Rainbow trout discriminate 2-D photographs of conspecifics from distracting stimuli using an innovative operant conditioning device.
Alternative forced-choice test
Categorization
Conspecific recognition
Object recognition
Operant conditioning
Rainbow trout
Journal
Learning & behavior
ISSN: 1543-4508
Titre abrégé: Learn Behav
Pays: United States
ID NLM: 101155056
Informations de publication
Date de publication:
09 2021
09 2021
Historique:
accepted:
23
11
2020
pubmed:
8
1
2021
medline:
11
9
2021
entrez:
7
1
2021
Statut:
ppublish
Résumé
Cognitive abilities were studied in rainbow trout, the first continental fish production in Europe. Increasing public concern for the welfare of farmed-fish species highlighted the need for better knowledge of the cognitive status of fish. We trained and tested 15 rainbow trout with an operant conditioning device composed of self-feeders positioned in front of visual stimuli displayed on a screen. The device was coupled with a two-alternative forced-choice (2-AFC) paradigm to test whether rainbow trout can discriminate 2-D photographs of conspecifics (S+) from different visual stimuli (S-). The S- were applied in four stages, the last three stages representing increasing discrimination difficulty: (1) blue shapes; (2) black shape (star); (3) photograph of an object (among a pool of 60); (4) photograph of another fish species (among a pool of 60). Nine fish (out of 15) correctly managed to activate the conditioning device after 30-150 trials. The rainbow trout were able to discriminate images of conspecifics from an abstract shape (five individuals out of five) or objects (four out of five) but not from other fish species. Their ability to learn the category "fish shape" rather than distinguishing between conspecifics and heterospecifics is discussed. The successful visual discrimination task using this complex operant conditioning device is particularly remarkable and novel for this farmed-fish species, and could be exploited to develop cognitive enrichments in future farming systems. This device can also be added to the existing repertoire of testing devices suitable for investigating cognitive abilities in fish.
Identifiants
pubmed: 33409895
doi: 10.3758/s13420-020-00453-2
pii: 10.3758/s13420-020-00453-2
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
292-306Informations de copyright
© 2021. The Psychonomic Society, Inc.
Références
Agrillo, C., Piffer, L., & Bisazza, A. (2010). Large number discrimination by mosquitofish. PLoS One, 5(12), e15232. https://doi.org/10.1371/journal.pone.0015232 .
doi: 10.1371/journal.pone.0015232
pubmed: 21203508
pmcid: 3008722
Agrillo, C., & Bisazza, A. (2014). Spontaneous versus trained numerical abilities. A comparison between the two main tools to study numerical competence in non-human animals. Journal of Neuroscience Methods, 234, 82–91. https://doi.org/10.1016/j.jneumeth.2014.04.027 .
doi: 10.1016/j.jneumeth.2014.04.027
pubmed: 24793399
Alanara, A., & Brannas, E. (1996). Dominance in demand-feeding behaviour in arctic charr and rainbow trout: the effect of stocking density. Journal of Fish Biology, 48(2), 242–254. https://doi.org/10.1111/j.1095-8649.1996.tb01116.x .
doi: 10.1111/j.1095-8649.1996.tb01116.x
Ben-Simon, A., Ben-Shahar, O., Vasserman, G., Ben-Tov, M., & Segev, R. (2012). Visual acuity in the archerfish: behavior, anatomy, and neurophysiology. Journal of Vision, 12(12), 18. https://doi.org/10.1167/12.12.18 .
doi: 10.1167/12.12.18
pubmed: 23197770
Bloch, S., Froc, C., Pontiggia, A., & Yamamoto, K. (2019). Existence of working memory in teleosts: establishment of the delayed matching-to-sample task in adult zebrafish. Behavioural Brain Research, 370, 111924. https://doi.org/10.1016/j.bbr.2019.111924 .
doi: 10.1016/j.bbr.2019.111924
pubmed: 31028766
Brock, A. J., Sudwarts, A., Daggett, J., Parker, M. O., & Brennan, C. H. (2017). A fully automated computer-based ‘Skinner Box’ for testing learning and memory in zebrafish. BioRxiv, 110478. https://doi.org/10.1101/110478 .
Broglio, C., Rodriguez, F., & Salas, C. (2003). Spatial cognition and its neural basis in teleost fishes. Fish and Fisheries, 4(3), 247–255. https://doi.org/10.1046/j.1467-2979.2003.00128.x .
doi: 10.1046/j.1467-2979.2003.00128.x
Brown, G. E., & Smith, R. J. F. (1997). conspecific skin extracts elicit antipredator responses in juvenile rainbow trout (oncorhynchus mykiss). Canadian Journal of Zoology-Revue Canadienne De Zoologie, 75(11), 1916–1922. https://doi.org/10.1139/z97-821 .
doi: 10.1139/z97-821
Bshary, R., & Grutter, A. S. (2006). Image scoring and cooperation in a cleaner fish mutualism. Nature, 441(7096), 975–978. https://doi.org/10.1038/nature04755 .
doi: 10.1038/nature04755
pubmed: 16791194
Bshary, R., Wickler, W., & Fricke, H. (2002). Fish cognition: a primate's eye view. Animal Cognition, 5(1), 1–13. https://doi.org/10.1007/s10071-001-0116-5 .
doi: 10.1007/s10071-001-0116-5
pubmed: 11957395
Cañon Jones, H. A., Noble, C., Damsgård, B., & Pearce, G. P. (2012). Investigating the influence of predictable and unpredictable feed delivery schedules upon the behaviour and welfare of Atlantic salmon parr (Salmo salar) using social network analysis and fin damage. Applied Animal Behaviour Science, 138(1–2), 132–140. https://doi.org/10.1016/j.applanim.2012.01.019 .
Catania, A. C. (1975). Pigeons preference for free choice over forced choice as a function of number of free-choice alternatives. Bulletin of the Psychonomic Society, 6(4), 424–424.
Champ, C., Wallis, G., Vorobyev, M., Siebeck, U., & Marshall, J. (2014). Visual acuity in a species of coral reef fish: rhinecanthus aculeatus. Brain Behavior and Evolution, 83(1), 31–42. https://doi.org/10.1159/000356977 .
doi: 10.1159/000356977
Champagne, D. L., Hoefnagels, C. C. M., de Kloet, R. E., & Richardson, M. K. (2010). Translating rodent behavioral repertoire to zebrafish (danio rerio): relevance for stress research. Behavioural Brain Research, 214(2), 332-342. https://doi.org/10.1016/j.bbr.2010.06.001 .
Clark, D. L., & Stephenson, K. R. (1999). Response to video and computer-animated images by the tiger barb, puntius tetrazona. Environmental Biology of Fishes, 56(3), 317–324. https://doi.org/10.1023/A:1007549721631 .
doi: 10.1023/A:1007549721631
Colson, V., Cousture, M., Damasceno, D., Valotaire, C., Nguyen, T., Le Cam, A., & Bobe, J. (2019). Maternal temperature exposure impairs emotional and cognitive responses and triggers dysregulation of neurodevelopment genes in fish. PeerJ, 7, e6338. https://doi.org/10.7717/peerj.6338 .
doi: 10.7717/peerj.6338
pubmed: 30723624
pmcid: 6360074
Colson, V., Sadoul, B., Valotaire, C., Prunet, P., Gaumé, M., & Labbé, L. (2015). Welfare assessment of rainbow trout reared in a recirculating aquaculture system: comparison with a flow-through system. Aquaculture, 436(0), 151–159. https://doi.org/10.1016/j.aquaculture.2014.10.047 .
doi: 10.1016/j.aquaculture.2014.10.047
Culumber, Z. W. (2015). Early recognition and response to predator, heterospecific, and conspecific visual cues by multiple species of poeciliid fry. Behaviour, 152(11), 1463–1479. https://doi.org/10.1163/1568539x-00003287 .
doi: 10.1163/1568539x-00003287
DeLong, C. M., Barbato, S., O’Leary, T., & Wilcox, K. T. (2017). Small and large number discrimination in goldfish (Carassius auratus) with extensive training. Behavioural Processes, 141, 172–183. https://doi.org/10.1016/j.beproc.2016.11.011 .
doi: 10.1016/j.beproc.2016.11.011
pubmed: 27890598
FEAP (2017). FEAP Annual Report 2017. https://issuu.com/feapsec/docs/feap_ar2017 .
Fuss, T., Bleckmann, H., & Schluessel, V. (2014). Visual discrimination abilities in the gray bamboo shark (chiloscyllium griseum). Zoology (Jena), 117(2), 104–111. https://doi.org/10.1016/j.zool.2013.10.009 .
doi: 10.1016/j.zool.2013.10.009
Franks, B. (2018). Cognition as a cause, consequence, and component of welfare. In Advances in agricultural animal welfare: science and practice (p. 22). https://doi.org/10.1016/B978-0-08-101215-4.00001-8 .
doi: 10.1016/B978-0-08-101215-4.00001-8
Gabor, V., & Gerken, M. (2012). Cognitive testing in horses using a computer based apparatus. Applied Animal Behaviour Science, 139(3-4), 242–250. https://doi.org/10.1016/j.applanim.2012.04.010 .
doi: 10.1016/j.applanim.2012.04.010
Gaikwad, S., Stewart, A., Hart, P., Wong, K., Piet, V., Cachat, J., & Kalueff, A. V. (2011). Acute stress disrupts performance of zebrafish in the cued and spatial memory tests: the utility of fish models to study stress-memory interplay. Behavioural Processes, 87(2), 224–230. https://doi.org/10.1016/j.beproc.2011.04.004 .
doi: 10.1016/j.beproc.2011.04.004
pubmed: 21545830
Gerullis, P., & Schuster, S. (2014). Archerfish actively control the hydrodynamics of their jets. Current Biology, 24(18), 2156–2160. https://doi.org/10.1016/j.cub.2014.07.059 .
doi: 10.1016/j.cub.2014.07.059
pubmed: 25201684
Gierszewski, S., Bleckmann, H., & Schluessel, V. (2013). Cognitive abilities in malawi cichlids (Pseudotropheus sp.): matching-to-sample and image/mirror-image discriminations. PLoS One, 8(2), e57363. https://doi.org/10.1371/journal.pone.0057363 .
doi: 10.1371/journal.pone.0057363
pubmed: 23437376
pmcid: 3577734
Goldman, M., & Shapiro, S. (1979). Matching-to-sample and oddity-from-sample in goldfish. Journal of the Experimental Analysis of Behavior, 31(2), 259–266. https://doi.org/10.1901/jeab.1979.31-259 .
doi: 10.1901/jeab.1979.31-259
pubmed: 448261
pmcid: 1332827
Gómez-Laplaza, L. M., Díaz-Sotelo, E., & Gerlai, R. (2018). Quantity discrimination in angelfish, Pterophyllum scalare: A novel approach with food as the discriminant. Animal Behaviour, 142, 19–30. https://doi.org/10.1016/j.anbehav.2018.06.001 .
doi: 10.1016/j.anbehav.2018.06.001
Gómez-Laplaza, L. M., & Gerlai, R. (2013). The role of body surface area in quantity discrimination in angelfish (pterophyllum scalare). PLoS One, 8(12), e83880. https://doi.org/10.1371/journal.pone.0083880 .
doi: 10.1371/journal.pone.0083880
pubmed: 24386299
pmcid: 3873975
Goncalves, D. M., Oliveira, R. F., Korner, K., Poschadel, J. R., & Schlupp, I. (2000). Using video playbacks to study visual communication in a marine fish, salaria pavo. Animal Behaviour, 60, 351–357. https://doi.org/10.1006/anbe.2000.1459 .
doi: 10.1006/anbe.2000.1459
pubmed: 11007644
Griffiths, S. W., & Magurran, A. E. (1999). Schooling decisions in gunnies (poecilia reticulata) are based on familiarity rather than kin recognition by phenotype matching. Behavioral Ecology and Sociobiology, 45(6), 437–443. https://doi.org/10.1007/s002650050582 .
doi: 10.1007/s002650050582
Grosenick, L., Clement, T. S., & Fernald, R. D. (2007). Fish can infer social rank by observation alone. Nature, 445(7126), 429–432. https://doi.org/10.1038/nature05511 .
doi: 10.1038/nature05511
pubmed: 17251980
Herman, L. M., Gory, J. D., Hovancik, J. R., & Bradshaw, G. L. (1989). Generalization of visual matching by a bottlenosed dolphin (tursiops-truncatus) - evidence for invariance of cognitive performance with visual and auditory materials. Journal of Experimental Psychology-Animal Behavior Processes, 15(2), 124–136. https://doi.org/10.1037/0097-7403.15.2.124 .
doi: 10.1037/0097-7403.15.2.124
Hester, F. J. (1968). Visual contrast thresholds of the goldfish (Carassius auratus). Vision Research, 8(10), 1315–1336.
doi: 10.1016/0042-6989(68)90053-9
Höjesjö, J., Axelsson, M., Dahy, R., Gustavsson, L., & Johnsson, J. I. (2015). Sight or smell? Behavioural and heart rate responses in subordinate rainbow trout exposed to cues from dominant fish. PeerJ, 3. https://doi.org/10.7717/peerj.1169 .
Holmes, T. H., & McCormick, M. I. (2010). Smell, learn and live: the role of chemical alarm cues in predator learning during early life history in a marine fish. Behavioural Processes, 83(3), 299–305. https://doi.org/10.1016/j.beproc.2010.01.013 .
doi: 10.1016/j.beproc.2010.01.013
pubmed: 20117187
Horner, A. E., Heath, C. J., Hvoslef-Eide, M., Kent, B. A., Kim, C. H., Nilsson, S. R. O., et al. (2013). The touchscreen operant platform for testing learning and memory in rats and mice. Nature Protocols, 8(10), 1961–1984. https://doi.org/10.1038/nprot.2013.122 .
doi: 10.1038/nprot.2013.122
pubmed: 24051959
pmcid: 3914026
Ingraham, E., Anderson, N. D., Hurd, P. L., & Hamilton, T. J. (2016). Twelve-day reinforcement-based memory retention in african cichlids (labidochromis caeruleus). Frontiers in Behavioral Neuroscience, 10, 157. https://doi.org/10.3389/fnbeh.2016.00157 .
doi: 10.3389/fnbeh.2016.00157
pubmed: 27582695
pmcid: 4987340
Ioannou, C. C., Couzin, I. D., James, R., Croft, D. P., & Krause, J. (2011). Social organization and information transfer in schooling fish. In C. Brown, K. Laland, & J. Krause (Eds.), Fish cognition and behaviour (2nd ed.). Oxford: Wiley-Blackwell. https://doi.org/10.1002/9781444342536.ch10 .
doi: 10.1002/9781444342536.ch10
Johnsson, J. I. (1997). Individual recognition affects aggression and dominance relations in rainbow trout, oncorhynchus mykiss. Ethology, 103(4), 267–282. https://doi.org/10.1111/j.1439-0310.1997.tb00017.x .
doi: 10.1111/j.1439-0310.1997.tb00017.x
Johnsson, J. I., & Åkerman, A. (1998). Watch and learn : Preview of the fighting ability of opponents alters contest behaviour in rainbow trout. Animal Behaviour, 56(3), 771–776. https://doi.org/10.1006/anbe.1998.0824 .
doi: 10.1006/anbe.1998.0824
pubmed: 9784229
Johnston, N. K., & Dixson, D. L. (2017). Anemonefishes rely on visual and chemical cues to correctly identify conspecifics. Coral Reefs, 36, 903–912. https://doi.org/10.1007/s00338-017-1582-9 .
doi: 10.1007/s00338-017-1582-9
Jurado-Parras, M. T., Sanchez-Campusano, R., Castellanos, N. P., Pdel- Pozo, F., Gruart, A., & Delgado-Garcia, J. M. (2013). Differential contribution of hippocampal circuits to appetitive and consummatory behaviors during operant conditioning of behaving mice. Journal of Neuroscience, 33(6), 2293–2304. https://doi.org/10.1523/JNEUROSCI.1013-12.2013 .
doi: 10.1523/JNEUROSCI.1013-12.2013
pubmed: 23392660
Knight, M. E., & Turner, G. F. (1999). Reproductive isolation among closely related Lake Malawi cichlids : Can males recognize conspecific females by visual cues? Animal Behaviour, 58(4), 761–768. https://doi.org/10.1006/anbe.1999.1206 .
doi: 10.1006/anbe.1999.1206
pubmed: 10512649
Knolle, F., Goncalves, R. P., & Morton, A. J. (2017). Sheep recognize familiar and unfamiliar human faces from two-dimensional images. Royal Society Open Science, 4(11), 171228. https://doi.org/10.1098/rsos.171228 .
doi: 10.1098/rsos.171228
pubmed: 29291109
pmcid: 5717684
Kotrschal, A., & Taborsky, B. (2010). Environmental change enhances cognitive abilities in fish. PLoS Biology, 8(4), e1000351. https://doi.org/10.1371/journal.pbio.1000351 .
doi: 10.1371/journal.pbio.1000351
pubmed: 20386729
pmcid: 2850384
Kuroda, T., Mizutani, Y., Cancado, C. R. X., & Podlesnik, C. A. (2017). Reversal learning and resurgence of operant behavior in zebrafish (danio rerio). Behavioural Processes, 142, 79–83. https://doi.org/10.1016/j.beproc.2017.06.004 .
doi: 10.1016/j.beproc.2017.06.004
pubmed: 28633953
Langbein, J., Nurnberg, G., & Manteuffel, G. (2004). Visual discrimination learning in dwarf goats and associated changes in heart rate and heart rate variability. Physiology & Behavior, 82(4), 601–609. https://doi.org/10.1016/j.physbeh.2004.05.007 .
doi: 10.1016/j.physbeh.2004.05.007
Luchiari, A. C., & Pirhonen, J. (2008). Effects of ambient colour on colour preference and growth of juvenile rainbow trout oncorhynchus mykiss (walbaum). Journal of Fish Biology, 72(6), 1504–1514. https://doi.org/10.1111/j.1095-8649.2008.01824.x .
doi: 10.1111/j.1095-8649.2008.01824.x
Lucon-Xiccato, T., & Bisazza, A. (2014). Discrimination reversal learning reveals greater female behavioural flexibility in guppies. Biology Letters, 10(6), 20140206. https://doi.org/10.1098/rsbl.2014.0206 .
doi: 10.1098/rsbl.2014.0206
pmcid: 4090544
Maia, C. M., Ferguson, B., Volpato, G. L., & Braithwaite, V. A. (2017). Physical and psychological motivation tests of individual preferences in rainbow trout. Journal of Zoology, 302(2), 108–118. https://doi.org/10.1111/jzo.12438 .
doi: 10.1111/jzo.12438
Manteuffel, G., Langbein, J., & Puppe, B. (2009). From operant learning to cognitive enrichment in farm animal housing: bases and applicability. Animal Welfare, 18(1), 87–95.
Martins, C. I. M., Galhardo, L., Noble, C., Damsgard, B., Spedicato, M. T., Zupa, W., Beauchaud, M., Kulczykowska, E., Massabuau, J. C., Carter, T., Planellas, S. R., & Kristiansen, T. (2012). Behavioural indicators of welfare in farmed fish. Fish Physiology and Biochemistry, 38(1), 17–41. https://doi.org/10.1007/s10695-011-9518-8 .
doi: 10.1007/s10695-011-9518-8
pubmed: 21796377
Meehan, C. L., & Mench, J. A. (2007). The challenge of challenge: Can problem solving opportunities enhance animal welfare? Applied Animal Behaviour Science, 102(3-4), 246–261. https://doi.org/10.1016/j.applanim.2006.05.031 .
doi: 10.1016/j.applanim.2006.05.031
Mueller, K., & Neuhauss, S. (2012). Automated visual choice discrimination learning in zebrafish (Danio rerio). Journal of Integrative Neuroscience, 11, 73–85. https://doi.org/10.1142/S0219635212500057 .
doi: 10.1142/S0219635212500057
pubmed: 22744784
Näslund, J., & Johnsson, J. I. (2016). Environmental enrichment for fish in captive environments: effects of physical structures and substrates. Fish and Fisheries, 17(1), 1–30. https://doi.org/10.1111/faf.12088 .
doi: 10.1111/faf.12088
Neumeyer, C. (2003). Wavelength dependence of visual acuity in goldfish. Journal of Comparative Physiology A: Sensory, Neural, and Behavioral Physiology, 189(11), 811–821. https://doi.org/10.1007/s00359-003-0457-4 .
doi: 10.1007/s00359-003-0457-4
Newport, C., Wallis, G., & Siebeck, U. E. (2015). Same/different abstract concept learning by archerfish (toxotes chatareus). PLoS One, 10(11), e0143401. https://doi.org/10.1371/journal.pone.0143401 .
doi: 10.1371/journal.pone.0143401
pubmed: 26599071
pmcid: 4658121
Newport, C., Wallis, G., Temple, S. E., & Siebeck, U. E. (2013). Complex, context-dependent decision strategies of archerfish, toxotes chatareus. Animal Behaviour, 86(6), 1265–1274. https://doi.org/10.1016/j.anbehav.2013.09.031 .
doi: 10.1016/j.anbehav.2013.09.031
Oesterwind, S., Nürnberg, G., Puppe, B., & Langbein, J. (2016). Impact of structural and cognitive enrichment on the learning performance, behavior and physiology of dwarf goats (Capra aegagrus hircus). Applied Animal Behaviour Science, 177, 34–41. https://doi.org/10.1016/j.applanim.2016.01.006 .
doi: 10.1016/j.applanim.2016.01.006
Oliveira, J., Silveira, M., Chacon, D., & Luchiari, A. (2015). The zebrafish world of colors and shapes: preference and discrimination. Zebrafish, 12(2), 166–173. https://doi.org/10.1089/zeb.2014.1019 .
doi: 10.1089/zeb.2014.1019
pubmed: 25674976
Overli, O., Sorensen, C., Pulman, K. G., Pottinger, T. G., Korzan, W., Summers, C. H., & Nilsson, G. E. (2007). Evolutionary background for stress-coping styles: relationships between physiological, behavioral, and cognitive traits in non-mammalian vertebrates. Neuroscience & Biobehavioral Reviews, 31(3), 396–412. https://doi.org/10.1016/j.neubiorev.2006.10.006 .
doi: 10.1016/j.neubiorev.2006.10.006
Parker, M. O., Gaviria, J., Haigh, A., Millington, M. E., Brown, V. J., Combe, F. J., & Brennan, C. H. (2012). Discrimination reversal and attentional sets in zebrafish (danio rerio). Behavioural Brain Research, 232(1), 264–268. https://doi.org/10.1016/j.bbr.2012.04.035 .
doi: 10.1016/j.bbr.2012.04.035
pubmed: 22561034
pmcid: 4167590
Paśko, Ł. (2010). Tool-like behavior in the sixbar wrasse, Thalassoma hardwicke (Bennett, 1830). Zoo Biology, 29(6), 767–773. https://doi.org/10.1002/zoo.20307 .
doi: 10.1002/zoo.20307
pubmed: 20095003
Rodriguez, F., Duran, E., Vargas, J. P., Torres, B., & Salas, C. (1994). Performance of goldfish trained in allocentric and egocentric maze procedures suggests the presence of a cognitive mapping system in fishes. Animal Learning & Behavior, 22(4), 409–420. https://doi.org/10.3758/bf03209160 .
doi: 10.3758/bf03209160
Roux, N., Duran, E., Lanyon, R. G., Frederich, B., Berthe, C., Besson, M., Dixson, D. L., & Lecchini, D. (2016). Brain lateralization involved in visual recognition of conspecifics in coral reef fish at recruitment. Animal Behaviour, 117, 3–8. https://doi.org/10.1016/j.anbehav.2016.04.011 .
doi: 10.1016/j.anbehav.2016.04.011
Roy, T., Suriyampola, P. S., Flores, J., López, M., Hickey, C., Bhat, A., & Martins, E. P. (2019). Color preferences affect learning in zebrafish, Danio rerio. Scientific Reports, 9, 14531. https://doi.org/10.1038/s41598-019-51145-5 .
doi: 10.1038/s41598-019-51145-5
pubmed: 31601932
pmcid: 6787237
Santacà, M., Busatta, M., Lucon-Xiccato, T., & Bisazza, A. (2019). Sensory differences mediate species variation in detour task performance. Animal Behaviour, 155, 153–162. https://doi.org/10.1016/j.anbehav.2019.05.022 .
doi: 10.1016/j.anbehav.2019.05.022
Satoh, S., Tanaka, H., & Kohda, M. (2016). Facial recognition in a discus fish (cichlidae): experimental approach using digital models. PLoS One, 11(5). https://doi.org/10.1371/journal.pone.0154543 .
Salvanes, A. G., Moberg, O., Ebbesson, L. O., Nilsen, T. O., Jensen, K. H., & Braithwaite, V. A. (2013). Environmental enrichment promotes neural plasticity and cognitive ability in fish. Proceedings Biological Sciences, 280(1767), 20131331. https://doi.org/10.1098/rspb.2013.1331 .
doi: 10.1098/rspb.2013.1331
pubmed: 23902903
pmcid: 3735255
Schluessel, V., Fricke, G., & Bleckmann, H. (2012). Visual discrimination and object categorization in the cichlid Pseudotropheus sp. Animal Cognition, 15(4), 525–537. https://doi.org/10.1007/s10071-012-0480-3 .
doi: 10.1007/s10071-012-0480-3
pubmed: 22434402
Seger, C. A., & Miller, E. K. (2010). Category learning in the brain. Annual Review of Neuroscience, 33, 203–219. https://doi.org/10.1146/annurev.neuro .
doi: 10.1146/annurev.neuro
pubmed: 20572771
pmcid: 3709834
Shettleworth, S. J. (2009). Cognition, evolution, and behavior. Oxford University Press.
Sidman, M., Rauzin, R., Lazar, R., Cunningham, S., Tailby, W., & Carrigan, P. (1982). A Search for symmetry in the conditional discriminations of rhesus monkeys, baboons, and children. Journal of the Experimental Analysis of Behavior, 37(1), 23–44. https://doi.org/10.1901/jeab.1982.37-23 .
doi: 10.1901/jeab.1982.37-23
pubmed: 7057127
pmcid: 1333116
Siebeck, U. E., Litherland, L., & Wallis, G. M. (2009). Shape learning and discrimination in reef fish. Journal of Experimental Biology, 212(13), 2113–2119. https://doi.org/10.1242/jeb.028936 .
doi: 10.1242/jeb.028936
Sovrano, V. A., & Bisazza, A. (2008). Recognition of partly occluded objects by fish. Animal Cognition, 11(1), 161–166. https://doi.org/10.1007/s10071-007-0100-9 .
doi: 10.1007/s10071-007-0100-9
pubmed: 17636365
Speedie, N., & Gerlai, R. (2008). Alarm substance induced behavioral responses in zebrafish (danio rerio). Behavioural Brain Research, 188(1), 168–177. https://doi.org/10.1016/j.bbr.2007.10.031 .
doi: 10.1016/j.bbr.2007.10.031
pubmed: 18054804
Strand, D. A., Utne-Palm, A. C., Jakobsen, P. J., Braithwaite, V. A., Jensen, K. H., & Salvanes, A. G. V. (2010). Enrichment promotes learning in fish. Marine Ecology Progress Series, 412, 273–282. https://doi.org/10.3354/meps08682 .
doi: 10.3354/meps08682
Vavrek, M. A., & Brown, G. E. (2009). Threat-sensitive responses to disturbance cues in juvenile convict cichlids and rainbow trout. Annales Zoologici Fennici, 46(3), 171–180. https://doi.org/10.5735/086.046.0302 .
doi: 10.5735/086.046.0302
von der Emde, G., & Fetz, S. (2007). Distance, shape and more: recognition of object features during active electrolocation in a weakly electric fish. Journal of Experimental Biology, 210(17), 3082-3095. https://doi.org/10.1242/jeb.005694 .
Vonk, J. (2003). Gorilla (gorilla gorilla gorilla) and orangutan (pongo abelii) understanding of first- and second-order relations. Animal Cognition, 6(2), 77–86. https://doi.org/10.1007/s10071-003-0159-x .
doi: 10.1007/s10071-003-0159-x
pubmed: 12687418
Wyzisk, K., & Neumeyer, C. (2007). Perception of illusory surfaces and contours in goldfish. Visual Neuroscience, 24, 291–298. https://doi.org/10.1017/S095252380707023X .
doi: 10.1017/S095252380707023X
pubmed: 17822573
Zerbolio, D. J., & Royalty, J. L. (1983). Matching and oddity conditional discrimination in the goldfish as avoidance responses: evidence for conceptual avoidance learning. Animal Learning & Behavior, 11(3), 341–348. https://doi.org/10.3758/bf03199786 .
doi: 10.3758/bf03199786