Abstract
Selection favors females that make use of reliable information on the genetic quality of males, which affects mating decisions. Although studies have shown that females prefer dominant males, it may not be adaptive for females to choose very aggressive males, as aggression can be misdirected towards females. The Nile tilapia Oreochromis niloticus is an appropriate model species for testing this dilemma because it shows dominance hierarchy, in which dominant males defend territories, build nests, court females and have priority of access to mating. In addition, in this species, odor recognition affects sexual and social status. We tested whether females can select, by means of chemical cues, dominant males with aggressive profiles. Females were allowed to choose between the odors of two dominant males differing in their aggression level. Our findings show that females discriminate dominant males that have a high aggressivity profile in favor of males that are less aggressive.
Similar content being viewed by others
References
Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P (2002) Molecular biology of the cell, 4th edn. In: Cells and genomes. Garland Science, New York
Alvarenga CMD, Volpato GL (1995) Agonistic profile and metabolism in alevins of the Nile tilapia. Physiol Behav 57:75–80
Andersson MB (1994) Sexual selection. Princeton University Press, USA
Barata EN, Hubbard PC, Almeida OG, Miranda A, Canário AV (2007) Male urine signals social rank in the Mozambique tilapia (Oreochromis mossambicus). BMC Biol 5:54
Barreto RE, Carvalho GGA, Volpato GL (2011) The aggressive behavior of Nile tilapia introduced into novel environments with variation in enrichment. Zoology 114:53–57
Beeching SC (1995) Colour pattern and inhibition of aggression in the cichlid fish Astronotus ocellatus. J Fish Biol 47:50–58
Bierbach D, Sassmannshausen V, Streit B, Arias-Rodriguez L, Plath M (2013) Females prefer males with superior fighting abilities but avoid sexually harassing winners when eavesdropping on male fights. Behav Ecol Sociobiol 67:675–683
Blengini FR, Tassino B, Passos C (2018) Females of the annual killifish Austrolebias reicherti (Cyprinodontiformes: Rivulidae) recognize conspecific mates based upon chemical cues. Behav Process 155:33–37
Candolin U (2000) Male–male competition ensures honest signaling of male parental ability in the three-spined stickleback (Gasterosteus aculeatus). Behav Ecol Sociobiol 49:57–61
Carvalho TB, Gonçalves-de-Freitas E (2008) Sex group composition, social interaction, and metabolism in the fish Nile tilapia. Braz J Biol 68:1678–4375
Castro ALS, Gonçalves-de-Freitas E, Volpato GL, Oliveira C (2009) Visual communication stimulates reproduction in Nile tilapia, Oreochromis niloticus (L.). Braz J Med Biol Res 42:368–374
DeBose JL, Nevitt GA (2008) The use of odors at different spatial scales: comparing birds with fish. J Chem Ecol 34:867–881
Doutrelant C, McGregor PK (2000) Eavesdropping and mate choice in female fighting fish. Behaviour 137:1655–1669
Dugatkin LA, Druen M (2004) The social implications of winner and loser effects. Proc R Soc Lond B Biol Sci 271:488–489
Dugatkin LA, FitzGerald GJ (1997) Sexual selection. In: Godin GJ (ed) Behavioural ecology of teleost fishes. Oxford University Press, Oxford
Falter U (1983) Agonistic behavior of Sarotherodon niloticus and the evolutionary significance of buccal incubation. Academie Royale des Sciences, des Lettres et des Beaux-Arts de Belgique. Classe des Sciences. Bulletin 69(10):566–594
Fernandes MO, Volpato GL (1993) Heterogeneous growth in the Nile tilapia: social stress and carbohydrate metabolism. Physiol Behav 54:319–323
Freeland WJ (1981) Parasitism and behavioural dominance among male mice. Science 213:461–462
Fuller RC (2001) Patterns in male breeding behaviors in the bluefin killifish, Lucania goodei: a field study (Cyprinodontiformes: Fundulidae). Copeia 3:823–828
Gasparini C, Devigili A, Pilastro A (2012) Cross-generational effects of sexual harassment on female fitness in the guppy. Evolution 66:532–543
Giaquinto PC, Volpato GL (1997) Chemical communication, aggression, and conspecific recognition in the fish Nile tilapia. Physiol Behav 62:1333–1338
Giaquinto PC, Militão C, Delicio HC (2010) Female preferences based on male nutritional chemical traits. Behav Ecol Sociobiol 64:1029–1035
Golan M, Levavi-Sivan B (2013) Social dominance in tilapia is associated with gonadotroph hyperplasia. Gen Comp Endocrinol 192:126–135
Goldstein JS (2001) War and gender: how gender shapes the war system and vice versa. Cambridge University Press, Cambridge
Gómez-La Plaza LM, Morgan E (1993) Social isolation, aggression, and dominance in attacks in juvenile angelfish, Pterophyllum scalare. Aggress Behav 19:213–222
Gonçalves-De-Freitas E, Teresa FB, Gomes FS, Giaquinto PC (2008) Effect of water renewal on dominance hierarchy of the Nile tilapia. Appl Anim Behav Sci 112:187–195
Gozlan RE, Flower CJ, Pinder AC (2003) Reproductive success in male sunbleak, a recent invasive fish species in the UK. J Fish Biol 63:131–143
Haller J, Wittenberger C (1988) Biochemical energetics of hierarchy formation in Betta splendens. Physiol Behav 43:447–450
Halliday TR (1994) Sex and evolution. In: Slater PJB, Halliday TR (eds) Behaviour and evolution. Cambridge University Press, Cambridge
Hannes RP, Franck D, Liemann F (1984) Effects of rank-order fights on whole-body and blood concentrations of androgens and corticosteroids in the male swordtail (Xiphophorus helleri). Z Tierpsychol 65:53–65
Hirschenhauser K, Canario AVM, Ros Albert FH et al (2008) Social context may affect urinary excretion of 11-ketotestosterone in African cichlids. Behaviour 145:1367–1388
Hubbard PC, Baduy F, Saraiva JL, Guerreiro PM, Canário AVM (2017) High olfactory sensitivity to conspecific intestinal fluid in the chameleon cichlid Australoheros facetus: could faeces signal dominance? J Fish Biol 90(5):2148–2156
Johnstone RA (1998) Game theory and communication. In: Dugatkin LA, Reeve HK (eds) Game theory and animal behavior. Oxford University Press, New York
Keller-Costa T, Hubbard PC, Paetz C, Nakamura Y, da Silva JP, Rato A, Barata EN, Schneider B, Canario AV (2014) Identity of a tilapia pheromone released by dominant males that primes females for reproduction. Curr Biol 24:2130–2135
Keller-Costa T, Adelino VM, Hubbard PC (2015) Chemical communication in cichlids: a mini-review. Gen Comp Endocr 221:64–74
Keller-Costa T, Saraiva JL, Hubbard PC, Barata EN, Canário AV (2016) A multi-component pheromone in the urine of dominant male tilapia (Oreochromis mossambicus) reduces aggression in rivals. J Chem Ecol 42(2):173–182
Kodric-Brown A (1983) Determinants of male reproductive success in pupfish. Anim Behav 31:128–137
Köhler A, Hildenbrand P, Schleucher E, Riesch R, Arias-Rodriguez L, Streit B, Plath M (2011) Effects of male sexual harassment on female time budgets, feeding behavior, and metabolic rates in a tropical livebearing fish (Poecilia mexicana). Behav Ecol Sociobiol 65:1513–1523
Kutsyna O, Velez Z, Canário AV, Keller-Costa T, Hubbard PC (2016) Variation in urinary amino acids in the Mozambique tilapia: a potential signal of dominance or individuality? In: Schulte B, Goodwin T, Ferkin M (eds) Chemical signals in vertebrates 13. Springer, Cham, pp 189–203
Le Boeuf BJ, Mesnick S (1990) Sexual behaviour of male northern elephant seals. I. Lethal injuries to adult females. Behaviour 116:1–2
Magurran AE (2011) Sexual coersion. In: Evans J, Pilastro A, Schlupp I (eds) Ecology and evolution of poeciliid fishes. University of Chicago Press, Chicago, pp 209–217
Maruska KP, Fernald RD (2012) Contextual chemosensory urine signaling in an African cichlid fish. J Exp Biol 215:68–74
Maynard Smith J (1979) Game theory and the evolution of animals conflicts. J Theor Biol 47:209–221
McGhee KE, Fuller RC, Travisa J (2007) Male competition and female choice interact to determine mating success in the bluefin killifish. Behav Ecol 18:822–830
McGregor P, Doutreland C (2000) Eavesdroping and mate choice in female fighting fish. Behaviour 137:12
Mennill DJ, Ratcliffe LM, Boag PT (2002) Female eavesdropping on male song contests in songbirds. Science 296:873
Miranda A, Almeida OG, Hubbard PC, Barata EN, Canário AV (2005) Olfactory discrimination of female reproductive status by male tilapia (Oreochromis mossambicus). J Exp Biol 208:2037–2043
Oliveira RF, Almada VC (1996) Dominance hierarchies and social structure in captive groups of the Mozambique tilapia Oreochromis mossambicus (Teleostei Cichlidae). Ethol Ecol Evol 8:39–55
Ophir AG, Galef BG (2003) Female Japanese quail that ‘eavesdrop’ on fighting males prefer losers to winners. Anim Behav 66:399–407
Ophir AG, Galef BG (2004) Sexual experience can affect use of public information in mate choice. Anim Behav 68:1221–1227
Otter K, McGregor PK, Terry AMR, Burford FRL, Peake TM, Dabelsteen T (1999) Do female great tits (Parus major) assess males by eavesdropping? A field study using interactive song playback. Proc R Soc Lond B Biol Sci 266:1305–1309
Pinho-Neto CF, Miyai CA, Sanches FHC, Giaquinto PC, Delicio HC, Barcellos LJG, Volpato GL, Barreto RE (2014) Does sex influence intraspecific aggression and dominance in Nile tilapia juveniles? Behav Process 105:15–18
Pizzari T, Froman DP, Birkhead TR (2002) Pre- and post-insemination episodes of sexual selection in the fowl, Gallus g. domesticus. Heredity 88:112–116
Plenderleith M, van Oosterhout C, Robinson RL, Turner GF (2005) Female preference for conspecific males based on olfactory cues in a Lake Malawi cichlid fish. Biol Lett 1:411–414
Qvarnström A, Forsgren E (1998) Should females prefer dominant males? Trends Ecol Evol 13:498–501
Ridley M (1995) Animal behavior: an introduction to behavioral mechanisms, development and ecology, 2nd edn. Blackwell, Cambridge
Saraiva JL, Keller-Costa T, Hubbard PC, Rato A, Canário AV (2017) Chemical diplomacy in male tilapia: urinary signal increases sex hormone and decreases aggression. Sci Rep 7(1):7636
Serrano RM, Barata EN, Birkett MA, Hubbard PC, Guerreiro PS, Canário AV (2008) Behavioral and olfactory responses of female Salaria pavo (Pisces: Blenniidae) to a putative multi-component male pheromone. J Chem Ecol 34:647–658
Smadja C, Butlin RK (2009) On the scent of speciation: the chemosensory system and its role in premating isolation. Heredity 102:77–97
Tinbergen N (1972) Social behaviour in animals. Chapman and Hall, London
Trivers RL (1974) Parent-offspring conflict. Am Zool 14:249–264
Volpato GL, Fernandes MO (1994) Social control of growth in fish. Braz J Med Biol Res 7:797–810
Wong BBM, Candolin U (2005) How is female mate choice affected by male competition? Biol Rev 80:559–571
Wong BBM, Jennions MD, Keogh JS (2004) Sequential male mate choice in a fish, the Pacific blue-eye Pseudomugil signifer. Behav Ecol Sociobiol 56:253–256
Giaquinto PC (2010) Female pintado catfish choose well-fed males. Behaviour 147:319–332
Zahavi A (1979) Ritualisation and the evolution of movement signals. Behaviour 72:77–81
Acknowledgments
We thank Dr. Assaf Barki for improving the manuscript. This study was supported by a grant to Marina B. de Sá from the Fundacao de Amparo a Pesquisa Estado de Sao Paulo—FAPESP (2012/06565-7).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
All authors involved in this study declare no conflict of interest.
Ethical approval
All applicable international, national, and institutional guidelines for the care and use of animals were followed. This study is in agreement with the precepts of the Brazilian College for Animal Experimentation (protocol no. 484) (http://www.cobea.org.br). This article does not contain any studies with human participants performed by any of the authors.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Rossi, V.S., de Sá, M.B., Sugihara, V.S. et al. Effect of male aggressivity profile on female chemical choice in Nile tilapia. J Ethol 37, 335–342 (2019). https://doi.org/10.1007/s10164-019-00608-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10164-019-00608-3