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Research | Open Access

Do migrant and resident species differ 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 Zhao1Lijun Gao1Wenyu Yang1Xianglong Xu1Weiwei Wang1Wei Liang2Shuping Zhang1( )
College of Life and Environment Sciences, Minzu University of China, Beijing 100081, China
Ministry of Education Key Laboratory for Tropical Animal and Plant Ecology, College of Life Sciences, Hainan Normal University, Haikou 571158, China
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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 reproduction. 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 and T3 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 affect 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.

References

 

Adkinsregan E. Do hormonal control systems produce evolutionary inertia? Phil Trans R Soc B. 2008;363:1599-609.

 

Aurélie G, Frédéric A, Clément CC, Colette T, Børge M, Claus B, Geir WG, Olivier C. Stress and the timing of breeding: glucocorticoid-luteinizing hormones relationships in an arctic seabird. Gen Comp Endocr. 2010;169:108-16.

 

Both C, Visser ME. The effect of climate change on correlation between avian life-history traits. Glob Change Biol. 2005;11:1606-13.

 

Carey C. Female reproductive energetics. In: Carey C, editor. Avian energetics and nutritional ecology. New York: Chapman & Hall; 1996. p. 324-74.

 

Chastel O, Lacroix A, Kersten M. Pre-breeding energy requirements: thyroid hormone, metabolism and the timing of reproduction in house sparrows Passer domesticus. J Avian Biol. 2003;34:298-306.

 

Chastel O, Lacroix A, Weimerskirch H, Gabrielsen GW. Modulation of prolactin but not corticosterone responses to stress in relation to parental effort in a long-lived bird. Horm Behav. 2005;47:459-66.

 

Christensen A, Bentley GE, Cabrera R, Ortega HH, Perfito N, Wu TJ, Micevych P. Hormonal regulation of female reproduction. Horm Metab Res. 2012;44:587-91.

 

Cooper SJ. Daily and seasonal variation in body mass and visible fat in mountain chickadees and juniper titmice. Wilson J Ornithol. 2007;119:720-4.

 

Davies S, Behbahaninia H, Giraudeau M, Meddle SL, Waites K, Deviche P. Advanced seasonal reproductive development in a male urban bird is reflected in earlier plasma luteinizing hormone rise but not energetic status. Gen Comp Endocr. 2015;181:1-10.

 

Dawson A, King VM, Bentley GE, Ball GF. Photoperiodic control of seasonality in birds. J Biol Rhythm. 2001;16:365-80.

 

Dawson A. Control of the annual cycle in birds: endocrine constraints and plasticity in response to ecological variability. Phil Trans R Soc B. 2008;363:1621-33.

 

Dominoni DM, Hof TJV, Partecke J. Social cues are unlikely to be the single cause for early reproduction in urban European blackbirds (Turdus merula). Physiol Behav. 2015;142:14-9.

 

Eda-Fujiwara H, Suzuki M, Kimura T. Behavioral responses of males to estradiol-treated females in the budgerigar (Melopsittacus undulatus). J Ethol. 2003;21:23-8.

 

Eising CM, Eikenaar C, Schwabl H, Groothuis TGG. Maternal androgens in black-headed gull (Larus ridibundus) eggs: consequences for chick development. Proc R Soc Lond B. 2001;268:839-46.

 

Fischer B, Dieckmann U, Taborsky B. When to store energy in a stochastic environment. Evolution. 2010;65:1221-32.

 

Garamszegi LZ, Hirschenhauser K, Bokony V, Eens M, Hurtrez-Bousses S, Møller AP, Oliveira RF, Wingfield JC. Latitudinal distribution, migration, and testosterone levels in birds. Am Nat. 2008;172:533-46.

 

Greives TJ, Fudickar AM, Atwell JW, Meddle SL, Ketterson ED. Early spring sex differences in luteinizing hormone response to gonadotropin releasing hormone in co-occurring resident and migrant dark-eyed juncos (Junco hyemalis). Gen Comp Endocr. 2016;236:17-23.

 

Griffiths R, Daan S, Dijkstra C. Sex identification in birds using two CHD genes. Proc R Soc Lond B. 1996;263:1251-6.

 

Hegemann A, Matson KD, Versteegh MA, Tieleman BI. Wild Skylark seasonally modulate energy budgets but maintain energetically costly inflammatory immune responses throughout the annual cycle. PLoS ONE. 2012;7:e36358.

 

Hunt KE, Wingfield JC. Effect of estradiol implants on reproductive behavior of female Lapland longspurs (Calcarius lapponicus). Gen Comp Endocr. 2004;137:248-62.

 

Jenni L, Jenni-Eiermann S, Spina F, Schwabl H. Regulation of protein breakdown and adrenocortical response to stress in birds during migratory flight. Am J Physiol Regul Integr Comp Physiol. 2000;278:1182-9.

 

Jodie MJ, Joel WM, Joseph MC, Timothy JG, Eric AS, George EB, Ellen DK. Testosterone response to GnRH in a female songbird varies with stage of reproduction: implications for adult behaviour and maternal effects. Funct Ecol. 2007;21:767-75.

 

Jorg W, Speakman JR, Elliott KH, Hatch SA, Kitaysky AS. Resting and daily energy expenditures during reproduction are adjusted in opposite directions in free-living birds. Funct Ecol. 2014;29:250-8.

 

Li M, Yin YJ, Hie CY, Qu LN, Zhang GF, Liang YT, Zhao XJ, Liu JS. Seasonal variations of plasma thyroid hormone and its effect on thermoregulation in tree sparrow (Passer montanus). Sichuan J Zool. 2010;29:530-4.

 

Lou LX. Preliminary observation of Eurasian Skylark breeding behaviors. Chin J Zool. 1966;1:19-22.

 

McGlothlin JW, Ketterson ED. Hormone-mediated suites as adaptations and evolutionary constraints. Phil Trans R Soc B. 2008;363:1611-20.

 

McNab BK. Ecological factors affect the level and scaling of avian BMR. Comp Biochem Physiol A. 2009;152:22-45.

 

McWilliams SR, Karasov WH. Phenotypic flexibility in digestive system structure and function in migratory birds and its ecological significance. Comp Biochem Physiol A. 2001;128:579-93.

 

Morbey YE, Ydenberg C. Protandrous arrival to breeding areas: a review. Ecol Lett. 2001;4:663-73.

 

Neto JM, Gosler AG. Variation in body condition of breeding Savi's Warblers Locustella luscinioides: the reproductive stress and flight adaptation hypothesis revisited. J Ornithol. 2010;151:201-10.

 

Nilsson JA, Raberg L. The resting metabolic cost of egg laying and nestling feeding in great tits. Oecologia. 2001;128:187-92.

 

Pathak VK, Chandola A. Seasonal variations in circulating thyroxine and triiodothyronine concentrations in spotted munia Lonchura punctulata. Gen Comp Endocr. 1983;50:201-4.

 

Peng LJ, Tang XL, Liu JS, Meng HT. The effect of thyroid hormone on basal thermogenesis (Pycnonotus sinensis). Acta Ecol Sin. 2010;30:1500-7.

 

Ricklefs RE. Energetics of reproduction in birds. In: Paynter RA, editor. Avian energetics. Cambridge: Chapman & Hall; 1974. p. 152-292.

 

Silverin B, Wingfield J, Stokkan KA, Massa R, Järvinen A, Andersson NA, Lambrechts M, Sorace A, Blomqvist D. Ambient temperature effects on photo induced gonadal cycles and hormonal secretion patterns in Great Tits from three different breeding latitudes. Horm Behav. 2008;54:60-8.

 

Smith JP. Changes in blood levels of thyroid hormones in two species of passerine birds. Condor. 1982;84:160-70.

 

Sol D, Lefebvre L, Rodriguez-Teijeiro JD. Brain size, innovative propensity and migratory behaviour in temperate Palaearctic birds. Phil Trans R Soc B. 2005;272:1433-41.

 

Stevenson IR, Bryant DM. Climate change and constraints on breeding. Nature. 2000;406:366-7.

 

Tian S, Wang WW, Zhang SP, Dou HS, Wu MR, Liu ST. The breeding ecology of Calandrella cheleensis in Dalai Lake National Nature Reserve of Inner Mongolia. Sichuan J Zool. 2015;34:453-7.

 

Tonra CM, Marra PP, Holberton RL. Migration phenology and winter habitat quality are related to circulating androgen in a long-distance migratory bird. J Avian Biol. 2011;42:397-404.

 

Vézina F, Dekinga A, Piersma T. Shorebirds' seasonal adjustments in thermogenic capacity are reflected by changes in body mass: how preprogrammed and instantaneous acclimation work together. Integr Comp Biol. 2011;51:394-408.

 

Wang AZ, Lei FM. Periodical variations of weight and fat reserves in Onychostruthus taczanowskii. Sichuan J Zool. 2011;30:560-3.

 

Washburn BE, Millspaugh JJ, Morris DL, Schulz JH, Faaborg J. Using a commercially available enzyme immunoassay to quantify testosterone in avian plasma. Condor. 2007;109:181-6.

 

Welcker J, Chastel O, Gabrielsen GW, Guillaumin J, Kitaysky AS, Speakman JR, Tremblay Y, Bech C. Thyroid hormones correlate with basal metabolic rate but not field metabolic rate in a wild bird species. PLoS ONE. 2013;8:e56229.

 

Wingfield JC, Lynn S, Soma K. Avoiding the "costs" of testosterone: ecological bases of hormone-behavior interactions. Brain Behav Evol. 2001;57:239-51.

 

Yasuo S, Yoshimura T. Comparative analysis of the molecular basis of photoperiodic signal transduction in vertebrates. Integr Comp Biol. 2009;49:507-18.

 

Yen PM. Physiological and molecular basis of thyroid hormone action. Physiol Rev. 2001;81:1097-142.

 

Zhang Y, Yao X, Song YY, Ying H. Thyroid hormone and metabolic regulation. Chin Bull Life Sci. 2013;25:176-83.

 

Zhao LD, Wang RM, Wu YN, Wu MS, Zhang WH, Liu JS. Daily variation in body mass and thermoregulation in male Hwamei (Garrulax canorus) at different seasons. Avian Res. 2015;6:4.

 

Zheng WH, Lin L, Liu JS, Xu XJ, Li M. Geographic variation in basal thermogenesis in little buntings: relationship to cellular thermogenesis and thyroid hormone concentrations. Comp Biochem Physiol A. 2013;164:483-90.

 

Zina FV, Salvante KG. Behavioral and physiological flexibility are used by birds to manage energy and support investment in the early stages of reproduction. Curr Zool. 2010;56:767-92.

Avian Research
Article number: 10
Cite this article:
Zhao L, Gao L, Yang W, et al. Do migrant and resident species differ 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. Avian Research, 2017, 8(1): 10. https://doi.org/10.1186/s40657-017-0068-3

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Received: 16 November 2016
Accepted: 20 March 2017
Published: 05 April 2017
© 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.

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