Trematode Diplostomum pseudospathaceum (Diplostomidae) Larvae Penetrate the Underyearlings of Oncorhynchus mykiss (Salmonidae) and Manipulate Their Behavior

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

Abstract

Experiments with underyearlings of Oncorhynchus mykiss and cercariae of the trematode Diplostomum pseudospathaceum show that the first parasites that infect the fish have an excitatory influence on it and triple the rate of cercaria income with water through the oral cavity and gills. This effect is considered as manipulation of fish behavior at the stage of parasite transmission from the first intermediate host (mollusk) to the second (fish) one. Experimental data on the effect of fish odor on locomotor activity and the vertical distribution of cercariae have been obtained. Analysis of the data made it possible to determine a set of conditions that ensure the successful infection of fish by diplostomum larvae.

About the authors

V. N. Mikheev

Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Moscow, Russia

Author for correspondence.
Email: vicnikmik@gmail.com
Россия, Москва

References

  1. Михеев В.Н. 2006. Неоднородность среды и трофические отношения у рыб. М.: Наука, 191 с.
  2. Михеев В.Н., Жохов А.Е., Сливко В.М. 2013. Может ли риск заражения паразитами служить причиной экологической дифференциации в популяции плотвы, Rutilus rutilus (Cyprinidae)? // Вопр. ихтиологии. Т. 53. № 5. С. 613–620. https://doi.org/10.7868/S004287521305007X
  3. Шигин А.А. 1986. Трематоды фауны СССР. Род Diplostomum. Метацеркарии. М.: Наука, 253 с.
  4. Barber I., Hoare D., Krause J. 2000. Effects of parasites on fish behaviour: a review and evolutionary perspective // Rev. Fish Biol. Fish. V. 10. № 2. P. 131–165. https://doi.org/10.1023/A:1016658224470
  5. Bethel W.M., Holmes J.C. 1973. Altered evasive behavior and responses to light in amphipods harboring acanthocephalan cystacanths // J. Parasitol. V. 59. № 6. P. 945–956. https://doi.org/10.2307/3278623
  6. Bethel W.M., Holmes J.C. 1977. Increased vulnerability of amphipods to predation owing to altered behavior induced by larval acanthocephalans // Can. J. Zool. V. 55. № 1. P. 110–115. https://doi.org/10.1139/z77-013
  7. Chivers D.P., Smith R.J.F. 1998. Chemical alarm signaling in aquatic predator-prey systems: a review and prospectus // Écoscience. V. 5. № 3. P. 338–352. https://doi.org/10.1080/11956860.1998.11682471
  8. Combes C., Fournier A., Moné H., Théron A. 1994. Behaviours in trematode cercariae that enhance parasite transmission: patterns and processes // Parasitology. V. 109. Suppl. 1. P. S3–S13. https://doi.org/10.1017/S0031182000085048
  9. Combes C., Bartoli P., Théron A. 2002. Trematode transmission strategies // The behavioural ecology of parasites. Wallingford: CABI Publ. P. 1–12. https://doi.org/10.1079/9780851996158.0001
  10. Dawkins R. 1999. The extended phenotype: the long reach of the gene. Oxford: Oxford Univ. Press, 336 p.
  11. Dianne L., Perrot-Minnot M.-J., Bauer A. et al. 2011. Protection first then facilitation: a manipulative parasite modulates the vulnerability to predation of its intermediate host according to its own developmental stage // Evolution. V. 65. № 9. P. 2692–2698. https://doi.org/10.1111/j.1558-5646.2011.01330.x
  12. Gopko M.V., Mikheev V.N., Taskinen J. 2017. Positive density-dependent growth supports costs sharing hypothesis and population density sensing in a manipulative parasite // Parasitology. V. 144. № 11. P. 1511–1518. https://doi.org/10.1017/S0031182017001020
  13. Grant J. 1997. Territoriality // Behavioural ecology of teleost fishes. Oxford: Oxford Univ. Press. P. 81–103.
  14. Grant J.W.A., Noakes D.L.G. 1987. Movers and stayers: foraging tactics of young-of-the-year brook charr, Salvelinus fontinalis // J. Anim. Ecol. V. 56. № 3. P. 1001–1013. https://doi.org/10.2307/4962
  15. Haas W., Stiegeler P., Keating A. et al. 2002. Diplostomum spathaceum cercariae respond to a unique profile of cues during recognition of their fish host // Int. J. Parasitol. V. 32. № 9. P. 1145–1154. https://doi.org/10.1016/s0020-7519(02)00089-9
  16. Haas W., Beran B., Loy C. 2008. Selection of the host’s habitat by cercariae: from laboratory experiments to the field // J. Parasitol. V. 94. № 6. P. 1233–1238. https://doi.org/10.1645/GE-1192.1
  17. Hendrickson G.L., Kingston N. 1974. Cercaria laramiensis sp. n., a freshwater zygocercous cercaria from Physa gyrina Say, with a discussion of cercarial aggregation // Ibid. V. 60. № 5. P. 777–781. https://doi.org/10.2307/3278899
  18. Johnsson J.I., Carlsson M., Sundström L.F. 2000. Habitat preference increases territorial defence in brown trout (Salmo trutta) // Behav. Ecol. Sociobiol. V. 48. № 5. P. 373–377. https://doi.org/10.1007/s002650000244
  19. Karvonen A., Seppälä O., Valtonen E.T. 2004. Parasite resistance and avoidance behaviour in preventing eye fluke infections in fish // Parasitology. V. 129. № 2. P. 159–164. https://doi.org/10.1017/S0031182004005505
  20. Laitinen M., Siddall R., Valtonen E.T. 1996. Bioelectronic monitoring of parasite-induced stress in brown trout and roach // J. Fish Biol. V. 48. № 2. P. 228–241. https://doi.org/10.1111/j.1095-8649.1996.tb01115.x
  21. Mikheev V.N., Pasternak A.F., Taskinen J., Valtonen E.T. 2010. Parasite-induced aggression and impaired contest ability in a fish host // Parasit. Vectors. V. 3. Article 17. https://doi.org/10.1186/1756-3305-3-17
  22. Mikheev V.N., Pasternak A.F., Taskinen J., Valtonen E.T. 2013. Grouping facilitates avoidance of parasites by fish // Ibid. V. 6. Article 301. https://doi.org/10.1186/1756-3305-6-301
  23. Mikheev V.N., Pasternak A.F., Taskinen J., Valtonen E.T. 2014. Increased ventilation by fish leads to a higher risk of parasitism // Ibid. V. 7. Article 281. https://doi.org/10.1186/1756-3305-7-281
  24. Mikheev V.N., Pasternak A.F., Morozov A.Yu., Taskinen J. 2020. Innate antipredator behavior can promote infection in fish even in the absence of predators // Behav. Ecol. V. 31. № 1. P. 267–276. https://doi.org/10.1093/beheco/arz188
  25. Odening K., Bockhardt I. 1976. On the seasonal occurrence of Azygia lucii (Trematoda) in Esox lucius (Pisces) // Zool. Anzeiger. V. 196. № 3–4. P. 182–188.
  26. Parker G.A., Ball M.A., Chubb J.C. et al. 2009. When should a trophically transmitted parasite manipulate its host? // Evolution. V. 63. № 2. P. 448–458. https://doi.org/10.1111/j.1558-5646.2008.00565.x
  27. Poulin R. 2010. Parasite manipulation of host behaviour: an update and frequently asked questions // Adv. Stud. Behav. V. 41. P. 151–186. https://doi.org/10.1016/S0065-3454(10)41005-0
  28. Poulin R., FitzGerald G.J. 1989. Risk of parasitism and microhabitat selection in juvenile sticklebacks // Can. J. Zool. V. 67. № 1. P. 14–18. https://doi.org/10.1139z89-003
  29. Poulin R., Marcogliese D.J., McLaughlin J.D. 1999. Skin-penetrating parasites and the release of alarm substances in juvenile rainbow trout // J. Fish. Biol. V. 55. № 1. P. 47–53. https://doi.org/10.1111/j.1095-8649.1999.tb00655.x
  30. Seppälä O., Karvonen A., Valtonen E.T. 2005. Impaired crypsis of fish infected with a trophically transmitted parasite // Anim. Behav. V. 70. № 4. P. 895–900. https://doi.org/10.1016/j.anbehav.2005.01.021
  31. Smyth J.D. 1966. The physiology of trematodes. Edinburgh; London: Oliver and Boyd, 256 p.
  32. Stumbo A.D., James C.T., Goater C.P., Wisenden B.D. 2012. Shoaling as an antiparasite defence in minnows (Pimephales promelas) exposed to trematode cercariae // J. Anim. Ecol. V. 81. № 6. P. 1319–1326. https://doi.org/10.1111/j.1365-2656.2012.02012.x
  33. Sukhdeo M.V.K., Sukhdeo S.C. 2004. Trematode behaviours and the perceptual worlds of parasites // Can. J. Zool. V. 82. № 2. P. 292–315. https://doi.org/10.1139/z03-212
  34. Weinreich F., Benesh D.P., Milinski M. 2012. Suppression of predation on the intermediate host by two trophically-transmitted parasites when uninfective // Parasitology. V. 140. № 1. P. 129–135. https://doi.org/10.1017/S0031182012001266
  35. Whyte S.K., Secombes C.J., Chappell L.H. 1991. Studies on the infectivity of Diplostomum spathaceum in rainbow trout (Oncorhynchus mykiss) // J. Helminthol. V. 65. № 3. P. 169–178. https://doi.org/10.1017/s0022149x0001066x

Supplementary files

Supplementary Files
Action
1. JATS XML
Download
2.

Download (2KB)
Indexing metadata
3.

Download (2KB)
Indexing metadata
4.

Download (241KB)
Indexing metadata

Copyright (c) 2023 В.Н. Михеев