The tight regulation of body temperature is essential for the maintenance of homeostasis in homeothermic endotherms. However, newborn altricial mammals are limited in their ability to maintain body temperature independently because they usually lack an insulating layer of fur, they have a relatively large body surface to volume ratio, and they have immature vasomotor control. Thus, altricial young are generally considered ectothermic poikilotherms at birth, but rapidly develop homeothermic endothermy. However, in polytocous species it is not known whether there are differences among littermates in the temporal development of endothermy and if so, what might account for this. Our aim was to determine the contribution of interactions among littermates to possible individual differences in the onset of homeothermic endothermy in altricial pups of the domestic rabbit. In 10 litters we evaluated individual differences in pups' position within the litter huddle on differences in their ability to maintain a stable body temperature when exposed individually to an acute daily cold challenge across the first 15 postnatal days. Greater relative body mass at birth was associated with greater body mass gain, occupancy of central positions in the litter huddle, and more rapid growth of fur, which together were associated with the earlier development of homeothermic endothermy. We conclude that early interactions among littermates associated with relative differences in initial body mass contribute to individual differences in the development of endothermy, with possible long-term consequences for individuals' fitness and metabolic phenotype.
In altricial mammal species, isolation calls are vocalisations the young produce when they are separated from the mother. While mother/offspring interactions during the postnatal period affect pups’ isolation calls rate, the contribution of interactions with other adults in shaping this response remains to be explored.We took advantage of the variation in the composition of the parental environment in the wild in a monogamous species (Mus spicilegus) to investigate how the vocal response of pups during separation could be affected by the number of adults that provide daily care in the nest. Three types of parental environments were studied: monoparental, biparental and polygynous. First, we quantified the parental care received by pups during the first postnatal week in the different parental units. Second, pups’ vocal responses to isolation were recorded on postnatal day 9.Pups received less care (licking and handling) in monoparental than in biparental or polygynous units, and no difference was observed between biparental and polygynous units. Pups that emitted higher call rates in response to isolation were the ones which were less often left alone in the nest and which received a larger amount of maternal care.
For many mammals, siblings are an important part of the developmental environment, probably contributing to the formation of individual differences in personality. Specifically, in humans sibling effects are thought to be associated with birth order. However, the findings have been controversial. This might be due in part to the use of self- report methods, which depend on subjective perceptions. Thus, it is necessary to also use physiological measures not under voluntary control. We tested the behavioral and physiological responses of 80 young adults-40 men and 40 women, 20 firstborn and 20 lastborn of each sex-to 3 commonly used psychological stressors during a 13- min experimental session. Participants' behavioral responses were recorded on video, and their physiological reactions were registered via facial infrared thermography. As predicted by birth order theory, firstborns showed significantly greater signs of stress than lastborns, with lower nose temperatures on all tests and for both sexes. Behavior did not differ between the 2 groups. Thus, contradictory findings among previous studies of the association of birth order with personality differences between siblings might be partly due to the low resolution of behavioral evaluation in contrast to the registration of autonomic nervous system activity as, for example, measured by noninvasive, easily implemented facial infrared thermography.
Individual-level sibling interactions in the litter huddle have been studied extensively, especially in the domestic rabbit (Oryctolagus cuniculus). However, little is known about inter-litter differences in pup activity patterns during early postnatal life, in particular regarding the drivers of such variation. In our study on 2-3-day-old rabbit pups, we predicted lower locomotor activity in litters with lower mean body masses on the day of birth (starting body mass) and with lower daily milk intake per pup, possibly constituting a behavioral strategy of pups to cope with associated energetic constraints. For an automatized assessment of pup locomotor activity in the litter huddle, we successfully developed and validated a method based on the quantification of dissimilarities between consecutive frames of video footage. Using this method, we could confirm a U-shaped time course of litter-level locomotor activity, with maximum values shortly before and after the once-daily nursing typical for the rabbit. As predicted, between-litter variation in mean starting body mass and in daily milk intake affected the degree of locomotor activity in the litter huddle, in an interactive way. That is, in litters with heavier starting body masses, pup locomotor activity was greater in pups with an initially higher milk intake, suggesting that only pups with better body condition and a higher energy intake could afford higher levels of activity. This interaction was exclusively apparent during the middle phase of the 24 h inter-nursing interval, when litter activity was low. Shortly before nursing, when pups show higher levels of locomotor behavior in anticipation of the mother's arrival, and shortly after nursing when the pups were more active possibly due to adjustments of their positions in the huddle, activity levels were decoupled from pups' starting body mass and previous milk intake. Our findings highlight the importance of pup body mass and daily energy intake, two parameters known to be related to maternal characteristics, in shaping inter-litter differences in pup locomotor activity.
It is increasingly recognized that alterations of the cellular oxidative status might be an important cost underlying challenging early life conditions. For example, an increased litter size can impose challenges as the offspring will face increased competition for maternal resources. Within a litter, individuals with relatively higher starting mass typically show higher growth rates, which can lead to increased oxidative damage. We investigated the long-term consequences of these early life parameters on the oxidative status in mature mound-building mice (Mus spicilegus). Individual differences in the animals' exploration tendency were assessed by repeated open field and novel object tests. We predicted less exploratory phenotypes, which typically show a higher stress responsiveness, to be particularly susceptible to possible effects of these early life parameters on oxidative status. We quantified oxidative damage of DNA (8-hydroxy-2'-deoxyguanosine levels, 8-OHdG) and proteins (protein carbonyl content, PCC), and activities of the antioxidants catalase (CAT), glutathione peroxidase (GPx), and superoxide dismutase (SOD) in liver and skeletal muscle tissue. 8-OHdG levels were positively associated with CAT and SOD in both tissues, indicating that increased oxidative DNA damage was associated with an upregulation of antioxidant production. Hepatic DNA damage after maturity was increased in animals from larger litters. In less exploratory animals, DNA damage and the activity of CAT and SOD in the muscle were increased, but only in individuals with higher relative starting mass (measured on postnatal day 9). This interaction may be explained by the typically higher adrenocortical activity in less exploratory phenotypes and by the higher growth in relatively heavier pups, two factors known to increase oxidative stress. These findings contribute to enlightening the complex interplay between early life conditions, personality, and oxidative status.
Judgment bias tests have become an important tool in the assessment of animals' affective states. Subjects are first trained to discriminate between two cues associated with a positive and a less-positive outcome. After successful training, they are confronted with an ambiguous cue, and responses are used for judgment bias assessment. In spatial settings, ambiguous cue presentation is typically linked with novelty, i.e. to yet unexplored areas or areas to which the animal has a low degree of habituation. We hypothesized that in such settings, responses to ambiguity might be biased by the animals' perception of novelty. We conducted judgment bias tests in mound-building mice phenotyped for their exploration tendency. After subjects had learned to distinguish between the positively and less-positively rewarded arms of a maze, a new ambiguous middle-arm was introduced. During the first test trial, more exploratory, less neophobic individuals displayed higher bidirectional locomotion in the ambiguous arm, indicating intensive exploration. Although this resulted in longer latencies to the reward in more exploratory animals, we conclude that this did not reflect a 'more pessimistic judgment of ambiguity'. Indeed, during the following two trials, with increasing habituation to the ambiguous arm, the direction of the association was inversed compared to the first trial, as more exploratory individuals showed relatively shorter approach latencies. We suggest that in spatial test settings associating the ambiguous cue to novel areas, results can be confounded by subjects' personality-dependent motivational conflict between exploration and reaching the reward. Findings obtained under such conditions should be interpreted with care.
The social transmission of food preference (STFP) is a phenomenon that allows rodents to use food information perceived from their conspecifics to guide their own food choices. This social information can be collected via olfactory cues, during direct social interactions, or indirectly, via faeces left in the environment by individuals. Although reducing the risks associated with a social confrontation, faeces also convey different types of information about traits and states of individuals which could affect the indirect STFP. Here, we evaluated in the house mouse, Mus musculus domesticus, which conspecifics could be good providers of food cues for indirect STFP. Our results indicated that female mice acquire an indirect STFP from faeces of adult females, familiar or not and from faeces of adult unfamiliar males. On the contrary, males do not establish an indirect STFP from faeces of males, whether they are familiar or not, nor from those of unfamiliar females. Indirect STFP was however effective in males when the faeces were those of an unfamiliar juvenile male. A prior habituation to the odour of an unfamiliar female allowed the establishment of indirect STFP in males. Conversely, the presence of faeces of another adult male during the presentation of faeces of an accustomed female precluded the acquisition of indirect STFP in males. This study suggested that in the context of the indirect STFP, females prioritize socio-olfactory information relative to food, whereas food cues were not priority information for males. Under these conditions, females appear to be the best vectors for disseminating food information within the population. These results are discussed according to the socio-spatial organization of the species.
Exploration tendency, one of the most investigated animal personality traits, may be driven by either positive (when seeking interesting information) or negative (to reduce the uncertainty of the environment) affective/emotional profiles. To disentangle the valence of the affective state associated with exploration trait, we applied a judgment bias test to evaluate the animals’ responses in an ambiguous situation, allowing an assessment of their affective state or mood. Experiments were carried out in male house mice (Mus musculus) of wild origin. Individual differences in exploration tendency were assessed by repeated open field and novel object tests. To evaluate the animals’ judgment bias, we trained the subjects for 8 days in a 3-arm maze to discriminate between two extreme locations (outer arms: either positively reinforced with sugary water or less-positively reinforced with plain water), in terms of a shorter latency to approach the positively reinforced arm. After this learning criterion was reached, we repeatedly tested their responses to an ambiguous location (intermediate arm). The latencies to approach and consume the ambiguous reward were highly repeatable over the 3 days of testing; hence individuals expressed a stable judgment bias. Most importantly, more exploratory animals showed a more negative judgment bias, which supports the hypothesis that a higher exploration tendency was associated with a negative affective state. Further studies should investigate whether exploration in different situations might be due to distinct affective states.
Isolation calls are emitted by the offspring of many mammalian species when separated from caregivers and siblings. Some studies indicate that isolation call rates constitute a consistent individual trait; others show that the young adjust their vocalization rate to the current situation. We studied this in the house mouse (Mus musculus domesticus) by exploring individual consistencies in pup isolation call rates and their potential modulation in different social situations. We carried out experiments including three treatments (repeated measurements) during consecutive days, all starting with an initial isolation of the pup, followed by (a) a reunion with mother and littermates and a second isolation hereafter, (b) the confrontation of isolated pup with cues of its own nest or (c) with cues of an unfamiliar adult male. The first treatment induced a significant increase, while the others induced significant decreases in pup isolation call rates. Pups showed consistent individual differences in initial call rates across the three days of testing (postnatal days 9-11), which were significantly associated with individual differences in call rates during the different treatments. We conclude that pup isolation calls represent a consistent, trait-like behaviour in the house mouse, which can also express flexibility in response to social cues.
Animals of different behavioral types typically show associated differences in their physiological stress response, including differential reactivity of the sympathetic nervous system. Infrared thermography offers the possibility to explore this link in a non-invasive way via the quantification of fine-scale changes in peripheral body temperature due to changes in cutaneous blood flow. We used this technique to investigate the association between exploration tendency, a behavioral trait frequently used to phenotype mammals and birds, and short-term thermal responses to challenge in a small rodent of wild origin, the mound-building mouse (Mus spicilegus). We applied a brief handling procedure consisting in the transfer of subjects into a small arena. This procedure led to a significant increase in subjects' maximum peripheral body temperature (mainly reflecting the temperature of the eyes) and to significant decreases in maximum temperatures at different positions on the tail. Maximum peripheral body and tail temperatures showed significant individual-level consistencies in response to repeated applications of the handling procedure, suggesting stable individual differences in the animals' sympathetic activity. We then compared the thermal responses to handling between 'fast' and 'slow' explorers, who were phenotyped through repeated open field and novel object tests. Fast explorers showed significantly lower tail temperatures than slow explorers shortly after handling, suggesting a stronger sympathetic reactivity in the former. Comparisons within sibling groups kept in different cages showed that the differences between explorer types were particularly pronounced during the first minute after handling, and increased in magnitude along the first millimeters distal to the tail base.
Rodents obtain information about a new food source through olfactory cues of conspecifics and consequently develop an attraction for this diet. Generally, physical contact between an observer and a demonstrator that has recently consumed a novel food item is required to allow the social transmission of food preference (STFP). However, in natural populations of house mice, social encounters between unfamiliar individuals usually turn into a fight. Thus, social intolerance between the individuals involved could prevent STFP. It has been shown that the feces of rodents can act as a social stimulus and promote STFP in mice, which could reduce the social constraints associated with an encounter. Here, we examined the acquisition of the STFP in female house mice of wild origin (Mus musculus domesticus) after a direct encounter with a familiar and unfamiliar female, and after the presentation of olfactory marks of an unfamiliar female. Unlike in encounters between familiar females, our results did not provide significant support for the existence of STFP after encounters between two unfamiliar females, independently of the occurrence or absence of offensive agonistic behavior. However, STFP through olfactory marks of an unfamiliar female was effective. We suggest that the social context might strongly impair direct STFP, not necessarily via the unfamiliarity of the information provider but rather via its physical presence. (PsycINFO Database Record
Mice can obtain information about a new food source through olfactory cues of conspecifics and consequently develop an attraction for this diet. The social transmission of food preference (STFP) takes place directly, during an encounter with a conspecific or indirectly, via feces. In indirect STFP, the digestive process can degrade odorant compounds characterizing the food, impairing the matching between feces and food. In a previous study, indirect STFP was efficient when the information support was a composite odorant. We, thus, hypothesized that the acquisition of indirect STFP depends on the multiplicity of the odorant compounds present in diets. Tested in female house mice (Mus musculus domesticus) our results showed that a single odorant compound as information support was not sufficient to induce an indirect STFP. Chemical analysis did not reveal the presence of the compounds in feces suggesting that the degradation of diet cues during the digestive process prevented the pairing between feces and food. By using a process that limits the degradation of molecules, we performed indirect STFP when the pertinent information was represented by a single odorant compound and multiple odorant compounds. Unlike with multiple odorant compounds, our results did not show a clear indirect STFP with single odorant compound, despite their presence in feces confirmed by chemical analysis. We conclude that constraints associated to indirect STFP can be removed by the multiplicity of information characterizing the diet both by reducing the degradation risk during the digestive process and by allowing an accurate assessment of diet consumed by the conspecific.
Exposure to predator cues is believed to induce fear-like responses in prey species and compounds found in the smells of predators, such as TMT (2,5-dihydro-2,4,5-trimethylthiazole) are frequently used to induce such responses. While behavioral changes of rodents after exposure to TMT have been well characterized, only few studies described the associated sympathetic responses. Here, we used non-invasive infrared thermography to assess short-term and fine-scale changes in peripheral body temperature of wild-origin house mice (Mus musculus domesticus) subjected to TMT. Peripheral temperature changes are associated with blood flow regulation occurring when mammals are subjected to emotion-eliciting situations. Our results revealed that confrontation to TMT induced clear peripheral thermal responses characterized by a significant increase in tail temperature and in the maximum peripheral body temperature. The increase in tail temperature is not the typical physiological stress response expected when mice are exposed to a fear-eliciting situation. In addition, mice did not express typical defensive behaviors such as freezing and avoidance. These results suggest that in our experimental conditions, TMT, as an indirect, chemical predator cue, induced arousal rather than fear. In conclusion, this study stresses the need for a deeper exploration of the behavioral and physiological response to predator odors to better understand the emotional responses they induce.
We asked whether within-litter differences in early body mass are associated with differences in house mouse pups' thermogenic performance and whether such variation predicts individual differences in competitive interactions for thermally more advantageous positions in the huddle. We explored pups' thermogenic performance in isolation by measuring changes in (maximal) peripheral body temperatures during a 5-min thermal challenge using infrared thermography. Changes in peripheral body temperature were significantly explained by individual differences in body mass within a litter; relatively lighter individuals showed an overall quicker temperature decrease leading to lower body temperatures toward the end of the thermal challenge compared to heavier littermates. Within the litter huddle, relatively lighter pups with a lower thermogenic performance showed consistently more rooting and climbing behavior, apparently to reach the thermally advantageous center of the huddle. This suggests that within-litter variation in starting body mass affects the pups' thermal and behavioral responses to environmental challenges.
Altricial mammals typically lack the physiological capacity to thermoregulate independently during the early postnatal period, and in litter-bearing species the young benefit strongly from huddling together with their litter siblings. Such litter huddles are highly dynamic systems, often characterized by competition for energetically favorable, central positions. In the present study, carried out in domestic rabbits Oryctolagus cuniculus, we asked whether individual differences in body mass affect changes in body temperature during changes in the position within the huddle. We predicted that pups with relatively lower body mass should be more affected by such changes arising from huddle dynamics in comparison to heavier ones. Changes in pups' maximum body surface temperature (determined by infrared thermography) were significantly affected by changes in the number of their neighbors in the litter huddle, and indeed these temperature changes largely depended on the pups' body mass relative to their litter siblings. Lighter pups showed significant increases in their maximum body surface temperature when their number of huddling partners increased by one or two siblings whereas pups with intermediate or heavier body mass did not show such significant increases in maximum body temperature when experiencing such changes. A similar pattern was found with respect to average body surface temperature. This strong link between changes in the number of huddling partners and body surface temperature in lighter pups might, on the one hand, arise from a higher vulnerability of such pups due to their less favorable body surface area-to-volume ratio. On the other hand, as lighter pups generally had fewer neighbors than heavier ones and thus typically a comparatively smaller body surface in contact with siblings, they potentially had more to gain from increasing their number of neighbors. The present findings might help to understand how individual differences in body mass within a litter lead to the emergence of individual differences in sibling interactions during early postnatal life in different species of altricial and litter-bearing mammals.
Due to their direct inaccessibility, affective states are classically assessed by gathering concomitant physiological and behavioral measures. Although such a dual approach to assess emotional states is frequently used in different species including humans, the invasiveness of procedures for physiological recordings particularly in smaller-sized animals strongly restricts their application. We used infrared thermography, a non-invasive method, to assess physiological arousal during open field and elevated plus maze tests in mice. By measuring changes in surface temperature indicative of the animals' emotional response, we aimed to improve the inherently limited and still controversial information provided by behavioral parameters commonly used in these tests. Our results showed significant and consistent thermal responses during both tests, in accordance with classical physiological responses occurring in stressful situations. Besides, we found correlations between these thermal responses and the occurrence of anxiety-related behaviors. Furthermore, initial temperatures measured at the start of each procedure (open field, elevated plus maze), which can be interpreted as a measure of the animals' initial physiological arousal, predicted the levels of activity and of anxiety-related behaviors displayed during the tests. Our results stress the strong link between physiological correlates of emotions and behaviors expressed during unconditioned fear tests.
Facial expressions have been extensively used to assess emotions in humans and thus could be extended to other species that also display facial movements. In mice both painful and fearful situations have been associated with particular shifts in facial expressions. Like other species, mice frequently show a great inter-individual variability when exposed to emotional situations, but so far no study has been conducted to investigate if facial expressions are related to these differences. The aim of this study is to explore if mice of wild origin (Mus spicilegus) express different facial expressions when confronted to novelty and to relate these mimics to their emotional reactivity profile. We used individual exploration scores in a novel odour test and in the elevated plus maze test as proxy measures of individual emotional reactivity. Our results showed that exploration scores in both tests were positively correlated, and both were related to the ear postures expressed by the individuals during their first exploration of the novel odour. This single component of facial expression was in fact a good indicator of inter-individual differences expressed in these two different tests suggesting a strong link between this marker and the individual emotional reactivity. These results highlight the great potential of facial expressions to assess emotional states in animals.
Animal personality, i.e. stable individual differences in behaviour, is considered to be subject to evolutionary processes, as it has been shown to be heritable and to entail fitness consequences. Different hypotheses have been developed to explain why personality variation is maintained within populations, most likely via processes of balancing selection. One mechanism discussed is that combinations of similar personalities within breeding pairs could increase fitness. We investigated this purported mechanism by studying the association between personality combinations within nulliparous pairs and their onset of reproduction in a monogamous rodent, the mound-building mouse, Mus spicilegus. In seasonal iteroparous breeders, reproductive timing is relevant to fitness, as a delayed onset of breeding potentially limits the number of breeding occasions and lowers the chance that offspring will start reproducing during the same season. Repeated standardized tests carried out prior to pairing revealed consistent individual differences in subjects' behavioural responses with respect to anxiety and exploratory activity, indicating the existence of personality types. Within-pair similarity in anxiety levels affected the chance of reproduction: pairs with similar anxiety scores had a higher probability of breeding, and were quicker to start, during the observation period, independently of the scores of both partners of the pair. We propose that this association between ‘personality matching’ and the onset of reproduction could have important life history consequences in this species and might be one of the mechanisms leading to the maintenance of personality variation within populations.
To cope with seasonally varying ecological constraints, some mammals temporally suppress breeding or delay their first reproduction. In field conditions, mound-building mice (Mus spicilegus) born in spring begin to reproduce when 2-3 months old, whereas individuals born at the end of summer delay their first reproduction for 6-8 months until the following spring. In order to test age effects on reproductive performance in M. spicilegus, sexually naïve mice were paired when 2-3 months old or at 6-8 months of age, and surveyed for reproduction. We show here that under laboratory conditions the aging of these mice does not impair their reproductive efficiency. Thus, the hypothesis of a lower reproductive potential in these relatively aged females seems to be contradicted. More surprisingly, the latency from pairing to the first reproduction was greater in the 2-3-month-old adults than in the delayed reproducers (6-8-month-old mice). Mound-building mice that are old enough to have overwintered do not suffer significant reproductive declines, but appear to reproduce as well and more quickly than younger first-time breeders.
Palatability of pet food has been mainly assessed by intake ratios. In the present study we have searched for behavioural clues of food palatability in domestic cats Felis catus. Two diets differing in palatability (Very Palatable Kibbles and Low Palatable Kibbles) were evaluated by a panel of 17 cats using an automated feeding station and video recordings. The cats tested each diet in two different sessions, with only one diet during a given session. A session lasted for two consecutive days with food continuously available during 20 h per 24 h period. At each of their visit to the feeding station, the quantity of food eaten by a cat, the speed of consumption and the latency to eat were recorded. The behaviour of the cat was also analysed for each visit. All the cats made at least four visits to the feeding station during a 24 h period. We compared the different quantitative variables between the two diets for the first three visits and for the last visit of each of the two days of a session. Our results showed that, as expected, cats ate more VPK than LPK. Addressing behavioural patterns, the length of sniffing was significantly reduced with VPK on the two first visits of the first day, suggesting less hesitation in this situation. Neither the latency nor the speed of consumption was affected by the palatability of the kibbles. (C) 2014 Elsevier B.V. All rights reserved.