Brain-encysting trematodes and altered monoamine activity in naturally infected killifish Fundulus parvipinnis

Journal of Fish Biology

Volumn 81, Issue 7, 2012, Pages 2213-2222

  Shaw, J C ^a   Øverli, Ø ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

Author keywords

5 HIAA; 5 HT; DOPAC; Heterophyidae; Monoamine; Serotonin

Indexed keywords

AVES; CYPRINODONTIFORMES; CYPRINODONTOIDEI; EUHAPLORCHIS CALIFORNIENSIS; FUNDULUS PARVIPINNIS; HETEROPHYIDAE; HIPPOCAMPUS (FISH); PISCES; TREMATODA; VERTEBRATA;

EID: 84871333018     PISSN: 00221112     EISSN: 10958649     Source Type: Journal    
DOI: 10.1111/j.1095-8649.2012.03439.x     Document Type: Article

References (58)

1. Adamo, S. A. (2002). Modulating the modulators: parasites, neuromodulators and host behavioral change. Brain, Behavior and Evolution 60, 370-377.
2. Adamo, S. A. (2010). Why should an immune response activate the stress response? Insights from the insects (the cricket Gryllus texensis). Brain Behavior and Immunity 24, 194.
3. Aman, T. K., Shen, R. Y. & Haj-Dahmane, S. (2007). D-2-like dopamine receptors depolarize dorsal raphe serotonin neurons through the activation of nonselective cationic conductance. Journal of Pharmacology and Experimental Therapeutics 320, 376-385.
4. Anken, R. & Bourrat, F. (1998). Brain Atlas of the Medakafish Oryzias latipes. Paris: INRA Editions.
5. Barber, I., Walker, P. & Svensson, P. A. (2004). Behavioural responses to simulated avian predation in female three spined sticklebacks: The effect of experimental Schistocephalus solidus infections. Behaviour 141, 1425.
6. Benjamini, Y. & Hochberg, Y. (1995). Controlling the false discovery rate - a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society B 57, 289-300.
7. Berdoy, M., Webster, J. P. & Macdonald, D. W. (2000). Fatal attraction in rats infected with Toxoplasma gondii. Proceedings of the Royal Society B 267, 1591-1594.
8. Biron, D. G., Ponton, F., Marche, L., Galeotti, N., Renault, L., Demey-Thomas, E., Poncet, J., Brown, S. P., Jouin, P. & Thomas, F. (2006). 'Suicide' of crickets harbouring hairworms: a proteomics investigation. Insect Molecular Biology 15, 731-742.
9. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Analytical Biochemisty 72, 248-254.
10. Burghardt, N. S., Sullivan, G. M., McEwen, B. S., Gorman, J. M. & LeDoux, J. E. (2004). The selective serotonin reuptake inhibitor citalopram increases fear after acute treatment but reduces fear with chronic treatment: a comparison with tianeptine. Biological Psychiatry 55, 1171.
11. Butler, A. B. & Hodos, W. (2005). Comparative Vertebrate Neuroanatomy: Evolution and Adaptation New York, NY: Wiley-Liss.
12. Chaouloff, F. (2000). Serotonin, stress and corticoids. Journal of Psychopharmacology 14, 139-151.
13. Clements, S., Moore, F. L. & Schreck, C. B. (2003). Evidence that acute serotonergic activation potentiates the locomotor-stimulating effects of corticotropin-releasing hormone in juvenile chinook salmon (Oncorhynchus tshawytscha). Hormones and Behavior 43, 214-221.
14. Cools, R., Roberts, A. C. & Robbins, T. W. (2008). Serotoninergic regulation of emotional and behavioural control processes. Trends in Cognitive Sciences 12, 31.
15. Crowden, A. E. & Broom, D. M. (1980). Effects of the eyefluke, Diplostomum spathaceum, on the behavior of dace (Leuciscus leuciscus). Animal Behaviour 28, 287-294.
16. Dahlbom, S. J., Backstrom, T., Lundstedt-Enkel, K. & Winberg, S. (2012). Aggression and monoamines: effects of sex and social rank in zebrafish (Danio rerio). Behavioural Brain Research 228, 333.
17. Fillenz, M. (1993). Neurochemistry of stress: Introduction to techniques. In Stress From Synapse to Syndrome (Stanford, S. C. & Salmon, P., eds.), pp. 247-279. London: Academic Press.
18. Guiard, B. P., El Mansari, M., Merali, Z. & Blier, P. (2008). Functional interactions between dopamine, serotonin and norepinephrine neurons: an in-vivo electrophysiological study in rats with monoaminergic lesions. International Journal of Neuropsychopharmacology 11, 625.
19. Helluy, S. & Thomas, F. (2003). Effects of Microphallus papillorobustus (Platyhelminthes : Trematoda) on serotonergic immunoreactivity and neuronal architecture in the brain of Gammarus insensibilis (Crustacea: Amphipoda). Proceedings of the Royal Society B 270, 563-568.
20. Höglund, E., Weltzien, F. A., Schjolden, J., Winberg, S., Ursin, H. & Doving, K. B. (2005). Avoidance behavior and brain monoamines in fish. Brain Research 1032, 104-110.
21. Holmes, J. C. & Bethel, W. M. (1972). Modification of intermediate host behaviour by parasites. In Behavioural Aspects of Parasite Transmission (Canning, E. U. & Wright, C. A., eds), pp. 123-150. New York, NY: Academic Press Inc.
22. de Jong-Brink, M., Bergamin-Sassen, M. & Soto, M. S. (2001). Multiple strategies of schistosomes to meet their requirements in the intermediate snail host. Parasitology 123, S129-S141.
23. Kannan, G., Moldovan, K., Xiao, J. C., Yolken, R. H., Jones-Brando, L. & Pletnikov, M. V. (2010). Toxoplasma gondii strain-dependent effects on mouse behaviour. Folia Parasitologica 57, 151-155.
24. Klein, S. L. (2003). Parasite manipulation of the proximate mechanisms that mediate social behavior in vertebrates. Physiology and Behavior 79, 441-449.
25. Korzan, W. J., Summers, T. R. & Summers, C. H. (2000). Monoaminergic activities of limbic regions are elevated during aggression: influence of sympathetic social signaling. Brain Research 870, 170-178.
26. Korzan, W. J., Forster, G. L., Watt, M. J. & Summers, C. H. (2006). Dopaminergic activity modulation via aggression, status, and a visual social signal. Behavioral Neuroscience 120, 93-102.
27. Lafferty, K. D. & Morris, A. K. (1996). Altered behavior of parasitized killifish increases susceptibility to predation by bird final hosts. Ecology 77, 1390-1397.
28. Lefevre, T., Adamo, S. A., Biron, D. G., Misse, D., Hughes, D. & Thomas, F. (2009). Invasion of the body snatchers: the diversity and evolution of manipulative strategies in host-parasite interactions. Advances in Parasitology 68, 45-83.
29. Libersat, F. & Pflueger, H. J. (2004). Monoamines and the orchestration of behavior. Bioscience 54, 17-25.
30. Libersat, F., Delago, A. & Gal, R. (2009). Manipulation of host behavior by parasitic insects and insect parasites. Annual Review of Entomology 54, 189-207.
31. Love, M. S. & Moser, M. (1983). A Checklist of Parasites of California, Oregon, and Washington Marine and Estuarine Fishes Washington, DC: US Department of Commerce.
32. Mok, E. Y. M. & Munro, A. D. (1998). Effects of dopaminergic drugs on locomotor activity in teleost fish of the genus Oreochromis (Cichlidae): involvement of the telencephalon. Physiology and Behavior 64, 227-234.
33. Moore, J. (2002). Parasites and the Behavior of Animals New York, NY: Oxford University Press, Inc.
34. Northcutt, R. G. (1983). Telencephalic organization in ray-finned fishes. In Fish Neurobiology (Davis, R. E. & Northcutt, R. G., eds), pp. 203-236. Ann Arbor, MI: The University of Michigan Press.
35. Øverli, Ø., Harris, C. A. & Winberg, S. (1999). Short-term effects of fights for social dominance and the establishment of dominant-subordinate relationships on brain monoamines and cortisol in rainbow trout. Brain, Behavior and Evolution 54, 263-275.
36. Øverli, Ø., Pall, M., Borg, B., Jobling, M. & Winberg, S. (2001). Effects of Schistocephalus solidus infection on brain monoaminergic activity in female three-spined sticklebacks Gasterosteus aculeatus. Proceedings of the Royal Society B 268, 1411-1415.
37. Øverli, Ø., Korzan, W. J., Larson, E. T., Winberg, S., Lepage, O., Pottinger, T. G., Renner, K. J. & Summers, C. H. (2004). Behavioral and neuroendocrine correlates of displaced aggression in trout. Hormones and Behavior 45, 324-329.
38. Parent, A. (1983). The monoamine-containing neuronal systems in the teleostean brain. In Fish Neurobiology (Davis, R. E. & Northcutt, R. G., eds.), pp. 285-315. Ann Arbor, MI: The University of Michigan Press.
39. Peter, R. E., Macey, M. J. & Gill, V. E. (1975). Stereotaxic atlas and technique for forebrain nuclei of killifish, Fundulus heteroclitus. Journal of Comparative Neurology 159, 103-127.
40. Poulin, R. (2010). Parasite manipulation of host behavior: an update and frequently asked questions. In Advances In The Study of Behavior (Brockmann, H. J., ed.), pp. 151-186. Burlington, MA: Academic Press.
41. Prandovszky, E., Gaskell, E., Martin, H., Dubey, J. P., Webster, J. P. & McConkey, G. A. (2011). The neurotropic parasite Toxoplasma gondii increases dopamine metabolism. PLoS ONE 6, e23866.
42. Renner, K. J. & Luine, V. N. (1984). Determination of monoamines in brain nuclei by high-performance liquid-chromatography with electrochemical detection - young vs middle-aged rats. Life Sciences 34, 2193-2199.
43. Salas, C., Broglio, C. & Rodriguez, F. (2003). Evolution of forebrain and spatial cognition in vertebrates: conservation across diversity. Brain, Behavior and Evolution 62, 72-82.
44. Seppälä, O., Karvonen, A. & Valtonen, E. T. (2006). Susceptibility of eye fluke-infected fish to predation by bird hosts. Parasitology 132, 575-579.
45. Shaw, J. C., Korzan, W. J., Carpenter, R. E., Kuris, A. M., Lafferty, K. D., Summers, C. H. & Øverli, Ø. (2009). Parasite manipulation of brain monoamines in California killifish (Fundulus parvipinnis) by the trematode Euhaplorchis californiensis. Proceedings of the Royal Society B 276, 1137-1146.
46. Shaw, J. C., Hechinger, R. F., Lafferty, K. D. & Kuris, A. M. (2010). Ecology of the brain trematode Euhaplorchis californiensis and its host, the California killifish (Fundulus parvipinnis). Journal of Parasitology 96, 482.
47. Shirakashi, S. & Goater, C. P. (2002). Intensity-dependent alteration of minnow (Pimephales promelas) behavior by a brain-encysting trematode. Journal of Parasitology 88, 1071-1074.
48. Stanford, S. C. (1993). Monoamines in response and adaptation to stress. In Stress From Synapse to Syndrome (Stanford, S. C. & Salmon, P., eds), pp. 282-331. London: Academic Press.
49. Summers, C. H. & Winberg, S. (2006). Interactions between the neural regulation of stress and aggression. Journal of Experimental Biology 209, 4581-4589.
50. Thomas, F., Schmidt-Rhaesa, A., Martin, G., Manu, C., Durand, P. & Renaud, F. (2002). Do hairworms (Nematomorpha) manipulate the water seeking behaviour of their terrestrial hosts? Journal of Evolutionary Biology 15, 356-361.
51. Thomas, F., Adamo, S. & Moore, J. (2005). Parasitic manipulation: where are we and where should we go? Behavioural Processes 68, 185-199.
52. Vyas, A., Kim, S.-K., Giacomini, N., Boothroyd, J. C. & Sapolsky, R. M. (2007). Behavioral changes induced by Toxoplasma infection of rodents are highly specific to aversion of cat odors. Proceedings of the National Academy of Sciences of the United States of America 104, 6442-6447.
53. Webster, J. P. & McConkey, G. A. (2010). Toxoplasma gondii-altered host behaviour: clues as to mechanism of action. Folia Parasitologica 57, 95-104.
54. Weiger, W. A. (1997). Serotonergic modulation of behaviour: a phylogenetic overview. Biological Reviews of the Cambridge Philosophical Society 72, 61-95.
55. Winberg, S. & Nilsson, G. E. (1993). Roles of brain monoamine neurotransmitters in agonistic behavior and stress reactions, with particular reference to fish. Comparative Biochemistry and Physiology C 106, 597-614.
56. Winberg, S., Nilsson, A., Hylland, P., Soderstom, V. & Nilsson, G. E. (1997). Serotonin as a regulator of hypothalamic-pituitary-interrenal activity in teleost fish. Neuroscience Letters 230, 113-116.
57. Wullimann, M. F. & Mueller, T. (2004). Teleostean and mammalian forebrains contrasted: Evidence from genes to behavior. Journal of Comparative Neurology 475, 143-162.
58. Wullimann, M. F., Rupp, B. & Reichert, H. (1996). Neuroanatomy of the Zebrafish Brain: A Topological Atlas Basel: Birkhäuser Verlag.