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To pee or not to pee: urine signals mediate aggressive interactions in the cooperatively breeding cichlid Neolamprologus pulcher

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Abstract

The communication of aggressive propensity is an important component of agonistic interactions. For this purpose, animals use different sensory modalities involving visual, acoustical and chemical cues. While visual and acoustic communication used in aggressive encounters has been studied extensively in a wide range of taxa, the role of chemical communication received less attention. Here, we studied the role of chemical cues used during agonistic interactions of territory owners in the cooperative cichlid Neolamprologus pulcher. During staged encounters, we allowed either visual and chemical contact between two contestants or visual contact only. As chemical information in this species is most likely transferred via urine, we measured urination patterns using dye injections. Furthermore, we recorded aggressive and submissive behaviours of both contestants in response to the experimental treatment. Fish that had only visual contact with each other significantly increased their urination frequency and showed more aggressive displays compared to fish with both visual and chemical contact. Furthermore, appropriate agonistic responses appear to be dependent on available chemical information. This indicates that N. pulcher actively emits chemical signals to communicate their aggressive propensity via urine. Chemical communication thus plays a crucial role in multimodal communication of aggression in these fish, which highlights the need of studying the role of chemical communication during agonistic encounters in general, even if other signals are more obvious to the human observer.

Significance statement

The communication of aggressive tendencies can be achieved by transmitting visual, acoustical and chemical information. In this context chemical communication received less attention than other modalities thus far. We studied the importance of chemical information released via urine during agonistic encounters in the cooperatively breeding cichlid N. pulcher. Using dye injections, we measured urination patterns as well as the aggressive and submissive behaviours of two contestants. We show that N. pulcher actively signals aggressive tendencies via altered urination patterns. Furthermore, we show that appropriate agonistic responses appear to be dependent on the availability of such chemical information. Thus, our results suggest that chemical communication plays a crucial role in multimodal communication of aggression in these fish. These findings highlight the importance of chemical communication during agonistic encounters in general, even if other signals are more obvious to the human observer.

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References

  • Almeida OG, Miranda A, Frade P, Hubbard PC, Barata EN, Canário AVM (2005) Urine as a social signal in the Mozambique tilapia (Oreochromis mossambicus). Chem Senses 30:309–310

    Article  Google Scholar 

  • Appelt CW, Sorensen PW (1999) Freshwater fish release urinary pheromones in a pulsatile manner. In: Johnston RE, Müller-Schwarze D, Sorensen PW (eds) Advances in chemical signals in vertebrates. Plenum Press, New York, pp 247–256

    Chapter  Google Scholar 

  • Arnott G, Elwood RW (2009) Gender differences in aggressive behaviour in convict cichlids. Anim Behav 78:1221–1227

    Article  Google Scholar 

  • ASAB (2012) Guidelines for the treatment of animals in behavioural research and teaching. Anim Behav 83:301–309

    Article  Google Scholar 

  • Auffarth B (2013) Understanding smell—the olfactory stimulus problem. Neurosci Biobehav Rev 37:1667–1679

    Article  PubMed  Google Scholar 

  • Aureli F, Cords M, van Schaik CP (2002) Conflict resolution following aggression in gregarious animals: a predictive framework. Anim Behav 64:325–343

    Article  Google Scholar 

  • Bakker TCM (1984) Two-way selection for aggression in juvenile female and male sticklebacks (Gasterosteus aculeatus), with some notes on hormonal factors. Behaviour 93:69–81

    Article  Google Scholar 

  • Balshine S, Leach B, Neat F, 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

    Article  Google Scholar 

  • Balshine-Earn S, McAndrew BJ (1995) Sex-role reversal in the black-chinned tilapia, Sarotherodon melanotheron (Rüppel) (Cichlidae). Behaviour 132:861–874

    Article  Google Scholar 

  • Balzarini V, Taborsky M, Wanner S, Koch F, Frommen JG (2014) Mirror, mirror on the wall: the predictive value of mirror tests for measuring aggression in fish. Behav Ecol Sociobiol 68:871–878

    Article  Google Scholar 

  • Balzarini V, Taborsky M, Villa F, Frommen JG (2016) Computer animations of color markings reveal the function of visual threat signals in Neolamprologus pulcher. Curr Zool (published online, doi: 10.1093/cz/zow086)

  • Barata EN, Hubbard PC, Almeida OG, Miranda A, Canário AVM (2007) Male urine signals social rank in the Mozambique tilapia (Oreochromis mossambicus). BMC Biol 5:54

    Article  PubMed  PubMed Central  Google Scholar 

  • Barata EN, Fine JM, Hubbard PC, Almeida OG, Frade P, Sorensen PW, Canário AVM (2008) A sterol-like odorant in the urine of Mozambique tilapia males likely signals social dominance to females. J Chem Ecol 34:438–449

    Article  CAS  PubMed  Google Scholar 

  • Bates D, Mächler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  • Beeching SC (1992) Visual assessment of relative body size in a cichlid fish, the Oscar, Astronotus ocellatus. Ethology 90:177–186

    Article  Google Scholar 

  • Bergmüller R, Heg D, Peer K, Taborsky M (2005) Extended safe havens and between-group dispersal of helpers in a cooperatively breeding cichlid. Behaviour 142:1643–1667

    Article  Google Scholar 

  • Bolker BM, Skaug H, Laake J (2015) R2admb: “ADMB” to R interface functions. R package version:0.7.13 http://CRAN.R-project.org/package=R2admb

  • Boyle KS, Tricas TC (2014) Discrimination of mates and intruders: visual and olfactory cues for a monogamous territorial coral reef butterflyfish. Anim Behav 92:33–43

    Article  Google Scholar 

  • Bryant BP, Atema J (1987) Diet manipulation affects social behavior of catfish: importance of body odor. J Chem Ecol 13:1645–1661

    Article  CAS  PubMed  Google Scholar 

  • Derex M, Godelle B, Raymond M (2014) How does competition affect the transmission of information? Evol Hum Behav 35:89–95

    Article  Google Scholar 

  • Desjardins JK, Hazelden MR, Van der Kraak GJ, Balshine S (2005) Male and female cooperatively breeding fish provide support for the “Challenge Hypothesis.”. Behav Ecol 17:149–154

    Article  Google Scholar 

  • Dey CJ, Reddon AR, O’Connor CM, Balshine S (2013) Network structure is related to social conflict in a cooperatively breeding fish. Anim Behav 85:395–402

    Article  Google Scholar 

  • Drews C (1993) The concept and definition of dominance in animal behaviour. Behaviour 125:283–313

    Article  Google Scholar 

  • East ML, Dehnhard M (eds) (2013) Chemical signals in vertebrates 12. Springer, New York

  • Engqvist L (2005) The mistreatment of covariate interaction terms in linear model analyses of behavioural and evolutionary ecology studies. Anim Behav 70:967–971

    Article  Google Scholar 

  • Frade P, Hubbard PC, Barata EN, Canário AVM (2002) Olfactory sensitivity of the Mozambique tilapia to conspecific odours. J Fish Biol 61:1239–1254

    Article  Google Scholar 

  • Frostman P, Sherman PT (2004) Behavioral response to familiar and unfamiliar neighbors in a territorial cichlid, Neolamprologus pulcher. Ichthyol Res 51:283–285

    Article  Google Scholar 

  • Galef BG, Giraldeau L-A (2001) Social influences on foraging in vertebrates: causal mechanisms and adaptive functions. Anim Behav 61:3–15

    Article  PubMed  Google Scholar 

  • Gese EM, Ruff RL (1997) Scent-marking by coyotes, Canis latrans: the influence of social and ecological factors. Anim Behav 54:1155–1166

    Article  CAS  PubMed  Google Scholar 

  • Giaquinto PC, Volpato GL (1997) Chemical communication, aggression, and conspecific recognition in the fish Nile tilapia. Physiol Behav 62:1333–1338

    Article  CAS  PubMed  Google Scholar 

  • Giaquinto PC, Volpato GL (2005) Chemical cues related to conspecific size in pintado catfish, Pseudoplatystoma coruscans. Acta Ethol 8:65–69

    Article  Google Scholar 

  • Groenewoud F, Frommen JG, Josi D, Tanaka H, Jungwirth A, Taborsky M (2016) Predation risk drives social complexity in cooperative breeders. P Natl Acad Sci USA 113:4104–4109

    Article  CAS  Google Scholar 

  • Hand JL (1986) Resolution of social conflicts: dominance, egalitarianism, spheres of dominance, and game theory. Q Rev Biol 61:201–220

    Article  Google Scholar 

  • Hardy IC, Briffa M (2013) Animal contests. Cambridge University Press, Cambridge

  • Hasson O (1994) Cheating signals. J Theor Biol 167:223–238

    Article  Google Scholar 

  • Hauser MD (1996) Evolution of communication. MIT Press, Cambridge

  • Heymann EW (2006) Scent marking strategies of New World primates. Am J Primatol 68:650–661

    Article  PubMed  Google Scholar 

  • Hirschenhauser K, Taborsky M, Oliveira T, Canário AVM, Oliveira RF (2004) A test of the 'challenge hypothesis' in cichlid fish: simulated partner and territory intruder experiments. Anim Behav 68:741–750

    Article  Google Scholar 

  • Hirschenhauser K, Canário AVM, Ros AFH, Taborsky M, Oliveira RF (2008) Social context may affect urinary excretion of 11-ketotestosterone in African cichlids. Behaviour 145:1367–1388

    Article  Google Scholar 

  • Huck UW, Banks EM, Wang SC (1981) Olfactory discrimination of social status in the brown lemming. Behav Neural Biol 33:364–371

    Article  Google Scholar 

  • Hurd PL, Enquist M (2001) Threat display in birds. Can J Zool 79:931–942

    Article  Google Scholar 

  • Jordan NR (2007) Scent-marking investment is determined by sex and breeding status in meerkats. Anim Behav 74:531–540

    Article  Google Scholar 

  • Jordan NR, Cherry MI, Manser MB (2007) Latrine distribution and patterns of use by wild meerkats: implications for territory and mate defence. Anim Behav 73:613–622

    Article  Google Scholar 

  • Keller-Costa T, Lopes O, Almeida O (2012) Muscular hypertrophy of urinary bladders in dominant tilapia facilitates the control of aggression through urinary signals. Behaviour 149:953–975

    Article  Google Scholar 

  • Keller-Costa T, Canario AVM, Hubbard PC (2015) Chemical communication in cichlids: a mini-review. Gen Comp Endocrinol 221:64–74

    Article  CAS  PubMed  Google Scholar 

  • Maruska KP, Fernald RD (2012) Contextual chemosensory urine signaling in an African cichlid fish. J Exp Biol 215:68–74

    Article  PubMed  PubMed Central  Google Scholar 

  • Maynard Smith J, Harper D (2003) Animal Signals. Oxford University Press, Oxford

  • Mehlis M, Bakker TCM, Frommen JG (2008) Smells like sib spirit: kin recognition in three-spined sticklebacks (Gasterosteus aculeatus) is mediated by olfactory cues. Anim Cogn 11:643–650

    Article  PubMed  Google Scholar 

  • Mehlis M, Bakker TCM, Langen K, Frommen JG (2009) Cain and Abel reloaded? Kin recognition and male-male aggression in three-spined sticklebacks Gasterosteus aculeatus L. J Fish Biol 75:2154–2162

    Article  CAS  PubMed  Google Scholar 

  • Otovic P, Partan S (2009) Multimodal signaling in animals. In: Squire LR (ed) Encyclopedia of neuroscience. Academic Press, Oxford, pp 1095–1105

    Chapter  Google Scholar 

  • Pal SK (2003) Urine marking by free-ranging dogs (Canis familiaris) in relation to sex, season, place and posture. Appl Anim Behav Sci 80:45–59

    Article  Google Scholar 

  • Parker GA (1974) Assessment strategy and the evolution of fighting behaviour. J Theor Biol 47:223–243

    Article  CAS  PubMed  Google Scholar 

  • Partan S, Marler P (1999) Communication goes multimodal. Science 283:1272–1273

    Article  CAS  PubMed  Google Scholar 

  • Péter A (2015) Solomon Coder© A simple and free solution for behavior coding, www.solomoncoder.com

  • Riebli T, Avgan B, Bottini A-M, Duc C, Taborsky M, Heg D (2011) Behavioural type affects dominance and growth in staged encounters of cooperatively breeding cichlids. Anim Behav 81:313–323

    Article  Google Scholar 

  • Robison RR, Fernald RD, Stacey NE (1998) The olfactory system of a cichlid fish responds to steroidal compounds. J Fish Biol 53:226–229

    Article  CAS  Google Scholar 

  • Rowell TE (1974) The concept of social dominance. Behav Biol 11:131–154

    Article  CAS  PubMed  Google Scholar 

  • RStudio Team (2015) RStudio: Integrated development for R. RStudio Inc., Boston, MA, http://ww.rstudio.com/

  • Sorensen PW, Wisenden BD (2015) Fish pheromones and related cues. John Wiley & Sons Inc., London

  • Taborsky M (1984) Broodcare helpers in the cichlid fish Lamprologus brichardi: their costs and benefits. Anim Behav 32:1236–1252

    Article  Google Scholar 

  • Taborsky M (1985) Breeder-helper conflict in a cichlid fish with broodcare helpers: an experimental analysis. Behaviour 95:45–75

    Article  Google Scholar 

  • Taborsky M (2016) Cichlid fishes: a model for the integrative study of social behavior. In: Koenig WD, Dickinson JL (eds) Cooperative breeding in vertebrates: studies of ecology, evolution, and behavior. Cambridge University Press, Cambridge, pp 272–293

    Chapter  Google Scholar 

  • Taborsky M, Grantner A (1998) Behavioural time-energy budgets of cooperatively breeding Neolamprologus pulcher (Pisces: Cichlidae). Anim Behav 56:1375–1382

    Article  CAS  PubMed  Google Scholar 

  • Taborsky M, Limberger D (1981) Helpers in fish. Behav Ecol Sociobiol 8:143–145

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • van Staaden MJ, Smith AR (2011) Cutting the Gordian knot: complex signaling in African cichlids is more than multimodal. Curr Zool 57:237–252

    Article  Google Scholar 

  • van Staaden MJ, Searcy WA, Hanlon RT (2011) Signaling aggression. Adv Genet 75:23–49

    PubMed  Google Scholar 

  • Ward AJW, Currie S (2013) Shoaling fish can size-assort by chemical cues alone. Behav Ecol Sociobiol 67:667–673

    Article  Google Scholar 

  • Wisenden BD (2000) Olfactory assessment of predation risk in the aquatic environment. Phil Trans R Soc B 355:1205–1208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wong M, Balshine S (2010) Fight for your breeding right: hierarchy re-establishment predicts aggression in a social queue. Biol Lett 7:190–193

    Article  PubMed  PubMed Central  Google Scholar 

  • Zöttl M, Heg D, Chervet N, Taborsky M (2013) Kinship reduces alloparental care in cooperative cichlids where helpers pay-to-stay. Nat Commun 4:1341

    Article  PubMed  Google Scholar 

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Acknowledgments

We thank Evi Zwygart for her help with fish welfare and maintenance, Leif Engqvist and Frank Groenewoud for their statistical advice and Marcel Moser for his IT support. Valentina Balzarini provided drawings of fish. This work benefitted from discussions with Hirokazu Tanaka, Valentina Balzarini, Jon Andreja Nuotclá, Corinna von Kürthy and the members of the Jo-club. We are grateful to Manon Schweinfurth, Andrea Pilastro and two anonymous referees for thoughtful comments on earlier drafts of the manuscript. This research was funded by grants of the Swiss National Science Foundation (31003A_156152 to MT and 31003A_144191 to JGF).

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  1. Department of Behavioural Ecology, Institute of Ecology and Evolution, University of Bern, Wohlenstraße 50a, 3032, Hinterkappelen, Switzerland

    Dario-Marcos Bayani, Michael Taborsky & Joachim G. Frommen

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  1. Dario-Marcos Bayani
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  2. Michael Taborsky
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  3. Joachim G. Frommen
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Correspondence to Dario-Marcos Bayani.

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The experiments adhered to the ‘Guidelines for the treatment of animals in behavioural research and teaching (ASAB 2012)’ and comply with the current laws of Switzerland (license number BE74/15).

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Communicated by A. Pilastro

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Bayani, DM., Taborsky, M. & Frommen, J.G. To pee or not to pee: urine signals mediate aggressive interactions in the cooperatively breeding cichlid Neolamprologus pulcher . Behav Ecol Sociobiol 71, 37 (2017). https://doi.org/10.1007/s00265-016-2260-6

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