Something worth remembering: visual discrimination in sharks
Tóm tắt
This study investigated memory retention capabilities of juvenile gray bamboo sharks (Chiloscyllium griseum) using two-alternative forced-choice experiments. The sharks had previously been trained in a range of visual discrimination tasks, such as distinguishing between squares, triangles and lines, and their corresponding optical illusions (i.e., the Kanizsa figures or Müller–Lyer illusions), and in the present study, we tested them for memory retention. Despite the absence of reinforcement, sharks remembered the learned information for a period of up to 50 weeks, after which testing was terminated. In fish, as in other vertebrates, memory windows vary in duration depending on species and task; while it may seem beneficial to retain some information for a long time or even indefinitely, other information may be forgotten more easily to retain flexibility and save energy. The results of this study indicate that sharks are capable of long-term memory within the framework of selected cognitive skills. These could aid sharks in activities such as food retrieval, predator avoidance, mate choice or habitat selection and therefore be worth being remembered for extended periods of time. As in other cognitive tasks, intraspecific differences reflected the behavioral breadth of the species.
Tài liệu tham khảo
Aronson LR (1951) Orientation and jumping behavior in the gobiid fish Bathygobius soporator. Am Mus Nov 1486:1–22
Aronson LR (1971) Further studies on orientation and jumping behavior in the gobiid fish, Bathygobius soporator. Ann N Y Acad Sci 188:378–392. doi:10.1111/j.1749-6632.1971.tb13110.x
Berryhill ME, Olson IR (2008) The right parietal lobe is critical for visual working memory. Neuropsychologia 46(7):1767–1774
Beukema JJ (1970) Angling experiments with carp (Cyprinus carpio L.). II: decreasing catchability through one-trial learning. Neth J Zool 20:81–92
Brown C (2001) Familiarity with the test environment improves the escape responses in the crimson spotted rainbow fish, Melanotaenia duboulayi. Anim Cogn 4:109–113
Brown C, Gardner C, Braithwaite VA (2004) Population variation in lateralised eye use in the poeciliid Brachyraphis episcopi. Proc R Soc Lond B 271:S455–S457
Bryan JE, Larkin PA (1972) Food specialization by individual trout. J Bull Fish Res Board Can 29:1615–1624
Bshary R, Wickler W, Fricke H (2002) Fish cognition: a primate’s eye view. Anim Cogn 5:1–13
Burns JG, Foucaud J, Mery F (2011) Costs of memory: lessons from ‘mini’ brains. Proc R Soc B 278:923–929
Chittka L, Niven J (2009) Are bigger brains better? Curr Biol 19(21):R995–R1008
Clark E (1959) Instrumental conditioning of lemon sharks. Science 130:217–218
Clayton NA, Krebs JA (1994) Memory for spatial and object-specific cues in food-storing and non-storing birds. J Comp Physiol A 174:371–379
Croy MI, Hughes RN (1991) The role of learning and memory in the feeding behavior of the fifteen-spined stickleback, Spinachia spinachia L. Anim Behav 41:149–159
Csányi V, Csizmadia G, Miklósi Á (1989) Long-term memory and recognition of another species in the paradise fish. Anim Behav 37:908–911
Cuthill IC, Kacelnik A, Krebs JR, Haccou P, Iwasa Y (1990) Starlings exploiting patches: the effect of recent experience on foraging decisions. Anim Behav 40:625–640
Davis KM, Burghardt GM (2012) Long-term retention of visual tasks by two species of emydid turtles, Pseudemys nelsoni and Trachemys scripta. J Comp Pyschol 126(3):213–223
De Haan EHF, Appels B, Aleman A, Postma A (2000) Inter- and intramodal encoding of auditory and visual presentation of material: effects on memory performance. Psychol Rec 50:577–586
Dudai Y (1989) The neurobiology of memory: concepts, findings, trends. Oxford University Press, Oxford
Dugatkin LA, Wilson DS (1992) The prerequisites for strategic behavior in bluegill sunfish, Lepomis macrochirus. Anim Behav 44:223–230
Dukas R (1999) Costs of memory: ideas and predictions. J Theor Biol 197(1):41–50
Fricke H (1974) Öko-Ethologie des monogamen Anemonenfisches Amphiprion bicinctus. Z Tierpsychol 36:429–512
Fukumori K, Okuda N, Yamaoka K, Yanagisawa Y (2009) Remarkable spatial memory in a migratory cardinalfish. Anim Cogn 13:385–389
Fuss T, Bleckmann H, Schluessel V (2014a) Visual discrimination abilities in the gray bamboo shark (Chiloscyllium griseum). Zoology 17(2):104–111
Fuss T, Bleckmann H, Schluessel V (2014b) The brain creates illusions not just for us: sharks (Chiloscyllium griseum) can see the magic as well. Front Neural Circuits 8:1–17
Fuster JM (1995) Memory in the cerebral cortex. MIT Press, Cambridge
Gegear RJ, Laverty TM (1998) How many flower types can bumblebees forage on at the same time? Can J Zool 76(7):1358–1365
Goelet P, Castellucci VF, Schacher S, Kandel ER (1986) The long and the short of long-term memory—a molecular framework. Nature 322:419–422
Goldsmith M (1914) Les reactions physiologiques et psychiques des poissons. Bull Inst Gén Psychol 14:97–228
Goulson D, Stout JC, Hawson SA (1997) Can flower constancy in nectaring butterflies be explained by Darwin’s interference hypothesis? Oecologia 112:225–231
Guttridge TL, Brown C (2014) Learning and memory in the Port Jackson shark, Heterodontus portusjacksoni. Anim Cogn 17(2):415–425
Hampton RR, Shettleworth S (1996) Hippocampal lesions impair memory for location but not color in passerine birds. Behav Neurosci 110:831–835
Kamil AC, Balda RP (1985) Cache recovery and spatial memory in Clark’s nutcrackers (Nucifraga columbiana). J Exp Psychol Anim B 11(1):95–111
Kamil AC, Balda RP (1990) Spatial memory in seed-caching corvids. Psychol Learn Motiv 26:1–25
Kelley CR (1969) What is adaptive training? Hum Factors 11(6):547–556
Kimber J, Sims D, Bellamy P, Gill AB (2014) Elasmobranch cognitive ability: using electroreceptive foraging behaviour to demonstrate learning, habituation and memory in a benthic shark. Anim Cogn 17(1):55–65
Kraemer PJ, Golding JM (1997) Adaptive forgetting in animals. Psychon Bull Rev 4:480–491
Lewis CA (1986) Memory constraints and flower choice in Pieris rapae. Science 232:863–865
Mackney PA, Hughes RN (1995) Foraging behaviour and memory window in sticklebacks. Behaviour 132:1231–1253
Mahut H, Zola-Morgan S, Moss M (1982) Hippocampal resections impair associative learning and recognition memory in the monkey. J Neurosci 2:1214–1229
McClelland JL, McNaughton BL, O’Reilly RC (1995) Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. Psychol Rev 102:419–457
Mishkin M (1978) Memory in monkeys severely impaired by combined but not by separate removal of amygdala and hippocampus. Nature 273:297–298
Murray EA, Mishkin M (1984) Severe tactual as well as visual memory deficits follow combined removal of the amygdala and hippocampus in monkeys. J Neurosci 4:2565–2580
Nilsson J, Kristiansen TS, Fosseidengen JE, Ferno A, van den Bos R (2008a) Learning in cod (Gadus morhua): long trace interval retention. Anim Cogn 11:215–222
Nilsson J, Kristiansen TS, Fosseidengen JE, Fernö A, van den Bos R (2008b) Sign- and goal-tracking in Atlantic cod (Gadus morhua). Anim Cogn 11(4):651–659
Nilsson J, Kristiansen TS, Fosseidengen JE, Stien LH, Ferno A, van den Bos R (2010) Learning and anticipatory behaviour in a “sit-and-wait” predator: the Atlantic halibut. Behav Process 83(3):257–266
Odling-Smee L, Braithwaite VA (2003) The influence of habitat stability on landmark use during spatial learning in the three-spined stickleback. Anim Behav 65:701–707
Odling-Smee LC, Boughman JW, Braithwaite VA (2008) Sympatric species of three-spined stickleback differ in their performance in a spatial learning task. Behav Ecol Sciobiol 62:1935–1945
Saigusa T, Tero A, Nakagaki T, Kuramoto Y (2008) Amoebae anticipate periodic events. Phys Rev Lett 100:018101
Schluessel V, Bleckmann H (2012) Spatial learning and memory retention in the grey bamboo shark (Chiloscyllium griseum). Zoology 115(6):346–353
Schneiders JA, Opitz B, Krick CM, Mecklinger A (2011) Separating intra-modal and across-modal training effects in visual working memory: an fMRI investigation. Cereb Cortex 21:2555–2564
Shapiro ML, Olton DS (1994) Hippocampal function and interference. In: Schacter DL, Tulving E (eds) Memory systems 1994. MIT Press, Cambridge
Spear EN, Riccio DC (1994) Memory: phenomena and principles. Allyn & Bacon, Boston
Squire LR, Zola-Morgan S (1985) The neuropsychology of memory: new links between humans and experimental animals. In: Olton DS, Gamzu E, Corkin S (eds) Memory dysfunctions: an integration of animal and human research from preclinical and clinical perspectives. Annals of the New York Academy of Sciences, New York: New York Academy of Sciences 444: 137–149
Stanton ML (1983) Short-term learning and the searching accuracy of egg-laying butterflies. Anim Behav 31:33–40
Tarrant RM (1964) Rate of extinction of a conditional response in juvenile sockeye salmon. Trans Am Fish Soc 93:399–401
Tlusty MF, Andrew J, Baldwin K, Bradley TM (2008) Acoustic conditioning for recall/recapture of scaped Atlantic salmon and rainbow trout. Aquaculture 274:57–64
Tully T (1996) Discovery of genes involved with learning and memory: an experimental synthesis of Hirschian and Benzerian perspectives. Proc Natl Acad Sci USA 93:13460–13467
Warburton K (2003) Learning of foraging skills by fish. Fish Fish 4:203–215
Ware DM (1971) Predation by rainbow trout (Salmo gairdneri): the effect of experience. J Fish Res Board Can 28:1847–1852
White KG (2001) Forgetting functions. Anim Learn Behav 29:193–207
Woodward G, Laverty TM (1992) Recall of flower handling skills by bumble bees: a test of Darwin’s interference hypothesis. Anim Behav 44:1045–1051
Zion B, Barki A, Grinshpon J, Rosenfeld L, Karplus I (2011) Retention of acoustic conditioning in St. Peter’s fish Sarotherodon galilaeus. J Fish Biol 78(3):838–847
Zola-Morgan S, Squire L, Alvarez-Royo P, Clower RP, Morgan-Zola S (1991) Independence of memory functions and emotional behavior: separate contributions of the hippocampal formation and the amygdala. Hippocampus 1(2):207–220