Skip to main content
SpringerLink
Log in

Disruption of energy homeostasis by food restriction or high ambient temperature exposure affects gonadal function in male house finches (Haemorhous mexicanus)

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

Reproductive success requires that individuals acquire sufficient energy resources. Restricting food availability or increasing energy expenditure (e.g., thermoregulation) inhibits reproductive development in multiple avian species, but the nature of the energy-related signal mediating this effect is unclear. To investigate this question, we examined reproductive and metabolic physiology in male house finches that either underwent moderate food restriction (FR) or were exposed to high temperature (HT), in which birds were held at a high, but not locally atypical, ambient temperature cycle (37.8 °C day, 29.4 °C night) compared to a control group (CT; 29.4 °C day, 21.1 °C night). We hypothesized that FR and HT inhibit reproductive development by lowering available metabolic fuel, in particular plasma glucose (GLU) and free fatty acids (FFA). Following FR for 4 weeks, finches lost body mass, had marginally higher plasma FFA, and experienced a 90% reduction in testis mass compared to CT birds. Four weeks of HT exposure resulted in reduced voluntary food consumption and muscle mass, as well as an 80% reduction in testis mass relative to CT birds. Both FR and HT birds expressed less testicular 17β-hydroxysteroid dehydrogenase (17β-HSD) mRNA than controls but the expression of other testicular genes measured was unaffected by either treatment. Neither treatment significantly influenced plasma GLU. This study is among the first to demonstrate a negative effect of HT on reproductive development in a wild bird. Further studies are needed to clarify the role of metabolic mediators and their involvement under various conditions of energy availability and demand.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data availability

The datasets generated during and analyzed during the current study are available in the Mendeley Data repository, https://dx.doi.org/10.17632/p2xmrvrf9t.1.

Abbreviations

17β-HSD:

17β-Hydroxysteroid dehydrogenase

ANOVA:

Analysis of variance

AL:

Ad libitum

CP:

Cloacal protuberance

CORT:

Corticosterone

FR:

Food-restricted

FFA:

Free fatty acids

FSHR:

Follicle-stimulating hormone receptor

GLU:

Glucose

GnIH:

Gonadotropin-inhibitory hormone

GR:

Glucocorticoid receptor

GSI:

Gonadosomatic index

HPG:

Hypothalamic-pituitary–gonadal

HSP60:

Heat shock protein 60

HSP70:

Heat shock protein 70

HT:

High temperature

LHR:

Luteinizing hormone receptor

MR:

Mineralocorticoid receptor

StAR:

Steroid acute regulatory protein

T:

Testosterone

TNZ:

Thermoneutral zone

References

  • Albright TP, Pidgeon AM, Rittenhouse CD, Clayton MK, Flather CH, Culbert PD, Radeloff VC (2011) Heat waves measured with MODIS land surface temperature data predict changes in avian community structure. Remote Sens Environ 115:245–254

    Google Scholar 

  • Albright TP, Mutiibwa D, Gerson AR, Smith EK, Talbot WA, O’Neill JJ, McKechnie AE, Wolf BO (2017) Mapping evaporative water loss in desert passerines reveals an expanding threat of lethal dehydration. Proc Natl Acad Sci 114:2283–2288

    CAS  PubMed  Google Scholar 

  • Badyaev AV, Belloni V, Hill GE (2020) House finch (Haemorhous mexicanus), version 1.0. In: Poole AF (ed) Birds of the world. Cornell Lab of Ornithology, Ithaca

    Google Scholar 

  • Ball GF (1993) The neural integration of environmental information by seasonally breeding birds. Am Zool 33:185–199

    Google Scholar 

  • Bentley GE, Ubuka T, McGuire NL, Chowdhury VS, Morita Y, Yano T, Hasunuma I, Binns M, Wingfield JC, Tsutsui K (2008) Gonadotropin-inhibitory hormone and its receptor in the avian reproductive system. Gen Comp Endocrinol 156:34–43

    CAS  PubMed  Google Scholar 

  • Blas J (2015) Stress in birds. In: Scanes C (ed) Sturkie’s avian physiology, 6th edn. Academic Press, San Diego, pp 769–810

    Google Scholar 

  • Bronson FH (1989) Mammalian reproductive biology. University of Chicago Press, Chicago

    Google Scholar 

  • Brown NL, Follett BK (1977) Effects of androgens on the testes of intact and hypophysectomized Japanese quail. Gen Comp Endocrinol 33:267–277

    CAS  PubMed  Google Scholar 

  • Cho RN, Hahn TP, MacDougall-Shackleton S, Ball GF (1998) Seasonal variation in brain GnRH in free-living breeding and photorefractory house finches (Carpodacus mexicanus). Gen Comp Endocrinol 109:244–250

    CAS  PubMed  Google Scholar 

  • Chowdhury VS, Tomonaga S, Nishimura S, Tabata S, Furuse M (2012a) Physiological and behavioral responses of young chicks to high ambient temperature. J Poult Sci 49:212–218

    Google Scholar 

  • Chowdhury VS, Tomonaga S, Nishimura S, Tabata S, Cockrem JF, Tsutsui K, Furuse M (2012b) Hypothalamic gonadotropin-inhibitory hormone precursor mRNA is increased during depressed food intake in heat-exposed chicks. Comp Biochem Physiol A 162:227–233

    CAS  Google Scholar 

  • Cohen J (1988) Statistical power analysis for the behavioral sciences, 2nd edn. Erlbaum, Hillsdale

    Google Scholar 

  • Cooper CE, Hurley LL, Deviche P, Griffith SC (2020) Physiological responses of wild zebra finches (Taeniopygia guttata) to heatwaves. J Exp Biol 223:jeb225524

    PubMed  Google Scholar 

  • Davies S, Deviche P (2014) At the crossroads of physiology and ecology: food supply and the timing of avian reproduction. Horm Behav 66:41–55

    PubMed  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  • Davies S, Lane S, Meddle SL, Tsutsui K, Deviche P (2016) The ecological and physiological bases of variation in the phenology of gonad growth in an urban and desert songbird. Gen Comp Endocrinol 230:17–25

    PubMed  Google Scholar 

  • Dawson A (1986) The effect of restricting the daily period of food availability on testicular growth of Starlings (Sturnus vulgaris). Ibis 128:572–575

    Google Scholar 

  • Dawson A (2005) Seasonal differences in the secretion of luteinising hormone and prolactin in response to N-methyl-dl-aspartate in starlings (Sturnus vulgaris). J Neuroendocrinol 17:105–110

    CAS  PubMed  Google Scholar 

  • Dawson A (2008) Control of the annual cycle in birds: endocrine constraints and plasticity in response to ecological variability. Philos Trans R Soc B 363:1621–1633

    Google Scholar 

  • Dawson A (2018) Both low temperature and shorter duration of food availability delay testicular regression and affect the daily cycle in body temperature in a songbird. Physiol Biochem Zool 91:917–924

    PubMed  Google Scholar 

  • Dawson WR, Buttemer WA, Carey C (1985) A reexamination of the metabolic response of house finches to temperature. Condor 87:424–427

    Google Scholar 

  • del Rio CM, Stevens BR, Daneke DE, Andreadis PT (1988) Physiological correlates of preference and aversion for sugars in three species of birds. Physiol Zool 61:222–229

    Google Scholar 

  • Deviche P, Cortez L (2005) Androgen control of immunocompetence in the male house finch, Carpodacus mexicanus. J Exp Biol 208:1287–1295

    CAS  PubMed  Google Scholar 

  • Deviche P, Hurley LL, Fokidis HB (2011) Avian testicular structure, function, and regulation. Hormones and reproduction of vertebrates: birds. Academic Press, Cambridge, pp 27–70

    Google Scholar 

  • Downs CT, Wellmann AE, Brown M (2010) Diel variations in plasma glucose concentrations of Malachite Sunbirds (Nectarinia famosa). J Ornithol 151:235

    Google Scholar 

  • Drent RH, Daan S (1980) The prudent parent: energetic adjustments in avian breeding. Ardea 68:225–252

    Google Scholar 

  • Dupont J, Reverchon M, Bertoldo MJ, Froment P (2014) Nutritional signals and reproduction. Mol Cell Endocrinol 382:527–537

    CAS  PubMed  Google Scholar 

  • Edwards EK, Mitchell NJ, Ridley AR (2015) The impact of high temperatures on foraging behaviour and body condition in the Western Australian Magpie Cracticus tibicen dorsalis. Ostrich 86:137–144

    Google Scholar 

  • Ernst DK, Lynn SE, Bentley GE (2016) Differential response of GnIH in the brain and gonads following acute stress in a songbird. Gen Comp Endocrinol 227:51–57

    CAS  PubMed  Google Scholar 

  • Fokidis HB, Hurley L, Rogowski C, Sweazea K, Deviche P (2011) Effects of captivity and body condition on plasma corticosterone, locomotor behavior, and plasma metabolites in curve-billed thrashers. Physiol Biochem Zool 84:595–606

    CAS  PubMed  Google Scholar 

  • Fokidis HB, Des Roziers MB, Sparr R, Rogowski C, Sweazea K, Deviche P (2012) Unpredictable food availability induces metabolic and hormonal changes independent of food intake in a sedentary songbird. J Exp Biol 215:2920–2930

    PubMed  Google Scholar 

  • Gao L, Gao J, Zhang S (2018) Temperature effect on luteinizing hormone secretion of Eurasian Skylark (Alauda arvensis) and Great Tit (Parus major) in China. Avian Res 9:3

    Google Scholar 

  • Geraert PA, Padilha JCF, Guillaumin S (1996) Metabolic and endocrine changes induced by chronic heat exposure in broiler chickens: growth performance, body composition and energy retention. Br J Nutr 75:195–204

    CAS  PubMed  Google Scholar 

  • Habashy WS, Milfort MC, Fuller AL, Attia YA, Rekaya R, Aggrey SE (2017) Effect of heat stress on protein utilization and nutrient transporters in meat-type chickens. Int J Biometeorol 61:2111–2118

    PubMed  Google Scholar 

  • Hahn TP (1995) Integration of photoperiodic and food cues to time changes in reproductive physiology by an opportunistic breeder, the red crossbill, Loxia curvirostra. J Exp Zool 272:213–226

    Google Scholar 

  • Halupka L, Halupka K (2017) The effect of climate change on the duration of avian breeding seasons: a meta-analysis. Proc Biol 284:20171710

    Google Scholar 

  • Hamner WM (1966) Photoperiodic control of the annual testicular cycle in the house finch, Carpodacus mexicanus. Gen Comp Endocrinol 7:51–57

    Google Scholar 

  • Hamner WM (1968) The photorefractory period of the house finch. Ecology 49:211–227

    Google Scholar 

  • Hänninen L, Pastell M (2009) CowLog: Open source software for coding behaviors from digital video. Behav Res Methods 41:472–476

    PubMed  Google Scholar 

  • Helms CW, Drury WH (1960) Winter and migratory weight and fat field studies on some North American buntings. Bird Banding 31:1–40

    Google Scholar 

  • Jenni L, Jenni-Eiermann S (1996) Metabolic responses to diurnal feeding patterns during the postbreeding, moulting and migratory periods in passerine birds. Funct Ecol 10:73–80

    Google Scholar 

  • Jenni-Eiermann S, Jenni L, Kvist A, Lindström Å, Piersma T, Visser GH (2002) Fuel use and metabolic response to endurance exercise: a wind tunnel study of a long-distance migrant shorebird. J Exp Biol 205:2453–2460

    PubMed  Google Scholar 

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

    Google Scholar 

  • Kirby JD, Froman DP (2000) Reproduction in male birds. In: Whittow GC (ed) Sturkie’s avian physiology. Academic Press, San Diego, pp 597–615

    Google Scholar 

  • Klasing KC (1998) Comparative avian nutrition. CAB International, London

    Google Scholar 

  • Kojika S, Sugita K, Inukai T, Saito M, Iijima K, Tezuka T, Goi K, Shiraishi K, Mori T, Okazaki T, Kagami K (1996) Mechanisms of glucocorticoid resistance in human leukemic cells: implication of abnormal 90 and 70 kDa heat shock proteins. Leukemia 10:994–999

    CAS  PubMed  Google Scholar 

  • Krause JS, Pérez JH, Meddle SL, Wingfield JC (2017) Effects of short-term fasting on stress physiology, body condition, and locomotor activity in wintering male white-crowned sparrows. Physiol Behav 177:282–290

    CAS  PubMed  Google Scholar 

  • Lack DL (1968) Ecological adaptations for breeding in birds. Methuen, London

    Google Scholar 

  • Landys MM, Ramenofsky M, Guglielmo CG, Wingfield JC (2004) The low-affinity glucocorticoid receptor regulates feeding and lipid breakdown in the migratory Gambel’s white-crowned sparrow (Zonotrichia leucophrys gambelii). J Exp Biol 207:143–154

    CAS  PubMed  Google Scholar 

  • Lattin CR, Waldron-Francis K, Richardson JW, de Bruijn R, Bauer CM, Breuner CW, Romero LM (2012) Pharmacological characterization of intracellular glucocorticoid receptors in nine tissues from house sparrow (Passer domesticus). Gen Comp Endocrinol 179:214–220

    CAS  PubMed  Google Scholar 

  • Lewis RA, Farner DS (1973) Temperature modulation of photoperiodically induced vernal phenomena in White-crowned Sparrows (Zonotrzihia leucouhrvs). Condor 75:279–286

    Google Scholar 

  • Liew PK, Zulkifli I, Hair-Bejo M, Omar AR, Israf DA (2003) Effects of early age feed restriction and heat conditioning on heat shock protein 70 expression, resistance to infectious bursal disease, and growth in male broiler chickens subjected to heat stress. Poult Sci 82:1879–1885

    CAS  PubMed  Google Scholar 

  • Lowell BB, Spiegelman BM (2000) Towards a molecular understanding of adaptive thermogenesis. Nature 404:652–666

    CAS  PubMed  Google Scholar 

  • Lynn SE, Perfito N, Guardado D, Bentley GE (2015) Food, stress, and circulating testosterone: cue integration by the testes, not the brain, in male zebra finches (Taeniopygia guttata). Gen Comp Endocrinol 215:1–9

    CAS  PubMed  Google Scholar 

  • Ma X, Lin Y, Zhang H, Chen W, Wang S, Ruan D, Jiang Z (2014) Heat stress impairs the nutritional metabolism and reduces the productivity of egg-laying ducks. Anim Reprod Sci 145:182–190

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • McGuire NL, Koh A, Bentley GE (2013) The direct response of the gonads to cues of stress in a temperate songbird species is season-dependent. PeerJ 1:e139

    PubMed  PubMed Central  Google Scholar 

  • McLachlan RI, O’Donnell L, Stanton PG, Balourdos G, Frydenberg M, de Kretser DM, Robertson DM (2002) Effects of testosterone plus medroxyprogesterone acetate on semen quality, reproductive hormones, and germ cell populations in normal young men. J Clin Endocrinol Metab 87:546–556

    CAS  PubMed  Google Scholar 

  • Mehaisen GM, Ibrahim RM, Desoky AA, Safaa HM, El-Sayed OA, Abass AO (2017) The importance of propolis in alleviating the negative physiological effects of heat stress in quail chicks. PLoS ONE 12:1–17

    Google Scholar 

  • 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

    Google Scholar 

  • Meijer T, Drent R (1999) Re-examination of the capital and income dichotomy in breeding birds. Ibis 141:399–414

    Google Scholar 

  • Nager RG, Ruegger C, Van Noordwijk AJ (1997) Nutrient or energy limitation on egg formation: a feeding experiment in great tits. J Anim Ecol 495–507

  • O’Brien S, Hau M (2005) Food cues and gonadal development in neotropical spotted antbirds (Hylophylax naevioides). J Ornithol 146:332–337

    Google Scholar 

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

    PubMed  Google Scholar 

  • Perfito N, Meddle SL, Tramontin AD, Sharp PJ, Wingfield JC (2005) Seasonal gonadal recrudescence in song sparrows: response to temperature cues. Gen Comp Endocrinol 143:121–128

    CAS  PubMed  Google Scholar 

  • Perfito N, Kwong JM, 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

    PubMed  Google Scholar 

  • Perrins CM (1970) The timing of birds’ breeding seasons. Ibis 112:242–255

    Google Scholar 

  • Polakof S, Mommsen TP, Soengas JL (2011) Glucosensing and glucose homeostasis: from fish to mammals. Comp Biochem Physiol B 160:123–149

    CAS  PubMed  Google Scholar 

  • Pollock C (2002) Carbohydrate regulation in avian species. Semin Avian Exot Pet Med 11(2):57–64

    Google Scholar 

  • Pratt WB, Toft DO (1997) Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocr Rev 18:306–360

    CAS  PubMed  Google Scholar 

  • Pyle P (1997) Identification guide to North American Birds. Part I. Columbidae to Ploceidae. Slate Creek Press, Bolinas

    Google Scholar 

  • Rajaei-Sharifabadi H, Ellestad L, Porter T, Donoghue A, Bottje WG, Dridi S (2017) Noni (Morinda citrifolia) modulates the hypothalamic expression of stress- and metabolic-related genes in broilers exposed to acute heat stress. Front Genet 8:1–13

    Google Scholar 

  • Ricklefs RE (1974) The energetics of reproduction in birds. Avian Energ 15:152–297

    Google Scholar 

  • Romero LM (2004) Physiological stress in ecology: lessons from biomedical research. Trends Ecol Evol 19:249–255

    PubMed  Google Scholar 

  • Romero LM, Romero RC (2002) Corticosterone responses in wild birds: the importance of rapid initial sampling. Condor 104:129–135

    Google Scholar 

  • Rozenboim I (2004) The role of prolactin in reproductive failure associated with heat stress in the domestic Turkey. Biol Reprod 71:1208–1213

    CAS  PubMed  Google Scholar 

  • Ruffino L, Salo P, Koivisto E, Banks PB, Korpimäki E (2014) Reproductive responses of birds to experimental food supplementation: a meta-analysis. Front Zool 11:80

    PubMed  PubMed Central  Google Scholar 

  • Sachs BD (1967) Photoperiodic control of the cloacal gland of the Japanese quail. Science 157:201–203

    CAS  PubMed  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

    PubMed  Google Scholar 

  • Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21:55–89

    CAS  PubMed  Google Scholar 

  • Scanes CG (2015) Avian endocrine system. In: Scanes C (ed) Sturkie’s avian physiology, 6th edn. Academic Press, San Diego, pp 489–496

    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 179:55–69

    Google Scholar 

  • Schneider JE (2004) Energy balance and reproduction. Physiol Behav 81:289–317

    CAS  PubMed  Google Scholar 

  • Schneider JE, Klingerman CM, Abdulhay A (2012) Sense and nonsense in metabolic control of reproduction. Front Endocrinol 3:26

    Google Scholar 

  • Schoech SJ, Bowman R, Reynolds SJ (2004) Food supplementation and possible mechanisms underlying early breeding in the Florida Scrub-Jay (Aphelocoma coerulescens). Horm Behav 46:565–573

    CAS  PubMed  Google Scholar 

  • Shochat E, Lerman SB, Katti M, Lewis DB (2004) Linking optimal foraging behavior to bird community structure in an urban-desert landscape: field experiments with artificial food patches. Am Nat 164:232–243

    PubMed  Google Scholar 

  • Silverin B, Wingfield J, Stokkan KA, Massa R, Järvinen A, Andersson NÅ, Lambrechts M, Sorace A, 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 54:60–68

    CAS  PubMed  Google Scholar 

  • Smith EK, O’Neill J, Gerson AR, Wolf BO (2015) Avian thermoregulation in the heat: resting metabolism, evaporative cooling and heat tolerance in Sonoran Desert doves and quail. J Exp Biol 218:3636–3646

    PubMed  Google Scholar 

  • Sperry TS, Thompson CK, Wingfield JC (2003) Effects of acute treatment with 8-OH-DPAT and fluoxetine on aggressive behaviour in male song sparrows (Melospiza melodia morphna). J neuroendocrinol 15:150–160

    CAS  PubMed  Google Scholar 

  • Swain SD (1987) Overnight changes in circulating energy substrate concentrations in the Vesper Sparrow (Pooecetes gramineus). Comp Biochem Physiol A 86:439–441

    Google Scholar 

  • Thomas DW, Blondel J, Perret P, Lambrechts MM, Speakman JR (2001) Energetic and fitness costs of mismatching resource supply and demand in seasonally breeding birds. Science 291:2598–2600

    CAS  PubMed  Google Scholar 

  • Tsutsui K, Saxena T, Saxena RN (1994) Effects of season and photoperiod on the plasma and intratesticular testosterone levels in Indian weaver birds inhabiting the subtropical zone. J Exp Zool 270:381–387

    CAS  Google Scholar 

  • Tsutsui K, Bentley GE, Ubuka T, Saigoh E, Yin H, Osugi T, Inoue K, Chowdhury VS, Ukena K, Ciccone N, Sharp PJ (2007) The general and comparative biology of gonadotropin-inhibitory hormone (GnIH). Gen Comp Endocrinol 153:365–370

    CAS  PubMed  Google Scholar 

  • Tsutsui K, Bentley GE, Bedecarrats G, Osugi T, Ubuka T, Kriegsfeld LJ (2010) Gonadotropin-inhibitory hormone (GnIH) an:d its control of central and peripheral reproductive function. Front Neuroendocrinol 31:284–295

    CAS  PubMed  Google Scholar 

  • Turner TT, Jones CE, Howards SS, Ewing LL, Zegeye B, Gunsalus GL (1984) On the androgen microenvironment of maturing spermatozoa. Endocrinology 115:1925–1932

    CAS  PubMed  Google Scholar 

  • Valle S (2019) Disruption of energy homeostasis by food restriction or high ambient temperature exposure affects gonadal function in male House finches (Haemorhous mexicanus). Mendeley Data. https://doi.org/10.17632/p2xmrvrf9t.1

    Article  Google Scholar 

  • Valle S, Carpentier E, Vu B, Tsutsui K, Deviche P (2015) Food restriction negatively affects multiple levels of the reproductive axis in male house finches, Haemorhous mexicanus. J Exp Biol 218:2694–2704

    PubMed  Google Scholar 

  • Valle S, Das C, Meddle SL, Deviche P (2019) The effect of food restriction on the regulation of gonadotropin-releasing hormone in male house finches (Haemorhous mexicanus). Gen Comp Endocrinol 282:113196

    CAS  PubMed  Google Scholar 

  • Vizcarra J, Alan R, Kirby J (2015) Reproduction in male birds. In: Scanes C (ed) Sturkie’s avian physiology, 6th edn. Academic Press, San Diego, pp 667–693

    Google Scholar 

  • Wade GN, Schneider JE, Li HY (1996) Control of fertility by metabolic cues. Am J Physiol 270:1–19

    Google Scholar 

  • Weathers WW (1981) Physiological thermoregulation in heat-stressed birds: consequences of body size. Physiol Zool 54:345–361

    Google Scholar 

  • Wegge P, Rolstad J (2017) Climate change and bird reproduction: warmer springs benefit breeding success in boreal forest grouse. Proc R Soc B 284:20171528

    PubMed  Google Scholar 

  • Wei T, Simko V (2017) R package “corrplot”: visualization of a correlation matrix (version 0.84). https://github.com/taiyun/corrplot. Accessed 15 Oct 2019

  • Whelan S, Strickland D, Morand-Ferron J, Norris DR (2017) Reduced reproductive performance associated with warmer ambient temperatures during incubation in a winter-breeding, food-storing passerine. Ecol Evol 7:3029–3036

    PubMed  PubMed Central  Google Scholar 

  • Wilson WO, Siopes TD, Itho S (1972) Production of traits of leghorn pullets in controlled temperatures. Poult Sci 51:1014

    Google Scholar 

  • Wingfield JC (2003) Effects of temperature on photoperiodically induced reproductive development, circulating plasma luteinizing hormone and thyroid hormones, body mass, fat deposition and molt in mountain white-crowned sparrows, Zonotrichia leucophrys oriantha. Gen Comp Endocrinol 131:143–158

    CAS  PubMed  Google Scholar 

  • Wingfield JC (2015) Coping with change: a framework for environmental signals and how neuroendocrine pathways might respond. Front Neuroendocrinol 37:89–96

    PubMed  Google Scholar 

  • Wingfield JC, Smith JP, Farner DS (1982) Endocrine responses of white-crowned sparrows to environmental stress. Condor 84:399–409

    Google Scholar 

  • Wingfield JC, Hahn TP, Wada M, Schoech SJ (1997) Effects of day length and temperature on gonadal development, body mass, and fat depots in white-crowned sparrows, Zonotrichia leucophrys pugetensis. Gen Comp Endocrinol 107:44–62

    CAS  PubMed  Google Scholar 

  • Xie J, Tang L, Lu L, Zhang L, Lin X, Liu HC, Odle J, Luo X (2015) Effects of acute and chronic heat stress on plasma metabolites, hormones and oxidant status in restrictedly fed broiler breeders. Poult Sci 94:1635–1644

    CAS  PubMed  Google Scholar 

  • Xie S, Romero LM, Htut ZW, McWhorter TJ (2017) Stress responses to heat exposure in three species of Australian desert birds. Physiol Biochem Zool 90:348–358

    PubMed  Google Scholar 

  • Zinzow-kramer WM, Horton BM, Maney DL (2014) Hormones and behavior evaluation of reference genes for quantitative real-time PCR in the brain, pituitary, and gonads of songbirds. Horm Behav 66:267–275

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zirkin BR, Santulli R, Awoniyi CA, Ewing LL (1989) Maintenance of advanced spermatogenic cells in the adult rat testis: quantitative relationship to testosterone concentration within the testis. Endocrinol 124:3043–3049

    CAS  Google Scholar 

  • Zuckerberg B, Ribic CA, McCauley LA (2018) Effects of temperature and precipitation on grassland bird nesting success as mediated by patch size. Conserv Biol 32:872–882

    PubMed  Google Scholar 

Download references

Acknowledgements

We thank Kevin McGraw, Miles Orchinik, Catherine Propper, and Karen Sweazea for providing helpful comments on drafts of the manuscript. This work was supported by the National Science Foundation under grant number DEB-1832016, Central Arizona-Phoenix Long-Term Ecological Research Program (CAP LTER), and under grant number IOB 1026620 to PD.

Author information

Author notes

  1. Shelley Valle

    Present address: Lerner Research Institute, Cleveland Clinic, Cleveland, OH, USA

  2. Daphne Eagleman

    Present address: Department of Molecular and Integrative Physiology, University of Illinois at Urbana-Champaign, Urbana, IL, USA

Authors and Affiliations

  1. School of Life Sciences, Arizona State University, Tempe, AZ, USA

    Shelley Valle, Daphne Eagleman, Natalie Kieffer & Pierre Deviche

Authors
  1. Shelley Valle
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daphne Eagleman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Natalie Kieffer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pierre Deviche
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

SV and PD contributed to the study conception and design. SV, DE, and NK performed experimental manipulations, collected blood samples, and conducted behavioral analyses. SV performed morphological measurements, and conducted plasma assays, qPCR, and statistical analyses. SV and PD drafted the manuscript.

Corresponding author

Correspondence to Shelley Valle.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures were approved by the Arizona State University Institutional Animal Care and Use Committee (Protocol #15-1414R). All necessary permits to capture animals were obtained from the US Fish and Wildlife Service and the Arizona Game and Fish Department.

Additional information

Communicated by K. H. Dausmann.

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Valle, S., Eagleman, D., Kieffer, N. et al. 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, 611–628 (2020). https://doi.org/10.1007/s00360-020-01295-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-020-01295-0

Keywords

Search

Navigation