Brain levels of arginine-vasotocin and isotocin in dominant and subordinate males of a cichlid fish

Hormones and Behavior

Volumn 61, Issue 2, 2012, Pages 212-217

  Almeida, Olinda ^a   Gozdowska, Magdalena ^b   Kulczykowska, Ewa ^b   Oliveira, Rui F ^a,c  

^a INSTITUTO SUPERIOR DE PSICOLOGIA APLICADA   (Portugal)

^b INSTITUTE OF OCEANOLOGY   (Poland)

^c INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

Author keywords

AVT; Brain; Fish; Isotocin; Social status; Tilapia; Vasotocin

Indexed keywords

ARGIPRESTOCIN; ISOTOCIN;

ANATOMICAL VARIATION; ANIMAL EXPERIMENT; ARTICLE; BRAIN; BRAIN LEVEL; CEREBELLUM; CICHLID; CONTROLLED STUDY; CORRELATION ANALYSIS; DIENCEPHALON; ENZYME ACTIVITY; ENZYME REGULATION; FEMALE; FLUORESCENCE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MALE; NERVE CELL PLASTICITY; NONHUMAN; OPTIC TECTUM; PHENOTYPE; PRIORITY JOURNAL; PROTEIN SECRETION; RHOMBENCEPHALON; SOCIAL STATUS; SOCIAL STRESS;

ANIMALS; BRAIN; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CICHLIDS; DOMINANCE-SUBORDINATION; HYDROCORTISONE; MALE; OXYTOCIN; PITUITARY GLAND; STRESS, PSYCHOLOGICAL; URINE; VASOTOCIN;

EID: 84856965681     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2011.12.008     Document Type: Article

References (68)

1. Abbott D.H., Keverne E.B., Bercovitch F.B., Shively C.A., Mendoza S.P., Saltzman W., Snowdon C.T., Ziegler T.E., Banjevic M., Garland T., Sapolsky R.M. Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates. Horm. Behav. 2003, 43:67-82.
2. Almeida O.G., Miranda A., Frade P., Hubbard P.C., Barata E.N., Canário A.V.M. Urine as a social signal in the Mozambique tilapia (Oreochromis mossambicus). Chem. Senses 2005, 30:309-310.
3. Amer S., Brown J.A. Glomerular actions of arginine vasotocin in the in situ perfused trout kidney. Am. J. Physiol. 1995, 269(4 Pt 2):R775-R780.
4. Backström T., Schjolden J., Øverli Ø., Thörnqvist P.O., Winberg S. Stress effects on AVT and CRF systems in two strains of rainbow trout (Oncorhynchus mykiss) divergent in stress responsiveness. Horm. Behav. 2011, 59:180-186.
5. Baerends G.P., Baerends van Roon J.M. An introduction to the ethology of cichlid fishes. Behaviour 1950, Suppl. 1:1-242.
6. Baker B.I., Bird D.J., Buckingham J.C. In the trout, CRH and AVT synergize to stimulate ACTH release. Regul. Pept. 1996, 67:207-210.
7. Balment R.J., Warne J.M., Tierney M., Hazon N. Arginine vasotocin and fish osmoregulation. Fish Physiol. Biochem. 1993, 11:189-194.
8. Balment R.J., Lu W., Weybourne E., Warne J.M. Arginine vasotocin a key hormone in Wsh physiology and behaviour: a review with insights from mammalian models. Gen. Comp. Endocrinol. 2006, 147:9-16.
9. Barata E.N., Hubbard P.C., Almeida O.G., Miranda A., Canário A.V.M. Male urine signals social rank in Mozambique tilapia (Oreochromis mossambicus, Peters 1852). BMC Biol. 2007, 5:54.
10. Bastian J., Schniederjan S., Nguyenkim J. Arginine vasotocin modulates a sexually dimorphic communication behavior in the weakly electric fish Apteronotus leptorhynchus. J. Exp. Biol. 2001, 204:1909-1923.
11. Bruton M.N., Boltt R.E. Aspects of the biology of Tilapia mossambica Peters (Pisces: Cichlidae) in a natural freshwater lake (Lake Sibaya, South Africa). J. Fish Biol. 1975, 7:423-446.
12. Carneiro L.A., Oliveira R.F., Canário A.V.M., Grober M.S. The effect of arginine vasotocin on courtship behaviour in a blenniid fish with alternative reproductive tactics. Fish Physiol. Biochem. 2003, 28:241-243.
13. Creel S. Social dominance and stress hormones. Trends Ecol. Evol. 2001, 16:491-497.
14. Cumming R., Reaves T.A., Hayward J.N. Ultrastructural immunocytochemical characterization of isotocin, vasotocin and neurophysin neurons in the magnocellular preoptic nucleus of the goldfish. Cell Tissue Res. 1982, 223:685-694.
15. Dewan A.K., Tricas T.C. Arginine vasotocin neuronal phenotypes and their relationship to aggressive behavior in the territorial monogamous multiband butterflyfish, Chaetodon multicinctus. Brain Res. 2011, 1401:74-84.
16. Dewan A.K., Maruska K.P., Tricas T.C. Arginine vasotocin neuronal phenotypes among congeneric territorial and shoaling reef butterflyfishes: species, sex and reproductive season comparisons. J. Neuroendocrinol. 2008, 20:1382-1394.
17. Dewan A.K., Ramey M.L., Tricas T.C. Arginine vasotocin neuronal phenotypes, telencephalic fiber varicosities, and social behavior in butterflyfishes (Chaetodontidae): potential similarities to birds and mammals. Horm. Behav. 2011, 59:56-66.
18. Foo J.T.W., Lam T.J. Serum cortisol response to handling stress and the effect of cortisol implantation on testosterone level in the tilapia, Oreochromis mossambicus. Aquaculture 1993, 115:145-158.
19. Frade P., Hubbard P.C., Barata E.N., Canário A.V.M. Olfactory sensitivity of the Mozambique tilapia to conspecific odours. J. Fish Biol. 2002, 61:1239-1254.
20. Fryer G., Iles T.D. The Cichlid Fishes of the Great Lakes of Africa-Their Biology and Evolution 1972, Oliver and Boyd, Edinburgh.
21. Gerlach G., Hodgins-Davis A., Avolio C., Schunter C. Kin recognition in zebrafish: a 24-hour window for olfactory imprinting. Proc. Biol. Sci. 2008, 275:2165-2170.
22. Gilchriest B.J., Tipping D.R., Hake L., Levy A., Baker B.I. The effects of acute and chronic stresses on vasotocin gene transcripts in the brain of the rainbow trout (Oncorhynchus mykiss). J. Neuroendocrinol. 2000, 12:795-801.
23. Goodson J.L. Nonapeptides and the evolutionary patterning of sociality. Prog. Brain Res. 2008, 170:3-15.
24. Goodson J.L., Bass A.H. Forebrain peptides modulate sexually polymorphic vocal circuitry. Nature 2000, 403:769-772.
25. Goodson J.L., Bass A.H. Vasotocin innervation and modulation of vocal-acoustic circuitry in the teleost Porichthys notatus. J. Comp. Neurol. 2000, 422:363-379.
26. Goodson J.L., Bass A.H. Social behavior functions and related anatomical characteristics of vasotocin/vasopressin systems in vertebrates. Brain Res. Rev. 2001, 35:246-265.
27. Goodson J.L., Thompson R.R. Nonapeptide mechanisms of social cognition, behavior and species-specific social systems. Curr. Opin. Neurobiol. 2010, 20:784-794.
28. Goodson J.L., Evans A.K., Bass A.H. Putative isotocin distributions in sonic fish: relation to vasotocin and vocal-acoustic circuitry. J. Comp. Neurol. 2003, 462:1-14.
29. Gozdowska M., Kulczykowska E. Determination of arginine-vasotocin and isotocin in fish plasma with solid-phase extraction and fluorescence derivatization followed by high-performance liquid chromatography. J. Chromatogr. B 2004, 807:229-233.
30. Gozdowska M., Kleszczyńska A., Sokołowska E., Kulczykowska E. Arginine vasotocin (AVT) and isotocin (IT) in fish brain: diurnal and seasonal variations. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2006, 143:330-334.
31. Greenwood A.K., Wark A.R., Fernald R.D., Hofmann H.A. Expression of arginine vasotocin in distinct preoptic regions is associated with dominant and subordinate behaviour in an African cichlid fish. Proc. Biol. Sci. 2008, 275:2393-2402.
32. Hausmann H., Meyerhof W., Zwiers H., Lederis K., Richter D. Teleost isotocin receptor: structure, functional expression, mRNA distribution and phylogeny. FEBS Lett. 1995, 370:227-230.
33. Holmqvist B.I., Ekstrom P. Hypophysiotrophic systems in the brain of the Atlantic salmon. Neuronal innervation of the pituitary and the origin of pituitary dopamine and nonapeptides identified by means of combined carbocyanine tract tracing and immunocytochemistry. J. Chem. Neuroanat. 1995, 8:125-145.
34. Kleszczyńska A., Vargas-Chacoff L., Gozdowska M., Kalamarz H., Martínez-Rodríguez G., Mancera J.M., Kulczykowska E. Arginine vasotocin, isotocin and melatonin responses following acclimation of gilthead sea bream (Sparus aurata) to different environmental salinities. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2006, 145:268-273.
35. Kleszczyńska A., Dumont E., Cornelis R., Gozdowska M., Kulczykowska E., Sandra P. Determination of the neuropeptides arginine vasotocin and isotocin in brains of three-spined sticklebacks (Gasterosteus aculeatus) by off-line solid phase extraction-liquid chromatography-electrospray tandem mass spectrometry. J. Chromatogr. A 2007, 1150:290-294.
36. Kline R.J., O'Connell L.A., Hofmann H.A., Holt G.J., Khan I.A. The distribution of an AVT V1a receptor in the brain of a sex changing fish, Epinephelus adscensionis. J. Chem. Neuroanat. 2011, 42:72-88.
37. Konno N., Hyodo S., Yamaguchi Y., Matsuda K., Uchiyama M. Vasotocin/V2-type receptor/aquaporin axis exists in African lungfish kidney but is functional only in terrestrial condition. Endocrinology 2010, 151:1089-1096.
38. Kulczykowska E. Arginine vasotocin and isotocin: towards their role in fish osmoregulation. Fish Osmoregulation 2007, 151-176. Science Publisher, Enfield, N.H. B. Baldisserotto, J.M. Mancero Romero, B.G. Kapoor (Eds.).
39. Larson E.T., O'Malley D.M., Melloni R.H. Aggression and vasotocin are associated with dominant-subordinate relationships in zebrafish. Behav. Brain Res. 2006, 167:94-102.
40. Lema S.C. Identification of multiple vasotocin receptor cDNAs in teleost fish: sequences, phylogenetic analysis, sites of expression, and regulation in the hypothalamus and gill in response to hyperosmotic challenge. Mol. Cell. Endocrinol. 2010, 321:215-230.
41. Lema S.C., Nevitt G.A. Exogenous vasotocin alters aggression during agonistic exchanges in male Amargosa River pupfish (Cyprinodon nevadensis amargosae). Horm. Behav. 2004, 46:628-637.
42. Lema S.C., Wagstaff L.J., Gardner N.M. Diurnal rhythms of behavior and brain mRNA expression for argininevasotocin, isotocin, and their receptors in wild Amargosa pupfish (Cyprinodon nevadensis amargosae). Mar. Freshwater Behav. Physiol. 2010, 43:257-281.
43. Ludwig M., Leng G. Dendritic peptide release and peptide-dependent behaviours. Nat. Rev. Neurosci. 2006, 7:126-136.
44. McEwen B.B. The roles of vasopressin and oxytocin in memory processing. Adv. Pharmacol. 2004, 50:1-740.
45. Neil E.H. An analysis of colour changes and social behaviour of Tilapia mossambica. Univ. Calif. Publ. Zool. 1964, 75:1-58.
46. Oliveira, R.F. 1995. Etologia social e endocrinologia comportamental da tilapia Oreochromis mossambicus (Teleostei, Cichlidae). Ph.D. Thesis, University of Lisbon, Lisbon.
47. Oliveira, R.F. 2006. Neuroendocrine mechanisms of alternative reproductive tactics in fish. In: K.A. Sloman, R.W. Wilson, S. Balshine (Guest Editors; W.S. Hoar, D.J. Randall, A.P. Farrell, Series editors), Fish Physiology, vol. 24: Behaviour: Interactions with Physiology. Elsevier, New York.
48. Oliveira R.F., Almada V.C. Dominance hierarchies and social structure in captive groups of the Mozambique tilapia Oreochromis mossambicus (Teleostei: Cichlidae). Ethol. Ecol. Evol. 1996, 8:39-55.
49. Oliveira R.F., Almada V.C. On the (In)stability of dominance hierarchies in the cichlid fish Oreochromis mossambicus. Aggress. Behav. 1996, 22:37-45.
50. Oliveira R.F., Almada V.C. Mating tactics and male-male courtship in the lek-breeding cichlid Oreochromis mossambicus. J. Fish Biol. 1998, 52:1115-1129.
51. Oliveira R.F., Almada V.C., Canario A.V.M. Social modulation of sex steroid concentrations in the urine of male cichlid fish Oreochromis mossambicus. Horm. Behav. 1996, 30:2-12.
52. Pickford G.E., Strecker E.L. The spawning reflex response of the killifish, Fundulus heteroclitus: isotocin is relatively inactive in comparison with arginine vasotocin. Gen. Comp. Endocrinol. 1977, 32:132-137.
53. Saito D., Urano A. Synchronized periodic Ca2+ pulses define neurosecretory activities in magnocellular vasotocin and isotocin neurons. J. Neurosci. 2001, 21:178.
54. Saito D., Komatsuda M., Urano A. Functional organization of preoptic vasotocin and isotocin neurons in the brain of rainbow trout: central and neurohypophysial projections of single neurons. Neuroscience 2004, 124:973-984.
55. Salek S.J., Sullivan C.V., Godwin J. Arginine vasotocin effects on courtship behavior in male white perch (Morone americana). Behav. Brain Res. 2002, 133:177-183.
56. Santangelo N., Bass A.H. New insights into neuropeptide modulation of aggression: field studies of arginine vasotocin in a territorial tropical damselfish. Proc. R. Soc. Lond. 2006, 273:3085-3092.
57. Semsar K., Kandel F.L., Godwin J. Manipulations of the AVT system shift social status and related courtship and aggressive behavior in the bluehead wrasse. Horm. Behav. 2001, 40:21-31.
58. Stacey N.E., Sorensen P.W. Hormonal sex pheromones in fish. Hormones, Brain, and Behavior 2002, 375-434. Editors Academic Press, New York. D.W. Pfaff, A.P. Arnold, A.M. Etgen, S.E. Fahrbach, R.T. Rubin (Eds.).
59. StatSoft, Inc. STATISTICA (data analysis software system), version 10 http://www.statsoft.com.
60. Taborsky M. Bourgeois and parasitic tactics: do we need collective, functional terms for alternative reproductive behaviours?. Behav. Ecol. Sociobiol. 1997, 41:361-362.
61. Thompson R.R., Walton J.C. Peptide effects on social behavior: effects of vasotocin and isotocin on social approach behavior in male goldfish (Carassius auratus). Behav. Neurosci. 2004, 118:620-626.
62. Thompson R.R., Walton J.C. Vasotocin immunoreactivity in goldfish brains: characterizing primitive circuits associated with social regulation. Brain Behav. Evol. 2009, 73:153-164.
63. Thompson R.R., Walton J.C., Bhalla R., George K.C., Beth E.H. A primitive social circuit: vasotocin-substance P interactions modulate social behavior through a peripheral feedback mechanism in goldfish. Eur. J. Neurosci. 2008, 27(9):2285-2293.
64. Tobin V.A., Hashimoto H., Wacker D.W., Takayanagi Y., Langnaese K., Caquineau C., Noack J., Landgraf R., Onaka T., Leng G., Meddle S.L., Engelmann M., Ludwig M. An intrinsic vasopressin system in the olfactory bulb is involved in social recognition. Nature 2010, 464:413-417.
65. Wacker D.W., Tobin V.A., Noack J., Bishop V.R., Duszkiewicz A.J., Engelmann M., Meddle S.L., Ludwig M. Expression of early growth response protein 1 in vasopressin neurones of the rat anterior olfactory nucleus following social odour exposure. J. Physiol. 2010, 588:4705-4717.
66. Wacker D.W., Engelmann M., Tobin V.A., Meddle S.L., Ludwig M. Vasopressin and social odor processing in the olfactory bulb and anterior olfactory nucleus. Ann. N. Y. Acad. Sci. 2011, 1220:106-116.
67. Warne J.M., Harding K.E., Balment R.J. Neurohypophysial hormones and renal function in fish and mammals. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2002, 132:231-237.
68. Wullimann M.F., Mueller T. Teleostean and mammalian forebrains contrasted: evidence from genes to behavior. J. Comp. Neurol. 2004, 475:143-162.