Claire Saraux

Memory allows animals to utilize ecologically relevant information, yet whether it endures through prolonged metabolic shutdown is poorly understood. We tested spatial memory retention in a long-term, free-living hibernator, the Columbian ground squirrel (Urocitellus columbianus), using a field-based spatial maze over two consecutive active seasons. Ten individuals were tested before and after a 9-month hibernation period and compared with eight naive individuals. Maze-solving performances—time to exit, path sinuosity and navigational errors—were analysed over 10 consecutive trials using Bayesian nonlinear learning curves to separate retained memory from relearning. Strikingly, post-hibernation individuals with prior exposure to the task significantly outperformed naive individuals by 41–98% across all metrics, with initial performance after hibernation approaching pre-hibernation asymptotes. We show that spatial memory survives prolonged hibernation in the wild, supporting the hypothesis that neural plasticity during hibernation reflects adaptive retention rather than memory loss.

Early environmental conditions experienced during juvenile growth are known to have marked effects on adult phenotypes in animal populations. Yet, the life‐history outcomes of variable growth strategies have rarely been investigated in wild populations. The aim of this study was to examine the natural variation of growth patterns displayed within a seabird population and assess their impact on juvenile survival, age at first reproduction, lifetime reproductive outputs (LRO) and longevity. Using a 26‐year study on the ecology of little penguins, we compiled over 2200 chick growth curves and defined 11 growth parameters classified by magnitude, form and rate. Although the growth curves formed a continuum according to these 11 growth parameters, non‐supervised statistical clustering showed that growth trajectories clustered into three main groups: fast, slow and light. Fast chicks ( n = 48%) attained the highest maximum mass in the shortest amount of time, whereas slow chicks ( n = 33%) stood out by a prolonged (+7 days, i.e. +13% in comparison to fast chicks) and irregular period of juvenile growth. Finally, light chicks ( n = 19%) reached low maximum and fledging masses (~−350 g; −37% and −36% of fast and slow chicks). We tested for the effects of chick growth parameters on subsequent annual vital rates estimated through capture–mark–recapture methods as well as longer term effects on life‐history outcomes using Markov chain models. Fast and slow individuals had the highest survival rates from hatching to yearling age (19% and 17%, respectively), while light chicks were at a disadvantage during this initial period (3% survival). Fast individuals reproduced 12% earlier (2.6 years old) than slow individuals, had 12.5%–88% greater longevity (up to 21 years old), and produced 1.2–3.8 times more eggs over their lifespan than slow and light individuals, respectively. Fast chicks reached maturity faster and produced more offspring during their lifetime without discernible negative effects to their longevity, highlighting possible silver spoon effects.

In marine ecosystems, the presence of trace elements resulting from anthropogenic activities has raised concerns regarding their potential effects on marine organisms. This study delves into the intricate relationship between trace element contamination and the physiological responses of a key marine species in the Mediterranean Sea: the European sardine. Since 2008, this species has been experiencing a significant crisis in the region, prompting numerous studies to investigate the potential factors behind the dramatic decline in sardines size, age, and body condition. However, thorough information on chemical contamination by trace elements and its physiological impact on this species was lacking. We found evidence for the accumulation of multiple elements in sardines, with a light East-West contamination gradient within the Gulf of Lions. While macro-physiological parameters (i.e. body condition) were not affected by contamination, pathways involved in cellular organization and response to stress were clearly upregulated, particularly in the liver, but also in muscle. In addition, a global upregulation in processes linked to the immune system, lipid homeostasis and oxidative stress was recorded in the liver. The associated energetic cost may add a substantial burden to sardines that already face multi-factorial constraints. This study also allows to pinpoint biomarkers of exposure and effects that may be important for monitoring Mediterranean sardine health. The results of this study and particularly the complex changes in protein expression demonstrate the need for future studies to test the concomitant effects of multiple stressors acting simultaneously, including large scale contamination.

Demography of herbivorous mammal populations may be affected by changes in predation, population density, harvesting, and climate. Whereas numerous studies have focused on the effect of single environmental variables on individual demographic processes, attempts to integrate the consequences of several environmental variables on numerous functional traits and demographic rates are rare. Over a 32-year period, we examined how forage availability (vegetation assessed through NDVI) and population density affected the functional traits and demographic rates of a population of Columbian ground squirrels (Urocitellus columbianus), a herbivorous hibernating rodent. We focused on mean population phenology, body mass, breeding success, and survival. We found a negative effect of population density on demographic rates, including on breeding success and pup and adult survival to the next year. We found diverging effects of vegetation phenology on demographic rates: positive effects of a later start of the growing season on adult and yearling female survival, and juvenile survival, but no clear effect on male survival. Interestingly, neither population density nor vegetation affected population phenology or body condition in the following year. Vegetative growth rate had a positive influence on female mass gain (somatic investment) over a season, but both vegetative growth rate and biomass, surprisingly, had negative effects on the survival of young through their first hibernation. Thus, ground squirrels appeared to benefit more from later timing of vegetation than increases in vegetative biomass per se. Our study provides evidence for complex ecological effects of vegetation and population density on functional traits and demographic rates of small mammal populations.

Phenotypic plasticity of life-history traits is well known among vertebrate species. We estimated reproductive and somatic efforts of female Columbian ground squirrels ( Urocitellus columbianus (Ord, 1815)) to test for plasticity of these important resource allocations. We examined a 27-year dataset of life-history traits on these long-living (8–10 years), hibernating, montane-living mammals. Environmental variation was estimated from two important traits of mothers, their relative timing of breeding and spring maternal body mass (initial “capital” for use in subsequent reproduction). Results from 183 known-aged mothers and 508 litters revealed considerable variation in the relative timing of breeding, initial maternal mass, and reproductive and somatic efforts, as well as significant variation among ages and years. Results from 125 mothers that reproduced more than once (and 450 litters) revealed significant plasticity of reproductive and somatic efforts with respect to relative timing of breeding and spring maternal mass. A within-subject centering statistical approach showed that phenotypically plastic reproductive and somatic efforts were due to variation within individuals, but were not always reflected by the pattern of responses among individuals in the population. The plastic responses of different mothers appeared to be similar in strength.

In marine ecosystems, the presence of trace elements resulting from anthropogenic activities has raised concerns regarding their potential effects on marine organisms. This study delves into the intricate relationship between trace element contamination and the physiological responses of a key marine species in the Mediterranean Sea: the European sardine. Since 2008, this species has been experiencing a significant crisis in the region, prompting numerous studies to investigate the potential factors behind the dramatic decline in sardines’ size, age, and body condition. However, thorough information on chemical contamination by trace elements and its physiological impact on this species was lacking. We found evidence for the accumulation of multiple elements in sardines, with a light East-West contamination gradient within the Gulf of Lions. While macro-physiological parameters (i.e. body condition) were not affected by contamination, pathways involved in cellular organization and response to stress were clearly upregulated, particularly in the liver, but also in muscle. In addition, a global upregulation in processes linked to the immune system, lipid homeostasis and oxidative stress was recorded in the liver. The associated energetic cost may add a substantial burden to sardines that already face multi-factorial constraints. This study also allows to pinpoint biomarkers of exposure and effects that may be important for monitoring Mediterranean sardine’s health. The results of this study and particularly the complex changes in protein expression demonstrate the need for future studies to test the concomitant effects of multiple stressors acting simultaneously, including large scale contamination.

The COVID-19 pandemic and its lock-down measures have resulted in periods of reduced human activity, known as anthropause. While this period was expected to be favorable for the marine ecosystem, due to a probable reduction of pollution, shipping traffic, industrial activity and fishing pressure, negative counterparts such as the increased use of disposable plastic and reduced fisheries surveillance and enforcement could counterbalance these positive effects. Simultaneously, on-land pressure due to human disturbance and tourism should have drastically decreased, potentially benefiting land-based marine breeders such as seabirds. Thus, long-term datasets became crucial to differentiate between historical trends and any evident changes resulting from the anthropause. We analyzed 11 years of data on several biological parameters of little penguins ( Eudyptula minor ) from the Penguin Parade ®, a popular tourist attraction at Phillip Island, Australia. We investigated the impact of anthropogenic activities on penguin behavior during the breeding season measured by (1) distribution at sea, (2) colony attendance, (3) isotopic niche (4) chick meal mass, and (5) offspring investment against shipping traffic and number of tourists. The 2020 lock-downs resulted in a near absence of tourists visiting the Penguin Parade ®, which was otherwise visited by 800,000+ visitors on average per year. However, our long-term analysis showed no effect of the presence of visitors on little penguins’ activities. Surprisingly, the anthropause did not triggered any changes in maritime traffic intensity and distribution in the region. While we found significant inter- and intra-annual variations for most parameters, we detected a negative effect of marine traffic on the foraging efficiency. Our results suggest that environmental variations have a greater influence on the breeding behavior of little penguins compared to short-term anthropause events. Our long-term dataset was key to test whether changes in anthropogenic activities affected the wildlife during the COVID-19 pandemic. Impact statement: We found that marine traffic, but not tourist presence, negatively impact the foraging and provisioning behavior of little penguins.

Aquatic ecosystems can exhibit seasonal variation in resource availability and animals have evolved to cope with the associated caloric restriction. During winter in the NW Mediterranean Sea, the European sardine Sardina pilchardus naturally experiences caloric restriction owing to a decrease in the diversity and quantity of plankton. However, ongoing global warming has had deleterious effects on plankton communities such that food shortages may occur throughout the year, especially under warm conditions in the summer. We investigated the interactive effects of temperature and food availability on sardine metabolism by continuously monitoring whole-animal respiration of groups of control (fed) and food-deprived sardines over a 60-day experiment in winter (12°C) or summer (20°C) conditions under natural photoperiod. In addition, we measured mitochondrial respiration of red muscle fibres, biometric variables and energy reserves of individuals sampled at 30 and 60 days. This revealed that winter food deprivation elicits energy saving mechanisms at whole animal and cellular levels by maintaining a low metabolism to preserve energy reserves, allowing high levels of survival. By contrast, despite energy saving mechanisms at the mitochondrial level, whole animal metabolic rate was high during food deprivation in summer, causing increased consumption of energy reserves at the muscular level and high mortality after 60 days. Furthermore, a 5-day re-feeding did not improve survival, and mortalities continued, suggesting that long-term food deprivation at high temperatures causes profound stress in sardines that potentially impairs nutrient absorption.

Phenological shifts associated with directional changes in climate, resulting in earlier spring activities, have been documented in several animal species. However, the extent to which species respond to overall climate change versus local climate variation is rarely studied. In addition, climate data are usually averaged over large spatial scales, even though local heterogeneity in habitats may be high, and species might be more susceptible to changes in local rather than global climate conditions. In this study, we examined the effects of spatiotemporal climate variation and climate change on the phenology of a hibernating mountain rodent, the Columbian ground squirrel (Urocitellus columbianus). Over 28 years of research (1992–2019), we studied the relationship between the microclimatic conditions experienced by adult and juvenile ground squirrels from four neighboring meadows, and their dates of emergence from hibernation. We used a microclimate model to calculate microclimate variables (local snow depth, soil temperature, air temperature, wind speed, and humidity) at an hourly scale, a 5‐m spatial resolution, and at animal height on the study sites over 28 years. Emergence dates varied with age and sex, among years, as well as among and within meadows, with some areas averaging up to 10 days earlier emergence dates from hibernation than others. While emergence dates tended to be delayed throughout the study period, long‐term temporal changes and interannual variability in emergence dates differed among meadows and depended on individual age and sex. Dates of hibernation emergence were correlated with local climate variables considered either during hibernation or during the preceding summer. Ground squirrels emerged earlier in years or at locations when/where snow melted earlier (years: all individuals excluding 2‐year‐old males, locations: yearlings and older females), and when the previous summer was less windy (≥3‐year‐old individuals) and more humid (2‐year‐old males). Two‐year‐old male ground squirrels also emerged later in locations where snow depth during winter was higher. Using a microclimate model allowed realistic predictions of phenological responses to climate, highlighting its potential for research on animal responses to abiotic change.

Alert distance (AD) and flight initiation distance (FID) are popular measures used to explore the reaction of prey to approaching predators, and thus the economics underlying optimal escape strategies. AD likely mirrors the effort invested into vigilance, while FID provides an estimate of the perceived risk of an approaching threat. Although individual variation in AD and FID is influenced by environmental factors such as variation in predation pressure and human disturbance, the repeatabilities of these traits (especially AD), and therefore their designation as personality traits, remain under‐investigated. Here, we studied the repeatability of AD, FID, and the decision to flee in a flightless, ground‐breeding seabird, the king penguin (Aptenodytes patagonicus). A single experimenter approached three times over three consecutive days 47 incubating king penguins from two different colonies with varying human disturbance levels. We explored the effects of weather, time of day, and approach speed of the experimenter on these behaviors. Weather had an effect on all three behaviors. In warm, sunny weather AD increased. In rainy, windy weather birds were more likely to flee, but waited longer before initiating flight. Faster approach speeds between AD and FID increased FID. Weather conditions and speed of approach affected repeatability estimates, highlighting the need to consider external sources of variation when refining such estimates. FID and the decision to flee were significantly and moderately repeatable (r = 0.26 and 0.57, respectively), while AD was not. There was no evidence of behavioral habituation or sensitization in either colony.