure will enable naive (captive-bred) hamsters to develop an adequate anti-predator behaviour that will increase their immediate survival probability upon release into the wild. We believe that such measure will be of great importance for hamster conservation programs.

Telomere length positively correlates with pace-of-life in a sex- and cohort-specific way and elongates with age in a wild mammal.

Understanding ageing and the diversity of life histories is a cornerstone in biology. Telomeres, the protecting caps of chromosomes, are thought to be involved in ageing, cancer risks and life-history strategies. They shorten with cell division and age in somatic tissues of most species, possibly limiting lifespan. The resource allocation trade-off hypothesis predicts that short telomeres have thus coevolved with early reproduction, proactive behaviour and reduced lifespan, that is, a fast pace-of-life syndrome (POLS). Conversely, since short telomeres may also reduce the risks of cancer, the anticancer hypothesis advances that they should be associated with slow POLS. Conclusion on which hypothesis best supports the role of telomeres as mediators of life-history strategies is hampered by a lack of study on wild short-lived vertebrates, apart from birds. Using seven years of data on wild Eastern chipmunks Tamias striatus, we highlighted that telomeres elongate with age (n = 204 and n = 20) and do not limit lifespan in this species (n = 51). Furthermore, short telomeres correlated with a slow POLS in a sex-specific way (n = 37). Females with short telomeres had a delayed age at first breeding and a lower fecundity rate than females with long telomeres, while we found no differences in males. Our findings support most predictions adapted from the anticancer hypothesis, but none of those from the resource allocation trade-off hypothesis. Results are in line with an increasing body of evidence suggesting that other evolutionary forces than resource allocation trade-offs shape the diversity of telomere length in adult somatic cells and the relationships between telomere length and life-histories.

Integrating Mortality Risk and the Adaptiveness of Hibernation.

Low mortality rate is often associated with slow life history, and so far, has mainly been assessed through examinations of specific adaptations and lifestyles that limit mortality risk. However, the organization of activity time budgets also needs to be considered, since some activities and the time afforded for performing them may expose animals to higher mortality risks such as increased predation and/or increased metabolic stress. We examined the extent of activity time budgets contribution to explaining variation in life history traits in mammals. We specifically focused on hibernating species because of their marked seasonal cycle of activity/inactivity associated with very different mortality risks. Hibernation is considered a seasonal adaptation to prolonged periods of food shortage and cold. This inactivity period may also reduce both extrinsic and intrinsic mortality risks, by decreasing exposure to predators and drastically reducing metabolic rate. In turn, reduction in mortality may explain why hibernators have slower life history traits than non-hibernators of the same size. Using phylogenetically controlled models, we tested the hypothesis that longevity was positively correlated with the hibernation season duration (the time spent between immergence and emergence from the hibernaculum or den) across 82 different mammalian species. We found that longevity increased significantly with hibernation season duration, an effect that was particularly strong in small hibernators (<1.5 kg) especially for bats. These results confirm that hibernation not only allows mammals to survive periods of energy scarcity, but further suggest that activity time budgets may be selected to reduce mortality risks according to life history pace.

Consumption of red maple in anticipation of beech mast-seeding drives reproduction in eastern chipmunks.

Understanding the determinants of reproduction is a central question in evolutionary ecology. In pulsed-resource environments, the reproduction and population dynamics of seed consumers are driven by pulsed production of seeds by trees or mast-seeding. In Southern Québec, eastern chipmunks Tamias striatus exclusively reproduce during the summer before and the spring after a mast-seeding event of American beech. They thus seem to anticipate beech mast by reproducing during early summer, so that juveniles can emerge at the time of maximum beechnut abundance during late summer. However, the cues allowing chipmunks to anticipate beech mast remain unknown, and the existence of the anticipation process itself has been questioned. To tackle those issues, we investigated the links between the nutritional ecology and reproduction of adult chipmunks and compared their spring diet in mast- versus post-mast years. We monitored female reproductive status (N = 446), analysed cheek pouch contents at capture (n = 3,761 captures) and recorded seed production by deciduous trees on three different sites in Mont-Sutton from 2006 to 2018. Results revealed a systematic shift in chipmunk diet towards red maple seeds in springs preceding a beech mast, with red maple seeds composing more than 77% of chipmunk diet. However, red maple consumption was unrelated to red maple production, but was related to beech seed production in the upcoming fall. We also found that red maple consumption best predicted the proportion of females in summer oestrus. Our results confirm that chipmunks anticipate beech mast-seeding and highlight a key role of red maple consumption in that anticipation. Results also suggest that red maple seeds may contain nutrients or secondary plant components essential to sustain or trigger the summer reproduction in chipmunks, which allow them to remain synchronized with pulsed productions of both red maple and beech and improve their fitness.

Captive-reared European hamsters follow an offensive strategy during risk-assessment.

Understanding whether captive-reared animals destined to reintroduction are still able to discriminate predators has important implications for conservation biology. The endangered European hamster benefits from conservation programs throughout Europe, in which several thousand individuals are released into the wild every year. Despite this, the anti-predator strategy of hamsters and their ability to maintain predator discrimination in captivity remain to be investigated. Here, we explore the predator discrimination behaviour of captive-reared European hamsters and their response to different predation cues. When first exposed to the urine of cats and goats in a Y-maze test, hamsters spent more time close to the cat scent rather than to the goat scent. In a second experiment, during which hamsters were exposed to a non-mobile European ferret (inside a cage), hamsters significantly increased the time spent close to the ferret's cage and displayed aggressive behaviour towards the ferret. Furthermore, they did not take refuge inside an anti-predation tube (APT), a device designed to upgrade wildlife underpasses and reconnect wild hamster populations. Finally, when exposed to a mobile ferret (but without physical contact), hamsters displayed mobbing and aggressive behaviours towards the ferret, before taking refuge inside the APT. Taken together, our results show that captive-reared hamsters are still able to detect and react to predation cues, but that they initially adopt an offensive strategy (grunting, spitting, mobbing) during the risk-assessment phase. After risk assessment, however, hamsters used the APT as a refuge. Our study provides important insights into the anti-predator behaviour of hamsters. Testing the efficacy of the APT, a device that will allow upgrading wildlife underpasses for the hamster and other rodents, is also of great importance and is instrumental in conservation efforts for these species.

Monocultural sowing in mesocosms decreases the species richness of weeds and invertebrates and critically reduces the fitness of the endangered European hamster.

Intensive cereal monoculture is currently the main cause of biodiversity decline in Europe. However, it is difficult to disentangle the effects of intensive monoculture (e.g. pesticide use, mechanical ploughing and reduced protective cover), let alone evaluate how far the reduction of crop diversity affects biodiversity. It remains unclear to which extent the consequent decrease in food resources affects farmland biodiversity, and particularly vertebrate species. We therefore designed this study in mesocosms to investigate the effects of monoculture crops (organic wheat or corn seeds) and mixed crops (a combination of organic wheat, corn, sunflower and alfalfa seeds) on (1) the species richness of weeds and invertebrates and (2) the reproductive success of the European hamster (Cricetus cricetus), a critically endangered umbrella species of European farmlands. We found a negative impact of organic monoculture crops on plant and invertebrate species richness, with values respectively 38% and 28% lower than those obtained for mixed organic crops. The reproductive success of hamsters was reduced by 82% in monoculture mesocosms. These results highlight that monoculture per se can be detrimental for farmland biodiversity (i.e. from plants to vertebrates), even before taking into account the use of pesticide and mechanization. We believe that future research should further consider how food reduction in agroecosystems affects farmland wildlife, including vertebrates. Moreover, we argue that conservation actions must focus on restoring plant diversity on farmland to reverse the observed trend in farmland wildlife decline.

Diets derived from maize monoculture cause maternal infanticides in the endangered European hamster due to a vitamin B3 deficiency.

From 1735 to 1940, maize-based diets led to the death of hundreds of thousands of people from pellagra, a complex disease caused by tryptophan and vitamin B3 deficiencies. The current cereal monoculture trend restricts farmland animals to similarly monotonous diets. However, few studies have distinguished the effects of crop nutritional properties on the reproduction of these species from those of other detrimental factors such as pesticide toxicity or agricultural ploughing. This study shows that maize-based diets cause high rates of maternal infanticides in the European hamster, a farmland species on the verge of extinction in Western Europe. Vitamin B3 supplementation is shown to effectively restore reproductive success in maize-fed females. This study pinpoints how nutritional deficiencies caused by maize monoculture could affect farmland animal reproduction and hence their fitness.

How maize monoculture and increasing winter rainfall have brought the hibernating European hamster to the verge of extinction.

Over the last decades, climate change and agricultural intensification have been identified as two major phenomena negatively affecting biodiversity. However, little is known about their effects on the life-history traits of hibernating species living in agro-ecosystems. The European hamster (Cricetus cricetus), once a common rodent on agricultural land, is now on the verge of extinction in France. Despite the implemented measures for its protection, populations are still in sharp decline but the reasons for it remain unclear. To investigate how environmental change has affected this hibernating rodent, we used a data set based on 1468 recordings of hamster body mass at emergence from hibernation from 1937 to 2014. We reveal the adverse effects of increasing winter rainfall and maize monoculture intensification on the body mass of wild hamsters. Given the links that exist between body mass, reproductive success and population dynamics in mammals, these results are of particular importance to understand the decline of this species. In view of the rates of maize monoculture intensification and the predicted increase in winter rainfall, it is of the utmost importance to improve land management in Western Europe to avoid the extinction of this species.

Starting with a handicap: effects of asynchronous hatching on growth rate, oxidative stress and telomere dynamics in free-living great tits.

A trade-off between resource investment into growth rate and body self-maintenance is likely to occur, but the underlying molecular mediators of such a trade-off remain to be determined. In many altricial birds, hatching asynchrony creates a sibling competitive hierarchy within the brood, with first-hatched nestlings enjoying substantial advantages compared to last-hatched nestlings. We used this opportunity to test for a trade-off between growth and self-maintenance processes (oxidative stress, telomere erosion) in great tit nestlings, since resource availability and allocation are likely to differ between first-hatched and last-hatched nestlings. We found that despite their starting competitive handicap (i.e. being smaller/lighter before day 16), last-hatched nestlings exhibited growth rate and mass/size at fledging similar to first-hatched ones. However, last-hatched nestlings suffered more in terms of oxidative stress, and ended growth with shorter telomeres than first-hatched ones. Interestingly, growth rate was positively related to plasma antioxidant capacity and early life telomere length (i.e. at 7 days old), but among last-hatched nestlings, those exhibiting the faster body size growth were also those exhibiting the greatest telomere erosion. Last-hatched nestlings exhibited elevated levels of plasma testosterone (T), but only at day 7. T levels were positively associated with oxidative damage levels and plasma antioxidant capacity, the latter being only significant for first-hatched nestlings. Our results suggest that last-hatched nestlings present a specific trade-off between growth rate and self-maintenance processes, which is possibly driven by their need to compete with their older siblings and potentially mediated by elevated levels of T.

Maternal effects underlie ageing costs of growth in the zebra finch (Taeniopygia guttata).

Maternal effects provide a mechanism to adapt offspring phenotype and optimize the mother's fitness to current environmental conditions. Transferring steroids to the yolk is one way mothers can translate environmental information into potential adaptive signals for offspring. However, maternally-derived hormones might also have adverse effects for offspring. For example, recent data in zebra finch chicks suggested that ageing related-processes (i.e. oxidative stress and telomere loss) were increased after egg-injection of corticosterone (CORT). Still, we have few experimental data describing the effect of maternal effects on the growth-ageing trade-off in offspring. Here, we chronically treated pre-laying zebra finch females (Taeniopygia guttata) with 17-ß-estradiol (E2) or CORT, and followed offspring growth and cellular ageing rates (oxidative stress and telomere loss). CORT treatment decreased growth rate in male chicks and increased rate of telomere loss in mothers and female offspring. E2 increased body mass gain in male offspring, while reducing oxidative stress in both sexes but without affecting telomere loss. Since shorter telomeres were previously found to be a proxy of individual lifespan in zebra finches, maternal effects may, through pleiotropic effects, be important determinants of offspring life-expectancy by modulating ageing rate during embryo and post-natal growth.