Animal Cognition

, Volume 22, Issue 1, pp 89–98 | Cite as

Environmental enrichment influences spatial learning ability in captive-reared intertidal gobies (Bathygobius cocosensis)

  • Penelope S. CarbiaEmail author
  • Culum Brown
Original Paper


Behavioural plasticity is an advantageous trait for animals living in dynamic environments, and can be induced through learning. While some behavioural traits are innate, others are framed by experience and learning during an individual’s lifetime. Many studies have investigated cognitive abilities in fish species from contrasting environments, but the relative contribution of natural selection versus behavioural plasticity in cognitive variability remains equivocal. Furthermore, rearing conditions in laboratories are often mundane, failing to encourage natural behaviour in the species used in these studies. Here, we captured juvenile gobies (Bathygobius cocosensis) from intertidal rockpools, and raised them in captivity under varied environmental enrichment treatments that mimic variation observed in coastal habitats. When tested in a simple spatial learning task, individuals from complex rearing treatments (rock or oyster substrate) reached learning criteria faster than those reared in less complex (seagrass) and homogenous environments (sand substrate). Interestingly, gobies reared in complex environments demonstrated longer latencies to start the task than gobies in homogeneous treatments. Our results indicate that cognitive ability is strongly shaped by individual experience during ontogeny, and exposure to reduced environmental complexity in early life leads to reduced cognitive abilities in intertidal gobies.


Behaviour Plasticity Environment Cognition Goby Structural complexity 



This research was carried out at, and funded by, the Department of Biological Sciences at Macquarie University. Additional funding was provided by an MQ10 (Ph.D.) Scholarship. We thank the SWF technician of Macquarie University, Josh Aldridge, for assistance in animal husbandry.

Compliance with ethical standards

Ethical note

Gobies were caught in compliance with NSW Fisheries (permit no. P08/0010-3.0). Husbandry and experimental conditions were approved by the Macquarie University Ethics Committee (ARA 2014/003). Following experimental trials, all gobies were released at the site of capture.


  1. Aronson LR (1951) Orientation and jumping behaviour in the gobiid fish Bathygobius soporator. Am Mus Novit 1286:1–22Google Scholar
  2. Aronson LR (1971) Further studies on orientation and jumping behavior in the gobiid fish, Bathygobius soporator. Ann N Y Acad Sci 188(1):378–392Google Scholar
  3. Bergendahl IA, Salvanes AGV, Braithwaite VA (2016) Determining the effects of duration and recency of exposure to environmental enrichment. Appl Anim Behav Sci 176:163–169Google Scholar
  4. Bloch G, Robinson GE (2001) Chronobiology: reversal of honeybee behavioural rhythms. Nature 410(6832):1048Google Scholar
  5. Braithwaite VA, Salvanes AG (2005) Environmental variability in the early rearing environment generates behaviourally flexible cod: implications for rehabilitating wild populations. Proc R Soc Lond B Biol Sci 272(1568):1107–1113Google Scholar
  6. Brown C (2001) Familiarity with the test environment improves escape responses in the crimson spotted rainbowfish, Melanotaenia duboulayi. Anim Cogn 4(2):109–113Google Scholar
  7. Brown C, Braithwaite VA (2004) Size matters: a test of boldness in eight populations of the poeciliid Brachyrhaphis episcopi. Anim Behav 68(6):1325–1329Google Scholar
  8. Brown C, Day RL (2002) The future of stock enhancements: lessons for hatchery practice from conservation biology. Fish Fish 3(2):79–94Google Scholar
  9. Brown C (2012) Experience and learning in changing environments. In: Candolin U, Wong BBM (eds) Behavioural responses to a changing world: mechanisms and consequences. Oxford University Press, Oxford, pp 46–60Google Scholar
  10. Brown C, Davidson T, Laland K (2003) Environmental enrichment and prior experience of live prey improve foraging behaviour in hatchery-reared Atlantic salmon. J Fish Biol 63:187–196Google Scholar
  11. Brydges NM, Braithwaite VA (2009) Does environmental enrichment affect the behaviour of fish commonly used in laboratory work? Appl Anim Behav Sci 118(3–4):137–143Google Scholar
  12. Burns JG, Saravanan A, Rodd FH (2009) Rearing environment affects the brain size of guppies: lab-reared guppies have smaller brains than wild-caught guppies. Ethology 115(2):122–133Google Scholar
  13. Camacho-Cervantes M, Ojanguren AF, Magurran AE (2015) Exploratory behaviour and transmission of information between the invasive guppy and native Mexican topminnows. Anim Behav 106:115–120Google Scholar
  14. Clark CW (1994) Antipredator behavior and the asset-protection principle. Behav Ecol 5(2):159–170Google Scholar
  15. Clayton NS, Krebs JR (1994) Hippocampal growth and attrition in birds affected by experience. Proc Natl Acad Sci 91(16):7410–7414Google Scholar
  16. Colgan P (1993) The motivational basis of feeding behaviour. In: Pitcher TJ (ed) Behaviour of teleost fishes. Chapman & Hall, London, pp 31–55Google Scholar
  17. Darwin C (1859) The origin of species by means of natural selection, or the preservation of favored races in the struggle for life. AL BurtGoogle Scholar
  18. Dinse HR (2004) Sound case for enrichment. Focus on “environmental enrichment improves response strength, threshold, selectivity, and latency of auditory cortex neurons”. J Neurophysiol 92(1):36–37Google Scholar
  19. Dodson JJ (1988) The nature and role of learning in the orientation and migratory behavior of fishes. Environ Biol Fish 23(3):161–182Google Scholar
  20. Dukas R (2013) Effects of learning on evolution: robustness, innovation and speciation. Anim Behav 85(5):1023–1030Google Scholar
  21. Ebbesson LOE, Braithwaite VA (2012) Environmental effects on fish neural plasticity and cognition. J Fish Biol 81(7):2151–2174Google Scholar
  22. Fox C, Merali Z, Harrison C (2006) Therapeutic and protective effect of environmental enrichment against psychogenic and neurogenic stress. Behav Brain Res 175(1):1–8Google Scholar
  23. Galef BG, Laland KN (2005) Social learning in animals: empirical studies and theoretical models. AIBS Bull 55(6):489–499Google Scholar
  24. Ghalambor CK, McKay JK, Carroll SP, Reznick DN (2007) Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct Ecol 21(3):394–407Google Scholar
  25. Harburger LL, Nzerem CK, Frick KM (2007) Single enrichment variables differentially reduce age-related memory decline in female mice. Behav Neurosci 121(4):679Google Scholar
  26. Healy SD, Gwinner E, Krebs JR (1996) Hippocampal volume in migratory and non-migratory warblers: effects of age and experience. Behav Brain Res 81(1–2):61–68Google Scholar
  27. Kelley JL, Magurran AE (2003) Learned predator recognition and antipredator responses in fishes. Fish Fish 4(3):216–226Google Scholar
  28. Kihslinger RL, Lema SC, Nevitt GA (2006) Environmental rearing conditions produce forebrain differences in wild Chinook salmon Oncorhynchus tshawytscha. Comp Biochem Physiol A Mol Integr Physiol 145(2):145–151Google Scholar
  29. Kistler C, Hegglin D, Würbel H, König B (2011) Preference for structured environment in zebrafish (Danio rerio) and checker barbs (Puntius oligolepis). Appl Anim Behav Sci 135(4):318–327Google Scholar
  30. Kotrschal A, Taborsky B (2010) Environmental change enhances cognitive abilities in fish. PLoS Biol 8(4):e1000351Google Scholar
  31. Kotrschal K, Van Staaden MJ, Huber R (1998) Fish brains: evolution and environmental relationships. Rev Fish Biol Fish 8(4):373–408Google Scholar
  32. Krebs JR (1990) Food-storing birds: adaptive specialization in brain and behaviour? Philos Trans R Soc Lond B 329(1253):153–160Google Scholar
  33. Krebs JR, Clayton NS, Healy SD, Cristol DA, Patel SN, Jolliffe AR (1996) The ecology of the avian brain: food-storing memory and the hippocampus. Ibis 138(1):34–46Google Scholar
  34. Leggio MG, Mandolesi L, Federico F, Spirito F, Ricci B, Gelfo F, Petrosini L (2005) Environmental enrichment promotes improved spatial abilities and enhanced dendritic growth in the rat. Behav Brain Res 163(1):78–90Google Scholar
  35. Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits, vol 1. Sinauer, Sunderland, pp 535–557Google Scholar
  36. Markel RW (1994) An adaptive value of spatial learning and memory in the blackeye goby, Coryphopterus nicholsi. Ani Behav 47(6):1462–1464Google Scholar
  37. Makino H, Masuda R, Tanaka M (2015) Environmental stimuli improve learning capability in striped knifejaw juveniles: the stage-specific effect of environmental enrichment and the comparison between wild and hatchery-reared fish. Fish Sci 81(6):1035–1042Google Scholar
  38. Martins J, Almada F, Gonçalves A, Duarte-Coelho P, Jorge PE (2017) Home sweet home: evidence for nest-fidelity in the rocky intertidal fish, the shanny Lipophrys pholis. J Fish Biol 90(1):156–166Google Scholar
  39. Mathews F, Orros M, McLaren G, Gelling M, Foster R (2005) Keeping fit on the ark: assessing the suitability of captive-bred animals for release. Biol Cons 121(4):569–577Google Scholar
  40. Mery F, Burns JG (2010) Behavioural plasticity: an interaction between evolution and experience. Evol Ecol 24(3):571–583Google Scholar
  41. Mery F, Kawecki TJ (2003) A fitness cost of learning ability in Drosophila melanogaster. Proc R Soc Lond B Biol Sci 270(1532):2465–2469Google Scholar
  42. Millidine KJ, Armstrong JD, Metcalfe NB (2006) Presence of shelter reduces maintenance metabolism of juvenile salmon. Funct Ecol 20(5):839–845Google Scholar
  43. Näslund J, Johnsson JI (2016) Environmental enrichment for fish in captive environments: effects of physical structures and substrates. Fish Fish 17(1):1–30Google Scholar
  44. Näslund J, Aarestrup K, Thomassen ST, Johnsson JI (2012) Early enrichment effects on brain development in hatchery-reared Atlantic salmon (Salmo salar): no evidence for a critical period. Can J Fish Aquat Sci 69(9):1481–1490Google Scholar
  45. Näslund J, Rosengren M, Del Villar D, Gansel L, Norrgård JR, Persson L, Winkowski JJ, Kvingedal E (2013) Hatchery tank enrichment affects cortisol levels and shelter-seeking in Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 70(4):585–590Google Scholar
  46. Nussey DH, Wilson AJ, Brommer JE (2007) The evolutionary ecology of individual phenotypic plasticity in wild populations. J Evol Biol 20(3):831–844Google Scholar
  47. Odling-Smee L, Braithwaite VA (2003) The influence of habitat stability on landmark use during spatial learning in the three-spined stickleback. Anim Behav 65(4):701–707Google Scholar
  48. Odling-Smee L, Boughman JW, Braithwaite VA (2008) Sympatric species of threespine stickleback differ in their performance in a spatial learning task. Behav Ecol Sociobiol 62(12):1935–1945Google Scholar
  49. Odling-Smee L, Simpson SD, Braithwaite VA (2011) The role of learning in fish orientation. In: Brown C, Laland K, Krause J (eds) Fish cognition and behavior. Wiley, Oxford, pp 166–185Google Scholar
  50. Park PJ, Chase I, Bell MA (2012) Phenotypic plasticity of the threespine stickleback Gasterosteus aculeatus telencephalon in response to experience in captivity. Curr Zool 58(1):189–210Google Scholar
  51. Pigliucci M (2001) Phenotypic plasticity: beyond nature and nurture. JHU Press, BaltimoreGoogle Scholar
  52. Price TD, Qvarnström A, Irwin DE (2003) The role of phenotypic plasticity in driving genetic evolution. Proc R Soc Lond B Biol Sci 270(1523):1433–1440Google Scholar
  53. Relyea RA (2003) Predators come and predators go: the reversibility of predator-induced traits. Ecology 84(7):1840–1848Google Scholar
  54. Robinson BW, Dukas R (1999) The influence of phenotypic modifications on evolution: the Baldwin effect and modern perspectives. Oikos 85:582–589Google Scholar
  55. Rosenzweig MR, Bennett EL (1996) Psychobiology of plasticity: effects of training and experience on brain and behavior. Behav Brain Res 78(1):57–65Google Scholar
  56. Salvanes AGV, Braithwaite VA (2005) Exposure to variable spatial information in the early rearing environment generates asymmetries in social interactions in cod (Gadus morhua). Behav Ecol Sociobiol 59(2):250Google Scholar
  57. Salvanes AG, Moberg O, Braithwaite VA (2007) Effects of early experience on group behaviour in fish. Anim Behav 74(4):805–811Google Scholar
  58. Salvanes AGV, Moberg O, Ebbesson LO, Nilsen TO, Jensen KH, Braithwaite VA (2013) Environmental enrichment promotes neural plasticity and cognitive ability in fish. Proc R Soc B 280(1767):20131331Google Scholar
  59. Sherwin CM (2004) The influences of standard laboratory cages on rodents and the validity of research data. Anim Welf 13(1):9–15Google Scholar
  60. Shettleworth SJ (1995) Memory in food-storing birds: from the field to the skinner box. In: Proceedings of NATO advanced study institute series Maratea, Italy, pp 158–179Google Scholar
  61. Shettleworth SJ, Hampton RR (1998) Adaptive specializations of spatial cognition in food storing birds? Approaches to testing a comparative hypothesis. In: Pepperberg I, Balda R, Kamil A (eds) Animal cognition in nature. Academic Press, San Diego, CA, pp 65–98Google Scholar
  62. Sih A, Bell A, Johnson JC (2004) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19(7):372–378Google Scholar
  63. Spence R, Magurran AE, Smith C (2011) Spatial cognition in zebrafish: the role of strain and rearing environment. Anim Cogn 14(4):607–612Google Scholar
  64. Strand DA, Utne-Palm AC, Jakobsen PJ, Braithwaite VA, Jensen KH, Salvanes AG (2010) Enrichment promotes learning in fish. Mar Ecol Prog Ser 412:273–282Google Scholar
  65. Thacker CE, Roje DM (2011) Phylogeny of Gobiidae and identification of gobiid lineages. Syst Biodivers 9(4):329–347Google Scholar
  66. Thia JA, Riginos C, Liggins L, Figueira WF, McGuigan K, Bassar R (2018) Larval traits show temporally consistent constraints, but are decoupled from postsettlement juvenile growth, in an intertidal fish. J Anim Ecol 87(5):1353–1363Google Scholar
  67. Toms CN, Echevarria DJ, Jouandot DJ (2010) A methodological review of personality-related studies in fish: focus on the shy-bold axis of behavior. Int J Comp Psychol 23:1–25Google Scholar
  68. Ullah I, Zuberi A, Khan KU, Ahmad S, Thörnqvist PO, Winberg S (2017) Effects of enrichment on the development of behaviour in an endangered fish mahseer (Tor putitora). Appl Anim Behav Sci 186:93–100Google Scholar
  69. West-Eberhard MJ (1989) Phenotypic plasticity and the origins of diversity. Ann Rev Ecol Syst 20(1):249–278Google Scholar
  70. White GE, Brown C (2014a) Cue choice and spatial learning ability are affected by habitat complexity in intertidal gobies. Behav Ecol 26(1):178–184Google Scholar
  71. White GE, Brown C (2014b) A comparison of spatial learning and memory capabilities in intertidal gobies. Behav Ecol Sociobiol 68(9):1393–1401Google Scholar
  72. White GE, Brown C (2015a) Microhabitat use affects brain size and structure in intertidal gobies. Brain Behav Evol 85(2):107–116Google Scholar
  73. White GE, Brown C (2015b) Microhabitat use affects goby (Gobiidae) cue choice in spatial learning task. J Fish Biol 86(4):1305–1318Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Biological SciencesMacquarie UniversityNorth RydeAustralia

Personalised recommendations