Date Published: October 1, 2018
Publisher: Public Library of Science
Author(s): Xiaolong Hu, Yuting Wei, Songlin Huang, Gang Liu, Yihua Wang, Defu Hu, Shuqiang Liu, Ludek Bartos.
The objective of this study was to evaluate the effects of sex, breeding center and age on fecal triiodothyronine levels in captive forest musk deer Moschus berezovskii, and to explore the age-intensity model of gastrointestinal parasites. Furthermore, the association between fecal triiodothyronine levels and parasite egg shedding was also analyzed. We collected musk deer fecal samples from two breeding centers located in Shaanxi and Sichuan province, China. Enzyme-linked immunosorbent assays were utilized to estimate the fecal triiodothyronine concentrations and profiles, and fecal parasite eggs or oocysts were counted using the McMaster technique. Female deer from both breeding centers consistently showed higher triiodothyronine concentrations than those observed in males, which indicates that a distinct physiology pattern occurs by sex. The triiodothyronine concentration in Sichuan breeding center was significantly higher than that in Shaanxi center for both sexes, suggesting that differences in environment, diet and management practices are likely to affect the metabolism. In addition, a negative relationship between triiodothyronine concentrations and age was found (r = – 0.75, p < 0.001), and parasite egg shedding was also negatively associated with age (r = - 0.51, p < 0.001), by which we can infer that older animals evolves a more developed immune system. Finally, a positive association between parasite egg shedding and triiodothyronine levels was found, which could be explained by the additional energy metabolism resulting from parasitic infection. Results from this study might suggest metabolic and immunological adaptations in forest musk deer. These baseline data could be used to unveil metabolic status and establish parasite control strategies, which has great potential in captive population management as well as their general health evaluations.
Thyroid hormones are important regulators of metabolism, growth, development, reproduction, and homeostasis in mammals and birds [1, 2]. Thyroid hormones include triiodothyronine (T3), reverse triiodothyronine (rT3), thyroxine (T4), and reverse thyroxine (rT4), and of these the most potent component is T3 [3, 4]. Levels of thyroid hormones are affected by several factors, including nutrition [5, 6], temperature , age [6, 8], sex [9, 10], and reproduction [8, 11]. Parasite infection poses serious threats to animal health, and creates burdens on the host physiological metabolism . The adaptive secretion of thyroid hormones is an important response mechanism to metabolic disorders and adverse environments. However, few studies have analyzed the associative pattern between gastrointestinal (GI) parasite infection and thyroid hormones.
Thyroid hormone levels tended to be sex biased, with higher T3 concentrations found in females than males, regardless of the breeding center and age. This trend is in agreement with those reported in dolphins Tursiops truncatus , Rhesus monkeys Macaca mulatta tcheliensis , pigs Susscrofa domestica , Moghani sheep Ovis aries irania , and white goat Capra aegagrus hircus . The sex-biased thyroid hormone levels are partly due to the differences in the metabolic physiology and reproduction mechanism between the female and the male. In mammalian species, thyroid hormones are essential for the maintenance of female reproductive behaviors (e.g. sustain pregnancy and raise offspring) . Our study found that lactating and non-lactating females showed similar T3 levels, whereas the baseline levels of T3 in females were higher than in males, which might indicate a higher energy consumption of female in breeding seasons than males. Furthermore, T3 levels may also be related to the activity of animals, and a previous study  reported that more rapid fecal excretion of T3 occurs in more active dogs. Female FMD are always allowed to wander within the enclosures every day, whereas males are only allowed outside occasionally.
The present study indicates a noteworthy relationship between biotic (sex, age, parasite burden) and abiotic (breeding center) factors with T3 levels in FMD. Meanwhile, the sex-related differences in T3 levels reflect distinct metabolic physiology between female and male FMD. The negative relationship between parasite egg shedding and age suggests an immune adaption with the aging of hosts. The results have great potential in future management of FMD and relative ruminants at several aspects: 1) the baseline information on fecal thyroid hormones with bovine T3 antibody has been established, which can be used to unveil physiological status and metabolic characteristics of FMD; 2) when breeders feed FMD, they should take consideration of factors of sex, age and even breeding center to guide the diet allocation, for example, the younger FMD should be given the diet containing more concentrate food to meet the higher energy demand; 3) the results have revealed a relationship between thyroid hormones and GI parasite infection, which may be a general pattern in ruminants, in turn may potentially improve techniques in disease diagnosis.