Urban environment alter the timing of progression of testicular recrudescence in tree sparrow (Passer montanus)

Abstract

Urbanization is a rapidly growing phenomenon that affects wildlife. Laboratory studies show the effects of night light on the physiology of the organisms. Limited studies have been conducted on birds in their natural habitat. Here, we studied the effects of the urban environment on reproduction-linked phenomenon and molecules involved in the regulation of seasonal breeding. Birds (N=5/time/site) were procured from urban and rural sites at specific times, i.e., in March (stimulatory phase), June (reproductive phase), September (refractory phase), and December (sensitive phase) of 2018. Immediately after procurement, birds were brought to the laboratory. Bodyweight, bill color, molt in body feathers, and testes size were recorded. The next day, all the birds were sacrificed in the middle of the day. Blood was collected and serum was used for ELISA of corticosterone, triiodothyronine (T3), and thyroxine (T4). mRNA levels of thyroid-stimulating hormone-β (Tshβ), type 2 deiodinase (Dio2), type 3 deiodinase (Dio3), gonadotropin-releasing hormone (GnRh), and gonadotropin inhibitory hormone (GnIh) were measured in hypothalamic tissue. Urban birds showed higher levels of corticosterone during the stimulatory phase. There was a delay in the initiation of testicular growth in urban birds and it was supported by reduced levels of T3 in blood plasma and relatively lower transcription of Dio2 and GnRH mRNA in urban birds. Our findings suggest that the urban environment delays the timing of reproduction in birds and could be the consequence of local environmental conditions.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. Aronson MFJ, La Sorte FA, Nilon CH et al (2014) A global analysis of the impacts of urbanization on bird and plant diversity reveals key anthropogenic drivers. Proc R Soc Lond B 281:20133–20330

    Google Scholar 

  2. Atwell JW, Cardoso GC, Whittaker DJ, Campbell-Nelson S, Robertson KW, Ketterson E (2012) Boldness behavior and stress physiology in a novel urban environment suggest rapid correlated evolutionary adaptation. Behav Ecol 23:960–969

    Article  Google Scholar 

  3. Batra T, Malik I, Kumar V (2019) Illuminated night alters behaviour and negatively affects physiology and metabolism in diurnal zebra finches. Environ Pollut 254:1129–1116

    Article  CAS  Google Scholar 

  4. Bentley GE (1997) Thyroxine and photorefractoriness in starlings. Poult Avian Biol Rev 8:123–139

    Google Scholar 

  5. Bhardwaj SK, Anushi (2006) Effect of photoperiod length on body mass and testicular growth in the house sparrow (Passer domesticus) and brahminy myna (Sturnus pagodarum). Reprod Nutr Dev 46:69–76

    Article  Google Scholar 

  6. Bonier F, Martin PR, Sheldon KS, Jensen JP, Foltz SL, Wingfield JC (2007) Sex-specific consequences of life in the city. Behav Ecol 18:121–129

    Article  Google Scholar 

  7. Borah BK, Renthlei Z, Trivedi AK (2020) Hypothalamus but not liver retains daily expression of clock genes during hibernation in terai tree frog (Polypedates teraiensis). Chronobiol Int 37:485–492

    CAS  Article  Google Scholar 

  8. Boswell T (1991) The Physiology of migratory fattening in the European quail (Coturnix coturnix). In PhD Thesis University of Bristol, UK

  9. Both C, Artemyev AV, Blauw B, Cowie RJ, Dekhuijzen AJ (2004) Large-scale geographical variation confirms that climate change causes birds to lay earlier. P Roy Soc B Biol Sci 271:1657–1662

    Article  Google Scholar 

  10. Brown JL, Li SH, Bhagabati N (1999) Long-term trend toward earlier breeding in an American bird: a response to global warming. Proc Nat Aca Sci U S A 96:5565–5569

    CAS  Article  Google Scholar 

  11. Budki P, Rani S, Kumar V (2008) Food deprivation during photosensitive and photorefractory life-history stages affects the reproductive cycle in the migratory redheaded bunting (Emberiza bruniceps). J Exp Biol 212:225–230

    Article  Google Scholar 

  12. Burley NT, Price DK, Zann RA (1992) Bill color, reproduction and condition effects in wild and domesticated zebra finches. Auk 109:13–23

    Article  Google Scholar 

  13. Caro SP, Schaper SV, Hut RA, Ball GF, Visser ME (2013) The case of the missing mechanism: how does temperature influence seasonal timing in endotherms? PLoS Biol 11:1–8

    Article  CAS  Google Scholar 

  14. Davies P, Deviche S (2014) Reproductive phenology of urban birds: environmental cues and mechanisms. In: Brumm H, Gil D (eds). Oxford Uniuversity Press, Oxford, pp 98–115

  15. Davies S, Cros T, Richard D, Meddle SL, Tsutsui K, Deviche P (2015a) Food availability, energetic constraints and reproductive development in a wild seasonally breeding songbird. Funct Ecol 29:1421–1434

    Article  Google Scholar 

  16. Davies S, Behbahaninia H, Giraudeau M, Meddle SL, Waites K, Deviche P (2015b) Advanced seasonal reproductive development in a male urban bird is reflected in earlier plasma luteinizing hormone rise but not energetic status. Gen Comp Endocrinol 224:1–10

    CAS  Article  Google Scholar 

  17. Dawson A (2005) The effect of temperature on photoperiodically regulated gonadal maturation, regression and moult in starlings—potential consequences of climate change. Funct Ecol 19:995–1000

    Article  Google Scholar 

  18. Dawson A, Howe PD (1983) Plasma corticosterone in wild starlins (Sturnus vulgaris) immediately following capture and in relation to body weight during the annual cycle. Gen Comp Endocrinol 51:303–308

    CAS  Article  Google Scholar 

  19. de Bruijn R, Romero LM (2013) Artificial rain and cold wind act as stressors to captive molting and non-molting European starlings (Sturnus vulgaris). Comp Biochem Physiol A Mol Integr Physiol 164:512–519

    Article  CAS  Google Scholar 

  20. Dixit AS, Bamon I, Singh NS (2018) Temperature modulates photoperiodic seasonal responses in the subtropical tree sparrow, Passer montanus. J Comp Physiol A 204:721–735

    Article  Google Scholar 

  21. Dixit AS, Byrsat S (2018) Photoperiodic control of GnRH-I expression in seasonal reproduction of the Eurasian tree sparrow. Photochem Photobiol Sci 17:934–945

    CAS  Article  Google Scholar 

  22. Dixit AS, Singh NS, Byrsat S (2017) Role of GnIH in photoperiodic regulation of seasonal reproduction in the Eurasian tree sparrow. J Exp Biol 220:3742–3750

    Article  Google Scholar 

  23. Dixit AS, Singh NS (2011) Photoperiod as a proximate factor in control of seasonality in the subtropical male Tree Sparrow, Passer montanus. Front Zool 8:1

    Article  Google Scholar 

  24. Dixit AS, Singh NS (2012) Seasonal variation in sensitivity of the photoperiodic response system in the subtropical Tree Sparrow (Passer montanus). J Exp Zool 317:488–498

    Article  Google Scholar 

  25. Dominoni DM, Nelson RJ (2018) Artificial light at night as an environmental pollutant: an integrative approach across taxa, biological functions, and scientific disciplines. J Exp Zool A Ecol Integr Physiol 329:387–393

    Google Scholar 

  26. Dominoni DM, Carmona-Wagner EO, Hofmann M, Kranstauber B, Partecke J (2014) Individual-based measurements of light intensity provide new insights into the effects of artificial light at night on daily rhythms of urban-dwelling songbirds. J Anim Ecol 83:681–692

    Article  Google Scholar 

  27. Dominoni DM, Quetting M, Partecke J (2013a) Artificial light at night advances avian reproductive physiology. Proc R Soc B 280:20123017

    Article  CAS  Google Scholar 

  28. Dominoni DM, Quetting M, Partecke J (2013b) Artificial light at night advances avian reproductive physiology. Proc R Soc B 280:20123017

    Article  CAS  Google Scholar 

  29. Dominoni DM, Kjellberg Jensen J, de Jong M, Visser ME, Spoelstra K (2020a) Artificial light at night, in interaction with spring temperature, modulates timing of reproduction in a passerine bird. Ecol Appl 30:e02062

    Article  Google Scholar 

  30. Dominoni DM, Jensen JK, Jong MD, Bisser ME, Spoelstra K (2020b) Artificial light at night, in interaction with spring temperature, modulates timing of reproduction in a passerine bird. Ecol Appl 30(3):e02062

    Article  Google Scholar 

  31. Faivre B, Grégoire A, Préault M, Cézilly F, Sorci G (2003) Immune activation rapidly mirrored in a secondary sex trait. Science 300:103

    CAS  Article  Google Scholar 

  32. Follett BK, Nicholls TJ (1988) Acute effect of thyroid hormones in mimicking photoperiodically induced release of gonadotropins in Japanese quail. J Comp Physiol B 157:837–843

    CAS  Article  Google Scholar 

  33. Fokidis HB, Orchinik M, Deviche P (2009) Corticosterone and corticosteroid binding globulin in birds: relation to urbanization in a desert city. Gen Comp Endocrinol 160:259–270

    CAS  Article  Google Scholar 

  34. Fuirst M, Veit RR, Hahn M, Dheilly N, Thorne LH (2018) Effects of urbanization on the foraging ecology and microbiota of the generalist seabird Larus argentatus. PLoS ONE 13:e0209200

    CAS  Article  Google Scholar 

  35. Helm B, Ben-Shlomo R, Sheriff MJ, Hut RA, Foster R, Barnes BM, Dominoni D (2013) Annual rhythms that underlie phenology: biological time-keeping meets environmental change. Proc Biol Sci 280:20130016

    Google Scholar 

  36. Honryo T, Kurata M, Okada T, Ishibashi Y (2012) Effects of night-time light intensity on the survival rate and stress responses in juvenile Pacific bluefin tuna Thunnus orientalis (Temminck and Schlegel). Aquac Res 44:1058–1065

    Article  Google Scholar 

  37. Klein SL, Nelson RJ (1999) Influence of social factors on immune function and reproduction. Rev Reprod 4(3):168–178

    CAS  Article  Google Scholar 

  38. Kumar V, Singh S, Misra M, Malik S (2001) Effects of duration and time of food availability on photoperiodic responses in the migratory male black headed bunting (Emberiza melanocephala). J Exp Biol 204:2843–2848

    CAS  Google Scholar 

  39. Lattin CR, Breuner CW, Romero LM (2016) Does corticosterone regulate the onset of breeding in free-living birds?: the CORT-Flexibility Hypothesis and six potential mechanisms for priming corticosteroid function. Horm Behav 78:107–120

    CAS  Article  Google Scholar 

  40. Lecomte N, Gauthier G, Giroux JF (2009) A link between water availability and nesting success mediated by predator-prey interactions in the Arctic. Ecology 90(2):465–475

    Article  Google Scholar 

  41. Liker A, Papp Z, Bókony V, Lendvai AZ (2008) Lean birds in the city: body size and condition of house sparrows along the urbanization gradient. J Anim Ecol 77:789–795

    CAS  Article  Google Scholar 

  42. Li PS, Wagner WC (1983) In vivo and in vitro studies on the effect of adrenocorticotro- pic hormone or cortisol on the pituitary response to gonadotropin releasing hormone. Biol Reprod 29:25–37

    CAS  Article  Google Scholar 

  43. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(ddC(T)) method. Methods 25:402–408

    CAS  Article  Google Scholar 

  44. Longcore T, Rich C (2004) Ecological light pollution. Front Ecol Environ 2:191–198

    Article  Google Scholar 

  45. McKinney M (2002a) Urbanization, biodiversity, and conservation. Biosci 52:883–890

    Article  Google Scholar 

  46. McKinney M (2002b) Urbanization as a major cause of biotichomogenization. Biol Conserv 127:247–260

    Article  Google Scholar 

  47. McKinney ML (2006) Urbanization as a major cause as a biotic homogenization. Biol Conserv 127:247–260

    Article  Google Scholar 

  48. Macdougall-Shackleton SA, Stevenson TJ, Watts HE, Pereyra ME, Hahn TP (2009) The evolution of photoperiod response systems and seasonal GnRH plasticity in birds. Integr Comp Biol 49:580–589

    CAS  Article  Google Scholar 

  49. McDonnell MJ, Hah AK (2008) The use of gradient analysis studies in advancing our understanding of the ecology of urbanizing landscapes: current status and future directions. Landsc Ecol 23:1143–1155

    Article  Google Scholar 

  50. McEwen BS, Wingfield JC (2003) The concept of allostasis in biology and biomedicine. Horm Behav 43:2–15

    Article  Google Scholar 

  51. Meijer T (1991) The effect of a period of food restriction on gonad size and moult of male and female starlings Sturnus vulgaris under constant photoperiod. Ibis 133:80–84

    Article  Google Scholar 

  52. Mishra I, Kumar V (2019) The quantity-quality trade-off: differential effects of daily food availability times on reproductive performance and offspring quality in diurnal zebra finches. J Exp Biol 3:277 (Pt7)

    Google Scholar 

  53. Nakao N, Ono H, Yamamura T, Anraku T, Takagi T, Higashi K, Yasuo S, Katou Y, Kageyama S, Uno Y, Kasukawa T, Iigo M, Sharp PJ, Iwasawa A, Suzuki Y, Sugano S, Niimi T, Mizutani M, Namikawa T, Ebihara S, Ueda HR, Yoshimura T (2008) Thyrotrophin in the pars tuberalis triggers photoperiodic response. Nature 452:317–322

    CAS  Article  Google Scholar 

  54. Oakley AE, Breen KM, Clarke IJ, Karsch FJ, Wagenmaker ER, Tilbrook AJ (2009) Cortisol reduces gonadotropin-releasing hormone pulse frequency in follicular phase ewes: influence of ovarian steroids. Endocrinol 150:341–349

    CAS  Article  Google Scholar 

  55. Partecke J, Schwable I, Gwinner E (2006) Stress and the city: urbanization and its effects on the stress physiology in European blackbirds. Ecology 87:1945–1952

    Article  Google Scholar 

  56. Partecke J, Van’t Hof TJ, Gwinner E (2005) Underlying physiological control of reproduction in urban and forest-dwelling European blackbirds Turdusmerula. J Avian Biol 36:295–305

    Article  Google Scholar 

  57. Pèczely P (1985) The role of thyroid and adrenal cortical hormones in the modulation of the gonadal function in birds. Acta Biol Hung 36:45–70

    Google Scholar 

  58. Perfito N, Kwong JMY, Bentley GE, Hau M (2008) Cue hierarchies and testicular development: is food a more potent stimulus than day length in an opportunistic breeder (Taeniopygia g. guttata)? Horm Behav 53:567–572

    Article  Google Scholar 

  59. Raap T, Sun J, Pinxten R, Eens M (2017) Disruptive effects of light pollution on sleep in free-living birds: season and/ or light intensity-dependent? Behav Process 144:13–19

    Article  Google Scholar 

  60. Rees M, Roe JH, Georges A (2009) Life in the suburbs: behavior and survival of a freshwater turtle in response to drought and urbanization. Biol Conserv 142:3172–3181

    Article  Google Scholar 

  61. Renthlei Z, Gurumayum T, Borah BK, Trivedi AK (2019) Daily expression of clock genes in central and peripheral tissues of tree sparrow (Passer montanus). Chronobiol Int 36:110–121

    CAS  Article  Google Scholar 

  62. Renthlei Z, Trivedi AK (2016) Regulation of seasonal reproduction in higher vertebrates. In: Hadar C, Gupta S, Goswami S (eds) Updates on integrative physiology & comparative endocrinology

  63. Renthlei Z, Trivedi AK (2019) Effect of urban environment on pineal machinery and clock genes expression of tree sparrow (Passer montanus). Environ Pollut 26:113278

    Article  CAS  Google Scholar 

  64. Renthlei Z, Bk B, Gurumayum T, Trivedi AK (2020) Season dependent effects of urban environment on circadian clock of tree sparrow ( Passer montanus). Photochem Photobiol Sci 19:1741–1749. https://doi.org/10.1039/d0pp00257g

    CAS  Article  Google Scholar 

  65. Riley SPD, Sauvajot RM, Fuller TK, York EC, Kamradt DA, Bromley C, Wayne RK (2003) Effects of urbanization and habitat fragmentation on bobcats and coyotes in Southern California. Conserv Biol 17:566–576

    Article  Google Scholar 

  66. Rivier C, Rivest S (1991) Effect of stress on the activity of the hypothalamic–pituitary–gonadal axis: peripheral and central mechanisms. Biol Reprod 45:523–532

    CAS  Article  Google Scholar 

  67. Romero LM, Soma KK, Wingfield JC (1998) Hypothalamic-pituitary-adrenal axis changes allow seasonal modulation of corticosterone in a bird. Am J Phys 274:R1338–R1344

    CAS  Google Scholar 

  68. Salmón P, Nilsson JF, Watson H, Bensch S, Isaksson C (2017) Selective disappearance of great tits with short telomeres in urban areas. Proc Biol Sci 284:20171349

    Google Scholar 

  69. Salmón P, Watson H, Nord A, Isaksson C (2018) Effects of the urban environment on oxidative stress in early life: insights from a cross-fostering experiment. Integr Comp Biol 58:986–994

    Google Scholar 

  70. Salvante KG, Williams TD (2003) Effects of corticosterone on the proportion of breeding females, reproductive output and yolk precursor levels. Gen Comp Endocrinol 130:205–214

    CAS  Article  Google Scholar 

  71. Sanz JJ, Potti J, Moreno J, Merino S, Frías O (2003) Climate change and fitness components of a migratory bird breeding in the Mediterranean region. Glob Chang Biol 9:461–472

    Article  Google Scholar 

  72. Santos CD, Miranda AC, Granadeiro JP, Lourenço PM, Saraiva S, Palmeirim JM (2010) Effects of artificial illumination on the nocturnal foraging of waders. Acta Oecologica 36:166–172

    Article  Google Scholar 

  73. Schoech SJ, Bowman R (2003) Does differential access to protein influence differences in timing of breeding of Florida scrub-jays (Aphelocoma coerulescens) in suburban and wildland habitats? Auk 120:1114–1127

    Article  Google Scholar 

  74. Seress G, Sándor K, Evans KL, Liker A (2020) Food availability limits avian reproduction in the city: an experimental study on great tits Parus major. J Avian Ecol 89:1570–1580

    Article  Google Scholar 

  75. Shini S, Shini A, Huff GR (2009) Effects of chronic and repeated corticosterone admin- istration in rearing chickens on physiology, the onset of lay and egg production of hens. Physiol Behav 98:73–77

    CAS  Article  Google Scholar 

  76. Shochat E, Lerman S, Anderies JM, Warren PS, Faeth SH, Nilon CH (2010) Invasion, competition, and biodiversity loss in urban ecosystems. Biosci 60:199–208

    Article  Google Scholar 

  77. Shochat E, Warren PS, Faeth SH, McIntyre NE, Hope D (2006) From patterns to emerging processes in mechanistic urban ecology. Trends Ecol Evol 21:186–191

    Article  Google Scholar 

  78. Silverin B (1986) Corticosterone-binding proteins and behavioral effects of high plasma levels of corticosterone during the breeding period in the pied flycatcher. Gen Comp Endocrinol 64:67–74

    CAS  Article  Google Scholar 

  79. Silverin B, Viebke PA (1994) Low temperature affects the photoperiodically induced LH and testicular cycles differentially in closely related species of tits (Parrus spp). Horm Behav 28:199–206

    CAS  Article  Google Scholar 

  80. Spée M, Marchal L, Lazin D, Maho YL, Chastel O, Beaulieu M, Raclot T (2011) Exogenous corticosterone and nest abandonment: a study in a long-lived bird, the adelie penguin. Horm Behav 60:362–370

    Article  CAS  Google Scholar 

  81. Spoelstra K, Verhagen I, Meijer D, Visser ME (2018) Artificial light at night shifts daily activity patterns but not the internal clock in the great tit (Parus major). Proc R Soc B 285:20172751

    Article  Google Scholar 

  82. Thomas DW, Bourgault P, Shipley B, Perret P, Blondel J (2010) Context-dependent changes in the weighting of environmental cues that initiate breeding in a temperate passerine, the Corsican blue tit (Cyanistes caeruleus). Auk 127:129–139

    Article  Google Scholar 

  83. Trivedi AK (2005) Seasonal responses of house sparrow (Passer domesticus) Linneaus at 270N. In PhD Thesis University of Lucknow, Lucknow, India

  84. Trivedi AK, Kumar J, Rani S, Kumar V (2014) Annual life history–dependent gene expression in the hypothalamus and liver of a migratory songbird: insights into the molecular regulation of seasonal metabolism. J Biol Rhythm 29:332–345

    CAS  Article  Google Scholar 

  85. Trivedi AK, Rani S, Kumar V (2006) Control of annual reproductive cycle in the subtropical house sparrow (Passer domesticus): evidence for conservation of photoperiodic control mechanisms in birds. Front Zool 3:12

    Article  Google Scholar 

  86. Trivedi AK, Sur S, Sharma A, Taufique ST, Gupta NJ, Kumar V (2019) Temperature alters the hypothalamic transcription of photoperiod responsive genes in induction of seasonal response in migratory redheaded buntings. Mol Cell Endocrinol 493:110454

    CAS  Article  Google Scholar 

  87. Tsutsui K, Saigoh E, Ukena K, Teranishi H, Fujisawa Y, Kikuchi M, Ishii S, Sharp PJ (2000) A novelavian hypothalamic peptide inhibiting gonadotropin release. Biochem Biophys Res Commun 275:661–667

    CAS  Article  Google Scholar 

  88. Valle S, Eagleman D, Kieffer N, Deviche P (2020) Disruption of energy homeostasis by food restriction or high ambient temperature exposure affects gonadal function in male house finches (Haemorhous mexicanus). J Comp Physiol B 190:611–628h

    CAS  Article  Google Scholar 

  89. Visser ME, Van Noordwijk AJ, Tinbergen JM, Lessells CM (1998) Warmer springs lead to mistimed reproduction in great tits (Parus major). Proc R Soc B Biol Sci 265:1867–1870

    Article  Google Scholar 

  90. Visser ME, Holleman L, Gienapp P (2006) Shifts in caterpillar biomass phenology due to climate change and its impact on the breeding biology of an insectivorous bird. Oecol 147:164–172

    Article  Google Scholar 

  91. Voigt CC, Schneeberger K, Voigt-Heucke SL, Lewanzik D (2011) Rain increases the energy cost of bat flight. Biol Lett 7:793–795

    Article  Google Scholar 

  92. Welsh TH, Jr Bambino TH, Hsueh AJ (1982) Mechanism of glucocorticoid-induced suppression of testicular androgen biosynthesis in vitro. Biol Reprod 27:1138–1146

    CAS  Article  Google Scholar 

  93. Wilson GR, Cooper SJ, Gessaman JA (2004) The effects of temperature and artificial rain on the metabolism of American kestrels (Falco sparverius). Comp Biochem Physiol A 139:389–394

    Article  CAS  Google Scholar 

  94. Wingfield JC (1994) Modulation of the adrenocortical response to stress in birds. In: Davey KG, Peter RE, Tobe SS (eds) Perspectives in comparative endocrinology. National Research Council of Canada, Ottawa, pp 520–528

    Google Scholar 

  95. Wingfield JC, Hahn TP, Maney DL, Schoech SJ, Wada M, Morton ML (2003) Effects of temperature on photoperiodically induced reproductive development, circulating plasma luteinizing hormone and thyroid hormones, body mass, and fat deposition in mountain white-crowned sparrows, Zonotrichia leucophrys oriantha. Gen Comp Endocrinol 131:143–158

    CAS  Article  Google Scholar 

  96. Wingfield JC, Kitaysky AS (2002) Endocrine responses to unpredictable environmental events: stress or anti-stress hormones. Integr Comp Biol 42:600–609

    CAS  Article  Google Scholar 

  97. Wingfield JC, Sapolsky RM (2003) Reproduction and resistance to stress: when and how. J Neuroendocrinol 15:711–724

    CAS  Article  Google Scholar 

  98. Yoshimura T (2010) Neuroendocrine mechanism of seasonal reproduction in birds and mammals. Anim Sci J 81:403–410

    CAS  Article  Google Scholar 

  99. Yamamura T, Yasuo S, Hirunagi K, Ebihara S, Yoshimura T (2006) T3 implantation mimics photoperiodically reduced encasement of nerve terminals by glial processes in the medianeminence of Japanese quail. Cell Tissue Res 324:175–179

    CAS  Article  Google Scholar 

  100. Yoshimura T, Yasuo S, Watanabe M, Iigo M, Yamamura T, Hirunagi K, Ebihara S (2003) Light-induced hormone conversion of T4 to T3 regulates photoperiodic response of gonads in birds. Nature 426:178–181

    CAS  Article  Google Scholar 

  101. Zhang S, Chen X, Zhang J, Li H (2014) Differences in the reproductive hormone rhythm of tree sparrows (Passer montanus) from urban and rural sites in Beijing: the effect of anthropogenic light sources. Gen Comp Endocrinol 206:24–29

    CAS  Article  Google Scholar 

  102. Zhang S, Lei F, Liu S, Li D, Chen C, Wang P (2011) Variation in baseline corticosterone levels of tree sparrow (Passer montanus) populations along an urban gradient in Beijing, China. J Ornithol 152:801–806

    Article  Google Scholar 

  103. Zhang X, Yang W, Liang W, Wang Y, Zhang S (2019) Intensity dependent disruptive effects of light at night on activation of the HPG axis of tree sparrows (Passer montanus). Environ Pollut 249:904–909

    CAS  Article  Google Scholar 

Download references

Availability of data and materials

Available on request.

Funding

This study was supported by the Science and Engineering Research Board (SERB), New Delhi, under ECR program (ECR/2016/000626). Funding from the Department of Science and Technology under the DST-FIST program to the Department of Zoology, Mizoram University, is greatly acknowledged.

Author information

Affiliations

Authors

Contributions

AKT conceived idea and designed the study. ZR and BKB carried out the experiments and data analysis. ZR and AKT wrote the manuscript.

Corresponding author

Correspondence to Amit Kumar Trivedi.

Ethics declarations

Ethics approval and consent to participate

The study was conducted in accordance with the guidelines laid down by the Institutional Animal Ethics Committee (IAEC) of Mizoram University (protocol no. MZU-IAEC/2016/09).

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Responsible Editor: Philippe Garrigues

Supplementary Information

ESM 1

(DOCX 14 kb)

ESM 2

(DOCX 15 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Renthlei, Z., Borah, B.K. & Trivedi, A.K. Urban environment alter the timing of progression of testicular recrudescence in tree sparrow (Passer montanus). Environ Sci Pollut Res (2021). https://doi.org/10.1007/s11356-021-12918-6

Download citation

Keywords

  • Tree sparrow
  • Urbanization
  • Seasonality
  • Thyroid hormones
  • Gonadotropin