Skip to main content
Log in

Social context affects aggression and brain vasotocin and isotocin level in the round goby

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

On the wild spawning grounds, the round gobies Neogobius melanostomus are subjected to different social cues, such as sex-separation and high fish density. We designed an experiment to stimulate natural social stress when fish are separated from opposite sex individuals and exposed to close proximity of same-sex conspecifics. We examined the effects of different sex compositions on aggressiveness and brain concentrations of arginine vasotocin (AVT) and isotocin (IT), as AVT and IT are known to be involved in aggressive interactions during reproduction. The round gobies were kept in three experimental groups: same-sex groups broken down into male-only and female-only groups and mixed-sex groups. In this study, males and females from same-sex groups showed overt aggression and competition. Separation stress stimulated aggressive responses in both sexes, but the link between brain AVT and IT concentration and aggressive behavior was evident only in male-only group. In the male-only group, AVT and IT levels were the highest. This study shows that sex composition of the social environment can affect aggressive behavior as well as AVT and IT concentration in the whole brain of the round goby.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Almeida O, Oliveira RF (2015) Social status and arginine vasotocin neuronal phenotypes in a cichlid fish. Brain Behav Evol 85:203–213

    PubMed  Google Scholar 

  • Aste N, Sakamoto E, Kagami M, Saito N (2013) Vasotocin mRNA expression is sensitive to testosterone and oestradiol in the bed nucleus of the stria terminalis in female Japanese quail. J Neuro-Oncol 25:811–825

    CAS  Google Scholar 

  • Aubin-Horth N, Desjardins JK, Martei YM, Balshine S, Hofmann HA (2007) Masculinized dominant females in a cooperatively breeding species. Mol Ecol 16:1349–1358

    PubMed  Google Scholar 

  • Balshine S, Leach B, Reid H, Taborsky M, Werner N (2001) Correlates of group size in a cooperatively breeding cichlid fish (Neolamprologus pulcher). Behav Ecol Sociobiol 50:134–140

    Google Scholar 

  • Balthazart J, Absil P, Viglietti-Panzica C, Panzica GC (1997) Vasotocinergic innervation of areas containing aromatase-immunoreactive cells in the quail forebrain. J Neurobiol 33:45–60

    CAS  PubMed  Google Scholar 

  • Bertucci F, Matos RJ, Dabelsteen T (2014) Knowing your audience affects male-male interactions in Siamese fighting fish (Betta splendens). Anim Cogn 17:229–236

    PubMed  Google Scholar 

  • Bond H, Warne JM, Balment RJ (2007) Effect of acute restraint on hypothalamic pro-vasotocin mRNA expression in flounder, Platichthys flesus. Gen Comp Endocrinol 153:221–227

    CAS  PubMed  Google Scholar 

  • Boyd SK (1994) Gonadal steroid modulation of vasotocin concentrations in the bullfrog brain. Neuroendocrinology 60:150–156

    CAS  PubMed  Google Scholar 

  • Brown-Peterson NJ, Wyanski DM, Saborido-Rey F, Macewicz BJ, Lowerre-Barbieri SK (2011) A standardized terminology for describing reproductive development in fishes. Mar Coast Fish 3:52–70

    Google Scholar 

  • Cádiz L, Román-Padilla J, Gozdowska M, Kulczykowska E, Martìnez-Rodrìguez G, Mancera JM, Martos-Sitcha JA (2015) Cortisol modulates vasotocinergic and isotocinergic pathways in the gilthead sea bream. J Exp Biol 218:1–10

    Google Scholar 

  • Capelle PM, McCallum ES, Balshine S (2015) Aggression and sociality: conflicting or complementary traits of a successful invader? Behaviour 152:127–146

    Google Scholar 

  • Charlebois PM, Marsden JE, Goettel RG, Wolfe RK, Jude DJ, Rudnicka S (1997) The round goby, Neogobius melanostomus (Pallas), a review of European and North American literature. Illinois-Indiana Sea Grant Program and Illinois Natural History Survey INHS Special Publication No 20, 76 pp.

  • Corkum LD, MacInnis AJ, Wickett RG (1998) Reproductive habits of round gobies. Great Lakes Res Rev 3:13–20

    Google Scholar 

  • Corkum LD, Sapota MR, Skóra KE (2004) The round goby, Neogobius melanostomus, a fish invader on both sides of the Atlantic Ocean. Biol Invasions 6:173–181

    Google Scholar 

  • Dewan AK, Tricas TC (2011) Arginine vasotocin neuronal phenotypes and their relationship to aggressive behavior in the territorial monogamous multiband butterfly fish, Chaetodon multicinctus. Brain Res 1401:74–84

    CAS  PubMed  Google Scholar 

  • Dzieweczynski TL, Gill CE, Perazio CE (2012) Opponent familiarity influences the audience effect in male-male interactions in Siamese fighting fish. Anim Behav 83:1219–1224

    Google Scholar 

  • Dzieweczynski TL, Perazio CE (2012) I know you: familiarity with an audience influences male-male interactions in Siamese fighting fish, Betta splendens. Behav Ecol Sociobiol 66:1277–1284

    Google Scholar 

  • Gilchriest BJ, Tipping DR, Hake L, Levy A, Baker BI (2000) The effects of acute and chronic stresses on vasotocin gene transcripts in the brain of the rainbow trout (Oncorhynchus mykiss). J Neuroendocrinol 12:795–801

    CAS  PubMed  Google Scholar 

  • Godwin J, Thompson R (2012) Nonapeptides and social behavior in fishes. Horm Behav 61:230–238

    CAS  PubMed  Google Scholar 

  • Goodson JL, Thompson RR (2010) Nonapeptide mechanisms of social cognition, behavior and species-specific social systems. Curr Opin Neurobiol 20:784–794

    CAS  PubMed  Google Scholar 

  • Greenwood AK, Wark AR, Fernald RD, Hofmann HA (2008) Expression of arginine vasotocin in distinct preoptic regions is associated with dominant and subordinate behaviour in an African cichlid fish. Proc R Soc B 275:2393–2402

    PubMed  Google Scholar 

  • Hillsman KD, Sanderson NS, Crews D (2007) Testosterone stimulates mounting behavior and arginine vasotocin expression in the brain of both sexual and unisexual whiptail lizards. Sex Dev 1:77–84

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kleszczyńska A, Sokołowska E, Kulczykowska E (2012) Variation in brain arginine vasotocin (AVT) and isotocin (IT) levels with reproductive stage and social status in males of three-spined stickleback (Gasterosteus aculeatus). Gen Comp Endocrinol 175:290–296

    PubMed  Google Scholar 

  • Kleszczyńska A, Kulczykowska E (2013) Stocking density influences brain arginine vasotocin (AVT) and isotocin (IT) levels in males and females of three-spined stickleback (Gasterosteus aculeatus). Gen Comp Endocrinol 183:14–16

    PubMed  Google Scholar 

  • Kovtun IF (1977) On the fecundity of the round goby, Gobius melanostomus, from the Sea of Azov. J Ichthyol 17:566–573

    Google Scholar 

  • Kovtun IF (1980) Significance of the sex ratio in the spawning population of the round goby, Neogobius melanostomus, in relation to year-class strength in the Sea of Azov. J Ichthyol 19:161–163

    Google Scholar 

  • Kulczykowska E (2008) Arginine vasotocin and isotocin as multifunctional hormones, neurotransmitters and neuromodulators in fish. In: AVANCES en Endocrinologìa Comparada. Munoz-Cueto, J.A., Mancera, J.M., Martìnez-Rodrìguez, G. (Eds). Servicio de Publicaciones, Universidad de Cádiz, Spain, vol. IV, ISBN 978-84-9828-152-1, pp 41–47

  • Kulczykowska E, Kleszczyńska A (2014) Brain arginine vasotocin and isotocin in breeding female three-spined sticklebacks (Gasterosteus aculeatus): the presence of male and egg deposition. Gen Comp Endocrinol 204:8–12

    CAS  PubMed  Google Scholar 

  • Larson ET, O’Malley DM, Melloni RH Jr (2006) Aggression and vasotocin are associated with dominant-subordinate relationships in zebrafish. Behav Brain Res 167:94–102

    CAS  PubMed  Google Scholar 

  • Lema SC, Sanders KE, Walti KA (2015) Arginine vasotocin, isotocin and nonapeptide receptor gene expression link to social status and aggression in sex-dependent patterns. J Neuroendocrinol 27:142–157

    CAS  PubMed  Google Scholar 

  • Loveland JL, Fernald RD (2017) Differential activation of vasotocin neurons in contexts that elicit aggression and courtship. Behav Brain Res 317:188–203

    CAS  PubMed  Google Scholar 

  • Lynch MP, Mensinger AF (2013) Temporal patterns in growth and survival of the round goby Neogobius melanostomus. J Fish Biol 82:111–124

    CAS  PubMed  Google Scholar 

  • Maekawa F, Nagino K, Yang J, Htike NTT, Tsukahara S, Ubuka T, Tsutsui K, Kawashima T (2018) Strain differences in intermale aggression and possible factors regulating increased aggression in Japanese quail. Gen Comp Endocrinol 256:63–70

    CAS  PubMed  Google Scholar 

  • Mancera JM, Vargas-Chacoff L, García-López A, Kleszczyńska A, Kalamarz H, Martínez-Rodríguez G, Kulczykowska E (2008) High density and food deprivation affect arginine vasotocin, isotocin and melatonin in gilthead sea bream (Sparus auratus). Comp Biochem Physiol A 149:92–97

    Google Scholar 

  • Martos-Sitcha JA, Cádiz L, Gozdowska M, Kulczykowska E, Martínez-Rodríguez G, Mancera JM (2019) Arginine vasotocin and cortisol co-regulate vasotocinergic, isotocinergic, stress, and thyroid pathways in the gilthead sea bream (Sparus aurata). Front Physiol 10:261

    PubMed  PubMed Central  Google Scholar 

  • Meunier B, Yavno S, Ahmed S, Corkum LD (2009) First documentation of spawning and nest guarding in the laboratory by the invasive fish, the round goby (Neogobius melanostomus). J Great Lakes Res 35:608–612

    Google Scholar 

  • Miller PJ (1984) The tokology of gobioid fishes. In: Potts GW, Wootton RJ (eds) Fish reproduction: strategies and tactics. Academic Press, London, pp 119–153

    Google Scholar 

  • Miller PJ (1986) Gobiidae. In: Whitehead PJP, Bauchot ML, Hureau JC, Nielsen J, Tortonese E (eds) Fishes of the Northeast Atlantic and the Mediterranean. United Nations Educational, Scientific and Cultural Organization, Paris, pp 1019–1065

    Google Scholar 

  • Moskalkova KI (1996) Ecological and morphological prerequisites to range extention in the round goby Neogobius melanostomus under conditions of anthropogenic pollution. Vopr Ichtiologii 36:615–621 (in Russian)

    Google Scholar 

  • O’Connell LA, Matthews BJ, Hofmann HA (2012) Isotocin regulates paternal care in a monogamous cichlid fish. Horm Behav 61:725–733

    PubMed  Google Scholar 

  • Panzica GC, García-Ojeda E, Viglietti-Panzica C, Thompson NE, Ottinger MA (1996) Testosterone effects on vasotocinergic innervation of sexually dimorphic medial preoptic nucleus and lateral septum during aging in male quail. Brain Res 712:190–198

    CAS  PubMed  Google Scholar 

  • Panzica GC, Aste N, Castagna C, Viglietti-Panzica C, Balthazart J (2001) Steroid-induced plasticity in the sexually dimorphic vasotocinergic innervation of the avian brain: behavioral implications. Brain Res Brain Res Rev 37:178–200

    CAS  PubMed  Google Scholar 

  • Ray WJ, Corkum LD (2001) Habitat and site affinity of the round goby. J Great Lakes Res 27:329–334

    Google Scholar 

  • Reddon AR, O’Connor CM, Marsh-Rollo SE, Balshine S, Gozdowska M, Kulczykowska E (2015) Brain nonapeptide levels are related to social status and affiliative behaviour in a cooperatively breeding cichlid fish. R Soc Open Sci 2:140072

    PubMed  PubMed Central  Google Scholar 

  • Sapota MR (2004) The round goby (Neogobius melanostomus) in the Gulf of Gdańsk – a species introduction into the Baltic Sea. Hydrobiologia 514:219–224

    Google Scholar 

  • Sapota MR, Skóra KE (2005) Spread of alien (non-indigenous) fish species Neogobius melanostomus in the Gulf of Gdansk (south Balic). Biol Invasions 7:157–164

    Google Scholar 

  • Sapota MR (2005) Biology and ecology of round goby Neogobius melanostomus (Pallas 1811), invasive species in the Gulf of Gdańsk. Institute of Oceanography, University of Gdańsk, Habilitation thesis, p 117 (in Polish)

    Google Scholar 

  • Sapota MR, Bałazy P, Mirny Z (2014) Modification in the nest guarding strategy – one of the reasons of the round goby (Neogobius melanostomus) invasion success in the Gulf of Gdańsk? Oceanol Hydrobiol Stud 43:21–28

    Google Scholar 

  • Skrzynska AK, Gozdowska M, Kulczykowska E, Martìnez-Rodrìguez G, Mancera JM, Martos-Sitcha JA (2017) The effect of starvation and re-feeding on vasotocinergic and isotocinergic pathways in immature gilthead sea bream (Sparus aurata). J Comp Physiol B 187:945–958

    CAS  Google Scholar 

  • Sokołowska E, Kleszczyńska A, Kalamarz-Kubiak H, Arciszewski B, Kulczykowska E (2013) Changes in brain arginine vasotocin, isotocin, plasma 11-ketotestosterone and cortisol in round goby, Neogobius melanostomus, males subjected to overcrowding stress during the breeding season. Comp Biochem Phys A 165:237–242

    Google Scholar 

  • Solomon-Lane TK, Willis MC, Pradhan DS, Grober MS (2014) Female, but not male, agonistic behaviour is associated with male reproductive success in stable bluebanded goby (Lythrypnus dalli) hierarchies. Behaviour 151:1367–1387

    Google Scholar 

  • Taves MD, Desjardins JK, Mishra S, Balshine S (2009) Androgens and dominance: sex-specific patterns in a highly social fish (Neolamprologus pulcher). Gen Comp Endocrinol 161:202–207

    CAS  PubMed  Google Scholar 

  • Teles MC, Gozdowska M, Kalamarz-Kubiak H, Kulczykowska E, Oliveira RF (2016) Agonistic interactions elicit rapid changes in brain nonapeptide levels in zebrafish. Horm Behav 84:57–63

    CAS  PubMed  Google Scholar 

  • Viglietti-Panzica C, Anselmetti GC, Balthazart J, Aste N, Panzica GC (1992) Vasotocinergic innervation of the septal region in the Japanese quail: sexual differences and the influence of testosterone. Cell Tissue Res 267:261–265

    CAS  Google Scholar 

  • Viglietti-Panzica C, Aste N, Balthazart J, Panzica GC (1994) Vasotocinergic innervation of sexually dimorphic medial preoptic nucleus of the male Japanese quail: influence of testosterone. Brain Res 657:171–184

    CAS  PubMed  Google Scholar 

  • Wandzel T (2003) Round goby Neogobius melanostomus (Pallas, 1811) – new component of ichthyocenosis of the southern Baltic. Morski Instytut Rybacki, Gdynia, p 76 (in Polish)

    Google Scholar 

  • Wickett RG, Corkum LD (1998) Nest defense by the non-indigenous fish, the round goby, Neogobius melanostomus (Gobiidae), on a shipwreck in Western Lake Ontario. Can Field Nat 112:653–656

    Google Scholar 

  • Yaeger C, Ros AM, Cross V, DeAngelis RS, Stobaugh DJ, Rhodes JS (2014) Blockade of arginine vasotocin signaling reduces aggressive behavior and c-Fos expression in the preoptic area and periventricular nucleus of the posterior tuberculum in male Amphiprion ocellaris. Neuroscience 267:205–218

    CAS  PubMed  Google Scholar 

  • Yamashita J, Kawabata Y, Okubo K (2017) Expression of isotocin is male-specifically up-regulated by gonadal androgen in the medaka brain. J Neuroendocrinol 29(12):e12545

    Google Scholar 

Download references

Acknowledgments

We would like to thank A. Kleszczyńska for determining the neuropeptides levels. We would like to express our gratitude to Head of the Hel Marine Station (Institute of Oceanography, University of Gdańsk) for the use of facility and equipment of the station during the experiment. We also thank B. Arciszewski from Hel Marine Station, and their students, K. Urbańska, D. Pachoł and D. Danił, for their efficient help in monitoring the experiment and assistance in sampling the fish. We thank Cambridge Proof-Reading-Service for their great professional proof reading and editing service.

Funding

This study was funded by the National Science Centre grant no. N N304 260740 and Institute of Oceanology of the Polish Academy of Sciences (statutory research task IV.2.1 to E. Sokołowska).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ewa Sokołowska.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures were carried out according to the regulations of the Polish Ethical Council for the use of laboratory animals.

Additional information

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

Sokołowska, E., Gozdowska, M. & Kulczykowska, E. Social context affects aggression and brain vasotocin and isotocin level in the round goby. Fish Physiol Biochem 46, 641–652 (2020). https://doi.org/10.1007/s10695-019-00741-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-019-00741-3

Keywords

Navigation