Thermopreferential behavior of the Senegal bichir Polypterus senegalus (Polypteridae) under chronic visual deprivation

Cover Page

Cite item

Abstract

The effect of chronic visual deprivation (eye lens removal, 3 months) on the thermopreferential behavior and preferred temperature in fish was studied for the first time on the example of the Senegal bichirPolypterus senegalus. In intact Senegal bichir, the thermopreferential range and mean preferred temperature are 32.0–35.0 and 33.8°C, whereas in visually deprived fish they are 26.0–35.0 and 30.2°C, respectively. Compared to intact individuals, the visually deprived fish are more mobile and make 10.3 times more travels from compartment to compartment in the thermogradient tray, their total travel distance is 16.9 times longer, and the distance swum without change of direction is 1.6 times longer and takes 8.7 times less time. The rate of temperature change during movements in visually deprived fish is 14.9 times higher than in intact individuals. Changes in thermal preference and movement activity found in fish experiencing chronic visual deprivation indicate the presence of complex relations between thermoreception and the visual system.

About the authors

A. O. Kasumyan

Lomonosov Moscow State University

Moscow, Russia

V. V. Zdanovich

Lomonosov Moscow State University

Email: zdanovich@mail.ru
Moscow, Russia

V. V. Sataeva

Lomonosov Moscow State University

Moscow, Russia

References

  1. Голованов В.К.2013а. Температурные критерии жизнедеятельности пресноводных рыб. М.: Полиграф-Плюс, 300 с.
  2. Голованов В.К.2013б. Эколого-физиологические закономерности распределения и поведения пресноводных рыб в термоградиентных условиях // Вопр. ихтиологии. Т. 53. № 3. С. 286–314. https://doi.org/10.7868/S0042875213030016
  3. Голованов В.К.,Смирнов А.К.2011. Особенности терморегуляционного поведения ранней молоди плотвыRutilus rutilusв термоградиентных условиях // Там же. Т. 51. № 4. С. 551–558.
  4. Девицина Г.В.,Марусов Е.А.2007. Взаимодействие сенсорных систем и пищевое поведение рыб // Успехи соврем. биологии. Т. 127. № 4. С. 387–395.
  5. Зданович В.В.1999. Некоторые особенности роста молоди мозамбикской тиляпииOreochromis mossambicusпри постоянных и переменных температурах // Вопр. ихтиологии. Т. 39. № 1. С. 105–110.
  6. Зданович В.В.2017. Поведение и двигательная активность интактного и сенсорно депривированного тетрагоноптерусаHemigrammus caudovittatusв термоградиентном поле // Тез. докл.VI Всерос. конф. по поведению животных. М.: Т-во науч. изд. КМК. С. 57.
  7. Зданович В.В.,Сатаева В.В.,Касумян А.О.2024. Термоизбирание у симпатрических многопёров: сенегальскогоPolypterus senegalusи Эндлихера P. endlicherii(Polypteridae) // Вопр. ихтиологии. Т. 64. № 6. С. 763–772. https://doi.org/10.31857/S0042875224060108
  8. Капшай Д.С.,Голованов В.К.2013. Поведение и распределение молоди теплолюбивых рыб в термоградиентных условиях в летний и зимний сезоны года // Вестн. Мордов. ун-та. № 3–4. С. 78–82.
  9. Касумян А.О.,Марусов Е.А.2002. Поведенческие ответы гольянаPhoxinus phoxinus(Cyprinidae) на химические сигналы в норме и после острой и хронической аносмии // Вопр. ихтиологии. Т. 42. № 5. С. 684–696.
  10. Касумян А.О.,Марусов Е.А.2007. Хеморецепция у хронически аносмированных рыб: феномен компенсаторного развития вкусовой системы // Там же. Т. 47. № 5. С. 684–693.
  11. Касумян А.О.,Зданович В.В.,Сатаева В.В.2024. Двигательная активность интактного и зрительно депривированного сенегальского многопёраPolypterus senegalus(Cladistia) при разной температуре воды // Там же. Т. 64. № 3. С. 354–362. https://doi.org/10.31857/S0042875224030097
  12. Константинов А.С.,Зданович В.В.1993. Некоторые характеристики поведения молоди рыб в термоградиентном поле // Вестн. МГУ. Сер. 16. Биология. № 1. С. 32–37.
  13. Мантейфель Б.П. 1987. Экологические и эволюционные аспекты поведения животных. М.: Наука, 270 с.
  14. Павлов Д.С.,Касумян А.О.1990. Сенсорные основы пищевого поведения рыб // Вопр. ихтиологии. Т. 30. № 5. С. 720–732.
  15. Павлов Д.С.,Садковский Р.В.,Костин В.В.,Лупандин А.И.1997. Влияние фото-, термо- и бароградиентов на поведение и вертикальное распределение молоди карповых рыб // Там же. Т. 37. № 1. С. 72–77.
  16. Boltz J.M.,Siemien M.J.,Stauffer J.R. Jr.1987. Influence of starvation on the preferred temperature ofOreochromis mossambicus(Peters) // Arch. Hydrobiol. V. 110. № 1. P. 143–146. https://doi.org/10.1127/archiv-hydrobiol/110/1987/143
  17. Braithwaite V.A.,De Perera T.B.2006. Short-range orientation in fish: how fish map space // Mar. Freshw. Behav. Physiol. V. 39. № 1. P. 37–47. https://doi.org/10.1080/10236240600562844
  18. Braun C.B.,Coombs S.,Fay R.R.2002. What is the nature of multisensory interaction between octavolateralis sub-systems? // Brain Behav. Evol. V. 59. № 4. P. 162–176. https://doi.org/10.1159/000064904
  19. Candolin U.2003. The use of multiple cues in mate choice // Biol. Rev. V. 78. № 4. P. 575–595. https://doi.org/10.1017/S1464793103006158
  20. Chapman B.B.,Morrell L.J.,Tosh C.R.,Krause J.2010. Behavioural consequences of sensory plasticity in guppies // Proc. R. Soc. B. V. 277. № 1686. P. 1395–1401. https://doi.org/10.1098/rspb.2009.2055
  21. Chen B.,Dai W.-Z.,Li X.-L. et al.2024. Wall-following — phylogenetic context of an enhanced behaviour in stygomorphicSinocyclocheilus(Cypriniformes: Cyprinidae) cavefishes // Ecol. Evol. V. 14. № 6. Article e11575. https://doi.org/10.1002/ece3.11575
  22. Christensen E.A.F.,Svendsen M.B.S.,Steffensen J.F.2020. The combined effect of body size and temperature on oxygen consumption rates and the size-dependency of preferred temperature in European perchPerca fluviatilis // J. Fish Biol. V. 97. № 3. P. 794–803. https://doi.org/10.1111/jfb.14435
  23. Coleman S.W.,Rosenthal G.G.2006. Swordtail fry attend to chemical and visual cues in detecting predators and conspecifics // PLoS ONE. V. 1. № 1. Article e118. https://doi.org/10.1371/journal.pone.0000118
  24. Coutant C.C. 1977. Compilation of temperature preference data // J. Fish. Res. Board Can. V. 34. № 5. P. 739–745. https://doi.org/10.1139/f77-115
  25. De Alba G.,Conti F.,Sánchez J. et al.2024. Effect of light and feeding regimes on the daily rhythm of thermal preference in Nile tilapia (Oreochromis niloticus) // Aquaculture. V. 578. Article 740122. https://doi.org/10.1016/j.aquaculture. 2023.740122
  26. Despatie S.-P.,Castonguay M.,Chabot D.,Audet C. 2001. Final thermal preferendum of Atlantic cod: effect of food ration // Trans. Am. Fish. Soc. V. 130. № 2. P. 263–275. https://doi.org/10.1577/1548-8659(2001)130<0263:FTPOAC>2.0.CO;2
  27. Dı́az F.,Bückle L.F.1999. Effect of the critical thermal maximum on the preferred temperatures ofIctalurus punctatusexposed to constant and fluctuating temperatures // J. Therm. Biol. V. 24. № 3. P. 155–160. https://doi.org/10.1016/S0306-4565(99)00005-4
  28. Ernst M.O.,Di Luca M.2011. Multisensory perception: from integration to remapping // Sensory cue integration. N.Y.: Oxford Univ. Press. P. 224–250. https://doi.org/10.1093/acprof:oso/9780195387247.003.0012
  29. Fangue N.A.,Podrabsky J.E.,Crawshaw L.I.,Schulte P.M.2009. Countergradient variation in temperature preference in populations of killifishFundulus heteroclitus // Physiol. Biochem. Zool. V. 82. № 6. P. 776–786. https://doi.org/10.1086/606030
  30. Fry F.E.J.1971. The effect of environmental factors on the physiology of fish // Fish physiology. V. 6. N.Y.: Acad. Press. P. 1–98. https://doi.org/10.1016/S1546-5098(08)60146-6
  31. Gonçalves-de-Freitas E.,Bolognesi M.C.,Gauy A.C.D.S. et al.2019. Social behavior and welfare in Nile tilapia // Fishes. V. 4. № 2. Article 23. https://doi.org/10.3390/fishes4020023
  32. Haesemeyer M.2020. Thermoregulation in fish // Mol. Cell. Endocrinol. V. 518. Article 110986. https://doi.org/10.1016/j.mce.2020.110986
  33. Hainer J.,Lutek K.,Maki H.,Standen E.M.2023. Sensorimotor control of swimmingPolypterus senegalusis preserved during sensory deprivation conditions across altered environments // J. Exp. Biol. V. 226. № 9. Article jeb245192. https://doi.org/10.1242/jeb.245192
  34. Hardy J.D.1961. Physiology of temperature regulation // Physiol. Rev. V. 41. № 3. P. 521–606. https://doi.org/10.1152/physrev.1961.41.3.521
  35. Hassan El.-S.,Abdel-Latif H.,Biebricher R.1992. Studies on the effects of Ca++and Co++on the swimming behavior of the blind Mexican cave fish // J. Comp. Physiol. A. V. 171. № 3. P. 413–419. https://doi.org/ 10.1007/BF00223971
  36. Hochachka P.W.,Somero G.N.2002. Biochemical adaptation: mechanism and process in physiological evolution. N.Y.: Oxford Univ. Press, 466 p. https://doi.org/10.1093/oso/9780195117028.001.0001
  37. Hughes R.N.,Blight C.M.2000. Two intertidal fish species use visual association learning to track the status of food patches in a radial maze // Anim. Behav. V. 59. № 3. P. 613–621. https://doi.org/10.1006/anbe.1999.1351
  38. Jobling M.1981. Temperature tolerance and the final preferendum — rapid methods for the assessment of optimum growth temperatures // J. Fish Biol. V. 19. № 4. P. 439–455. https://doi.org/10.1111/j.1095-8649.1981.tb05847.x
  39. Lafrance P.,Castonguay M.,Chabot D.,Audet C. 2005. Ontogenetic changes in temperature preference of Atlantic cod // Ibid. V. 66. № 2. P. 553–567. https://doi.org/10.1111/j.0022-1112.2005.00623.x
  40. Lessard N.,Paré M.,Lepore F.,Lassonde M.1998. Early-blind human subjects localize sound sources better than sighted subjects // Nature. V. 395. № 6699. P. 278–280. https://doi.org/10.1038/26228
  41. Maaswinkel H.,Li L.2003. Olfactory input increases visual sensitivity in zebrafish: a possible function for the terminal nerve and dopaminergic interplexiform cells // J. Exp. Biol. V. 206. № 13. P. 2201–2209. https://doi.org/10.1242/jeb.00397
  42. Moller P. 2002. Multimodal sensory integration in weakly electric fish: a behavioural account // J. Physiol. Paris. V. 96. № 5–6. P. 547–556. https://doi.org/10.1016/s0928-4257(03)00010-x
  43. Moller P.,Serrier J.,Squire A.,Boudinot M.1982. Social spacing in the mormyrid fishGnathonemus petersii(Pisces): a multisensory approach // Anim. Behav. V. 30. № 3. P. 641–650. https://doi.org/10.1016/S0003-3472(82)80134-6
  44. Montgomery J.C.,Coombs S.,Baker C.F.2001. The mechanosensory lateral line system of the hypogean form ofAstyanax fasciatus // Environ. Biol. Fish. V. 62. № 1–3. P. 87–96. https://doi.org/10.1023/A:1011873111454
  45. Nelson D.O.,Prosser C.L.1979. Effect of preoptic lesions on behavioral thermoregulation of green sunfish,Lepomis cyanellus, and of goldfish,Carassius auratus // J. Comp. Physiol. A. V. 129. № 3. P. 193–197. https://doi.org/10.1007/BF00657653
  46. New J.G.,Fewkes L.A.,Khan A.N.2001. Strike feeding behavior in the muskellunge,Esox masquinongy: contributions of the lateral line and visual sensory systems // J. Exp. Biol. V. 204. № 6. P. 1207–1221. https://doi.org/ 10.1242/jeb.204.6.1207
  47. Pavlov D.S.,Sadkovskii R.V.,Kostin V.V.,Lupandin A.I.2000. Experimental study of young fish distribution and behaviour under combined influence of baro-, photo- and thermo-gradients // J. Fish Biol. V. 57. № 1. P. 69–81. https://doi.org/10.1111/j.1095-8649.2000.tb00776.x
  48. Pfeiffer W.1968. Retina und Retinomotorik der Dipnoi und Brachiopterygii // Z. Zellforsch. V. 89. № 1. P. 62–72.https://doi.org/10.1007/BF00332652
  49. Pulgar J.M.,Aldana M.,Bozinovic F.,Ojeda F.P. 2003. Does food quality influence thermoregulatory behavior in the intertidal fishGirella laevifrons? // J. Therm. Biol. V. 28. № 8. P. 539–544. https://doi.org/10.1016/j.jtherbio.2003.08.001
  50. Reese E.S.1989. Orientation behaviour of butterflyfishes (family Chaetodontidae) on coral reefs: spatial learning of route specific landmarks and cognitive maps // Environ. Biol. Fish. V. 25. № 1–3. P. 79–86. https://doi.org/10.1007/BF00002202
  51. Rodríguez F.,Quintero B.,Amores L. et al.2021. Spatial cognition in teleost fish: strategies and mechanisms // Animals. V. 11. № 8. Article 2271. https://doi.org/10.3390/ani11082271
  52. Schakmann M.,Christensen E.A.F.,Steffensen J.F.,Svendsen M.B.S.2023. The influence of body size on behavioral thermal preference in Atlantic cod (Gadus morhua): larger fish favor colder waters // Fishes. V. 8. № 12. Article 596. https://doi.org/10.3390/fishes8120596
  53. Schram E.,Bierman S.,Teal L.R. et al.2013. Thermal preference of juvenile dover sole (Solea solea) in relation to thermal acclimation and optimal growth temperature // PLoS ONE. V. 8. № 4. Article e61357. https://doi.org/10.1371/journal.pone.0061357
  54. Schumacher S.,Burt de Perera T.,von der Emde G.2017. Electrosensory capture during multisensory discrimination of nearby objects in the weakly electric fishGnathonemus petersii // Sci. Rept. V. 7. Article 43665. https://doi.org/10.1038/srep43665
  55. Schurmann H.,Steffensen J.F.1992. Lethal oxygen levels at different temperatures and the preferred temperature during hypoxia of the Atlantic cod,Gadus morhuaL. // J. Fish Biol. V. 41. № 6. P. 927–934. https://doi.org/10.1111/j.1095-8649.1992.tb02720.x
  56. Schurmann H.,Steffensen J.F.,Lomholt J.P. 1991. The influence of hypoxia on the preferred temperature of rainbow troutOncorhynchus mykiss // J. Exp. Biol. V. 157. № 1. P. 75–86. https://doi.org/10.1242/jeb.157.1.75
  57. Teyke T.1990. Morphological differences in neuromasts of the blind cave fishAstyanax hubbsiand the sighted river fishAstyanax mexicanus // Brain Behav. Evol. V. 35. № 1. P. 23–30. https://doi.org/10.1159/000115853
  58. Vera L.M.,de Alba G.,Santos S. et al.2023. Circadian rhythm of preferred temperature in fish: behavioural thermoregulation linked to daily photocycles in zebrafish and Nile tilapia // J. Therm. Biol. V. 113. Article 103544. https://doi.org/10.1016/j.jtherbio.2023.103544
  59. Von Campenhausen C.,Riess I.,Weissert R.1981. Detection of stationary objects by the blind cave fishAnoptichthys jordani(Characidae) // J. Comp. Physiol. V. 143. № 3. P. 369–374. https://doi.org/10.1007/BF00611175
  60. Von der Emde G.,Zeymer M.2020. Multisensory object detection in weakly electric fish // The senses: a comprehensive reference. V. 7. Amsterdam et al.: Elsevier Inc. P. 281–297. https://doi.org/10.1016/B978-0-12-809324-5.24211-9
  61. Wagner H.-J.2001. Sensory brain areas in mesopelagic fishes // Brain Behav. Evol. V. 57. № 3. P. 117–133. https://doi.org/10.1159/000047231
  62. Warburton K.1990. The use of local landmarks by foraging goldfish // Anim. Behav. V. 40. № 3. P. 500–505. https://doi.org/10.1016/S0003-3472(05)80530-5
  63. Weissert R.,von Campenhausen C. 1981. Discrimination between stationary objects by the blind cave fishAnoptichthys jordani(Characidae) // J. Comp. Physiol. V. 143. № 3. P. 375–381. https://doi.org/10.1007/BF00611176
  64. Zdanovich V.V. 2006. Alteration of thermoregulation behavior in juvenile fish in relation to satiation level // J. Ichthyol. V. 46. Suppl. 2. P. S188–S193. https://doi.org/10.1134/S0032945206110087
  65. Znotinas K.R.,Standen E.M.2019. Aerial and aquatic visual acuity of the grey bichirPolypterus senegalus, as estimated by optokinetic response // J. Fish Biol. V. 95. № 1. P. 263–273. https://doi.org/10.1111/jfb.13724

Supplementary files

Supplementary Files
Action
1. JATS XML

Copyright (c) 2025 Russian Academy of Sciences

Согласие на обработку персональных данных

 

Используя сайт https://journals.rcsi.science, я (далее – «Пользователь» или «Субъект персональных данных») даю согласие на обработку персональных данных на этом сайте (текст Согласия) и на обработку персональных данных с помощью сервиса «Яндекс.Метрика» (текст Согласия).