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Temperature modulates photoperiodic seasonal responses in the subtropical tree sparrow, Passer montanus

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Abstract

We studied the effects of temperature on the photoperiodic regulation of seasonal reproduction and related events in the subtropical tree sparrow at Shillong, India. In the first experiment, one group of birds was maintained in an outdoor open aviary receiving natural photoperiod and temperature conditions, while the other group was exposed to natural photoperiod and constant temperature of 17 ± 2 °C in an outdoor closed aviary for 12 months. Although both sexes achieved peak gonadal growth at the same time (May) under the two conditions, gonadal regression and feathers molt were delayed under the temperature controlled condition. In the second experiment, the groups of birds were exposed to three different temperatures (17, 25 and 30 °C) under both long (LD-14L:10D) and short (SD-9L:15D) day lengths for 7 months. Birds showed relatively small but significant gonadal growth, darkening of bill color and feathers molt only at 30 °C under SD. However, they behaved as though they were under natural conditions and exhibited the above responses significantly at all temperatures under LD. There was delayed gonadal regression at the lower temperature (17 °C), while feathers molt delayed with increasing temperature (25, 30 °C) under LD. These results clearly indicate that temperature modulates photoperiodic seasonal responses in the tree sparrow.

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Abbreviations

ANOVA:

Analysis of variance

ASD:

Anand Shanker Dixit

B:

Bill completely black

BB:

Bill black with little straw patch left

BC:

Bill color

BF:

Body feathers

BM:

Body mass

CFL:

Compact fluorescent lamp

DBT:

Department of Biotechnology

DST:

Department of Science and Technology

FD:

Follicular diameter

HPG:

Hypothalamus–pituitary–gonadal

IB:

Iadalangki Bamon

IBM:

International Business Machines

LD:

Long day

NSS:

Namram Sushindrajit Singh

PF:

Primary feathers

S:

Bill straw in color

SD:

Short day

SS:

Bill slightly blackish in color

SSS:

Bill straw in color but with a little tinge of blackness

SPSS:

Statistical package for the social sciences

TV:

Testicular volume

References

  • Ball GF, Ketterson ED (2008) Sex differences in the response to environmental cues regulating seasonal reproduction in birds. Phil Trans R Soc B 363:231–246

    Article  PubMed  Google Scholar 

  • Balthazart J (1983) Hormonal correlates of behavior. In: Farner DS, King JR, Parkes KC (eds) Avian biology. Academic Press, New York, pp 221–365

    Chapter  Google Scholar 

  • Boswell T (1991) The physiology of migratory fattening in the European quail, Coturnix coturnix. Ph. D. thesis, University of Bristol, UK

  • Both C, Visser ME (2001) Adjustment to climate change is constrained by arrival date in a long distance migrant bird. Nature 411:296–298

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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 

  • Coppack T, Pulido F (2004) Photoperiodic response and the adaptability of avian life cycles to environmental change. Adv Ecol Res 35:131–147

    Article  Google Scholar 

  • 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 

  • Dawson A (2006) Control of molt in birds: association with prolactin and gonadal regression in starlings. Gen Comp Endocrinol 147:314–322

    Article  PubMed  CAS  Google Scholar 

  • Dawson A, Sharp PJ (1998) The role of prolactin in the development of reproductive photorefractoriness and postnuptial molt in the European starling (Sturnus vulgaris). Endocrinol 139:485–490

    Article  CAS  Google Scholar 

  • Dawson A, Visser ME (2010) The effects of temperature on photoperiodic responses: implications for climate change. In: BOU Proceedings-Climate Change and Birds

  • Dawson A, King VM, Bentley GE, Ball GF (2001) Photoperiodic control of seasonality in birds. J Biol Rhythms 16(4):365–380

    Article  PubMed  CAS  Google Scholar 

  • Diepens M (2009) Photodegradation and stability of bisphenol a polycarbonate in weathering conditions. Technische Universiteit Eindhoven, Eindhoven

    Google Scholar 

  • Dixit AS, Singh NS (2011) Photoperiod as a proximate factor in control of seasonality in the subtropical male tree sparrow, Passer montanus. Front Zool 8:1–12

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  • Dixit AS, Singh NS (2013) Environmental control of seasonal reproduction in the wild and captive Eurasian tree sparrow (Passer montanus) with respect to variations in gonadal mass, histology, and sex steroids. Can J Zool 91:302–312

    Article  CAS  Google Scholar 

  • Dixit AS, Singh NS (2014) Photoperiodic control of testicular growth, histomorphology and serum testosterone levels in the male Eurasian tree sparrow: involvement of circadian rhythm. Gen Comp Endocrinol 208:5–11

    Article  PubMed  CAS  Google Scholar 

  • Farner DS, Follett BK (1966) Light and other environmental factors affecting avian reproduction. J Anim Sci 25:90–118

    Article  PubMed  Google Scholar 

  • Gahali K, El Halawani ME, Rozenboim I (2001) Photostimulated prolactin release in the turkey hen: effect of ovariectomy and environmental temperature. Gen Comp Endocrinol 124:166–172

    Article  PubMed  CAS  Google Scholar 

  • Hahn TP, MacDougall-Shackleton SA (2008) Adaptive specialization, conditional plasticity and phylogenetic history in the reproductive cue response systems of birds. Phil Trans R Soc B 363(1490):267–286

    Article  PubMed  Google Scholar 

  • Jones LR (1986) The effect of photoperiod and temperature on testicular growth in captive black-billed magpies. Condor 88:91–93

    Article  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Kumar V, Singh BP, Rani S (2004) The bird clock: a complex, multi­oscillatory and highly diversified system. Biol Rhythm Res 35:121–144

    Article  Google Scholar 

  • Malik S, Rani S, Kumar V (2004) Wavelength dependency of light-induced effects on photoperiodic clock in the migratory blackheaded bunting (Emberiza melanocephala). Chronobiol Int 21:367–384

    Article  PubMed  Google Scholar 

  • Maney DL, Hahn TP, Schoech SJ, Sharp PJ, Morton ML, Wingfield JC (1999) Effects of ambient temperature on photo-induced prolactin in three subspecies of white-crowned sparrow, Zonotrichia leucophrys. Gen Comp Endocrinol 113:445–456

    Article  PubMed  CAS  Google Scholar 

  • McCleery RH, Perrins CM (1998) Temperature and egg-laying trends. Nature 391:30–31

    Article  CAS  Google Scholar 

  • Meijer T, Nienaber U, Langer U, Trillmich F (1999) Temperature and timing of egg-laying of European starlings. Condor 101:124–132

    Article  Google Scholar 

  • Nager RG, van Noordwijk AJ (1995) Proximate and ultimate aspects of phenotypic plasticity in timing of great tit breeding in a heterogeneous environment. Am Nat 146:454–474

    Article  Google Scholar 

  • Nakane Y, Ikegami K, Ono H, Yamamoto N, Yoshida S, Hirunagi K, Ebihara S, Kubo Y, Yoshimura T (2010) A mammalian neural tissue opsin (opsin 5) is a deep brain photoreceptor in birds. PNAS 107:15264–15268

    Article  PubMed  Google Scholar 

  • Nirmala T (2016) Food availability influences the seasonality of bird community in tropical forest, Western Ghats. Int J Cur Res Rev 8(2):74–83

    Google Scholar 

  • Nussey DH, Postma E, Gienapp P, Visser ME (2005) Selection on heritable phenotypic plasticity in a wild bird population. Science 310:304–306

    Article  PubMed  CAS  Google Scholar 

  • Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669

    Article  Google Scholar 

  • Perfito N, Tramontin AD, Meddle S, Sharp P, Afik D, Gee J, Ishii S, Wingfield JC (2004) Reproductive development according to elevation in a seasonally breeding male songbird. Oecologia 140:201–210

    Article  PubMed  Google Scholar 

  • 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  PubMed  Google Scholar 

  • Rajchard J (2009) Ultraviolet (UV) light perception by birds: a review. Vet Med 54(8):351–359

    Article  Google Scholar 

  • Rastogi A, Kumari Y, Rani S, Kumar V (2013) Neural correlates of migration: activation of hypothalamic clock(s) in and out of migratory state in the blackheaded bunting (Emberiza melanocephala). PLoS One 8:10

    Article  CAS  Google Scholar 

  • Salvante KG, Walzem RL, Williams TD (2007) What comes first, the zebra finch or the egg: temperature-dependent reproductive, physiological and behavioural plasticity in egg-laying zebra finches. J Exp Biol 210:1325–1334

    Article  PubMed  Google Scholar 

  • Schaper SV, Dawson A, Sharp PJ, Gienapp P, Caro SP, Visser ME (2012) Increasing temperature, not mean temperature, is a cue for avian timing of reproduction. Am Nat 179(2):E55-E69

    Article  Google Scholar 

  • Silverin B, Viebke PA (1994) Low temperatures affect the photoperiodically induced LH and testicular cycles differently in closely related species of tits (Parus spp.). Horm Behav 28(3):199–206

    Article  PubMed  CAS  Google Scholar 

  • Silverin B, Wingfield JC, Stokkan KA, Massa R, Jarvinen A, Andersson NA, Lambrechts MM, Blomqvist D (2008) Ambient temperature effects on photo induced gonadal cycles and hormonal secretion patterns in great tits from three different breeding latitudes. Horm Behav 54(1):60–68

    Article  PubMed  CAS  Google Scholar 

  • Smith EL, Greenwood VJ, Bennett ATD (2002) Ultraviolet colour perception in European starlings and Japanese quail. J Exp Biol 205:3299–3306

    PubMed  Google Scholar 

  • Spencer KA, Bryant DM (2002) State-dependent behaviour in breeding barn swallows (Hirundo rustica): consequences for reproductive effort. Proc R Soc Lond B Biol Sci 269(1489):403–410

    Article  CAS  Google Scholar 

  • Torti VM, Dunn PO (2005) Variable effects of climate change on six species of North American birds. Oecologia 145:486–495

    Article  PubMed  Google Scholar 

  • Veselovsky Z (2001) General ornithology (in Czech). Academia, Prague, p 357

    Google Scholar 

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

    Article  Google Scholar 

  • Visser ME, Adriaensen F, van Balen JH, Blondel J, Dhondt AA, van Dongen S, du Feu C, de Laet J (2003) Variable responses to large-scale climate change in European Parus populations. Proc R Soc Lond B Biol Sci 270(1513):367–372

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Visser ME, Holleman LJM, Caro SP (2009) Temperature has a causal effect on avian timing of reproduction. Proc R Soc Lond B Biol Sci 276:2323–2331

    Article  Google Scholar 

  • Visser ME, teMarvelde L, Schaper SV, Dawson A, Webber S, Husby A (2010) Seasonal timing in a warming world. In: Climate change and birds. Proceedings of a British Ornithologists’ Union conference

  • Walther GR, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Fromentin JM, Bairlein F (2002) Ecological responses to recent climate change. Nature 416(6879):389–395

    Article  PubMed  CAS  Google Scholar 

  • Watts HE, Hahn TP (2012) Non-photoperiodic regulation of reproductive physiology in the flexibly breeding pine siskin (Spinus pinus).Gen. Comp Endocrinol 178(2):259–264

    Article  CAS  Google Scholar 

  • Wikelski M, Hau M, Wingfield JC (2000) Seasonality of reproduction in a neotropical rain forest bird. Ecology 81(9):2458–2472

    Article  Google Scholar 

  • 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(3):389–394

    Article  CAS  Google Scholar 

  • Wingfield JC, Kenagy GJ (1991) Natural regulation of reproductive cycles. In: Schreibman M, Jones RE (eds) Vertebrate endocrinology: fundamentals and biomedical implications. Academic Press, New York, pp 181–241

    Google Scholar 

  • Wingfield JC, Hahn TP, Levin R, Honey P (1992) Environmental predictability and control of gonadal cycles in birds. J Exp Zool 261(2):214–231

    Article  Google Scholar 

  • Wingfield JC, Hahn TP, Wada M, Astheimer LB, Schoech S (1996) Interrelationship of day length and temperature on the control of gonadal development, body mass and fat score in white-crowned sparrows, Zonotrichia leucophrys gambelii. Gen Comp Endocrinol 101(3):242–255

    Article  PubMed  CAS  Google Scholar 

  • 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(2):143–158

    Article  PubMed  CAS  Google Scholar 

  • Withgott J (2000) Taking a bird’s-eye view in the UV. Bioscience 50:854–859

    Article  Google Scholar 

  • Wormworth J, Sekercioğlu CH (2011) Winged sentinels: birds and climate change. Cambridge University Press, New York

    Book  Google Scholar 

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Acknowledgements

We acknowledge the animal care committee of the Department of Zoology, North-Eastern Hill University, Shillong (permit number 1886 of 20.09.2011) for approving the procedures of the animal care used in the present study and also the Department of Forest and Environment, Government of Meghalaya, India for granting permission to capture and transport the birds and to carry out the experiments. Financial supports from the Science and Engineering Research Board—Department of Science and Technology (DST) and Department of Biotechnology (DBT), Government of India, New Delhi are gratefully acknowledged. We also wish to thank the anonymous reviewers for their valuable feedback. We are also thankful to Imsuchila Kichu, Cotton University for language editing.

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Authors and Affiliations

  1. Department of Zoology, North-Eastern Hill University, Shillong, Meghalaya, 793022, India

    Anand S. Dixit & Iadalangki Bamon

  2. Department of Zoology, Cotton University, Guwahati, Assam, 781001, India

    Namram S. Singh

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  1. Anand S. Dixit
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  2. Iadalangki Bamon
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  3. Namram S. Singh
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Contributions

ASD conceived the ideas and designed experiments. NSS and IB collected and analysed the data. All authors contributed critically in writing the manuscript. The authors declare no conflict of interest.

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Correspondence to Anand S. Dixit.

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Dixit, A.S., Bamon, I. & Singh, N.S. Temperature modulates photoperiodic seasonal responses in the subtropical tree sparrow, Passer montanus. J Comp Physiol A 204, 721–735 (2018). https://doi.org/10.1007/s00359-018-1272-2

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  • DOI: https://doi.org/10.1007/s00359-018-1272-2

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