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The influence of magnetic field on the spatial orientation in zebrafish Danio rerio (Hamilton) and roach Rutilus rutilus (L.)

Elena A. Osipova1, Vera V. Pavlova1, Anastasia A. Batrakova2 and Viacheslav V. Krylov1*
  • 1 I.D. Papanin Institute for biology of inland waters Russian Academy of Sciences, Russia
  • 2 P.G. Demidov Yaroslavl state university, Russia

Some Teleosts use geomagnetic field (GMF) for orientation (see review Krylov et al., 2013). However, there are very few experimental studies of the orientation with GMF in Cyprinids from natural populations. Recently, there have been studies on the influence of GMF on behavior in Cyprinids from laboratory strains (Hart et al., 2012; Ward et al., 2014). It was reported that zebrafish (Danio rerio) are able to perceive a static magnetic field of 100 µT (Shcherbakov et al., 2005). Takebe and the coauthors (2012) showed that zebrafish prefer the two opposite directions of the GMF after being released in the centre of a circular arena. Comparative studies of Cyprinids from laboratory strains and natural populations will expand knowledge of the magnetoreception used for orientation in GMF by these Teleosts. The aim was to study the influence of GMF and its modifications on the preferred directions in laboratory strains of D. rerio and Rutilus rutilus from the Rybinsk Reservoir under observation in a circular arena. Wild-type zebrafish were obtained from a commercial distributer. Roach underyearlings were caught at the channel joining the landing stage of IBIW RAS with the Rybinsk reservoir. Changes in the GMF were generated using three pairs of mutually orthogonal Helmholtz coils. These coils were connected to three constant current sources using an AKIP-1103 DC switching power supply. Fish were placed into an opaque tank without a bottom at the centre of the circular arena. The circular arena was placed inside the Helmholtz coils. After one minute, the observation tank was raised and the fish chose their initial direction of travel. Four artificial GMF modifications were tried: 1. 180 degrees reversal of both vertical and horizontal GMF components 2. 180 degrees reversal of the vertical GMF component 3. 180 degrees reversal of the horizontal GMF component 4. 90 degrees clockwise turn of the horizontal GMF component It is known that the behavioral responses of zebrafish to different influences are stable and they may persist through experiments on the assumption of a recovery period. All zebrafish individuals were tested in each of the four modifications and parallel controls. In the experiments with R. rutilus we only studied the influence of the 90 degrees clockwise turn of the horizontal GMF component on preferred direction. The fishes’ movements in the arena were recorded by a Panasonic-HC-X900M video camera. We recorded the angle of preferred direction as the fish crossed the 10 cm radius from the centre of the arena. A Northward direction corresponds to 0/360 degrees. Rayleigh’s z-test for unimodal and axial distribution was used to evaluate the significance of the preferred direction. The significance of the differences between preferred directions in the control and experimental groups was estimated using Watson’s U2-test. D. rerio. Significant preference of a single direction was not observed in any of the experiments. However, control groups (GMF) displayed a significant preference for the two opposite directions gravitating North and South (Figs. 1e, 1f, 1h). Among the experimental groups, bidirectional orientation was observed only by rotation of the horizontal component by 90 degrees clockwise (Fig. 1d). In this case, fish preferred Westward and Eastward directions. R. rutilus. Significant preference of the East-northeast direction was found. This direction matched the direction from the location where individuals were caught to the deep-water part of Rybinsk Reservoir (Fig. 2). On rotation of the horizontal component by 90 degrees clockwise, fish tended to move to the South-southeast. The angle between preferred directions in the experimental and control groups was 79.87 degrees. Differences in preferred directions between experimental and control groups were statistically significant (U2 = 0.38, p < 0.001). Many Teleosts are known to possess special cells which accumulate magnetite during ontogenesis and are used for magnetoreception (Walker, 2011). Magnetite was also found in tissues of zebrafish (Dixson, 2012). The results of our study confirm the bimodal distribution of D. rerio preferred directions in GMF observed by Takebe. Among the various modifications of GMF, only the rotation of the horizontal component by 90 degrees clockwise significantly changed the preferred direction of the zebrafish. The preference for two opposite directions that was observed in the GMF is associated with the use of the axial horizontal component of GMF for orientation, but with no reference to its direction. Similar preferences for two opposite directions were observed in Oncorhynchus nerka juveniles, as well as in Salmo trutta and Oncorhynchus mykiss embryos, under different magnetic conditions (Quinn and Brannon, 1982; Formicki et al., 1997). Adult fish from natural habitats usually choose only the direction of the GMF. It is possible that the importance of magnetosensitivity is currently declining in D. rerio due to both the human-induced changes of natural habitats and a long-term period of zebrafish strains being kept in aquaculture. Such reduction of magnetosensitivity may result in the inability to distinguish the direction and inclination of GMF vector and, as a consequence, bimodal distribution of preferred directions. This is the first study on the use of GMF for orientation in R. rutilus from a natural population. Our results confirm the presence of magnetosensitivity in roach. At the same time, the preferred direction in GMF matched the direction to the mouth of the channel where the fish were caught. It is possible that fish stressed by experimental manipulations have tried to “leave” the experimental arena in the usual direction of escape to the deep-water part of reservoir. Figure 1. Bimodal distribution of preferred directions in zebrafish by the reversal of vertical (a), horizontal (b), both vertical and horizontal (c) components of GMF, and by the rotation of the horizontal component by 90 degrees clockwise (d). Distributions of preferred directions in control conditions (GMF) for each experiment are given under corresponding diagrams (e, f, g, h). Figure 2. Distribution of preferred directions of roach in a GMF (a) and the rotation of the horizontal component of the GMF by 90 degrees clockwise (b). Sample area with designation of the direction of the channel to the Rybinsk Reservoir (c). Asterisk shows the point of sampling.

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Acknowledgements

This work was supported by grant from the Russian Foundation for Basic Research (Project #14-04-31157-mol_a).

References

Dixson, A. (2012). Zebrafish magnetite and long-lived rohon-beard neurons: expanding our view of two zebrafish sensory systems in development and adulthood. Ph.D. thesis. Pasadena: California Institute of Technology.
Formicki, K., Bonislavska, M., and Jasinski, M. (1997). Spatial orientation of trout (Salmo trutta L.) and rainbow trout (Oncorhynchus mykiss Walb.) embryos in natural and artificial magnetic fields. Acta Ichthyol. Piscat. 27, 29-40.
Hart,V., Kusta, T., Nemec, P. et al. (2012). Magnetic alignment in carps: evidence from the Czech Christmas fish market. PLoS ONE V. 7(12): e51100.
Krylov, V.V., Izyumov, Yu.G., Izvekov, E.I., and Nepomnyashchikh, V.A. (2014). Magnetic fields and fish behavior. Biol. Bull. Rev. 4, 222-231.
Quinn, T.P., and Brannon, E.L. (1982). The use of celestial and magnetic cues by orienting sockeye salmon smolts. Ibid 147, 547-552.
Shcherbakov, D., Winklhofer, M., Petersen, N. et al. (2005). Magnetosensation in zebrafish. Curr. Biol. 15, r161-r162.
Takebe, A., Furutani, T., Wada, T. et al. (2012). Zebrafish respond to the geomagnetic field by bimodal and group dependent orientation. Sci. Rep. 2: e727.
Ward, B.K., Tan, G.X.J., Roberts, D.C. et al. (2014). Strong static magnetic fields elicit swimming behaviors consistent with direct vestibular stimulation in adult zebrafish. PLoS ONE 9(3): e92109.
Walker, M.M. (2011). “Magnetic sense in fishes,” in Encyclopedia of fish physiology from genome to environment, Ed. A.P. Farrell (San Diego: Academic Press), 726-735.

Keywords: danio rerio, Rutilus rutilus, geomagnetic field, Preferred Direction, orientational behavior

Conference: XV European Congress of Ichthyology, Porto, Portugal, 7 Sep - 11 Sep, 2015.

Presentation Type: Poster Presentation

Topic: Physiology, Behavior and Toxicology

Citation: Osipova EA, Pavlova VV, Batrakova AA and Krylov VV (2015). The influence of magnetic field on the spatial orientation in zebrafish Danio rerio (Hamilton) and roach Rutilus rutilus (L.). Front. Mar. Sci. Conference Abstract: XV European Congress of Ichthyology. doi: 10.3389/conf.fmars.2015.03.00081

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Received: 31 Oct 2015; Published Online: 17 Nov 2015.

* Correspondence: Dr. Viacheslav V Krylov, I.D. Papanin Institute for biology of inland waters Russian Academy of Sciences, Borok, Russia, krylovviacheslav@mail.ru