Glucocorticoids in relation to behavior, morphology, and physiology as proxy indicators for the assessment of animal welfare. A systematic mapping review.

Translating theoretical concepts of animal welfare into quantitative assessment protocols is an ongoing challenge. Glucocorticoids (GCs) are frequently used as physiological measure in welfare assessment. The interpretation of levels of GCs and especially their relation to welfare, however, is not as straightforward, questioning the informative power of GCs. The aim of this systematic mapping review was therefore to provide an overview of the relevant literature to identify global patterns in studies using GCs as proxy for the assessment of welfare of vertebrate species. Following a systematic protocol and a-priory inclusion criteria, 509 studies with 517 experiments were selected for data extraction. The outcome of the experiments was categorized based on whether the intervention significantly affected levels of GCs, and whether these effects were accompanied by changes in behavior, morphology and physiology. Additional information, such as animal species, type of intervention, experimental set up and sample type used for GC determination was extracted, as well. Given the broad scope and large variation in included experiments, meta-analyses were not performed, but outcomes are presented to encourage further, in-depth analyses of the data set. The interventions did not consistently lead to changes in GCs with respect to the original authors hypothesis. Changes in GCs were not consistently paralleled by changes in additional assessment parameter on behavior, morphology and physiology. The minority of experiment quantified GCs in less invasive sample matrices compared to blood. Interventions showed a large variability, and species such as fish were underrepresented, especially in the assessment of behavior. The inconclusive effects on GCs and additional assessment parameter urges for further validation of techniques and welfare proxies. Several conceptual and technical challenges need to be met to create standardized and robust welfare assessment protocols and to determine the role of GCs herein.

Effects of the maternal and current social environment on female body mass and reproductive traits in Japanese quail (Coturnix japonica).

The social environment of breeding females can affect their phenotype, with potential adaptive maternal effects on offspring that experience a similar environment. We housed Japanese quail (Coturnix japonica) females in two group sizes (pairs versus groups of four) and studied the effects on their offspring under matched and mismatched conditions. We measured F1 body mass, reproduction, and plasma levels of androgens and corticosterone. F1 group housing led to an increase in body mass. In addition, F1 group housing had a positive effect on mass in daughters of pair-housed P0 females only, which were heaviest under mismatched conditions. At the time of egg collection for the F2 generation, F1 group-housed females were heavier, irrespective of the P0 treatment. F1 females in groups laid heavier eggs, with higher hatching success, and produced heavier offspring, most likely a maternal effect of F1 mass. F1 plasma hormones were affected by neither the P0 nor the F1 social environment. These results contrasted with effects in the P0 generation (reported previously), in which plasma hormone levels, but not mass, differed between social environments. This may be due to changes in adult sex ratios as P0 females were housed with males, whereas F1 females encountered males only during mating. Our study demonstrates potentially relevant mismatch effects of the social environment on F1 body mass and maternal effects on F2 offspring, but further study is needed to understand their adaptive significance and physiological mechanisms.

Correction: Social environment during egg laying: Changes in plasma hormones with no consequences for yolk hormones or fecundity in female Japanese quail, Coturnix japonica.

[This corrects the article DOI: 10.1371/journal.pone.0176146.].

No evidence for sex-specific effects of the maternal social environment on offspring development in Japanese quail (Coturnix japonica).

The social environment of reproducing females can cause physiological changes, with consequences for reproductive investment and offspring development. These prenatal maternal effects are often found to be sex-specific and may have evolved as adaptations, maximizing fitness of male and female offspring for their future environment. Female hormone levels during reproduction are considered a potential mechanism regulating sex allocation in vertebrates: high maternal androgens have repeatedly been linked to increased investment in sons, whereas high glucocorticoid levels are usually related to increased investment in daughters. However, results are not consistent across studies and therefore still inconclusive. In Japanese quail (Coturnix japonica), we previously found that pair-housed females had higher plasma androgen levels and tended to have higher plasma corticosterone levels than group-housed females. In the current study we investigate whether these differences in maternal social environment and physiology affect offspring sex allocation and physiology. Counter to our expectations, we find no effects of the maternal social environment on offspring sex ratio, sex-specific mortality, growth, circulating androgen or corticosterone levels. Also, maternal corticosterone or androgen levels do not correlate with offspring sex ratio or mortality. The social environment during reproduction therefore does not necessarily modify sex allocation and offspring physiology, even if it causes differences in maternal physiology. We propose that maternal effects of the social environment strongly depend upon the type of social stimuli and the timing of changes in the social environment and hormones with respect to the reproductive cycle and meiosis.

Social environment during egg laying: Changes in plasma hormones with no consequences for yolk hormones or fecundity in female Japanese quail, Coturnix japonica.

The social environment can have profound effects on an individual's physiology and behaviour and on the transfer of resources to the next generation, with potential consequences for fecundity and reproduction. However, few studies investigate all of these aspects at once. The present study housed female Japanese quail (Coturnix japonica) in pairs or groups to examine the effects on hormone concentrations in plasma and yolk and on reproductive performance. Circulating levels of androgens (testosterone and 5-α-dihydrotestosterone) and corticosterone were measured in baseline samples and after standardised challenges to assess the responsiveness of the females' endocrine axes. Effects of the social environment on female fecundity were analysed by measuring egg production, egg mass, fertilization rates, and number of hatched offspring. Counter to expectation, females housed in pairs had higher plasma androgen concentrations and slightly higher corticosterone concentrations than females housed in groups, although the latter was not statistically significant. Pair vs. group housing did not affect the females' hormonal response to standardised challenges or yolk testosterone levels. In contrast to previous studies, the females' androgen response to a gonadotropin-releasing hormone challenge was not related to yolk testosterone levels. Non-significant trends emerged for pair-housed females to have higher egg-laying rates and higher fertility, but no differences arose in egg weight or in the number, weight or size of hatchlings. We propose that our unexpected findings are due to differences in the adult sex ratio in our social treatments. In pairs, the male may stimulate female circulating hormone levels more strongly than in groups where effects are diluted due to the presence of several females. Future studies should vary both group size and sex composition to disentangle the significance of sexual, competitive and affiliative social interactions for circulating and yolk hormone levels, and their consequences for subsequent generations.