Temperature effect on luteinizing hormone secretion of Eurasian Skylark (Alauda arvensis) and Great Tit (Parus major) in China

Background

In mid to high latitude areas, birds use reliable environmental cues to anticipate the onset of predictable environmental change (Dawson et al. 2001). Change in photoperiod is both entirely predictable and closely related to local food availability, both within and among years. For this reason, photoperiod is the most important physiological cue for reproduction in birds (Wingfi eld 1993; Dawson et al. 2001; Gwinner 2003). Variation in photoperiod controls the initiation of reproduction through the hypothalamus-pituitary-gonad (HPG)axis. In spring, an increase in photoperiod leads to elevated secretion of gonadotrophin-releasing hormone-I(GnRH-I) from the median eminence at the base of the hypothalamus (Yamamura et al. 2006). This stimulates the synthesis and release of luteinizing hormone (LH)and follicle-stimulating hormone (FSH) in the pituitary (Pawson and McNeilly 2005). These two hormones are secreted into the blood and induce gonadal maturation which initiates reproductive behavior (Dawson 2008). Many birds rely on the availability of insects to feed their nestlings. By advancing the onset of warmer temperatures but not photoperiod, climate warming has caused the emergence of insects and the start of the avian breeding cycle to become asynchronous (Cotton 2003; Both et al. 2006, 2010; Visser et al. 2006, 2012). The resultant trophic mismatch between the peak of insect emergence and the avian reproductive cycle affects the breeding success, and in some cases, the survival of some bird species (Cotton 2003; Visser et al. 2006; Both et al.2006, 2010; Gullett et al. 2013). Therefore the ability of birds to change their reproduction rhythm under warmer condition determines their future probability of survival.

从数据中来，到实践中去。全面质量管理，控制病种成本，促进学科发展，推进医师执业能力评价。破旧立新，腾笼换鸟，病种分析引领医院精细化管理。

测试分类方法的标准通常采用准确率，准确率高，说明分类效果好，但对不平衡数据分类，采用准确率是不合适的，因为错分少数类的样本对整体分类准确率影响不大。因此，本次实验采用基于混淆矩阵(Confusion Matrix)的F-value，该值更能测验分类方法的性能。

(3)政府激励政策有效，相应的政策法规出台和宣传所花费的成本为C1；政府激励政策有效，购房者响应政府号召，积极购买和使用被动房，政府对这些购房者进行奖励所花费的成本C2，购房者购买被动房的额外增量成本C3。

Several studies have tested the ability of birds to change the initiation of reproductive endocrine axis in response to ambient temperature variation. The results show that the capacity to do this differs among species, among local populations of the same species, and between males and females. For example, although exposure to high temperature can enhance follicular development in the female White-crowned Sparrow (Zonotrichia leucophrys pugetensis) (Wingfield et al. 1997) and testicular growth rate and LH secretion in the Great Tit (Parus major; Silverin et al. 2008), temperature had no effect on testicular development in male White-crowned Sparrows (Wingfi eld et al. 1997) or Common Starlings (Sturnus vulgaris;Dawson 2005), testicular development and LH secretion in two Scandinavian populations of Great Tits (Silverin et al. 2008), or LH secretion in the Mountain Whitecrowned Sparrow (Z. l. oriantha; Wingfield et al. 2003).To shed further light on the effect of temperature on the activation of the reproduction endocrine axis, more bird species living at mid or high latitudes should be tested against the background of climate warming.

On the other hand, physiologists are in general less interested in variation among individuals (Wingfield et al. 1992; Ball and Balthazart 2008; Williams 2008), than in that between-species or between-populations. Phenotypic polymorphism exists within populations, and this variation may provide the basis for populations to adapt to environmental variation. From this perspective,individual variation in the timing of HPG axis activation refects the capacity of populations to cope with the challenge of climate warming.

In this paper, we hypothesized that higher temperature could accelerate the activation of HPG axis of birds and the individual variation on HPG axis endocrine rhythm should exist in the population of mid to high latitude birds. To test this hypothesis, we compared the photoperiod induced LH secretion rhythms of Eurasian Skylark (Alauda arvensis) and Great Tit (Parus major) in two temperature conditions at the population and individual levels.

Methods

Effect of temperature on plasma LH

The Eurasian Skylark is a common grassland species in northeast China, which is a cold temperate, high latitude area. The Great Tit is found in the broadleaf forests of north China, which is a warm temperate, mid-latitude area. The Eurasian Skylarks used in our experiments were captured at Hulunbell (47°45′N, 116°50′E), and the Great Tits were at Beijing (39°48′N, 115°25′E). All samples were collected with the permission of the Forestry Bureau of the local governments.

Experimental design

All birds used in the experiment were adults captured in February 2012. The body mass of two species are 34.13 ± 0.1 g (Eurasian Skylark) and 15 ± 0.16 g (Great Tit) respectively. Individuals of each species were kept in separate aviaries (one bird in one cage) and individually identified with numbered leg bands. Two artificially temperature and light controlled rooms were established. The temperature treatments were set as 15 and 20 °C, in which 15 °C was based on the average maximum daily temperatures recorded at the sample site of each bird species during the months the two species initiate reproduction, and 20 °C was the higher temperature compared to the 15 °C.Birds were randomly assigned to one of two temperature groups. The 15 °C group was comprised of 10 Great Tits and 13 Eurasian Skylarks, while the 20 °C group was comprised of 10 Great Tits and 12 Eurasian Skylarks. Birds were fed mixed seeds, boiled eggs and meal worms, and provided with water, during the experiment.

All birds were acclimatized to captivity and subjected to a short photoperiod (8L: 16D) for 1 month before the experiment began. The photoperiod of all groups was then lengthened by 2 h per week until the experiment concluded after 5 weeks, which is designed to mimic the chronic nature day time length variation in spring. All birds received the same food and water and were blooded on thefirst day of each long light treatment week. Some 50 μL whole blood was collected by puncturing a brachial wing vein with a disinfected 23 G needle. The skin around the puncture site was disinfected with medical grade alcohol before and after puncturing. Pressure was applied to the puncture site for 1 min with an alcoholsoaked cotton wool swab to staunch bleeding. Blood samples were stored at 4 °C for up to 8 h until centrifuged at 3000 r/min for 10 min. The resultant blood plasma and blood cells were then kept frozen in micro-centrifuge tubes until assayed. Blood plasma was used to measure plasma LH concentration. Each bird was sexed from DNA extracted from blood cells according to the method described by Griffth et al. (1999).

Additionalfile 1: Figure S1. The dose–response curves for LH of chicken, Eurasian Skylark and Great Tit.

赵集驾驶卡车，驶入木材场。一座座小山似原木，将被运往井下，支撑巷道，支撑掌子面，支撑起密如蛛网的地下世界。赵集和装卸工们搭跳板，卸木材。何良诸在木堆间转悠，一些孩子和老人，骑在一棵棵原木上，用刮刀铲下桦树皮，打成捆，拿回家引火，拿到集上卖。何良诸说不出的亲切，小时候，他没少剥树皮呀。何良诸对一个男孩说：“来，我帮你剥。”

Hormone assay

Plasma LH levels were measured using chicken enzyme immunoassay kits from MyBioSource (cat#MBS165746),which had been validated previously by our laboratory for use on Tree Sparrows (Passer montanus; Zhang et al.2014), Asian Short-toed Lark (Calandrella cheleensis) and Eurasian Skylark (Zhao et al. 2017). We used the method described by Chastel et al. (2005) to confi rm that the kits would work on the two species in this study. Briefy, the plasma samples from 20 birds of each species were pooled and diluted by 1, 1/2, 1/4, 1/8, 1/16 and 1/32, then we used the kits to analyze the concentration-dependent binding dynamics of the diluted samples of each species and draw a dilution VS B/Bo curve for each species. If the dilution VS B/Bo curves were parallel to the standard solution VS B/Bo curve (their slopes being not significantly different), the kit can be reliably used on the species. The dilution curves of the two species in our study were parallel to the standard solution VS B/Bo curve (slope: Chicken 2.35, Great Tit 2.32, Eurasian Skylark 2.33; Additionalfile 1: Figure S1), confirming that the kits could assess levels of LH of the two species. The respective inter- and intraplate coeffcients of variation for LH were 7.01 and 6.2%,respectively.

李高明的家乡瓦纳村以哈尼族为主，村子闭塞，来往县城的道路崎岖而危险，坐个摩托车都得小心翼翼，害怕掉下去。仅进过几次城的李高明只会说哈尼语，刚到工地时，和老板的沟通都得靠着同为哈尼族的“代办”朋友。“语言障碍非常大，会听30%。”基本不会讲。想回家啊，可语言不通，道路不识，走能走到哪里去？

Data analysis

Differences in plasma LH levels between the different temperature treatment groups of each species were analyzed with a Linear Mixed Model (LMM) in which temperature, sex, treatment week, and the interactions between these factors were modeled asfixed factors, and individual bird was included as a random factor. Plasma LH concentrations were log transformed to correct for departures from normality and homogeneity of variance.p values ＜ 0.05 were considered significant. All data analyses were performed in SPSS 18.0.

Results

Species in the study

The results of the LMM for Eurasian Skylark indicate that treatment week and temperature significantly infuenced the LH concentration of Eurasian Skylarks,whereas sex and all interaction terms were insignificant(Table 1). Mean plasma LH of the Eurasian Skylarks in 20 °C group were significantly higher than those in 15 °C group in thefirst (T test, n = 12, p = 0.037), second (T test, n = 12, p ＜ 0.001) and third (T test, n = 12,p ＜ 0.001) experimental weeks (Fig. 1a). However, the LMM results indicate that only treatment week signi ficantly infuenced LH concentration of Great Tit, and that temperature, sex and all interaction terms were insignificant (Fig. 1b, Table 1).

Table 1 Results of a linear mixed model of the effects of week, sex, and temperature on plasma LH concentrations in Eurasian Skylark and Great Tit

Species Explanatory variable df F p Eurasian Skylark Week 5, 124 8.331 ＜ 0.001 Sex 1, 124 1.212 0.325 Temperature 1, 124 6.578 0.045 Week * sex 5, 124 0.420 0.833 Week * temperature 5, 124 0.159 0.977 Sex * temperature 1, 124 0.888 0.390 Week * sex * temperature 5, 124 1.684 0.152 Great Tit Week 5, 96 14.079 ＜ 0.001 Sex 1, 96 0.017 0.896 Temperature 1, 96 0.288 0.592 Week * sex 5, 96 0.214 0.957 Week * temperature 5, 96 0.827 0.530 Sex * temperature 1, 96 0.034 0.853 Week * sex * temperature 5, 96 2.077 0.065

Individual differences in plasma LH trends

穿插了解对联在生活中的广泛运用，知道对联的分类、粘贴方法。介绍李渔的《声律启蒙》、诵读丁慈矿的《晨读对韵》、朗读《增广贤文》联句，进一步感受对联的特点与魅力。

Discussion

The LMM results indicate that temperature only signi ficantly infuenced the HPG axis activation of Eurasian Skylarks. Mean plasma LH of Eurasian Skylarks in the high temperature group was significantly higher than that of those in the low temperature group in the 1st, 2nd,and 3rd experimental week, suggesting that initiation of the HPG axis in this species can be advanced by higher temperature. Mean plasma LH in the Great Tit high temperature group was generally not significantly different to that in the low temperature group and the results of the LMM suggest that temperature had no effect on plasma LH. So far, researches on the infuence of temperature on light-induced HPG endocrine process have obtained different results in different species, or in populations of same species living at different latitudes. For example,exposure to higher temperature did not infuence lightinduced LH secretion in the White Crowned Sparrow(Wingfield and Sapolsky 2003), but did affect that of a southern European population of the Great Tit (Silverin et al. 2008). The results of previous studies and ours suggest that the effects of temperature on reproductive endocrine axis might differ among species; therefore,conclusions about the temperature effect on the activation of HPG axis should be concerned.

Fig. 1 The plasma LH level (mean ± SD) of Eurasian Skylark (a) and Great Tit (b) during experimental exposure to a long photoperiod.X-axis is the number of treatment week

Fig. 2 The peak plasma LH level of the individual birds in 15 °C (a)and 20 °C (b) group of Eurasian Skylark. X-axis is the number of treatment week

Our results shed light on the hypothesis that latitude may be an important factor contributing to this interspecies variation and that high latitude species display greater variation in the initiation of LH secretion with respect to temperature. There is some evidence that the degree of population decline caused by trophic mismatch is more pronounced in species that breed at lower latitudes (Jones and Cresswell 2010). This may be because temperature variation is less at lower latitudes and larger at higher latitudes. Bird populations at higher latitudes may have already undergone selection for plasticity in response to inter-annual variability in temperature(Charmantier et al. 2008). Our results provide possible physiological evidence for this hypothesis. The LH levels of the Eurasian Skylark, a high-latitude species, displayed high between-group variation, whereas the LH levels of the Great Tit, a mid latitude species, was relatively constant between groups. We suggest that more comparison studies among the species from different latitudes should be done in the future.

In contrast to previous studies, we also examined individual variation in the temporal pattern of LH response to temperature. We found marked individual variation in the timing of peak LH levels in both high and low temperature groups of Eurasian Skylarks and Great Tits. In Eurasian Skylarks and Great Tits, some members of both temperature treatment groups attained peak LH levels in thefirst or the second week of the experiment, suggesting that some individuals in these species have the potential to advance the timing of reproduction, irrespective of whether they are in a low or high temperature environment. This suggests that the activation of reproductive endocrine axis is polymorphic in some species, and that this variation could allow the population to cope with the possible challenge of trophic mismatch caused by climate warming.

Fig. 3 The peak plasma LH level of the individual birds in 15 °C (a)and 20 °C (b) group of Great Tit

Recent research indicates that the average breeding dates of several bird species, such as Ultramarin Jays(Aphelocoma ultramarine; Brown et al. 1999), European Pied Flycatchers (Ficedula hypoleuca; Both et al. 2004;Both and Visser 2005), and Great Tits (Parus major; Both et al. 2004; Visser et al. 2006), have advanced from a few days to over a week, presumably as a result of ambient temperature increases and the subsequent earlier availability of insect food sources. However, the laying dates of populations of some species, such as a European population of the Collared Flycatcher (Ficedula albicollis;Przybylo et al. 2000), have not displayed a commensurate advance. Even in the European Pied Flycatcher, which has been found to breed earlier in response to an earlier peak in caterpillar abundance, some individuals still bred later with the result that their nestling period did not coincide with the period of peak food abundance (Both et al. 2006). Ourfinding that the timing of reproductive endocrine axis activation is more fexible in individuals of some species than in others provides a potential physiological explanation for the above phenomenon. Individual variation in peak LH within populations may allow some individuals to breed earlier, thereby synchronizing breeding with peak food abundance. Therefore, species with either greater physiological plasticity in response to temperature, or that are more polymorphic with respect to the timing of breeding, may be better able to adjust their breeding dates in response to climate change,whereas species without these characteristics may be unable to synchronize their breeding with earlier peaks in food abundance.

Although individual variation in the activation of LH secretion is apparent in populations of some species, it remains to be determined if all such variation has a genetic basis. Circadian Locomotor Output Cycles Kaput (CLOCK) is a highly conserved transcription factor central to the rhythmicity of the circadian oscillator(Bourret and Garant 2015). The Clock gene possesses a poly-glutamine (poly-Q) binding region that is polymorphic in length (the number of Q repeats), which affects its binding affnity to its transcription factor (Darlington et al. 1998). Variation in Clock gene poly-Q length has been found to be related to both breeding site latitude(Johnsen et al. 2007) and breeding phenology (Liedvogel et al. 2009; Caprioli et al. 2012). The relationship between the timing of HPG axis activation and likely candidate genes should be investigated in the future. Furthermore,the relationship between HPG endocrine process and reproductive parameters, such as laying date and fedgling period, should be examined to confirm the ecological effects of any observed physiological polymorphism.

Conclusions

According to our results, we conclude that the effects of temperature on reproductive endocrine axis differ among species. Seasonal activation of the HPG axis in the high-latitude species can be advanced by higher temperature. Meanwhile the activation of reproductive axis is polymorphic in some species. Species with either greater physiological plasticity in response to temperature, or that are more polymorphic with respect to the timing of breeding, may be better able to adjust their breeding dates in response to climate change, whereas species without these characteristics may be unable to synchronize their breeding with earlier peaks in food abundance.

Individual variation in the timing of peak plasma LH concentration was apparent in Eurasian Skylarks and Great Tits. In the Eurasian Skylark 15 °C group, maximum plasma LH concentrations were observed in one bird in thefirst week, one in the second week, two birds in the third week, six in the fourth week, and three in thefifth week (Fig. 2a). In the Eurasian Skylark 20 °C group, three birds attained maximum plasma LH concentrations in each successive week after thefirst week (Fig. 2b). Individual variation among Great Tits was similar: in the 15 °C group, maximum plasma LH was attained by two birds in thefirst week, two birds in the second week,four birds in the fourth week, and two birds in thefifth week (Fig. 3a). In the 20 °C group, peak plasma LH was attained by three birds in thefirst week, two birds in the second week, two birds in the third week, one bird in the fourth week, and two birds in thefifth week (Fig. 3b).

Additionalfile

设计方案的提交形式多样化，可以手绘，可以建模渲染，也可以写出自己的想法并加以图示，只要能够清晰表达自己的想法即可。设计方案的信息栏带有方案编号、设计师代号、引用对象等信息，打分栏供实验管理者写入统计得到的方案平均得分。方案张贴在实验场所的软木墙上供所有参与者观察和参考引用(如图2)。

Authors’ contributions

SZ conceived the study and designed the experiments. LG and JG conducted the experiments. LG wrote thefirst draft of the article. SZ supervised the research and revised the draft. All authors read and approved thefinal manuscript.

Acknowledgements

We are grateful to Professor Jinsong Liu and Professor Weihong Zheng in Wenzhou University for their help on the experiment treatment.

对照组中，20例患者的年龄范围为26～41岁，年龄均值为（33.02±3.55）岁，其子宫肌瘤直径范围为 4.0～11.0 cm，均值为（6.20±1.33）cm，其中 14 例患者为单发肌瘤，6例患者为多发肌瘤。

近年，“一体化”、“城乡一体化”可谓是热门词语；当下，也正在推进“城乡一体化”的过程之中；于是，党的十七届六中全会又明确提出，加快城乡文化一体化发展。关于城乡文化一体化的涵义，似乎就是“城乡一体化”的内涵在文化方面的体现或扩展而已。但事实并非全部如此，因为城乡文化一体化的涵义与一般意义上的“城乡一体化”确有相似或相近之处，但并不完全一致，而且城乡文化一体化的实施也有特定的要求。那么，何为“城乡文化一体化”？实施“城乡文化一体化”的要求又是什么？本文将对此进行探讨。

本岛光照资源条件一般，且岛内土地资源主要围绕旅游和居住而建设开发，电力工程建设用地较为紧张，不适宜大规模发展传统集中式光伏。受土地及限高等影响，岛内风电机组选址较困难，不适宜大规模发展风电。因此，本文中暂不对发展风、光等可再生能源进行讨论。

The authors declare that they have no competing interests.

Availability of data and materials

The data used in the present study are available from the corresponding author on reasonable request.

Competing interests

Experimental procedures conformed to the relevant Chinese laws and had the approval of Hainan Normal University’s Animal Research Ethics Committee. In addition, all procedures followed standard protocols, such as the ARRIVE guidelines for reporting animal research.

Consent for publication

Not applicable.

Ethical statement

Our experimental procedures complied with the current laws on animal welfare and research in China and had the approval of the Animal Research Ethics Committee of Hainan Normal University. In addition, all procedures followed standard protocols, such as the ARRIVE guidelines for reporting animal research.

Funding

This study was supported by the National Natural Science Foundation of China (No. 31372225), Fund of Minzu University of China (No. ydzxxk201619),and “111” Project (2008-B0844).

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