How does agonistic behaviour differ in albino and pigmented fish?
Status PubMed-not-MEDLINE Language English Country United States Media electronic-ecollection
Document type Journal Article
PubMed
27114883
PubMed Central
PMC4841223
DOI
10.7717/peerj.1937
PII: 1937
Knihovny.cz E-resources
- Keywords
- Aggressive and Mobile display, Albinism, Catfish, Pleiotropic effect, Siluriformes,
- Publication type
- Journal Article MeSH
In addition to hypopigmentation of the skin and red iris colouration, albino animals also display distinct physiological and behavioural alterations. However, information on the social interactions of albino animals is rare and has mostly been limited to specially bred strains of albino rodents and animals from unique environments in caves. Differentiating between the effects of albinism and domestication on behaviour in rodents can be difficult, and social behaviour in cave fish changes according to species-specific adaptations to conditions of permanent darkness. The agonistic behaviours of albino offspring of pigmented parents have yet to be described. In this study, we observed agonistic behaviour in albino and pigmented juvenile Silurus glanis catfish. We found that the total number of aggressive interactions was lower in albinos than in pigmented catfish. The distance between conspecifics was also analysed, and albinos showed a tendency towards greater separation from their same-coloured conspecifics compared with pigmented catfish. These results demonstrate that albinism can be associated with lower aggressiveness and with reduced shoaling behaviour preference, as demonstrated by a tendency towards greater separation of albinos from conspecifics.
See more in PubMed
Abeelen van JHF, Kroes WH. Albinism and mouse behaviour. Genetica. 1967;38:419–429. doi: 10.1007/BF01507473. PubMed DOI
Barnett SA, Dickson RG, Hocking WE. Genotype and environment in the social interactions of wild and domestic “Norway” rats. Aggressive Behaviour. 1979;5:105–119. doi: 10.1002/1098-2337(1979)5:2¡105::AID-AB2480050202¿3.0.CO;2-U. DOI
Barnett SA, Hocking WE. Further experiments on the social interactions of domestic “Norway” rats. Aggressive Behavior. 1981;7:259–263. doi: 10.1002/1098-2337(1981)7:3¡259::AID-AB2480070309¿3.0.CO;2-V. DOI
Benca RM, Gilliland MA, Obermeyer WH. Effects of lighting conditions on sleep and wakefulness in albino Lewis and pigmented Brown Norway rats. Sleep. 1998;21:451–460. PubMed
Bilandžija H, Ma L, Parkhurst A, Jeffery WR. A potential benefit of albinism in Astyanax cavefish: downregulation of the oca2 gene increases tyrosine and catecholamine levels as an alternative to melanin synthesis. PloS ONE. 2013;8:e1937. doi: 10.1371/journal.pone.0080823. PubMed DOI PMC
Boulêtreau S, Cucherousset J, Villéger S, Masson R, Santoul F. Colossal aggregations of giant alien freshwater fish as a potential biogeochemical hotspot. PLoS ONE. 2011;6:e1937. doi: 10.1371/journal.pone.0025732. PubMed DOI PMC
Britton JR, Davies GD. First record of the white catfish Ameiurus catus in Great Britain. Journal of Fish Biology. 2006;69:1236–1238. doi: 10.1111/j.1095-8649.2006.01171.x. DOI
Buhusi CV, Perera D, Meck WH. Memory for timing and auditory signals in albino and pigmented rats. Journal of Experimental Psychology—Animal Behaviour. 2005;31:18–30. doi: 10.1037/0097-7403.31.1.18. PubMed DOI
Carden SM, Boissy RE, Schoettker PJ, Good WV. Albinism: modern molecular diagnosis. British Journal of Ophthalmology. 1998;82:189–1995. doi: 10.1136/bjo.82.2.189. PubMed DOI PMC
DeFries JC. Pleiotropic effects of albinism on open field behaviour in mice. Nature. 1969;221:65–66. doi: 10.1038/221065a0. PubMed DOI
Dijkstra PD, Hemelrijk CK, Seehausen O, Groothius TGG. Colour polymorphism reduces intrasexual selection in assemblages of cichlid fish. Behaviour Ecology. 2009;20:138–144. doi: 10.1093/beheco/arn125. DOI
Dijkstra PD, Lindström J, Metcalfe NB, Hemelrijk CK, Brendel M, Seehausen O, Groothius TGG. Frequency-dependent social dominance in a color polymorphic cichlid fish. Evolution. 2010;64:2797–2807. doi: 10.1111/j.1558-5646.2010.01046.x. PubMed DOI
Dijkstra PD, Seehausen O, Groothuis TGG. Direct male–male competition can facilitate invasion of new colour types in Lake Victoria cichlids. Behaviour Ecology and Socio-Biology. 2005;58:136–143. doi: 10.1007/s00265-005-0919-5. DOI
Dingerkus G, Seret B, Guilbert E. The first albino wels, Silurus glanis Linnaeus, 1758, from France, with a review of albinism in catfishes (Teleostei: Siluriformes) Cybium. 1991;15:185–188.
Duboué ER, Keene AC, Borowsky RL. Evolutionary convergence on sleep loss in cavefish populations. Current Biology. 2011;21:671–676. doi: 10.1016/j.cub.2011.03.020. PubMed DOI
Ducrest A-L, Keller L, Roulin A. Pleiotropy in the melanocortin system, coloration and behavioural syndromes. Trends in Ecology and Evolution. 2008;23:502–510. doi: 10.1016/j.tree.2008.06.001. PubMed DOI
Elipot Y, Hinaux H, Callebert J, Rétaux S. Evolutionary shift from fighting to foraging in blind cavefish through changes in the serotonin network. Current Biology. 2013;23:1–10. PubMed
Ellegren H, Lindgren G, Primmer RC, Møller PA. Fitness loss and germline mutations in barn swallows breeding in Chernobyl. Nature. 1997;389:593–596. doi: 10.1038/39303. PubMed DOI
Espinasa L, Yamamoto Y, Jeffery RW. Non-optical releasers for aggressive behaviour in blind and blinded Astyanax (Teleostei, Characidae) Behavioural Processes. 2005;70:144–148. doi: 10.1016/j.beproc.2005.06.003. PubMed DOI
Fuller LJ. Effects of the albino gene upon behaviour of mice. Animal Behaviour. 1967;15:467–470. doi: 10.1016/0003-3472(67)90045-0. PubMed DOI
Goméz-Laplaza ML. Recent social environment affects colour-assortative shoaling in juvenile angelfish (Pterophyllum scalare) Behavioural Processes. 2009;82:39–44. doi: 10.1016/j.beproc.2009.04.002. PubMed DOI
Gonzales MI, Varizi S, Wilson CA. Behavioural effects of a –MSH and MCH after central administration in female rat. Peptides. 1996;17:171–177. doi: 10.1016/0196-9781(95)02092-6. PubMed DOI
Griffith SW, Brockmark S, Höjesjö J, Johnsson IJ. Coping with divided attention: the advantage of familiarity. Proceedings of the Royal Society of London B: Biological Sciences. 2004;271:695–699. doi: 10.1098/rspb.2003.2648. PubMed DOI PMC
Harker KT, Whishaw IQ. Place and matching-to-place spatial learning affected by rat inbreeding (Dark-Agouti, Fischer 344) and albinism (Wistar, Sprague-Dawley) but no domestication (wild rat vs. Long-Evans, Fischer-Norway) Behavioural Brain Resources. 2002;134:467–477. doi: 10.1016/S0166-4328(02)00083-9. PubMed DOI
Himmler BT, Derksen SM, Stryjek R, Modlinska K, Pisula W, Pellis SM. How domestication modulates play behaviour: a comparative analysis between wild rats and a laboratory strain of Ratus norvegicus. Journal of Comparative Psychology. 2013;127:453–464. doi: 10.1037/a0032187. PubMed DOI
Himmler SM, Modlinska K, Stryjek R, Himmler BT, Pisula W, Pellis SM. Domestication and diversification: a comparative analysis of the play fighting of the Brown Norway, Sprague-Dawley, and Wistar Laboratory strains of (Rattus norvegicus) Journal of Comparative Psychology. 2014;128:318–327. doi: 10.1037/a0036104. PubMed DOI
Höglund E, Balm PHM, Winberg S. Skin darkening a potential social signal in subordinate Arctic charr (Salvenius alpinus): the regulatory role of brain monoamines and pro-opiomelanocorticon-derived peptides. Journal of Experimental Biology. 2000;203:1711–1721. PubMed
Horth L. Melanic body-color and aggressive mating behaviour are correlated traits in male mosquitofish, (Gambusia holbrooki) Proceedings of the Royal Society of London Series B. 2003;270:1033–1040. doi: 10.1098/rspb.2003.2348. PubMed DOI PMC
Hoste B, Simpson SJ, DeLoof A, Breuer M. Behavioural differences in Locusta migratoria associated with albinism and their relation to [His7]-corazonin. Physiology & Entomology. 2003;28:32–38. doi: 10.1046/j.1365-3032.2003.00312.x. DOI
Hsu Y, Wolf LL. The winner and looser effect: integrating multiple experiences. Animal Behaviour. 1999;57:903–910. doi: 10.1006/anbe.1998.1049. PubMed DOI
Hupfeld D, Hoffmann K-P. Motion perception in rats (Rattus norvegicus sp.): deficits in albino Wistar rats compared to pigmented Long-Evans rats. Behavioural Brain Resources. 2006;170:29–33. doi: 10.1016/j.bbr.2006.01.022. PubMed DOI
Jeffery RW. Cavefish as a model system in evolutionary developmental biology. Developmental Biology. 2001;291:1–12. PubMed
Keeler CA. The association of the black (non-agouti) gene with behaviour in the Norway rat. Journal of Heredity. 1942;33:371–384.
Kenward MG, Roger JH. Small sample inference for fixed effects from restricted maximum likelihood. Biometrics. 1997;53:983–997. doi: 10.2307/2533558. PubMed DOI
Kowalko EJ, Rohner N, Rompani BS, Peterson KB, Weber J, Hoekstra EH, Jeffery RW, Borowsky R, Tabin JC. Loss of schooling behaviour in cavefish through sight-dependent and sight-independent mechanism. Current Biology. 2013;23:1874–1883. doi: 10.1016/j.cub.2013.07.056. PubMed DOI PMC
Landeau L, Terborgh J. Oddity and the ‘confusion effect’ in predation. Animal Behaviour. 1986;34:1372–1380. doi: 10.1016/S0003-3472(86)80208-1. DOI
Leal ME, Schulz UH, Albornoz PL, Machado R, Ott PH. First record of partial albinism in two catfish species of genidens (siluriformes: ariidae) in an estuary of Southern Brazil. Brazilian Archives of Biology and Technology. 2013;56:237–240. doi: 10.1590/S1516-89132013000200008. DOI
Lehtonen TK. Colour biases in territorial aggression in a Neotropical cichlid fish. Oecologia. 2014;175:85–93. doi: 10.1007/s00442-013-2879-1. PubMed DOI
Liang KY, Zeger SL. Longitudinal data analysis using generalized linear models. Biometrika. 1986;73:13–22. doi: 10.1093/biomet/73.1.13. DOI
Marc RE, Jones BW, Watt CB, Vazquez-Chona F, Vaughan DK. Extreme retinal remodelling triggered, by light damage: implications for age related macular degeneration. Molecular Vision. 2008;14:782–806. PubMed PMC
Mazur A, Booth A. Testosterone and dominance in men. Behavioural Brain. Science. 1998;21:353–397. PubMed
McRobert PS, Bradner J. The influence of body coloration on shoaling preference in fish. Animal Behaviour. 1998;56:611–615. doi: 10.1006/anbe.1998.0846. PubMed DOI
O’Connor KL, Metcalfe NB, Taylor AC. Does darkening signal submission in territorial contest between juvenile Atlantic salmon, Salmo salar? Animal Behaviour. 1999;58:1269–1276. doi: 10.1006/anbe.1999.1260. PubMed DOI
Owen K, Thiessen DD, Lindzey G. Acrophobic and photophobic responses associated with the albino locus in mice. Behavior Genetics. 1970;1:249–255. doi: 10.1007/BF01074656. PubMed DOI
Parzefall J, Trajano E. Behavioral patterns in subterranean fishes. In: Trajano E, Bichuette ME, Kapoor BG, editors. Biology of subterranean fishes. Enfield, NH: Science Publishers; 2010. pp. 81–114.
Pauers MJ, Kapfer JM, Doehler K, Lee TJ, Berg CS. Gross colour pattern is used to distinguish between opponents during aggressive encounters in a Lake Malawi cichlid. Ecology of Freshwater Fish. 2012;21:34–41. doi: 10.1111/j.1600-0633.2011.00520.x. DOI
Pisula W, Turlejski K, Stryjek R, Nalęcy-Tolak A, Grabiec M, Djavadian RL. Response to novelty in the laboratory Wistar rat wild-captive WWCPS rat, and the grey short-tailed opossum (Monodelphis domestica) Behavioural Processes. 2012;91:145–151. doi: 10.1016/j.beproc.2012.06.010. PubMed DOI
Pohlmann K, Grasso FW, Breithaupt T. Tracking wakes: the nocturnal predatory strategy of piscivorous catfish. Proceedings of the National Academy of Sciences of the United States of America. 2001;98:7371–7374. doi: 10.1073/pnas.121026298. PubMed DOI PMC
Prusky GT, Harker KT, Douglas MR, Whishaw IQ. Variation in visual acuity within pigmented, and between pigmented and albino rat strains. Behavioural Brain Research. 2002;136:339–348. doi: 10.1016/S0166-4328(02)00126-2. PubMed DOI
Pryke SR. Is red an innate or learned signal of aggression and intimidation? Animal Behaviour. 2009;78:393–398. doi: 10.1016/j.anbehav.2009.05.013. DOI
Pryke SR, Griffith SC. Red dominants black: agonistic signalling among head morphs in the colour polymorphic Gouldina finch. Proceedings of the Royal Society of London Series B. 2006;273:949–957. doi: 10.1098/rspb.2005.3362. PubMed DOI PMC
Rebouças RCR, Schmidek RW. Handling and isolation in three strains of rats affect open field, exploration, hoarding and predation. Physiology & Behaviour. 1997;62:1159–1164. doi: 10.1016/S0031-9384(97)00312-0. PubMed DOI
Refinetti R. Enhanced circadian photoresponsiveness after prolonged dark adaptation in seven species of diurnal and nocturnal rodents. Physiology & Behaviour. 2007;90:431–437. doi: 10.1016/j.physbeh.2006.10.004. PubMed DOI PMC
Rodgers MG, Kelley LJ, Morell JL. Colour change and assortment in the western rainbowfish. Animal Behaviour. 2010;79:1025–1030. doi: 10.1016/j.anbehav.2010.01.017. DOI
Slavík O, Horký P, Bartoš L, Kolářová J, Randák T. Diurnal and seasonal behaviour of adult and juvenile European catfish as determined by radio-telemetry in the River Berounka, Czech Republic. Journal of Fish Biology. 2007;71:104–114.
Slavík O, Horký P, Maciak M. Ostracism of an albino individual by a group of pigmented catfish. PLoS ONE. 2015;10:e1937. doi: 10.1371/journal.pone.0128279. PubMed DOI PMC
Slavík O, Horký P, Maciak M, Wackermannová M. Familiarity, prior residency, resource availability and body mass as predictors of the movement activity of the European catfish. Journal of Ethology. 2016;34:23–30. doi: 10.1007/s10164-015-0441-9. DOI
Slavík O, Maciak M, Horký P. Shelter use of familiar and unfamiliar groups of juvenile European catfish Silurus glanis. Applied Animal Behaviour Science. 2012;142:116–123. doi: 10.1016/j.applanim.2012.09.005. DOI
Spence R, Smith C. The role of early learning in determining shoaling preferences based on visual cues in the Zebrafish, Danio rerio. Ethology. 2006;113:62–67.
Staffan F, Magnhagen C, Alanärä A. Variation in food intake within groups of juvenile perch. Journal of Fish Biology. 2002;60:606–614.
Stryjek R, Modlińska K, Pisula W. Species specific behavioural patterns (digging and swimming) and reaction to novel objects in wild type, Wistar, Sprague-Dawley and Brown Norway rats. PLoS ONE. 2012;7:e1937. doi: 10.1371/journal.pone.0040642. PubMed DOI PMC
Stryjek R, Modlińska K, Turlejski K, Pisula W. Circadian rhythm of outside-nest activity in wild (WWCPS), albino and pigmented laboratory rats. PloS ONE. 2013;8:e1937. doi: 10.1371/journal.pone.0066055. PubMed DOI PMC
Theodorakis CHW. Size segregation and effects of oddity on predation risk in minnow schools. Animal Behaviour. 1989;38:496–502. doi: 10.1016/S0003-3472(89)80042-9. DOI
Trajano E. The agonistic behaviour of Pimelodella kronei, a troglobitic catfish from Southeastern Brazil (Siluriformes, Pimelodidae) Behavioural Processes. 1991;23:113–124. doi: 10.1016/0376-6357(91)90062-5. PubMed DOI
Uieda W. Behavior of an albino vampire bat, Desmondus rotundus (E. Geoffroy) (Chiroptera, Phyllostomatideae), in captivity. Revista Brasiliera de Zoologica. 2001;18:641–644. doi: 10.1590/S0101-81752001000200031. DOI
Valdimarsson SK, Metcalfe NB. Is the level of aggression and dispersion in territorial fish dependent on light intensity? Animal Behaviour. 2001;61:1143–1149. doi: 10.1006/anbe.2001.1710. DOI
Wakida-Kusunoki AT, Amador-del-Angel LE. First record of albinism in gafftopsail catfish Barge marinus (Pisces: Ariidae) from southeast Mexico. Revista de Biologia Marina Y Oceanografia. 2013;48:203–206. doi: 10.4067/S0718-19572013000100019. DOI
Ward AJW, Hart PJB. Foraging benefits of shoaling with familiars may be exploited by outsiders. Animal Behaviour. 2005;69:329–335. doi: 10.1016/j.anbehav.2004.06.005. DOI
Yamamoto Y, Byerly MS, Jackman WR, Jeffery WR. Pleiotropic function of embryonic sonic hedgehog expression link jaw and taste bud amplification with eye loss during cavefish evolution. Developmental Biology. 2009;330:200–211. doi: 10.1016/j.ydbio.2009.03.003. PubMed DOI PMC
Yoshizawa M, Gorički Š, Soares D, Jeffery RW. Evolution of a behavioural shift mediated by superficial neuromasts helps cavefish find food in darkness. Current Biology. 2010;20:1631–1636. doi: 10.1016/j.cub.2010.07.017. PubMed DOI PMC
Yoshizawa M, Jeffery RW, Netten van MS, McHenry JM. The sensitivity of lateral line receptors and their role in the behaviour of Mexican blind cavefish (Astyanax mexicanus) Journal of Experimental Biology. 2014;217:886–895. doi: 10.1242/jeb.094599. PubMed DOI PMC
Yoshizawa M, O’Quin EK, Jeffery RW. Evolution of an adaptive behaviour and its sensory receptors promotes eye regression in blind cavefish: response to Borowsky (2013) BMS Biology. 2013;11:82. doi: 10.1186/1741-7007-11-82. PubMed DOI PMC