Skip to main content
SpringerLink
Log in

Annual variations of adrenal gland hormones in the lizard Podarcis sicula

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

Abstract

The adrenal gland regulates metabolism and maintains normal electrolyte balance. Adrenal hormones are equivalent in all vertebrates; the chromaffin tissue produces adrenaline and noradrenaline and the steroidogenic tissue produces most of the steroid hormones present in mammals. Podarcis sicula belongs to the Squamata family of lizards and it is the most abundant lizard species in southern Italy. This species shows a reproductive annual cycle and the presence of seasonal variations in the activity of the hypothalamus-hypophyseal-thyroid axis. To investigate the existence of an annual cycle of lizard adrenal gland, we have measured plasma concentrations of corticosterone, ACTH, noradrenaline and adrenaline. We have shown that corticosterone rapidly increased from January to March to reach a peak value that persisted until July, then, it slowly decreased until December. ACTH levels increased from January to May and slowly decreased from July to December. Noradrenaline levels were higher in March and then decreased until December. On the contrary, adrenaline levels increased from March to July and slowly decreased until December. Our results demonstrate the existence of an annual cycle of the lizard adrenal gland activity. This is very interesting because its activity is important to rightly regulate the reproductive status of the Podarcis sicula lizard.

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. 1a, b

Similar content being viewed by others

References

  • Andò S, Panno ML, Ciarcia G, Imbrogno E, Buffone M, Beraldi E, Sisci D, Angelini F, Botte V (1990) Plasma sex hormone concentrations during the reproductive cycle in the male lizard, Podarcis sicula. J Reprod Fertil 90:353–360

    PubMed  Google Scholar 

  • Andò S, Ciarcia G, Panno ML, Imbrogno E, Tarantino G, Buffone M, Beraldi E, Angelini F, Botte V (1992) Sex steroid levels in the plasma and testis during the reproductive cycle of lizard, Podarcis sicula Raf. Gen Comp Endocrinol 85:1–7

    PubMed  Google Scholar 

  • Andrews TJ, Summers CH (1996) Aggression and the acquisition and function of social dominance in female Anolis carolinensis. Behaviour 133:1265–1279

    Google Scholar 

  • Angelini F, Botte V (1992) Spermatogenesis in reptiles, dynamic and regulatory aspect. In: Dallai R (ed) Sex origin and evolution, vol 6. Mucchi Selected Symposia and Monographs. UZI, Modena, pp 211–230

  • Angelini F, Ghiara G (1984) Reproductive models and strategies in vertebrate evolution. Ital J Zool 51:121–203

    Google Scholar 

  • Angelini F, Picariello O, Botte V (1976) Influence of photoperiod and temperature on the testicular activity of the lizard, Lacerta s. sicula Raf. Boll Zool 43:111–123

    Google Scholar 

  • Angelini F, Ciarcia G, Botte V (1986) Ambient crues and sexual cycle in the lizard, Podarcis s. sicula Raf. In: Assenmacher I, Boissin J (eds) Endocrine regulations as adaptative mechanisms to environments. Editions CNRS, Paris, pp 227–232

  • Basserji TK, Callas G, Meyer WJ, Rassoli A (1986) ACTH increases adrenal medullary PNMT activity in neonatal rats. Life Sci 38:343–349

    Article  PubMed  Google Scholar 

  • Bornstein SR, Bornestein-Ehrhart M, Henning U, Bockmann M, Scherbaum W (1991) Morphological evidence for a close interaction of chromaffin cells with cortical cells within the adrenal gland. Cell Tissue Res 265:1–9

    CAS  PubMed  Google Scholar 

  • Borrelli L, De Stasio R, Motta CM, Parisi E, Filosa S (2000) Seasonal-dependent effect of temperature on the response of adenylate cyclase to FSH stimulation in the oviparous lizard, Podarcis sicula. J Endocrinol 167:275–280

    CAS  PubMed  Google Scholar 

  • Botte V, Angelini F (1980) Endocrine control of reproduction in reptiles: the refractory period. In: Delrio G, Brachet J (eds) Steroids and their mechanisms of action in nonmammalian vertebrates. Raven Press, New York, pp 201–212

  • Cardone A, Angelini F, Esposito T, Comitato R, Varriale B (2000) The expression of androgen receptor messenger RNA is regulated by tri-iodothyronine in lizard testis. J Steroid Biochem Mol Biol 72:133–141

    Article  CAS  PubMed  Google Scholar 

  • Cardone A, Comitato R, Bellini L, Angelini F (2002) Effects of the aromatase inhibitor fadrozole on plasma sex steroid secretion, spermatogenesis and epididymis morphology in the lizard Podarcis sicula. Mol Reprod Dev 63:63–70

    Article  CAS  Google Scholar 

  • Carsia RV, John-Alder H (2003) Seasonal alterations in adrenocorticali cell function associated with stress-responsiveness and sex in the eastern fence lizard (Sceloporus undulatus). Horm Behav 43:408–420

    Article  CAS  PubMed  Google Scholar 

  • Ciarcia G, Angelini F, Polzonetti A, Zerani M, Botte V (1986) Hormones and reproduction in the lizard, Podarcis s. sicula Raf. In: Assenmacher I, Boissin J (eds) Endocrine regulations as adaptative mechanisms to environments. Editions CNRS, Paris, pp 95–100

  • Coupland RD, MacDougall JDB (1966) Adrenaline formation in noradrenaline storing chromaffin cells in vitro induced by corticosterone. J Endocrinol 36:317–326

    CAS  PubMed  Google Scholar 

  • Dauphin-Villemant C, Xavier F (1985) In vitro steroid biosynthesis by the adrenal gland of the female Lacerta vivipara Jacquin: the metabolism of exogenous precursors. Gen Comp Endocrinol 58:1–9

    CAS  PubMed  Google Scholar 

  • Dauphin-Villemant C, Leboulenger F, Vaudry H (1990) Adrenal activity in the female lizard Lacerta vivipara Jacquin during artificial hibernation. Gen Comp Endocrinol 79:201–214

    CAS  PubMed  Google Scholar 

  • De Falco M, Sciarrillo R, Capaldo A, Laforgia V, Varano L, Cottone G, De Luca A (2003) Shift from noradrenaline to adrenaline production in the adrenal gland of the lizard, Podarcis sicula, after stimulation with vasoactive intestinal peptide (VIP). Gen Comp Endocrinol 131:325–337

    Article  PubMed  Google Scholar 

  • Doddamani LS (2000) Development of the adrenal gland in the tropical lizard Calotes versicolor. Gen Comp Endocrinol 117:89–102

    Article  CAS  PubMed  Google Scholar 

  • Filosa S (1973) Biological and cytological aspect of the ovarian cycle in Lacerta sicula sicula Rafinesque. Mon Zool Ital 7:151–165

    Google Scholar 

  • Fivizzani AJ, Oring LW (1986) Plasma steroid hormones in relation to behavioral sex role reversal in the spotted sandpiper, Actitis macularia. Biol Reprod 35:1195–1201

    CAS  PubMed  Google Scholar 

  • Gleeson TT, Dalessio PM, Carr JA, Wickler SJ, Mazzeo RS (1993) Plasma catecholamine and corticosterone and their in vitro effects on lizard skeletal muscle lactate metabolism. Am J Physiol 265:R632–R639

    CAS  PubMed  Google Scholar 

  • Gobbetti A, Zerani M, Di Fiore MM, Botte V (1993a) PGF2α, PGE2, progesterone, and estradiol-17β secretion by the corpus luteum of the oviparous lizard, Podarcis sicula sicula. In vitro studies. Prostaglandins 45:159–166

    Article  CAS  PubMed  Google Scholar 

  • Gobbetti A, Zerani M, Di Fiore MM, Botte V (1993b) Prostaglandins and sex steroids from reptilian (Podarcis sicula sicula) ovarian follicles at different developmental stages. Zool Sci 10:321–328

    CAS  Google Scholar 

  • Gowaty PA, Wagner SJ (1988) Breeding season aggression of female and male eastern bluebirds (Sialia sialis) to models of potential conspecific and interspecific egg dumpers. Ethology 78:238–250

    Google Scholar 

  • Grassman M, Crews D (1989) Ovarian and adrenal function in the parthenogenetic whiptail lizard Cnemidophorus uniparens in the field and laboratory. Gen Comp Endocrinol 76:444–450

    CAS  PubMed  Google Scholar 

  • Grassman M, Hess DL (1992a) Sex differences in adrenal function in the lizard Cnemidophorus uniparens: I. Seasonal variation in the field. J Exp Zool 264:177–182

    CAS  PubMed  Google Scholar 

  • Grassman M, Hess DL (1992b) Sex differences in adrenal function in the lizard Cnemidophorus uniparens: II. Responses to acute stress in the laboratory. J Exp Zool 264:183–188

    CAS  PubMed  Google Scholar 

  • Greenberg N, Chen T, Crews D (1984) Social status, gonadal state, and the adrenal stress response in the lizard, Anolis carolinensis. Horm Behav 18:1–11

    CAS  PubMed  Google Scholar 

  • Haller J, Makara GB, Kruk MR (1998) Catecholaminergic involvement in the control of aggression: hormones, the peripheral sympathetic, and central noradrenergic system. Neurosci Biobehav Rev 22:85–97

    Article  CAS  PubMed  Google Scholar 

  • Jaeger RG, Kalvarsky D, Shimizu N (1982) Territorial behavior of the redbacked salamander: expulsion of intruders. Anim Behav 30:490–496

    Google Scholar 

  • Jiang W, Uht R, Bohn MC (1989) Regulation of phenylethanolamine N-methyltransferase (PNMT) mRNA in the rat adrenal medulla by corticosterone. Int J Dev Neurosci 7:513–520

    Article  CAS  Google Scholar 

  • John-Alder H, Seitz L, Haenel G (1997) Ecological endocrinology of reptiles: hormonal causes and correlates of variation in exercise endurance in lizards. In: Kawashima S, Kikuyama S (eds) Advances in comparative endocrinology. Proceedings of the XIIIth International Congress of Comparative Endocrinology, Yokohama. Monduzzi, Bologna, pp 1661–1667

  • John-Alder H, Carsia RV, Smith LC, Haenel GJ (2002) Seasonal and sexual variation in plasma corticosterone and adrenocorticali cell function in eastern fence lizards (Sceloporus undulatus). In: Keller R, Dircksen H, Sedlmeier D, Vaudry H (eds) Proceedings of the 21st Conference of European Comparative Endocrinologists, Bonn. Monduzzi, Bologna, pp 141–146

  • Kent C, Parker KG (1993) ACTH and aminoglutethimide on the catecholamine content and chromaffin cell morphology of the adrenal medulla of the neonatal rat. J Anat 183:601–607

    CAS  PubMed  Google Scholar 

  • Kirshneer N, Goodall M (1957) The formation of adrenaline from noradrenaline. Biochim Biophys Acta 24:658–659

    Article  PubMed  Google Scholar 

  • Knapp R, Moore MC (1997) Male morphs in tree lizards have different testosterone responses to elevated levels of corticosterone. Gen Comp Endocrinol 107:273–279

    Article  CAS  PubMed  Google Scholar 

  • Korzan WJ, Summers TR, Summers CH (2002) Manipulation of visual sympathetic sign stimulus modifies social status and plasma catecholamines. Gen Comp Endocrinol 128:153–161

    Article  CAS  PubMed  Google Scholar 

  • Laforgia V, Muoio R (1997) Effects of ACTH and corticosteroids on phenylethanolamine-N-methyltransferase (PNMT) expression as determined by immunocytochemical localization in the adrenal gland of the lizard Podarcis sicula. Ital J Zool 64:301–306

    CAS  Google Scholar 

  • Laforgia V, Varano L (1978) The influence of the interrenal steroidogenic tissue on the chromaffin cells of the adrenal gland of Lacerta s. sicula Raf.: effects of ACTH administration during winter. Cell Mol Biol 23:379–390

    CAS  Google Scholar 

  • Manzo C, Zerani M, Gobetti A, Di Fiore MM, Angelini F (1994) Is corticosterone involved in the reproductive processes of the male lizard, Podarcis s. sicula?. Horm Behav 28:117–129

    Article  CAS  PubMed  Google Scholar 

  • Manzo C, Capaldo A, Laforgia V, Muoio R, Angelini F, Varano L (2000) Inhibin in the testis and adrenal gland of the male lacertid, Podarcis sicula Raf.: a light immunocytochemical study. Eur J Histochem 44:285–293

    CAS  PubMed  Google Scholar 

  • Moore MC, Thompson CW, Marler CA (1991) Reciprocal changes in corticosterone and testosterone levels following acute and chronic handling stress in the tree lizard, Urosaurus ornatus. Gen Comp Endocrinol 81:217–226

    CAS  PubMed  Google Scholar 

  • Pohorecky LA, Rust JH (1968) Studies on the cortical control of the adrenal medulla in the rat. J Pharmacol Exp Ther 162:227–238

    CAS  PubMed  Google Scholar 

  • Rupik W (2002) Early development of the adrenal glands in the grass snake Natrix natrix L. (Lepidosauria, Serpentes). Adv Anat Embryol Cell Biol 164:1–102

    Google Scholar 

  • Schuett GW, Harlow HJ, Rose JD, Van Kirk EA, Murdock WJ (1996) Levels of plasma corticosterone and testosterone in male copperheads (Agkistrodon contortrix) following staged fights. Horm Behav 30:60–68

    Article  CAS  PubMed  Google Scholar 

  • Sciarrillo R, Laforgia V, Cavagnuolo A, Varano L, Virgilio F (2000) Annual variations of thyroid activity in the lizard Podarcis sicula (Squamata, Lacertidae). Ital J Zool 67:263–267

    Google Scholar 

  • Summers CH, Greenberg N (1994) Somatic correlates of adrenergic activity during aggression in the lizard, Anolis carolinensis. Horm Behav 28:29–40

    Article  CAS  PubMed  Google Scholar 

  • Summers CH, Greenberg N (1995) Activation of central biogenic amines following aggressive interaction in male lizards, Anolis carolinensis. Brain Behav Evol 45:339–349

    CAS  PubMed  Google Scholar 

  • Varano L, Laforgia V (1991) Evolutionary trends in the adrenal gland of reptiles. In: Ghiara G et al (eds) Symposium on the evolution of terrestrial vertebrates. Mucchi, Modena, pp 291–303

  • Vivien-Roels B (1985) Interactions between photoperiod, temperature, pineal and seasonal reproduction in non-mammalian vertebrates. In: Mess B et al (eds) The pineal gland: current state of pineal research. Elsevier, Amsterdam, pp 187–209

  • Wilson BS, Wingfield JC (1994) Seasonal and interpopulational variation in plasma levels of corticosterone in the side-blotched lizard (Uta stransburiana). Physiol Zool 67:1025–1049

    CAS  Google Scholar 

  • Wingfield JC, Hegner RE, Dufty AM, Ball GF (1990) The “challenge hypothesis”: theoretical implications for patterns of testosterone secretion, mating systems and breeding strategies. Am Nat 136:829–846

    Article  Google Scholar 

  • Woodley SK, Moore MC (1999) Female territorial aggression and steroid hormones in mountain spiny lizards. Anim Behav 57:1083–1089

    Article  PubMed  Google Scholar 

  • Woodley SK, Matt KS, Moore MC (2000) Neuroendocrine responses in free-living female and male lizards after aggressive interactions. Physiol Behav 71:373–381

    Article  CAS  PubMed  Google Scholar 

  • Woodward JJ (1982) Plasma catecholamines in resting rainbow trout Salmo gairdneri Richardson, by high pressure liquid chromatography. J Fish Biol 21:429–432

    Google Scholar 

Download references

Acknowledgements

This work was supported in part by University of Naples “Federico II”; PRIN 2003 and I.S.S.C.O. (President: H.E. Kaiser).

Author information

Authors and Affiliations

  1. Department of Evolutive and Comparative Biology, University of Naples “Federico II”, Via Mezzocannone, 8, 80134, Naples, Italy

    M. De Falco, F. Virgilio, V. Fedele, S. Valiante, V. Laforgia & L. Varano

  2. Department of Biological and Environmental Sciences, Sannio University, Benevento, Italy

    R. Sciarrillo

Authors
  1. M. De Falco
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. Sciarrillo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. F. Virgilio
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. V. Fedele
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. S. Valiante
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. V. Laforgia
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. L. Varano
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. De Falco.

Rights and permissions

Reprints and permissions

About this article

Cite this article

De Falco, M., Sciarrillo, R., Virgilio, F. et al. Annual variations of adrenal gland hormones in the lizard Podarcis sicula . J Comp Physiol A 190, 675–681 (2004). https://doi.org/10.1007/s00359-004-0528-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-004-0528-1

Keywords

Search

Navigation