Multi-assay approach shows species-associated personality patterns in two socially distinct gerbil species.

We aimed to investigate whether two closely related but socially distinct species of gerbils differ in personality patterns. Using a suit of multivariate repeated assays (docility test, dark-light emergence test, startle test, novel object test, elevated platform test, and stranger test), we assessed contextual and temporal consistency of docility, boldness, exploration, anxiety, and sociability in the solitary midday gerbil, Meriones meridianus, and social Mongolian gerbil, M. unguiculatus. We revealed contextually consistent and highly repeatable sex-independent but species-specific personality traits. Species differed in temporal repeatability of different behaviours, and contextual consistency was more pronounced in solitary M. meridianus than in social M. unguiculatus. This finding contradicts the social niche specialization hypothesis, which suggests that personality traits should be more consistent in more social species. Instead, we hypothesize that social complexity should favour more flexible and less consistent behavioural traits. The habituation effect indicative of learning abilities was weak in both species yet stronger in social M. unguiculatus, supporting the relationship between the sociality level and cognitive skills. In both species, only a few different behavioural traits covaried, and the sets of correlated behaviours were species-specific such that the two species did not share any pair of correlated traits. Between-species differences in personality traits, habituation, and behavioural syndromes may be linked to differences in sociality. The lack of prominent behavioural syndromes is consistent with the idea that context-specific individual behavioural traits might be favoured to allow more flexible and adequate responses to changing environments than syndromes of correlated functionally different behaviours.

Juvenile survival curves in a solitary ground squirrel with a prolonged hibernation: effects of individual characteristics, environment, and maternal investment.

Juvenile survival is a key life-history influence on population dynamics and adaptive evolution. We analyzed the effects of individual characteristics, early environment, and maternal investment on juvenile survival in a large solitary hibernating rodent-yellow ground squirrel Spermophilus fulvus using Cox mixed-effects models. Only 48% of weaned pups survived to dispersal and 17% survived to hibernation. Early life expectancy was primarily determined by individual characteristics and, to a lesser extent, by the early environment. The strongest and positive predictor of juvenile survival was body mass which crucially affected mortality immediately after weaning. Males suffered higher mortality than females after the onset of dispersal; however, the overall difference between sexes was partly masked by high rates of mortality in the first days after emergence in both sexes. Later emerged juveniles had lower life expectancy than the earliest pups. The overall effect of local juvenile density was positive. Prolonged lactation did not enhance juvenile survival: Pups nursed longer survived shorter than the young nursed for a shorter period. Our findings support the hypothesis that females of S. fulvus cannot effectively regulate maternal expenditures to mitigate the effects of unfavorable conditions on their offspring. The strategy to deal with seasonal time constraints on life history in female S. fulvus suggests an early termination of maternal care at the cost of juvenile quality and survival. This female reproductive strategy corresponds to a "fast-solitary" life of folivorous desert-dwelling S. fulvus and other solitary ground squirrels with prolonged hibernation.

Sex ratio effects on reproductive success of male and female Daphnia.

The intensity of mating competition and the opportunity for sexual selection are thought to depend on the operational sex ratio, the ratio of sexually active males to fertilizable females. Cyclic parthenogens, organisms that alternate between sexual reproduction and female-only parthenogenesis, show particularly high variation in sex ratios in natural populations but the effects of this variation on mating competition and reproductive success of each sex are poorly understood. In a series of experiments with Daphnia magna, we experimentally imposed five sex ratio categories, varying from one male per 81 females to an even sex ratio. We found that, in males, reproductive success strongly and monotonically decreased with decreasing number of females per male. In females, in contrast, mating success and reproductive success were reduced only at the most female-biased sex ratio (1:81), when many females remained unmated and unfertilized, and then again at equal sex ratios, probably due to negative effects of high density or stress induced by numerous males. Our results suggest that females experienced male limitation at heavily female-biased sex ratios below one male to about 50 females. As this is well within the sex ratio variation observed in natural Daphnia populations, we conclude that mating competition and the opportunity for sexual selection may exist not only in males but, at least periodically, also in females.

Early predictors of female lifetime reproductive success in a solitary hibernator: evidence for "silver spoon" effect.

Fitness consequences of early-life conditions remain unclear and poorly studied in mammals. Based on long-term observations of yellow ground squirrels (Spermophilus fulvus), we identified early determinants of female fitness by analyzing the effects of early-life individual and environmental characteristics (weaning weight, weight gain rate, date of natal emergence, natal litter size, location of the natal burrow, local density of juveniles, population density and precipitation in the post-weaning period) on lifetime reproductive success (LRS). We found high variation and right-skewed distribution in all five LRS components (survival to adulthood, adult lifespan, and lifetime numbers of weaned litters, weanlings, and yearling offspring). Numbers of litters, weanlings, and adult offspring were correlated with each other and increased with lifespan, confirming that longevity is a better predictor of LRS than fecundity. Survival to adulthood was the most sensitive fitness component to early conditions and was higher in females (a) with greater weaning weight, (b) born further from human settlement and (c) born at lower population density. Population density at birth was the best early predictor of all LRS components and negatively influenced adult lifespan and numbers of weanlings and yearling offspring. Early growth rate positively affected the probability of reproducing after the first hibernation and the number of offspring weaned. Such syndrome of high-quality (heavy and fast-growing) young born in a favourable environment ("a silver spoon effect") with downstream damping fitness consequences has been observed so far in only a few mammalian species.

Sociability and pair-bonding in gerbils: a comparative experimental study.

In a study of gerbils with contrasting social and mating systems (group-living monogamous Mongolian gerbil Meriones unguiculatus, solitary nonterritorial promiscuous midday jird M. meridianus, and solitary territorial promiscuous pale gerbil Gerbillus perpallidus), we employed partner preference tests (PPTs) to assess among-species variation in sociability and pair-bonding patterns and tested whether the nature of contact between individuals: direct contact (DC) versus nondirect contact (NDC) affected our results. We measured male preferences as the time: 1) spent alone, 2) with familiar (partner), and 3) unfamiliar (stranger) female in the 3-chambered apparatus. Gerbil species differed strongly in sociability and male partner preferences. The time spent alone was a reliable indicator of species sociability independent of the nature of contact, whereas the pattern and level of between-species differences in male partner preferences depended on contact type: DC PPTs, unlike NDC-tests, discriminated well between monogamous and promiscuous species. In the DC-tests, stranger-directed aggression and stranger avoidance were observed both in the highly social monogamous M. unguiculatus and the solitary territorial promiscuous G. perpallidus, but not in the nonterritorial promiscuous M. meridianus. In M. unguiculatus, stranger avoidance in the DC-tests increased the time spent with the partner, thus providing evidence of a partner preference that was not found in the NDC-tests, whereas in G. perpallidus, stranger avoidance increased the time spent alone. This first comparative experimental study of partner preferences in gerbils provides new insights into the interspecific variation in gerbil sociality and mating systems and sheds light on behavioral mechanisms underlying social fidelity and pair-bonding.

Rodent burrow network dynamics under human-induced landscape transformation from desert to steppe in Kalmykian rangelands.

Rodents play an important role in rangelands through the engineering of extensive burrow systems, which provides key habitats for many animal and plant species. We have analyzed the long-term variation in the abundance and distribution of rodent burrows in grazing ecosystems of southern Russia (Kalmykia) under the landscape change from desert to steppe caused by the drastic reduction of livestock after the collapse of the USSR in the early 1990s. We conducted burrow surveys in the "desert" (1980) and "steppe" (2017) periods on 19 3-km transects. We found considerable changes in burrow abundance and distribution, as well as evidence of desert habitat fragmentation and isolation caused by the expansion of tall-grass communities. Burrows of the open-dwelling diurnal ground squirrel (Spermophilus pygmaeus), the dominant and the keystone species during the "desert" period, almost completely disappeared from the rodent burrow network by 2017, indicating significant habitat loss. In contrast, the burrows of the folivorous social vole (Microtus socialis) which was rare in the 1980s, became abundant and ubiquitously distributed. The burrow density of the desert-dwelling psammophilous midday gerbil (Meriones meridianus) decreased, while the distances between occupied patches increased, indicating desert habitat fragmentation and loss of population connectivity. Burrows of the folivorous tamarisk gerbils (M. tamariscinus) were recorded only sporadically in both 1980 and 2017. The observed changes in the rodent burrow network, the key component of grazing ecosystems, correlate with rodent species ecology and can have long-term and important consequences for ecosystem functioning.

Breeding versus survival: proximate causes of abrupt population decline under environmental change in a desert rodent, the midday gerbil (Meriones meridianus).

Studying abrupt ecological shifts under gradual environmental change caused, in particular, by human activity is important for understanding the fundamental aspects and underlying mechanisms of ecological resilience. One of the rare well-documented examples of an abrupt ecological shift is the delayed step transition of the population of a desert rodent, the midday gerbil (Meriones meridianus), from high-abundance (1994-2002) to low-abundance (2003-2017) regimes. This was in response to landscape transformation from desert to steppe caused by the drastic reduction of livestock in the rangelands of southern Russia after the collapse of the USSR in the early 1990s. In this study, we tested whether demographic parameters were correlated with the observed abrupt downward population shift. We found that reproductive activity (the percentage of breeding females, the number of litters, fecundity and the number of young recruited per female) showed no trend over time and did not differ between periods of high and low abundance. In contrast, the adult sex ratio (SR = males: females) decreased significantly with time and was as much as twice more female-biased for the low-abundance population regime. However, SR was not related to any reproductive parameter, including the percentage of breeding females. We conclude that proximate reasons for an abrupt population decline in M. meridianus are not associated with the changes in breeding patterns or mate limitation caused by the Allee effect but relate to the increased mortality as a result of the desert landscape being fragmented by steppezation. The mortality is expected to be higher for males as the mobile and dispersing sex.

The method matters: The effect of handling time on cortisol level and blood parameters in wild cats.

Blood analysis has recently become a popular tool to assess the welfare of the wild cats. However, the estimates of blood parameters may depend on the sampling method. We have tested (1) if the sampling procedure influences blood parameters and (2) what parameters are the most efficient in assessing the physiological status in wild cat species. We assessed the effect of handling time on red blood cells (RBC) and white blood cells (WBC) counts, the ratio of neutrophils to lymphocytes (N/L ratio), and serum cortisol level within 1 hr after the capture of the animal in six far-east wild cats (Prionailurus bengalensis euptilura). Also, we analyzed literature data in 17 cat species to assess the effect of place of study, type of immobilization, and handling time on WBC count and N/L ratio. Serum cortisol level varied significantly with the handling time. RBC and WBC counts were strongly affected by the handling time. N/L ratio was very robust and did not depend on the handling time. However, the analysis of literature data has shown that the prolonged handling time (over 1 hr) and the type of immobilization significantly influence the N/L ratio, whereas the WBC count does not depend on any of considered factors. We conclude that while most blood parameters of cats are affected by routine handling time, the N/L ratio does not vary if the samples are collected within 1 hr after the capture of the animal. All other tested parameters should be treated with caution.

Impacts of late Quaternary environmental change on the long-tailed ground squirrel (Urocitellus undulatus) in Mongolia.

Impacts of Quaternary environmental changes on mammal faunas of central Asia remain poorly understood due to a lack of geographically comprehensive phylogeographic sampling for most species. To help address this knowledge gap, we conducted the most extensive molecular analysis to date of the long-tailed ground squirrel (Urocitellus undulatus Pallas 1778) in Mongolia, a country that comprises the southern core of this species' range. Drawing on material from recent collaborative field expeditions, we genotyped 128 individuals at 2 mitochondrial genes (cytochrome b and cytochrome oxidase I; 1 797 bp total). Phylogenetic inference supports the existence of two deeply divergent infraspecific lineages (corresponding to subspecies U. u. undulatus and U. u. eversmanni), a result in agreement with previous molecular investigations but discordant with patterns of range-wide craniometric and external phenotypic variation. In the widespread westerneversmanni lineage, we recovered geographically-associated clades from the: (a) Khangai, (b) Mongolian Altai, and (c) Govi Altai mountain ranges. Phylogeographic structure in U. u. eversmanni is consistent with an isolation-by-distance model; however, genetic distances are significantly lower than among subspecies, and intra-clade relationships are largely unresolved. The latter patterns, as well as the relatively higher nucleotide polymorphism of populations from the Great Lakes Depression of northwestern Mongolia, suggest a history of range shifts into these lowland areas in response to Pleistocene glaciation and environmental change, followed by upslope movements and mitochondrial lineage sorting with Holocene aridification. Our study illuminates possible historical mechanisms responsible for U. undulatus genetic structure and contributes to a framework for ongoing exploration of mammalian response to past and present climate change in central Asia.

Delayed threshold response of a rodent population to human-induced landscape change.

Theory predicts that due to their resilience, ecosystems and populations are expected to respond to environmental changes not gradually, but in a nonlinear way with sudden abrupt shifts. However, it is not easy to observe and predict the state-and-transition dynamics in the real world because of time lags between exogenous perturbations and species response. Based on yearly surveys, during 21 years (1994-2014), we have studied population dynamics of a desert rodent (the midday gerbil, Meriones meridianus) in the rangelands of southern Russia under landscape change from desert to steppe caused by the drastic reduction of livestock after the collapse of the USSR in the early 1990s. The population of M. meridianus has remained robust to landscape change from desert to steppe for over 10 years, but then has suddenly dropped down and has not recovered since. The step transition from the high- to low-abundance density-regulated equilibrium was accompanied by an abrupt increase in the spatio-temporal population variability, which may indicate the loss of population resilience. We explain inertia in species response to landscape change and an abrupt regime shift in population dynamics by species-specific ecology and life-history combined with habitat fragmentation that had reached a certain critical threshold level by the early 2000s. This is a rare well-documented demonstration of a delayed threshold response of a wild unexploited mammal population to human-induced environmental change, which may shed light on the mechanisms of population resilience and underlying causes of threshold population dynamics in a changing world.

A shortage of males causes female reproductive failure in yellow ground squirrels.

Sexual conflict theory suggests that female breeding success is strongly influenced by individual life history and environmental conditions and is much less affected by mate availability. Female mating failure due to a shortage of males remains poorly studied and understood. We present data on the effects of male availability on female breeding success in a wild colony of yellow ground squirrels (Spermophilus fulvus). A female's probability of breeding increased with the local density of males and was higher with higher male-biased operational sex ratio (OSR) but was independent of local female density, female age, and body condition, which are factors commonly assumed to influence female reproduction. The positive effect of male availability (as measured by OSR) on female breeding success was consistent across the years, and we conclude that male limitation contributes to female mating failure. This pattern, which is not commonly recorded in species with conventional sex roles, can be explained by a combination of sociodemographic and life history traits (sex differences in age of maturation, female-skewed adult sex ratio and seasonally varying OSR, solitary living at low population density, and low mobility of females combined with mate-searching tactics of males) that are not confined to S. fulvus. Our findings indicate that the role of female mating failure (due to a shortage of males) in shaping mammalian life history may be underestimated.