Decreased basal thermogenesis is associated with the downregulation of cellular metabolic activity of organs and serum thyroid hormones in fasting Eurasian Tree Sparrows (Passer montanus)

Hong Jin^{^a^,^b^,¹}, Qi Xia^{^a^,^b^,¹}, Ziqing Gao^{^a^,^b}, Yujie XuanYuan^{^a^,^b}, Beibei Dong^{^c}, Ming Li^{^a^,^b}, Qingjian Liang^{^c}(), Jinsong Liu^{^a^,^b}

()

College of Life and Environmental Sciences, Wenzhou University, Wenzhou, 325035, China

Zhejiang Provincial Key Laboratory for Water Environment and Marine Biological Resources Protection, Wenzhou University, Wenzhou, 325035, China

Laboratory of Aquatic Animal Diseases and Immunity, School of Fishery, Zhejiang Ocean University, Zhoushan, 316022, China

¹ Hong Jin and Qi Xia contributed equally to this work.

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Abstract

Food is a critical environmental factor that influences animal survival, especially for small passerines due to their high mass-specific metabolic rates. Basal metabolic rate (BMR) reflects the energy expended by endothermic animals for basic physiological processes and constitutes a major part of their daily energy budget. Some birds have been shown to employ compensatory mechanisms during food shortages, temporarily reducing these self-maintenance expenditures without using hypothermia. However, the mechanisms of BMR adjustment remain unexplored. In the present study, we assessed the phenotypic variation in basal thermogenesis of Eurasian Tree Sparrows (Passer montanus) by comparing a control group to groups fasted for 6, 12, 18, and 24 h. We focused on the correlation between a reduction in energy metabolism and the alterations of cellular metabolic activities, mitochondrial substrate supply, and changes in serum thyroid hormones during fasting. Our data indicated that fasting groups had significantly lower body mass, BMR, body temperature, and body fat content. Furthermore, fasting groups had significantly lower glycogen levels, mitochondrial state 4 respiration and cytochrome c oxidase (CCO) activity in the liver, and CCO activity in pectoral muscle. The levels of avian uncoupling protein (av-UCP) mRNA were significantly reduced, while the levels of myostatin protein in pectoral muscle were significantly increased in the fasting groups. Furthermore, the groups subjected to fasting exhibited significantly lower levels of serum glucose, triglyceride, thyroxine (T₄), and triiodothyronine (T₃). Positive correlations were observed between the following pairs of variables: log BMR and log body mass, log body mass and log body fat, log BMR and log state 4 respiration in the liver, log BMR and log CCO activity in the liver and muscle, log BMR and log av-UCP mRNA expression, whereas a negative correlation was observed between log BMR and log myostatin level. In addition, a positive correlation was also detected between log T₃ and each of the following: log BMR, state 4 respiration, and log CCO activity in the liver. Our results suggested that decreased metabolic thermogenesis via down-regulation in cellular aerobic capacity of organs and serum thyroid hormones may be an important survival strategy for fasting Tree Sparrows to reduce energy expenditure.

Keywords

Basal metabolic rate Energy metabolism Fasting Passer montanusThyroid hormones av-UCPmRNA

References

Abe, T., Mujahid, A., Sato, K., Akiba, Y., Toyomizu, M., 2006. Possible role of avian uncoupling protein in down-regulating mitochondrial superoxide production in skeletal muscle of fasted chickens. FEBS Lett. 580, 4815–4822.

Parameters	0 h (n = 6)	6 h (n = 6)	12 h (n = 6)	18 h (n = 6)	24 h (n = 6)		P
Note: Statistical significance was determined by one-way ANCOVA except for pectoral muscle. For pectoral muscle, statistical significance was determined by Kruskal–Wallis. Data are shown as mean ± SE from 30 birds. Different superscript letters in the same row indicate significant differences among groups after Tukey’s post hoc test. P-values in bold indicate differences with statistical significance.
Wet mass (g)
Pectoral muscle	1.76 ± 0.13	1.89 ± 0.12	2.06 ± 0.12	1.89 ± 0.12	2.05 ± 0.13	χ² = 2.933	0.569
Liver	0.79 ± 0.07 ^a	0.80 ± 0.06 ^a	0.79 ± 0.06 ^a	0.65 ± 0.06 ^ab	0.49 ± 0.07 ^b	F_4,24 = 3.650	0.018
Heart	0.19 ± 0.01^ab	0.20 ± 0.01^a	0.20 ± 0.01^a	0.17 ± 0.01^b	0.17 ± 0.01^b	F_4,24 = 2.870	0.045
Kidney	0.16 ± 0.02	0.18 ± 0.01	0.19 ± 0.01	0.19 ± 0.01	0.16 ± 0.02	F_4,24 = 1.065	0.395
Lung	0.16 ± 0.01^b	0.20 ± 0.01^a	0.17 ± 0.01^b	0.16 ± 0.01^b	0.15 ± 0.01^b	F_4,24 = 3.950	0.013
Spleen	0.03 ± 0.00 ^a	0.03 ± 0.00 ^a	0.02 ± 0.00 ^ab	0.02 ± 0.00 ^bc	0.01 ± 0.00 ^c	F_4,24 = 4.316	0.009
Brain	0.77 ± 0.03^a	0.81 ± 0.03^a	0.69 ± 0.03^b	0.77 ± 0.03^a	0.77 ± 0.03^a	F_4,24 = 3.173	0.032
Gizzard	0.52 ± 0.03^ab	0.47 ± 0.03^abc	0.54 ± 0.03^a	0.46 ± 0.03^bc	0.41 ± 0.03^c	F_4,24 = 3.186	0.031
Small intestine	0.54 ± 0.05^a	0.55 ± 0.04^a	0.51 ± 0.04^a	0.42 ± 0.04^b	0.35 ± 0.05^b	F_4,24 = 3.061	0.036
Total digestive tract	1.10 ± 0.06^a	1.08 ± 0.05^a	1.11 ± 0.05^a	0.91 ± 0.05^b	0.80 ± 0.06^b	F_4,24 = 5.686	0.002

Allometric correlations^a	Pectoral muscle	Liver	Heart	Kidney	Lung	Spleen	Brain	Gizzard	Small intestine	Total digestive tract
^a Linear regression statistics for log organ mass versus log body mass (minus wet mass of the organ) allometric equations (allometric correlations).^b Linear regression statistics for log organ mass residuals versus log BMR residuals (residual correlations), or log organ mass versus log BMR raw values if allometric equations were not significant. P-values in bold indicate differences with statistical significance.
r	0.561	0.385	0.642	0.182	0.231	0.445	0.254	0.171	0.468	0.447
P	0.001	0.035	<0.001	0.337	0.221	0.014	0.175	0.366	0.009	0.013
Slope	1.012	0.979	0.855	0.325	0.333	1.988	0.223	0.237	1.389	0.767
Residual correlations^b
r	0.146	0.492	0.351	0.114	0.398	0.423	0.237	0.247	0.353	0.379
P	0.442	0.006	0.057	0.550	0.029	0.020	0.208	0.188	0.056	0.039
Slope	−0.094	0.202	0.332	0.091	0.398	0.102	0.389	0.258	0.130	0.238

Variable	Control (n = 6)	6 h (n = 6)	12 h (n = 6)	18 h (n = 6)	24 h (n = 6)	F_4,25	P
Note: statistical significance was determined by one-way ANOVA. Data are shown as mean ± SE from 30 birds. Different superscript letters in the same row indicate significant differences among groups after Tukey’s post hoc test. P-values in bold indicate differences with statistical significance.
Liver:
State 4 respiration (μmol O₂ min⁻¹ organ⁻¹)	0.27 ± 0.03^a	0.27 ± 0.01^a	0.26 ± 0.03^a	0.25 ± 0.02^ab	0.18 ± 0.01^b	2.846	0.045
Cytochrome c oxidase activity (μmol O₂ min⁻¹ organ⁻¹)	0.12 ± 0.01^a	0.12 ± 0.01^ab	0.11 ± 0.01^ab	0.10 ± 0.00^ab	0.09 ± 0.01^b	3.966	0.013
Muscle:
State 4 respiration (μmol O₂ min⁻¹ whole tissue⁻¹)	1.01 ± 0.13	1.05 ± 0.18	0.98 ± 0.08	0.91 ± 0.10	0.88 ± 0.05	0.379	0.822
Cytochrome c oxidase activity (μmol O₂ min⁻¹ whole tissue⁻¹)	0.49 ± 0.06^a	0.44 ± 0.02^a	0.45 ± 0.04^a	0.41 ± 0.03^ab	0.29 ± 0.03^b	4.398	0.008

Parameters	0 h (n = 6)	6 h (n = 6)	12 h (n = 6)	18 h (n = 6)	24 h (n = 6)	F_4,25	P
Note: statistical significance was determined by one-way ANOVA. Data are shown as mean ± SE from 30 birds. Different superscript letters in the same row indicate significant differences among groups after Tukey’s post hoc test. P-values in bold indicate differences with statistical significance.
Glucose (mg dL⁻¹)	241.07 ± 4.75^a	183.55 ± 19.14^ab	161.04 ± 14.11^bc	157.34 ± 22.76^bc	96.40 ± 16.25^c	9.918	<0.001
Triglyceride (mg dL⁻¹)	258.57 ± 36.37^a	210.48 ± 48.27^ab	98.62 ± 20.22^bc	65.69 ± 13.22^c	64.74 ± 7.25^c	9.303	<0.001
T₄ (ng mL⁻¹)	41.16 ± 6.65^a	40.01 ± 8.19^ab	32.37 ± 6.05^ab	23.64 ± 7.09^ab	14.04 ± 3.33^b	3.136	0.032
T₃ (ng mL⁻¹)	3.42 ± 0.14^ab	3.61 ± 0.10^a	3.65 ± 0.10^a	3.44 ± 0.15^ab	3.04 ± 0.07^b	3.416	0.023