Abstract
The ability to orient and navigate within a certain environment is essential for all animals, and spatial memory enables animals to remember the locations of such markers as predators, home, and food. Here we report that the migratory marine cardinalfish Apogon notatus has the potential to retain long-term spatial memory comparable to that of other animals. Female A. notatus establish a small territory on a shallow boulder bottom to pair and spawn with males. We carried out field research in two consecutive breeding seasons on territory settlement by individually marked females. Females maintained a territory at the same site throughout one breeding season. After overwintering in deep water, many of them (82.1%) returned to their breeding ground next spring and most occupied the same site as in the previous season, with only a 0.56 m shift on average. Our results suggest that female A. notatus have long-distance homing ability to pinpoint the exact location of their previous territory, and retain spatial memory for as long as 6 months.
This is a preview of subscription content, log in via an institution to check access.
References
Aronson LR (1971) Further studies on orientation and jumping behavior in the gobbied fish, Bathygobius soporator. Ann N Y Acad Sci 188:378–392. doi:10.1111/j.1749-6632.1971.tb13110.x
Balda RP, Kamil AC (1998) The ecology and evolution of spatial of spatial memory in corvids of the southwestern USA: the perplexing pinyon jay. In: Balda RP, Pepperberg IM, Kamil AC (eds) Animal cognition in nature. Academic Press, London, pp 29–64
Braithwaite VA, Armstrong JD, McAdam HM, Huntingford FA (1996) Can juvenile Atlantic salmon use multiple cue systems in spatial learning? Anim Behav 51:1409–1415. doi:10.1006/anbe.1996.0144
Broglio C, Gómez A, Durán E, Ocaña FM, Jiménez-Moya F, Rodríguez F, Salas C (2005) Hallmarks of a common forebrain vertebrate plan: Specialized pallial areas for spatial, temporal and emotional memory in actinopterygian fish. Brain Res Bull 57:499–503. doi:10.1016/j.brainresbull.2005.03.021
Brown C (2001) Familiarity with the test environment improves escape responses in the crimson spotted rainbowfish, Melanotaenia duboulayi. Anim Cogn 4:109–113. doi:10.1007/s100710100105
Chiandetti C, Vallortigara G (2008) Spatial reorientation in large and small enclosures: comparative and developmental perspectives. Cogn Process 9:229–238. doi:10.1007/s10339-008-0202-6
Clayton NS (1998) Memory and the hippocampus in food-storing birds: a comparative approach. Neuropharmacology 37:441–452. doi:10.1016/S0028-3908(98)00037-9
Cooper JC, Hasler AD (1974) Electroencephalographic evidence for retention of olfactory cues in homing coho salmon. Science 25:336–338. doi:10.1126/science.183.4122.336
Døving KB, Stabell OB, Östlund-Nilsson S, Fisher R (2006) Site fidelity and homing in tropical coral reef cardinalfish: are they using olfactory cues? Chem Senses 31:265–272. doi:oi:10.1111/j.1095-8649.2000.tb02234.x
Fukumori K, Okuda N, Hamaoka H, Fukumoto T, Takahashi D, Omori K (2008) Stable isotopes reveal life history polymorphism in the coastal fish, Apogon notatus. Mar Ecol Prog Ser 362:279–289. doi:10.3354/meps07397
Fukumori K, Okuda N, Yanagisawa Y (2009) Female territoriality in a paternal mouthbrooding cardinalfish to avoid predation against spawned eggs. Can J Zool 87:508–514. doi:10.1139-Z09-037
Gibson B, Kamil A (2009) The synthetic approach to the study of spatial memory: Have we properly addressed Tinbergen’s “four questions”? Behav Proc 80:278–287. doi:10.1016/j.beproc.2008.11.013
Hansen LP, Jonsson N, Jonsson B (1993) Oceanic migration in homing Atlantic salmon. Anim Behav 45:927–941. doi:10.1006/anbe.1993.1112
Healy SD, De Kort SR, Clayton NS (2005) The hippocampus, spatial memory and food hoarding: a puzzle revisited. Trends Ecol Evol 20:17–22. doi:10.1016/j.tree.2004.10.006
Hughes RN, Blight CM (1999) Algorithmic behaviour and spatial memory are used by two intertidal fish species to solve the radial maze. Anim Behav 58:601–613. doi:10.1006/anbe.1999.1193
Hughes RN, Blight CM (2000) Two intertidal fish species use visual association learning to track the status of food patches in a radial maze. Anim Behav 59:613–621. doi:10.1006/anbe.1999.1351
Kalmijn AJ (2000) Detection and processing of electromagnetic and near-eld acoustic signals in elasmobranch fishes. Phil Trans R Soc Lond B 355:1135–1141. doi:10.1098/rstb.2000.0654
Kolm N, Hoffman EA, Olsson J, Berglund A, Jones AG (2005) Group stability and homing behavior but no kin group structures in a coral reef fish. Behav Ecol 16:521–527. doi:10.1093/beheco/ari022
Lamanna JR, Eason PK (2003) Effects of landmarks on territorial establishment. Anim Behav 65:471–478. doi:10.1006/anbe.2003.2095
Lindauer M (1963) Allgemeine Sinnesphysiologie. Orientierung im Raum. Fortschr Zool 16:58–140
Macdonald IMV (1997) Field experiments on duration and precision of grey and red squirrel spatial memory. Anim Behav 54:879–891. doi:10.1006/anbe.1996.0528
Mackney PA, Hughes RN (1995) Foraging behaviour and memory window in sticklebacks. Behaviour 132:1241–1253. doi:10.1163/156853995X00559
Markel RW (1994) An adaptive value of spatial learning and memory in the blackeye goby, Coryphopterus nicholsi. Anim Behav 47:1462–1464. doi:10.1006/anbe.1994.1194
Marnane MJ (2000) Site fidelity and homing behaviour in coral reef cardinalfishes. J Fish Biol 57:1590–1600. doi:10.1111/j.1095-8649.2000.tb02234.x
Milinski M (1994) Long-term memory for food patches and implications for ideal free distributions in sticklebacks. Ecology 75:1150–1156
Nevitt GA, Dittman AH, Quinn TP, Moody WJJ (1994) Evidence for a peripheral olfactory memory in imprinted salmon. Proc Natl Acad Sci USA 91:4288–4292
Nishi T, Kawamura G (2005) Anguilla japonica is already magnetosensitive at the glass eel phase. J Fish Biol 67:1213–1224. doi:10.1111/j.1095-8649.2005.00817.x
Odling-Smee L, Simpson S, Braithwaite VA (2006) The role of learning in fish orientation. In: Brown C, Laland K, Krause J (eds) Fish cognition and behavior. Blackwell Publishing, West Sussex, pp 119–138
Okuda N (1999) Sex roles are not always reversed when the potential reproductive rate is higher in females. Am Nat 153:540–548. doi:10.1086/303196
Parkyn DC, Austin JD, Hawryshyn CW (2003) Acquisition of polarized-light orientation in salmonids under laboratory conditions. Anim Behav 65:893–904. doi:10.1006/anbe.2003.2136
Rosengren R (1971) Route fidelity, visual memory and recruitment behaviour in foraging wood ants of genus Formica (Hymenopterus, Formicidae). Acta Zool Fenn 133:1–106
Rosengren R, Fortelius W (1986) Ortstreue in foraging ants of the Formica rufa group—hierarchy of orienting cues and long-term memory. Insect Soc 33:306–334
Salas C, Broglio C, Rodríguez F, López JC, Portavella M, Torres B (1996) Telencephalic ablation in goldfish impairs performance in a ‘spatial constancy’ problem but not in a cued one. Behav Brain Res 79:193–200. doi:10.1016/0166-4328(96)00014-9
Sovrano VA, Bisazza A (2003) Modularity as a fish views it: conjoining geometric and nongeometric information for spatial reorientation. J Exp Psychol: Anim Behav Process 29:199–210. doi:10.1037/0097-7403.29.3.199
Sovrano VA, Bisazza A, Vallortigara G (2002) Modularity and spatial reorientation in a simple mind: encoding of geometric and non-geometric properties of a spatial environment by fish. Cognition 85:B51–B59. doi:10.1016/S0010-0277(02)00110-5
Sovrano VA, Bisazza A, Vallortigara G (2005) Animals’ use of land-marks and metric information to reorient: effects of the size of the experimental space. Cognition 97:121–133. doi:10.1016/j.cognition.2004.08.003
Sovrano VA, Bisazza A, Vallortigara G (2007) How fish do geometry in large and in small spaces. Anim Cogn 10:47–54. doi:10.1007/s10071-006-0029-4
Vargas JP, Lopez JC, Salas C, Thinus-Blanc C (2004) Encoding of geometric and featural spatial information by goldfish (Carassius auratus). J Comp Psychol 118:206–216
Warburton K (1990) The use of local landmarks by foraging goldfish. Anim Behav 40:500–505. doi:10.1016/S0003-3472(05)80530-5
Acknowledgments
We would like to thank three anonymous referees for their advices, which have significantly improved the paper. We are grateful to Sosuke Oguri for providing a photograph of A. notatus habitat. This study was financially supported by a Grant for Biodiversity Research of the 21st century COE (A14).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Fukumori, K., Okuda, N., Yamaoka, K. et al. Remarkable spatial memory in a migratory cardinalfish. Anim Cogn 13, 385–389 (2010). https://doi.org/10.1007/s10071-009-0285-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10071-009-0285-1