Unsaturated fatty acids (UFAs), such as omega-3 and omega-6 poly- and omega-9 monounsaturated fatty acids are important nutrients and major components of neuronal cell membranes. They play a major role in modulating brain functions and physiology and may therefore diminish behavioral and physiological stress reactions in corroboration with decreased cortisol concentrations. Functionally, cortisol itself can modulate several behaviors and also the fatty acid metabolism in the long term. But only little is known about the behavioral and physiological influences of dietary UFAs in a social group, where individuals are regularly exposed to stressful situations. Therefore, the aim of this study was to determine the effects of dietary UFAs on saliva cortisol concentrations and behavioral responses in socially confronted guinea pigs. Three groups of animals were additionally supplemented with 500 mg chia seeds (high in omega-3), walnuts (high in omega-6), or peanuts (high in omega-9) per kg bodyweight each day and compared to a control group. During social confrontation saliva cortisol concentrations significantly increased in all groups, which was accompanied by a loss in bodyweight. However, cortisol levels remained lower in the chia and walnut groups compared to controls. Additionally, the walnut group displayed significantly increased locomotion, while no differences between groups were detected in socio-positive, sexual, or aggressive behaviors. Total plasma omega-3, omega-6, and omega-9 fatty acids were significantly increased in the corresponding groups, due to the dietary supplementations. However, a significant decrease in plasma omega-3 and an increase in plasma n-6 fatty acids were detected in the chia group when comparing the measurements before and after social confrontation. We conclude that both omega-3 and omega-6 polyunsaturated fatty acids can diminish behavioral and physiological stress responses to the social environment, enabling individuals to cope with social stressors, but at the expense of plasma derived omega-3 fatty acids.
Non-invasive measurements of glucocorticoid (GC) concentrations, including cortisol and corticosterone, serve as reliable indicators of adrenocortical activities and physiological stress loads in a variety of species. As an alternative to invasive analyses based on plasma, GC concentrations in saliva still represent single-point-of-time measurements, suitable for studying short-term or acute stress responses, whereas fecal GC metabolites (FGMs) reflect overall stress loads and stress responses after a species-specific time frame in the long-term. In our study species, the domestic guinea pig, GC measurements are commonly used to indicate stress responses to different environmental conditions, but the biological relevance of non-invasive measurements is widely unknown. We therefore established an experimental protocol based on the animals’ natural stress responses to different environmental conditions and compared GC levels in plasma, saliva, and fecal samples during non-stressful social isolations and stressful two-hour social confrontations with unfamiliar individuals. Plasma and saliva cortisol concentrations were significantly increased directly after the social confrontations, and plasma and saliva cortisol levels were strongly correlated. This demonstrates a high biological relevance of GC measurements in saliva. FGM levels measured 20 h afterwards, representing the reported mean gut passage time based on physiological validations, revealed that the overall stress load was not affected by the confrontations, but also no relations to plasma cortisol levels were detected. We therefore measured FGMs in two-hour intervals for 24 h after another social confrontation and detected significantly increased levels after four to twelve hours, reaching peak concentrations already after six hours. Our findings confirm that non-invasive GC measurements in guinea pigs are highly biologically relevant in indicating physiological stress responses compared to circulating levels in plasma in the short- and long-term. Our approach also underlines the importance of detailed investigations on how to use and interpret non-invasive measurements, including the determination of appropriate time points for sample collections.
Hibernating animals can adjust torpor expression according to available energy reserves. Besides the quantity, the quality of energy reserves could play an important role for overwintering strategies. Common hamsters are food-storing hibernators and show high individual variation in hibernation performance, which might be related to the quality of food hoards in the hibernacula. In this study, we tested the effects of food stores high in fat content, particularly polyunsaturated fatty acids (PUFAs), on hibernation patterns under laboratory conditions. Control animals received standard rodent pellets only, while in the other group pellets were supplemented with sunflower seeds. We recorded body temperature during winter using subcutaneously implanted data loggers, documented total food consumption during winter, and analysed PUFA proportions in white adipose tissue (WAT) before and after the winter period. About half of the individuals in both groups hibernated and torpor expression did not differ between these animals. Among the high-fat group, however, individuals with high sunflower seeds intake strongly reduced the time spent in deep torpor. PUFA proportions in WAT decreased during winter in both groups and this decline was positively related to the time an individual spent in deep torpor. Sunflower seeds intake dampened the PUFA decline resulting in higher PUFA levels in animals of the high-fat group after winter. In conclusion, our results showed that common hamsters adjusted torpor expression and food intake in relation to the total energy of food reserves, underlining the importance of food hoard quality on hibernation performance.
Unsaturated fatty acids (UFAs), including omega-3, omega-6 polyunsaturated and omega-9 monounsaturated fatty acids, are essential components and modulators of neuromembranes and may affect various aspects of physiology and cognition. UFAs are suggested to positively affect spatial learning and memory and also to diminish the negative consequences of physiological stress on cognitive abilities. Due to pronounced sex differences in neurophysiological functions, we hypothesize that these UFA-related effects might differ between male and female individuals. We therefore determined the effects of dietary UFAs on cognitive performances in a radial-Y-maze in male and female guinea pigs in relation to saliva cortisol concentrations, a marker for physiological stress. Animals were assigned to four treatment groups and maintained on diets enriched in either chia seeds (omega-3), walnuts (omega-6), or peanuts (omega-9), or a control diet. Female learning abilities throughout a three-day learning phase were positively affected by omega-3 and omega-9, as determined by a decreasing latency to pass the test and the number of conducted errors, while males generally showed distinct learning abilities, irrespective of the diet. A sex difference in learning performances was found in the control group, with males outperforming females, which was not detected in the UFA-supplemented groups. This was paralleled by significantly increased saliva cortisol concentrations in males throughout the cognition test compared to females. Three days after this learning phase, UFA-supplemented males and all females showed unchanged performances, while control males showed an increased latency and therefore an impaired performance. These results were corroborated by pronounced differences in the plasma UFA-status, corresponding to the different dietary treatments. Our findings indicate sex-specific effects of dietary UFAs, apparently enhancing spatial learning abilities only in females and protecting males from long-term memory impairment, while male learning abilities seem to be more strongly affected by an acute physiological stress response to the maze task.
BackgroundUnbalanced dietary intakes of saturated (SFAs) and polyunsaturated (PUFAs) fatty acids can profoundly influence the hypothalamic-pituitary-adrenal (HPA)-axis and glucocorticoid secretions in relation to behavioral performances. The beneficial effects of higher dietary PUFA intakes and PUFA:SFA ratios may also affect social interactions and social-living per se, where adequate physiological and behavioral responses are essential to cope with unstable social environmental conditions.MethodsEffects of diets high in PUFAs or SFAs and a control diet were investigated in male and female guinea pigs after 60 days of supplementation. Plasma fatty acid patterns served as an indicator of the general fatty acid status. HPA-axis activities, determined by measuring saliva cortisol concentrations, social behaviors, and hierarchy ranks were analyzed during group housing of established single-sexed groups and during challenging social confrontations with unfamiliar individuals of the other groups.ResultsThe plasma PUFA:SFA ratio was highest in PUFA supplemented animals, with female levels significantly exceeding males, and lowest in SFA animals. SFA males and females showed increased saliva cortisol levels and decreased aggressiveness during group housing, while sociopositive behaviors were lowest in PUFA males. Males generally showed higher cortisol increases in response to the challenging social confrontations with unfamiliar individuals than females. While increasing cortisol concentrations were detected in control and PUFA animals, no such effect was found in SFA animals. During social confrontations, PUFA males showed higher levels of agonistic and sociopositive behaviors and also gained higher dominance ranks among males, which was not detected for females.ConclusionsWhile SFAs seemingly impaired cortisol responses and social behaviors, PUFAs enabled adequate behavioral responses in male individuals under stressful new social environmental conditions. This sex-specific effect was possibly related to a general sex difference in the n-3 PUFA bioavailability and cortisol responses, which may indicate that males are more susceptible to changing environmental conditions, and shows how dietary fatty acids can shape social systems.Electronic supplementary materialThe online version of this article (doi:10.1186/s13293-016-0107-5) contains supplementary material, which is available to authorized users.
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