Timing is crucial for social interactions. Animal behavior is synchronized with biotic and abiotic environment variables ensuring that the activity phase of conspecifics occurs during the same period of the day. As biological rhythms are embedded in the complex integrative control of the brain, it is fundamental to explore its interaction with environmental and social factors. This approach will unravel the link between external stimuli carrying information on environmental cycles and the neural commands for behavior, including social behavior, associated with precise phases of those cycles. Arousal in the solitary Gymnotus omarorum and in the gregarious Brachyhypopomus gauderio is characterized by a nocturnal increase in the basal discharge rate of electric behavior, which is mild and transient in G. omarorum and large and persistent in B. gauderio. In this study, we show that the major integrator of social behavior, AVT (arginine vasotocin), is not involved in the nocturnal increase of electric behavior basal rate in isolated animals of either species. On the other hand, endogenous melatonin, the major modulator of the circadian system, is responsible for the nocturnal increase in electric behavior in isolated individuals of both species.

Keywords:
Melatonin, Sociality, Behavior, Nocturnality, Vasotocin, Electric fish, Gymnotus omarorum, Brachyhypopomus gauderio, Circadian rhythms
1.
Aguilera PA, Castello ME, Caputi AA (2001): Electroreception in Gymnotus carapo: differences between self-generated and conspecific-generated signal carriers. J Exp Biol 204:185-198.
2.
Ben-Zaken I, Haim A, Zubidat AE (2013): Long-day photoperiod interacts with vasopressin and food restriction to modulate reproductive status and vasopressin receptor expression of male golden spiny mice. J Exp Biol 216:3495-3503.
3.
Bennett MV, Pappas GD, Aljure E, Nakajima Y (1967): Physiology and ultrastructure of electrotonic junctions. II. Spinal and medullary electromotor nuclei in mormyrid fish. J Neurophysiol 30:180-208.
4.
Boyd SK (2013): Vasotocin modulation of social behaviors in amphibians; in Pfaff DW, Choleris E (eds): Oxytocin, Vasopressin and Related Peptides in the Regulation of Behavior. Cambridge, Cambridge University Press, pp 97-109.
5.
Capurro A (1994): Respuesta de novedad en Gymnotus carapo: La frecuencia de un oscilador biológico como manifestación conductua; master thesis, Montevideo.
6.
Caputi A, Carlson B, Macadar O (2005): Electric organs and their control; in Bullock T, Hopkins C, Popper A, Fay R (eds): Electroreception. New York, Springer, vol 21, pp 410-451.
7.
Cassone VM, Westneat DF (2011): The bird of time: cognition and the avian biological clock. Front Mol Neurosci 5:32.
8.
Dewan AK, Maruska KP, Tricas TC (2008): Arginine vasotocin neuronal phenotypes among congeneric territorial and shoaling reef butterflyfishes: species, sex and reproductive season comparisons. J Neuroendocrinol 20:1382-1394.
9.
Engler G, Zupanc GK (2001): Differential production of chirping behavior evoked by electrical stimulation of the weakly electric fish, apteronotus leptorhynchus. J Comp Physiol A 187:747-756.
10.
Falcon J, Migaud H, Munoz-Cueto JA, Carrillo M (2010): Current knowledge on the melatonin system in teleost fish. Gen Comp Endocrinol 165:469-482.
11.
Franchina CR, Salazar VL, Volmar CH, Stoddard PK (2001): Plasticity of the electric organ discharge waveform of male Brachyhypopomus pinnicaudatus. II. Social effects. J Comp Physiol A 187:45-52.
12.
Franchina CR, Stoddard PK (1998): Plasticity of the electric organ discharge waveform of the electric fish Brachyhypopomus pinnicaudatus. I. Quantification of day-night changes. J Comp Physiol A 183:759-768.
13.
Freeman SM, Young L (2013): Oxytocin, vasopressin, and the evolution of mating systems in mammals; in Pfaff DW, Choleris E (eds): Oxytocin, Vasopressin and Related Peptides in the Regulation of Behavior. Cambridge, Cambridge University Press, pp 128-147.
14.
Gavassa S, Goldina A, Silva AC, Stoddard PK (2013): Behavioral ecology, endocrinology and signal reliability of electric communication. J Exp Biol 216:2403-2411.
15.
Giora J, Malabarba LR (2009): Brachyhypopomus gauderio, new species, a new example of underestimated species diversity of electric fishes in the southern South America (Gymnotiformes: Hypopomidae). Zootaxa 2093:60-68.
16.
Goodson JL (2008): Nonapeptides and the evolutionary patterning of sociality. Prog Brain Res 170:3-15.
17.
Goodson JL, Bass AH (2000): Forebrain peptides modulate sexually polymorphic vocal circuitry. Nature 403:769-772.
18.
Goodson JL, Kingsbury MA (2013): What's in a name? Considerations of homologies and nomenclature for vertebrate social behavior networks. Horm Behav 64:103-112.
19.
Howard CM, Lutterschmidt DI (2015): The effects of melatonin on brain arginine vasotocin: relationship with sex and seasonal differences in melatonin receptor type 1 in green treefrogs (Hyla cinerea). J Neuroendocrinol 27:670-679.
20.
Hurd MW, Debruyne J, Straume M, Cahill GM (1998): Circadian rhythms of locomotor activity in zebrafish. Physiol Behav 65:465-472.
21.
Insel TR, Young LJ (2001): The neurobiology of attachment. Nat Rev Neurosci 2:129-136.
22.
Jansen K, van der Zee EA, Gerkema MP (2000): Being circadian or not: vasopressin release in cultured SCN mirrors behavior in adult voles. Neuroreport 11:3555-3558.
23.
Jun JJ, Longtin A, Maler L (2014): Enhanced sensory sampling precedes self-initiated locomotion in an electric fish. J Exp Biol 217:3615-3628.
24.
Kronfeld-Schor N, Bloch G, Schwartz WJ (2013): Animal clocks: when science meets nature. Proc Biol Sci 280:20131354.
25.
Lima-Cabello E, Díaz-Casado ME, Guerrero JA, Otalora BB, Escames G, López LC, Reiter RJ, Acuña-Castroviejo D (2014): A review of the melatonin functions in zebrafish physiology. J Pineal Res 57:1-9.
26.
Lissmann HW (1958): On the function and evolution of electric organs in fish. J Exp Biol 35:156-191.
27.
Lutterschmidt DI, Wilczynski W (2012): Sexually dimorphic effects of melatonin on brain arginine vasotocin immunoreactivity in green treefrogs (Hyla cinerea). Brain Behav Evol 80:222-232.
28.
Maitra SK, Chattoraj A, Mukherjee S, Moniruzzaman M (2012): Melatonin: a potent candidate in the regulation of fish oocyte growth and maturation. Gen Comp Endocrinol 181:215-222.
29.
Maruska KP (2009): Sex and temporal variations of the vasotocin neuronal system in the damselfish brain. Gen Comp Endocrinol 160:194-204.
30.
Merrow M, Spoelstra K, Roenneberg T (2005): The circadian cycle: daily rhythms from behaviour to genes: first in the cycles review series. EMBO Rep 6:930-935.
31.
Miranda M, Silva A, Stoddard P (2008): Use of space as an indicator of social behavior and breeding systems in the gymnotiform electric fish Brachyhypopomus pinnicaudatus. Environ Biol Fish 83:379-389.
32.
Nelson ME, MacIver MA (2006): Sensory acquisition in active sensing systems. J Comp Physiol A 192:573-586.
33.
O'Connell LA, Hofmann HA (2012): Evolution of a vertebrate social decision-making network. Science 336:1154-1157.
34.
Perrone R (2012): La vasotocina modula el comportamiento social de dos especies de peces eléctricos con diferente socialidad; PhD thesis, Montevideo.
35.
Perrone R, Batista G, Lorenzo D, Macadar O, Silva A (2010): Vasotocin actions on electric behavior: interspecific, seasonal, and social context-dependent differences. Front Behav Neurosci 4:52.
36.
Perrone R, Migliaro A, Comas V, Quintana L, Borde M, Silva A (2014): Local vasotocin modulation of the pacemaker nucleus resembles distinct electric behaviors in two species of weakly electric fish. J Physiol Paris 108:203-212.
37.
Post N, von der Emde G (1999): The ‘novelty response' in an electric fish: response properties and habituation. Physiol Behav 68:115-128.
38.
Richer-de-Forges MM, Crampton WGR, Albert JS (2009): A new species of Gymnotus (Gymnotiformes, Gymnotidae) from Uruguay: description of a model species in neurophysiological research. Copeia 2009:538-544.
39.
Rodríguez-Illamola A, López Patiño MA, Soengas JL, Ceinos RM, Míguez JM (2011): Diurnal rhythms in hypothalamic/pituitary AVT synthesis and secretion in rainbow trout: evidence for a circadian regulation. Gen Comp Endocrinol 170:541-549.
40.
Salazar VL, Stoddard PK (2008): Sex differences in energetic costs explain sexual dimorphism in the circadian rhythm modulation of the electrocommunication signal of the gymnotiform fish Brachyhypopomus pinnicaudatus. J Exp Biol 211:1012-1020.
41.
Silva A, Perrone R, Macadar O (2007): Environmental, seasonal, and social modulations of basal activity in a weakly electric fish. Physiol Behav 90:525-536.
42.
Silva A, Perrone R, Zubizarreta L, Batista G, Stoddard PK (2013): Neuromodulation of the agonistic behavior in two species of weakly electric fish that display different types of aggression. J Exp Biol 216:2412-2420.
43.
Silva A, Quintana L, Galeano M, Errandonea P (2003): Biogeography and breeding in Gymnotiformes from Uruguay. Environ Biol Fish 66:329-338.
44.
Stoddard PK (2002): The evolutionary origins of electric signal complexity. J Physiol Paris 96:485-491.
45.
Stoddard PK, Markham MR, Salazar VL, Allee S (2007): Circadian rhythms in electric waveform structure and rate in the electric fish Brachyhypopomus pinnicaudatus. Physiol Behav 90:11-20.
46.
Thompson RR, Walton JC (2009): Vasotocin immunoreactivity in goldfish brains: characterizing primitive circuits associated with social regulation. Brain Behav Evol 73:153-164.
47.
Zhdanova IV, Reebs SG (2006): Circadian rhythms in fish; in Sloman KA, Wilson RW, Blashine S (eds): Fish Physiology: Behaviour and Physiology of Fish. New York, Elsevier, vol 24, p 41.
48.
Zhdanova IV, Tucci V (2003): Melatonin, circadian rhythms, and sleep. Curr Treat Options Neurol 5:225-229.
© 2016 S. Karger AG, Basel
2016
Copyright / Drug Dosage / Disclaimer
Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
You do not currently have access to this content.