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acta ethologica

, Volume 20, Issue 3, pp 263–277 | Cite as

Social organization and endocrine profiles of Australoheros facetus, an exotic freshwater fish in southern Portugal

  • Flávia Baduy
  • Pedro M. Guerreiro
  • Adelino V. Canário
  • João L. Saraiva
Original Paper

Abstract

Australoheros facetus is a neotropical cichlid and an exotic species in the Guadiana and Odelouca basins (Southern Portugal). In this research, we aimed to characterize the main behavioural patterns and circulating hormones, 17β-estradiol (E2) for females, and testosterone, 11-ketotestosterone (11KT) and cortisol for both sexes, during the formation of social groups, a crucial step in the life-history of A. facetus. A pair-breeding strategy with territorial behaviour and aggressive interactions was found, with a positive correlation between dominance and size for both sexes. There were no significant differences between non-territorial and territorial individuals in the baseline levels of hormones, but 11KT was higher in males when they became territorial, as E2 for territorial females, while there was no clear pattern for testosterone. In contrast, cortisol was higher in non-territorial males and correlated negatively with social dominance. These results suggest that size is the main driver for social dominance and that formation of stable hierarchies result in higher circulating 11KT and lowers stress in territorial males. Related to A. facetus’ behaviour, aggressiveness and biparental care may be an advantage during the invasion process of A. facetus, facilitating colonization of new habitats.

Keywords

Non-native fish Aggressiveness Hormonal profile Hierarchy formation Cichlid 

Notes

Acknowledgments

FB received a doctoral fellowship from the National Council for Technological and Scientific Development of Brazil (CNPq), Program Science without Borders (245971/2012­2). The FCT—Foundation for Science and Technology provided national funds through project UID/Multi/04326/2013 and a fellowship (SFRH/BPD/67008/2009) to JLS. The authors would like to thank Elsa Couto, Filipe Ribeiro and Carlos Carrapato for laboratory and logistic help.

Compliance with ethical standards

Fish collection in the wild was performed under licence from the National Institute for Nature Conservancy (ICNF) and CCMAR facilities; their staff and the authors are certified to house, design and conduct experiments with live animals by the Veterinary General Directorate, Ministry of Agriculture, Rural Development and Fisheries of Portugal (DGAV) in accordance to the three ‘R’ policy and national and European legislation.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Almeida O, Canario AV, Oliveira RF (2014a) Castration affects reproductive but not aggressive behavior in a cichlid fish. Gen Comp Endocrinol 207:34–40. doi: 10.1016/j.ygcen.2014.03.018 CrossRefPubMedGoogle Scholar
  2. Almeida O, Goncalves-de-Freitas E, Lopes JS, Oliveira RF (2014b) Social instability promotes hormone-behavior associated patterns in a cichlid fish. Horm Behav 66:369–382. doi: 10.1016/j.yhbeh.2014.05.007 CrossRefPubMedGoogle Scholar
  3. Alonso F, Canepa M, Moreira RG, Pandolfi M (2011) Social and reproductive physiology and behavior of the Neotropical cichlid fish Cichlasoma dimerus under laboratory conditions. Neotrop Ichthyol 9:559–570CrossRefGoogle Scholar
  4. Alonso F, Honji RM, Guimaraes Moreira R, Pandolfi M (2012) Dominance hierarchies and social status ascent opportunity: anticipatory behavioral and physiological adjustments in a Neotropical cichlid fish. Physiol Behav 106:612–618. doi: 10.1016/j.physbeh.2012.04.003 CrossRefPubMedGoogle Scholar
  5. Annett CA, Pierotti R, Baylis JR (1999) Male and female parental roles in the monogamous cichlid, Tilapia mariae, introduced in Florida. Environ Biol Fish 54:283–293. doi: 10.1023/A:1007567028017 CrossRefGoogle Scholar
  6. Awata S, Kohda M (2004) Parental roles and the amount of care in a bi-parental substrate brooding cichlid: the effect of size differences within pairs. Behaviour 141:1135–1149. doi: 10.1163/1568539042664623 CrossRefGoogle Scholar
  7. Beacham JL (1987) The relative importance of body size and aggressive experience as determinants of dominance in pumpkinseed sunfish, Lepomis gibbosus. Anim Behav 36:621–623CrossRefGoogle Scholar
  8. Bell AM (2001) Effects of an endocrine disrupter on courtship and aggressive behaviour of male three-spined stickleback, Gasterosteus aculeatus. Anim Behav 62:775–780. doi: 10.1006/anbe.2001.1824 CrossRefGoogle Scholar
  9. Bender N, Heg-Bachar Z, Oliveira RF, Canario AV, Taborsky M (2008) Hormonal control of brood care and social status in a cichlid fish with brood care helpers. Physiol Behav 94:349–358. doi: 10.1016/j.physbeh.2008.02.002 CrossRefPubMedGoogle Scholar
  10. Bergmuller R, Taborsky M (2005) Experimental manipulation of helping in a cooperative breeder: helpers ‘pay to stay’ by pre-emptive appeasement. Anim Behav 69:19–28. doi: 10.1016/j.anbehav.2004.05.009 CrossRefGoogle Scholar
  11. Birba A, Ramallo MR, Lo Nostro F, Guimaraes Moreira R, Pandolfi M (2015) Reproductive and parental care physiology of Cichlasoma dimerus males. Gen Comp Endocrinol 221:193–200. doi: 10.1016/j.ygcen.2015.02.004 CrossRefPubMedGoogle Scholar
  12. Bromage N, Porter M, Randall C (2001) The environmental regulation of maturation in farmed finfish with special reference to the role of photoperiod and melatonin. Aquaculture 197:63–98. doi: 10.1016/s0044-8486(01)00583-x CrossRefGoogle Scholar
  13. Bry C (1985) Plasma cortisol levels of female rainbow trout (Salmo Gairdneri) at the end of the reproductive cycle: relationship with oocyte stages. Gen Comp Endocrinol 57:47–52. doi: 10.1016/0016-6480(85)90199-6 CrossRefPubMedGoogle Scholar
  14. Canario AV, Scott AP (1989) Conjugates of ovarian steroids, including 17 alpha,20 beta-dihydroxy-4-pregnen-3-one (maturation-inducing steroid), accumulate in the urine of a marine teleost (plaice; Pleuronectes Platessa). J Endocrinol 123:R1–R4CrossRefPubMedGoogle Scholar
  15. Chapple DG, Simmonds SM, Wong BB (2012) Can behavioral and personality traits influence the success of unintentional species introductions? Trends Ecol Evol 27:57–64. doi: 10.1016/j.tree.2011.09.010 CrossRefPubMedGoogle Scholar
  16. Chase ID, Tovey C, Spangler-Martin D, Manfredonia M (2002) Individual differences versus social dynamics in the formation of animal dominance hierarchies. Proc Natl Acad Sci U S A 99:5744–5749. doi: 10.1073/pnas.082104199 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Chen WH, Sun LT, Tsai CL, Song YL, Chang CF (2002) Cold-stress induced the modulation of catecholamines, cortisol, immunoglobulin M, and leukocyte phagocytosis in tilapia. Gen Comp Endocrinol 126:90–100. doi: 10.1006/gcen.2001.7772 CrossRefPubMedGoogle Scholar
  18. Collares-Pereira MJ, Cowx IG, Ribeiro F, Rodrigues JA, Rogado L (2000) Threats imposed by water resource development schemes on the conservation of endangered fish species in the Guadiana River basin in Portugal fisheries. Manage Ecol 7:167–178. doi: 10.1046/j.1365-2400.2000.00202.x Google Scholar
  19. Colleter M, Brown C (2011) Personality traits predict hierarchy rank in male rainbowfish social groups. Anim Behav 81:1231–1237. doi: 10.1016/j.anbehav.2011.03.011 CrossRefGoogle Scholar
  20. Colman JR, Baldwin D, Johnson LL, Scholz NL (2009) Effects of the synthetic estrogen, 17alpha-ethinylestradiol, on aggression and courtship behavior in male zebrafish (Danio Rerio). Aquat Toxicol 91:346–354. doi: 10.1016/j.aquatox.2008.12.001 CrossRefPubMedGoogle Scholar
  21. Culbert BM, Gilmour KM (2016) Rapid recovery of the cortisol response following social subordination in rainbow trout. Physiol Behav 164:306–313. doi: 10.1016/j.physbeh.2016.06.012 CrossRefPubMedGoogle Scholar
  22. Dewsbury DA (1982) Dominance rank, copulatory behavior, and differential reproduction. Q Rev Biol 57:135–159CrossRefPubMedGoogle Scholar
  23. Doadrio I (2002) Atlas e libro rojo de los peces continentales de España. ELECE, MadridGoogle Scholar
  24. Drake JM (2007) Parental investment and fecundity, but not brain size, are associated with establishment success in introduced fishes. Funct Ecol 21:963–968. doi: 10.1111/j.1365-2435.2007.01318.x CrossRefGoogle Scholar
  25. Falahatkar B, Poursaeid S, Meknatkhah B, Khara H, Efatpanah I (2014) Long-term effects of intraperitoneal injection of estradiol-17beta on the growth and physiology of juvenile stellate sturgeon Acipenser stellatus. Fish Physiol Biochem 40:365–373. doi: 10.1007/s10695-013-9849-8 CrossRefPubMedGoogle Scholar
  26. Fernald RD (2014) Communication about social status. Curr Opin Neurobiol 28:1–4. doi: 10.1016/j.conb.2014.04.004 CrossRefPubMedGoogle Scholar
  27. Filby AL, Paull GC, Searle F, Ortiz-Zarragoitia M, Tyler CR (2012) Environmental estrogen-induced alterations of male aggression and dominance hierarchies in fish: a mechanistic analysis. Environ Sci Technol 46:3472–3479. doi: 10.1021/es204023d CrossRefPubMedGoogle Scholar
  28. Fox HE, White SA, Kao MH, Fernald RD (1997) Stress and dominance in a social fish. J Neurosci 17:6463–6469PubMedGoogle Scholar
  29. Gasith A, Resh VH (1999) Streams in Mediterranean climate regions: abiotic influences and biotic responses to predictable seasonal events. Annu Rev Ecol Syst 30:51–81. doi: 10.1146/annurev.ecolsys.30.1.51 CrossRefGoogle Scholar
  30. Guerreiro PM, Fuentes J, Canario AVM, Power DM (2002) Calcium balance in sea bream (Sparus aurata): the effect of oestradiol-17 beta. J Endocrinol 173:377–385. doi: 10.1677/joe.0.1730377 CrossRefPubMedGoogle Scholar
  31. Hau M, Goymann W (2015) Endocrine mechanisms, behavioral phenotypes and plasticity: known relationships and open questions. Front Zool 12(Suppl 1):S7. doi: 10.1186/1742-9994-12-S1-S7 CrossRefPubMedPubMedCentralGoogle Scholar
  32. He J, Qiang J, Yang H, Xu P, Zhu ZX, Yang RQ (2015) Changes in the fatty acid composition and regulation of antioxidant enzymes and physiology of juvenile genetically improved farmed tilapia Oreochromis niloticus (L.), subjected to short-term low temperature stress. J Therm Biol 53:90–97. doi: 10.1016/j.jtherbio.2015.08.010 CrossRefPubMedGoogle Scholar
  33. Hermoso V, Clavero M, Kennard MJ (2012) Determinants of fine-scale homogenization and differentiation of native freshwater fish faunas in a Mediterranean Basin: implications for conservation. Divers Distrib 18:236–247. doi: 10.1111/j.1472-4642.2011.00828.x CrossRefGoogle Scholar
  34. Hirschenhauser K, Taborsky M, Oliveira T, Canario AVM, Oliveira RF (2004) A test of the 'challenge hypothesis’ in cichlid fish: simulated partner and territory intruder experiments. Anim Behav 68:741–750. doi: 10.1016/j.anbehav.2003.12.015 CrossRefGoogle Scholar
  35. Holway DA, Suarez AV (1999) Animal behavior: an essential component of invasion biology. Trends Ecol Evol 14:328–330CrossRefPubMedGoogle Scholar
  36. Hubbard PC, Mota VC, Keller-Costa T, da Silva JP, Canario AV (2014) Chemical communication in tilapia: a comparison of Oreochromis mossambicus with O. niloticus. Gen Comp Endocrinol 207:13–20. doi: 10.1016/j.ygcen.2014.06.022 CrossRefPubMedGoogle Scholar
  37. Hubbard PC, Baduy F, Saraiva JL, Guerreiro PM, Canario AVM (2017) High olfactory sensitivity to conspecific intestinal fluid in the chameleon cichlid Australoheros facetus: could faeces signal dominance? J Fish Biol 90:2148–2156. doi: 10.1111/jfb.13297 CrossRefPubMedGoogle Scholar
  38. Huffman LS, O'Connell LA, Hofmann HA (2013) Aromatase regulates aggression in the African cichlid fish Astatotilapia burtoni. Physiol Behav 112-113:77–83. doi: 10.1016/j.physbeh.2013.02.004 CrossRefPubMedGoogle Scholar
  39. Itzkowitz M, Santangelo N, Richter M (2003) How does a parent respond when its mate emphasizes the wrong role? A test using a monogamous fish. Anim Behav 66:863–869. doi: 10.1006/anbe.2002.2291 CrossRefGoogle Scholar
  40. Itzkowitz M, Santangelo N, Cleveland A, Bockelman A, Richter M (2005) Is the selection of sex-typical parental roles based on an assessment process? A test in the monogamous convict cichlid fish. Anim Behav 69:95–105. doi: 10.1016/j.anbehav.2003.12.027 CrossRefGoogle Scholar
  41. Johnson DW, Hixon MA (2011) Sexual and lifetime selection on body size in a marine fish: the importance of life-history trade-offs. J Evol Biol 24:1653–1663. doi: 10.1111/j.1420-9101.2011.02298.x CrossRefPubMedGoogle Scholar
  42. Johnsson JJ, Winberg S, Sloman KA (2006) Social interactions. In: Sloman KA, Wilson RW, Balshine S (eds) Behaviour and physiology of fish, vol 24. Fish physiology. Elsevier Academic Press, BostonGoogle Scholar
  43. Keenleyside MHA (1985) Bigamy and mate choice in the biparental cichlid fish Cichlasoma nigrofasciatum. Behav Ecol Sociobiol 17:285–290. doi: 10.1007/Bf00300148 CrossRefGoogle Scholar
  44. Keenleyside MHA (ed) (1991) Cichlid fishes: behavior, ecology and evolution. Fish and Fisheries Series 2. Chapman & Hall, London, pp 378Google Scholar
  45. Keller-Costa T et al (2014) Identity of a tilapia pheromone released by dominant males that primes females for reproduction. Curr Biol 24:2130–2135. doi: 10.1016/j.cub.2014.07.049 CrossRefPubMedGoogle Scholar
  46. Keller-Costa T, Saraiva JL, Hubbard PC, Barata EN, Canario AV (2016) A multi-component pheromone in the urine of dominant male tilapia (Oreochromis mossambicus) reduces aggression in rivals. J Chem Ecol 42:173–182. doi: 10.1007/s10886-016-0668-0 CrossRefPubMedGoogle Scholar
  47. Kime DE, Manning NJ (1982) Seasonal patterns of free and conjugated androgens in the brown trout Salmo trutta. Gen Comp Endocrinol 48:222–231. doi: 10.1016/0016-6480(82)90020-X CrossRefPubMedGoogle Scholar
  48. Koporikov AR, Bogdanov VD (2013) Changes in the hepatosomatic index of semianadromous burbot, Lota lota L. (Lotidae), in the Ob River depending on fish physiological state and foraging conditions Russian. J Ecol 44:233–238. doi: 10.1134/s1067413613030077 Google Scholar
  49. Lamba VJ, Goswami SV, Sundararaj BI (1983) Circannual and circadian variations in plasma levels of steroids (cortisol, estradiol-17β estrone, and testosterone) correlated with the annual gonadal cycle in the catfish Heteropneustes fossilis (Bloch). Gen Comp Endocrinol 50:205–225. doi: 10.1016/0016-6480(83)90221-6 CrossRefPubMedGoogle Scholar
  50. Lennox R, Choi K, Harrison PM, Paterson JE, Peat TB, Ward TD, Cooke SJ (2015) Improving science-based invasive species management with physiological knowledge, concepts, and tools. Biol Invasions 17:2213–2227. doi: 10.1007/s10530-015-0884-5 CrossRefGoogle Scholar
  51. Lubzens E, Young G, Bobe J, Cerda J (2010) Oogenesis in teleosts: how eggs are formed. Gen Comp Endocrinol 165:367–389. doi: 10.1016/j.ygcen.2009.05.022 CrossRefPubMedGoogle Scholar
  52. Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710. doi: 10.2307/2641039 CrossRefGoogle Scholar
  53. Majewski AR, Blanchfield PJ, Palace VP, Wautier K (2002) Waterborne 17α-Ethynylestradiol affects aggressive behaviour of male fathead minnows (Pimephales promelas) under artificial spawning conditions. Water Qual Res J Can 37:697–710Google Scholar
  54. Marr SM et al (2013) A global assessment of freshwater fish introductions in mediterranean-climate regions. Hydrobiologia 719:317–329. doi: 10.1007/s10750-013-1486-9 CrossRefGoogle Scholar
  55. Martinovic-Weigelt D, Ekman DR, Villeneuve DL, James CM, Teng Q, Collette TW, Ankley GT (2012) Fishy aroma of social status: urinary chemo-signalling of territoriality in male fathead minnows (Pimephales promelas). PLoS One 7:e46579. doi: 10.1371/journal.pone.0046579 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Maruska KP (2014) Social regulation of reproduction in male cichlid fishes. Gen Comp Endocrinol 207:2–12. doi: 10.1016/j.ygcen.2014.04.038 CrossRefPubMedGoogle Scholar
  57. Maruska KP (2015) Social transitions cause rapid behavioral and neuroendocrine changes. Integr Comp Biol 55:294–306. doi: 10.1093/icb/icv057 CrossRefPubMedPubMedCentralGoogle Scholar
  58. Maruska KP, Becker L, Neboori A, Fernald RD (2013) Social descent with territory loss causes rapid behavioral, endocrine and transcriptional changes in the brain. J Exp Biol 216:3656–3666. doi: 10.1242/jeb.088617 CrossRefPubMedPubMedCentralGoogle Scholar
  59. McGraw KJ, Hill GE (1999) Induced homosexual behaviour in male house finches (Carpodacus mexicanus): the “prisoner effect”. Ethol Ecol Evol 11:197–201. doi: 10.1080/08927014.1999.9522837 CrossRefGoogle Scholar
  60. Mileva VR, Fitzpatrick JL, Marsh-Rollo S, Gilmour KM, Wood CM, Balshine S (2009) The stress response of the highly social African cichlid Neolamprologus pulcher. Physiol Biochem Zool 82:720–729. doi: 10.1086/605937 CrossRefPubMedGoogle Scholar
  61. Miyai CA, Carretero Sanches FH, Costa TM, Colpo KD, Volpato GL, Barreto RE (2011) The correlation between subordinate fish eye colour and received attacks: a negative social feedback mechanism for the reduction of aggression during the formation of dominance hierarchies. Zoology 114:335–339. doi: 10.1016/j.zool.2011.07.001 CrossRefPubMedGoogle Scholar
  62. Mommsen TP, Vijayan MM, Moon TW (1999) Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fish 9:211–268. doi: 10.1023/A:1008924418720 CrossRefGoogle Scholar
  63. Morse DH (1974) Niche breadth as a function of social dominance. Am Nat 108:818–830. doi: 10.1086/282957 CrossRefGoogle Scholar
  64. Mota VC, Martins CIM, Eding EH, Canario AVM, Verreth JAJ (2014) Steroids accumulate in the rearing water of commercial recirculating aquaculture systems. Aquac Eng 62:9–16. doi: 10.1016/j.aquaeng.2014.07.004 CrossRefGoogle Scholar
  65. Neat FC, Taylor AC, Huntingford FA (1998) Proximate costs of fighting in male cichlid fish: the role of injuries and energy metabolism. Anim Behav 55:875–882. doi: 10.1006/anbe.1997.0668 CrossRefPubMedGoogle Scholar
  66. O'Connell LA, Ding JH, Hofmann HA (2013) Sex differences and similarities in the neuroendocrine regulation of social behavior in an African cichlid fish. Horm Behav 64:468–476. doi: 10.1016/j.yhbeh.2013.07.003 CrossRefPubMedGoogle Scholar
  67. O'Connor KI, Metcalfe NB, Taylor AC (1999) Does darkening signal submission in territorial contests between juvenile Atlantic salmon, Salmo salar ? Anim Behav 58:1269–1276. doi: 10.1006/anbe.1999.1260 CrossRefPubMedGoogle Scholar
  68. Oliveira RF (2005) Social modulation of androgens in male vertebrates: mechanisms and function. In: Slater JB, Rosenblatt CS, Snowdon CT et al (eds) Advances in study of behavior, vol 34. Academic Press, Elsevier Science, pp 165–239Google Scholar
  69. Oliveira RF (2009) Social behavior in context: hormonal modulation of behavioral plasticity and social competence. Integr Comp Biol 49:423–440. doi: 10.1093/icb/icp055 CrossRefPubMedGoogle Scholar
  70. Oliveira RF, Canario AV (2000) Hormones and social behavior of cichlid fishes: a case study in the Mozambique tilapia vol IXGoogle Scholar
  71. Oliveira RF, Hirschenhauser K, Carneiro LA, Canario AV (2002) Social modulation of androgen levels in male teleost fish comparative biochemistry and physiology part B. Biochem Mol Biol 132:203–215CrossRefGoogle Scholar
  72. Pankhurst N, Porter M (2003) Cold and dark or warm and light: variations on the theme of environmental control of reproduction. Fish Physiol Biochem 28:385–389. doi: 10.1023/B:FISH.0000030602.51939.50 CrossRefGoogle Scholar
  73. Pankhurst NW, Van Der Kraak G (1997) Effects of stress on reproduction and growth of fish. In: Iwama GK, Pickering AD, Sumpter JP, Schreck CB (eds) Fish stress and health in aquaculture. Cambridge University Press, Cambridge, pp 73–95Google Scholar
  74. Pereira LS, Agostinho AA, Gomes LC (2014) Eating the competitor: a mechanism of invasion. Hydrobiologia 746:223–231. doi: 10.1007/s10750-014-2031-1 CrossRefGoogle Scholar
  75. Poursaeid S, Falahatkar B, Mojazi Amiri B, Van Der Kraak G (2012) Effects of long-term cortisol treatments on gonadal development, sex steroids levels and ovarian cortisol content in cultured great sturgeon Huso huso Comparative biochemistry and physiology part a. Mol Integr Physiol 163:111–119. doi: 10.1016/j.cbpa.2012.05.202 CrossRefGoogle Scholar
  76. Rahel FJ, Bierwagen B, Taniguchi Y (2008) Managing aquatic species of conservation concern in the face of climate change and invasive species. Conserv Biol 22:551–561. doi: 10.1111/j.1523-1739.2008.00953.x CrossRefPubMedGoogle Scholar
  77. Ramallo MR, Birba A, Honji RM, Morandini L, Moreira RG, Somoza GM, Pandolfi M (2015) A multidisciplinary study on social status and the relationship between inter-individual variation in hormone levels and agonistic behavior in a neotropical cichlid fish. Horm Behav 69:139–151. doi: 10.1016/j.yhbeh.2015.01.008 CrossRefPubMedGoogle Scholar
  78. Ribeiro F, Orjuela RL, Magalhães MF, Collares-Pereira MJ (2007) Variability in feeding ecology of a south American cichlid: a reason for successful invasion in mediterranean-type rivers? Ecol Freshw Fish 16:559–569. doi: 10.1111/j.1600-0633.2007.00252.x CrossRefGoogle Scholar
  79. Rìcan O, Kullander SO (2006) Character- and tree-based delimitation of species in the 'Cichlasoma' facetum group (Teleostei, Cichlidae) with the description of a new genus. J Zool Syst Evol Res 44:136–152. doi: 10.1111/j.1439-0469.2005.00347.x CrossRefGoogle Scholar
  80. Rotllant J, Guerreiro PM, Anjos L, Redruello B, Canario AV, Power DM (2005) Stimulation of cortisol release by the N terminus of teleost parathyroid hormone-related protein in interrenal cells in vitro. Endocrinology 146:71–76. doi: 10.1210/en.2004-0644 CrossRefPubMedGoogle Scholar
  81. Ruiz VHR, Moyano HG, Marchant MSM (1992) Aspectos biologicos del pez exotico Cichlasoma facetum (Jenyns, 1842) (Pisces, Cichlidae) en aguas dulces de Concepcion. Bol Soco Biol Concepc 63:193–201Google Scholar
  82. Schulz RW, de Franca LR, Lareyre JJ, Le Gac F, Chiarini-Garcia H, Nobrega RH, Miura T (2010) Spermatogenesis in fish. Gen Comp Endocrinol 165:390–411. doi: 10.1016/j.ygcen.2009.02.013 CrossRefPubMedGoogle Scholar
  83. Scott A et al (2008) Non-invasive measurement of steroids in fish-holding water: important considerations when applying the procedure to behaviour studies. Behaviour 145:1307–1328. doi: 10.1163/156853908785765854 CrossRefGoogle Scholar
  84. Snekser JL, Itzkowitz M (2009) Sex differences in retrieval behavior by the biparental convict. Cichlid Ethol 115:457–464. doi: 10.1111/j.1439-0310.2009.01625.x CrossRefGoogle Scholar
  85. 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. doi: 10.1016/j.ygcen.2008.12.018 CrossRefPubMedGoogle Scholar
  86. Teresa FB, Goncalves-de-Freitas E (2011) Reproductive behavior and parental roles of the cichlid fish Laetacara araguaiae. Neotrop Ichthyol 9:355–362CrossRefGoogle Scholar
  87. Thomaz SM, Kovalenko KE, Havel JE, Kats LB (2014) Aquatic invasive species: general trends in the literature and introduction to the special issue. Hydrobiologia 746:1–12. doi: 10.1007/s10750-014-2150-8 CrossRefGoogle Scholar
  88. Tibbetts EA, Crocker KC (2014) The challenge hypothesis across taxa: social modulation of hormone titres in vertebrates and insects. Anim Behav 92:281–290. doi: 10.1016/j.anbehav.2014.02.015 CrossRefGoogle Scholar
  89. Volpato GL, Luchiari AC, Duarte CRA, Barreto RE, Ramanzini GC (2003) Eye color as an indicator of social rank in the fish Nile tilapia. Braz J Med Biol Res 36:1659–1663. doi: 10.1590/S0100-879x2003001200007 CrossRefPubMedGoogle Scholar
  90. Wang H-P et al (2008) Effects of estradiol-17β on survival, growth performance, sex reversal and gonadal structure of bluegill sunfish Lepomis macrochirus. Aquaculture 285:216–223. doi: 10.1016/j.aquaculture.2008.08.041 CrossRefGoogle Scholar
  91. White SA, Nguyen T, Fernald RD (2002) Social regulation of gonadotropin-releasing hormone. J Exp Biol 205:2567–2581PubMedGoogle Scholar
  92. Wingfield JC, Grimm AS (1977) Seasonal changes in plasma cortisol, testosterone and oestradiol-17β in the plaice, Pleuronectes platessa L. Gen Comp Endocrinol 31:1–11. doi: 10.1016/0016-6480(77)90184-8 CrossRefPubMedGoogle Scholar
  93. Wingfield JC, Hegner RE, Dufty AM, Ball GF (1990) The challenge hypothesis—theoretical implications for patterns of testosterone secretion, Mating systems, and breeding strategies. Am Nat 136:829–846. doi: 10.1086/285134 CrossRefGoogle Scholar
  94. Wisenden BD (1994) Factors affecting reproductive success in free-ranging convict cichlids (Cichlasoma-Nigrofasciatum). Can J Zool 72:2177–2185. doi: 10.1139/Z94-291 CrossRefGoogle Scholar
  95. Yafe A, Loureiro M, Scasso F, Quintans F (2002) Feeding of two cichlidae species (Perciformes) in an hypertrophic lake. Iheringia 92:73–79CrossRefGoogle Scholar

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© Springer-Verlag GmbH Germany and ISPA 2017

Authors and Affiliations

  1. 1.CCMAR-CIMAR, Centre for Marine SciencesUniversity of AlgarveFaroPortugal

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