Zhao et al. Avian Res (2017) 8:10 DOI 10.1186/s40657-017-0068-3 Avian Research RESEARCH Open Access Do migrant and resident species difer in the timing of increases in reproductive and thyroid hormone secretion and body mass? A case study in the comparison of pre‑breeding physiological rhythms in the Eurasian Skylark and Asian Short‑toed Lark Lidan Zhao1, Lijun Gao1, Wenyu Yang1, Xianglong Xu1, Weiwei Wang1, Wei Liang2 and Shuping Zhang1* Abstract Background: Physiological preparation for reproduction in small passerines involves the increased secretion of reproductive hormones, elevation of the metabolic rate and energy storage, all of which are essential for reproduc- tion. However, it is unclear whether the timing of the physiological processes involved is the same in resident and migrant species that breed in the same area. To answer this question, we compared temporal variation in the plasma concentration of luteinizing hormone (LH), testosterone (T), estradiol ­(E2), triiothyronine ­(T3) and body mass, between a migrant species, the Eurasian Skylark (Alauda arvensis) and a resident species, the Asian Short-toed Lark (Calandrella cheleensis), both of which breed in northeastern Inner Mongolia, China, during the 2014 and 2015 breeding seasons. Methods: Twenty adult Eurasian Skylarks and twenty Asian Short-toed Larks were captured on March 15, 2014 and 2015 and housed in out-door aviaries. Plasma LH, T (males), ­E2 (females), ­T3 and the body mass of each bird were measured every six days from March 25 to May 6. Results: With the exception of T, which peaked earlier in the Asian Short-toed Lark in 2014, plasma concentrations of LH, T, ­E2 ­andT3 of both species peaked at almost the same time. However, Asian Short-toed Larks attained peak body mass earlier than Eurasian Skylarks. Plasma ­T3 concentrations peaked 12 days earlier than plasma LH in both species. Generally, plasma LH, T, ­E2, ­T3 and body mass, peaked earlier in both species in 2014 than 2015. Conclusions: The timing of pre-reproductive changes in the endocrine system and energy metabolism can be the same in migrant and resident species; however, residents may accumulate energy reserves faster than migrants. Although migration does not afect the timing of pre-breeding reproductive and metabolic changes, migrant species may need more time to increase their body mass. T levels in resident species may be accelerated by higher spring temperatures that may also advance the pre-breeding preparation of both migrants and residents. Keywords: Alauda arvensis, Calandrella cheleensis, Pre-breeding, Physiological preparation, Migratory birds *Correspondence: [email protected] 1 College of Life and Environment Sciences, Minzu University of China, Beijing 100081, China Full list of author information is available at the end of the article © The Author(s) 2017. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Zhao et al. Avian Res (2017) 8:10 Page 2 of 9 Background competition for breeding resources (Morbey and Reproduction is one of the most energetically demand- Ydenberg 2001). Because the duration of physiologi- ing activities in the life of birds. At mid and high latitudes, cal preparation for breeding determines the timing of suitable conditions for breeding are relatively brief and reproduction, it is important to determine if the timing birds that live at these latitudes must therefore time their of the physiological processes involved in activation of reproductive activity to coincide with periods when food the reproduction endocrine system and, at the same time, suitable for the survival of parents and ofspring is rela- increasing their metabolic rate and energy storage is the tively abundant (Dawson et al. 2001). Birds must complete same in migratory and resident species. To the best of three stages of physiological preparation to begin breed- our knowledge, no one has yet conducted the necessary ing. First, the hypothalamic-pituitary–gonadal axis (HPG) research to address this question in wild birds. is activated. Te hypothalamus secrets the gonadotro- In our study, we compared the timing of physiological phin-releasing hormone cGnRH-I when stimulated by the preparation for breeding in two members of the Alaudi- longer days of early spring (Yasuo and Yoshimura 2009). dae, the Eurasian Skylark (Alauda arvensis) and the Asian Tis hormone is then transported in the blood to the Short-toed Lark (Calandrella cheleensis), both of which pituitary where it stimulates the secretion of the lutein- breed in the grasslands of northeastern Inner Mongolia, izing hormone (LH) and the follicle-stimulating hormone China. Te Eurasian Skylark is a migratory species that (FSH). LH and FSH induce development of the ovaries arrives at the Inner Mongolian grasslands in early March or testes, which then regulate the production of the sex and begins nesting in mid-April (Lou 1966). Te Asian hormones, mainly estradiol (E 2) and testosterone (T) will Short-toed Lark is a resident that also starts breeding in enter the circulation to start the reproductive behavior mid-April. Te breeding periods of the two species are (Aurélie et al. 2010). Secondly, birds must increase their therefore highly synchronous, with the main food of nest- metabolic rate in preparation for higher energy consump- lings of both species as grasshopper nymphs which are tion during breeding (Ricklefs 1974; Carey 1996; Nilsson only seasonally abundant on the grasslands in the breeding and Raberg 2001). Pre-reproductive energy metabolism is season (Tian et al. 2015). In order to compare the timing an important factor afecting the timing of breeding (Ste- of physiological preparation of the reproductive endocrine venson and Bryant 2000). Tyroid hormones, especially system, energy metabolism and energy storage in these two triiothyronine (T3), play an important role in substrate species, we compared their pre-breeding temporal trends metabolism and thermogenesis, and T 3 plasma concen- in LH, T, E2 and T3, plasma concentrations and body mass tration is positively correlated with BMR (basic metabolic during the spring of 2014 and 2015. We hypothesize that rate) (Yen 2001; Chastel et al. 2003; Li et al. 2010; Wel- migratory and non-migratory birds will show diferences in cker et al. 2013; Zheng et al. 2013). Plasma T3 levels are elevating LH, T, E2 and T3 levels and body mass. known to increase before breeding in several bird species (Smith 1982; Pathak and Chandola 1983). It has also been Methods Study area found that individual birds that increase their plasma T3 levels sooner start breeding earlier (Chastel et al. 2003). Our study site was in the Dalai National Nature Reserve Tirdly, after going through a period of relative food (47°45′50″‒49°20′20″N; 116°50′10″‒118°10′10″E), located shortage in the winter, or depleting their energy reserves in the northeastern part of Inner Mongolia, China. Tis during migration, birds have to increase their food intake is a semiarid, steppe region where the mean annual tem- before breeding in order to meet the increased nutritional perature is −0.6 °C, with 283 mm precipitation and a requirements of the breeding season (Hegemann et al. potential evaporation of 1754 mm. Te dominant plant 2012). Body mass, which can be regarded as the balance species are Stipa krylovii, Leymus chinesis and Cleis- between energy intake and its expenditure (Zhao et al. togenes squarrosa. Winters are longer than summers and 2015) usually increases before breeding (Wang and Lei the approximate average maximum daytime temperature 2011; Hegemann et al. 2012). is −20.02 °C in January and 22.72 °C in July. Migratory species must compete with residents for breeding resources, including territories and food, after Study design their arrival at the breeding grounds. However, unlike Twenty adult Eurasian Skylarks and twenty adult Asian resident birds, migratory birds consume a large amount Short-toed Larks (sex ratio = 1:1) per year were cap- of energy in the course of migrating to the breeding tured in mist-nets on the same date, March 15, in grounds (Jenni et al. 2000). Terefore migratory species 2014 and 2015. Birds were housed in out-door aviaries might attain breeding condition later than residents for (50 cm × 40 cm × 35 cm) (one bird per aviary), in which their migration energy consumption. Tey would there- they were acclimatized to captivity for 10 days. Birds were fore be expected to be at a disadvantage in subsequent fed mixed seeds, boiled eggs, mealworms and provided Zhao et al. Avian Res (2017) 8:10 Page 3 of 9 with water during this period. At least 100 μL of whole factor. Te LMMs were also used to determine the efects blood was collected from each bird every four days from of sample date and species on T and E2 in both years. Sam- March 25 to May 6 in 2014 and 2015. Blood was collected ple date, species and the interactions between these factors into heparinized micro-capillary tubes within 1–3 min of were modeled as fxed factors, again with individual bird capture by puncturing a brachial wing vein with a disin- as a random factor. Te response variables LH, T, E 2 and fected 23G needle. Te skin around the puncture site was T3 and body mass were frst logarithmically transformed disinfected with medical alcohol before and after punctur- to correct for departures from normality and homogeneity ing.