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The role of extraocular photoreceptors in newt magnetic compass orientation: parallels between light-dependent magnetoreception and polarized light detection in vertebrates

John B. Phillips^*, Mark E. Deutschlander, Michael J. Freake and S. Chris Borland

Department of Biology, Indiana University, Bloomington, IN 47405, USA
Present address: Department of Biological Sciences, Rochester Institute of Technology, Rochester, NY 14623, USA

View larger version (31K): [in a new window]   Fig. 1. Effects of light and head caps on bimodal magnetic compass orientation in newts. (A–D) The predicted orientation of newts with respect to the wavelength conditions during training and testing (based on the findings in Phillips and Borland, 1992a). A diagram of a training tank with the shore towards magnetic North (mN) is shown for each training condition, and a diagram of the circular test arena shows the predicted magnetic response of the newts (double-headed arrow) under full-spectrum light (no color), short-wavelength light (in blue), or long-wavelength light (in yellow). (A,B) When trained under full-spectrum light, the newts should perceive the shore to be towards magnetic North (indicated by the single-headed arrow) and exhibit bimodal magnetic orientation along the shoreward axis when tested under full-spectrum (A) or short-wavelength (B) light. (C) When trained under full-spectrum light and tested under long-wavelength (>500nm) light, the newts’ perception of magnetic North during testing (mN'), and hence their orientation in the test arena, should be rotated by 90°. (D) When trained under long-wavelength light, the newts’ perception of magnetic North (mN') and, therefore, of the direction of shore, should be rotated by 90°. When subsequently tested under long-wavelength light, the newts’ perception of the direction of the magnetic field in the arena would be the same as it was in the outdoor tank, and they should orient in the correct shoreward direction. Wavelength conditions during training and testing, as well as the spectral properties of the caps (circle on the diagram of the head in I–L), are indicated in E–L. Each data point represents the magnetic bearing of a single newt. All data are plotted with respect to the magnetic direction of shore in the training tank (i.e. the shore direction=360°). Double-headed arrows at the center of each plot indicate the mean axis of orientation with the mean vector length proportional to the strength of orientation, r (the diameter of the circle corresponding to r=1). Dashed lines indicate the 95% confidence intervals for the mean axis. Each distribution for which a mean axis is shown is significant at P<0.05 (Rayleigh test). (E,F). Newts trained under natural sky light and tested under full-spectrum (E) or short-wavelength (450nm) (F) light oriented along the shoreward magnetic axis (mShore). (G) Newts trained under natural sky light and tested under long-wavelength light exhibited orientation rotated by 90° from the shoreward magnetic direction (filled circles were tested under broadband >500nm light; filled squares were tested under 550nm light). (H) Newts trained and tested under long-wavelength (>500nm) light oriented along the shoreward axis. (I) After training under natural sky light, newts with clear caps exhibited orientation rotated by 90° from the shoreward direction under long-wavelength (>500nm) light. (J) After training under natural sky light, newts with long-wavelength-transmitting caps oriented along the shoreward axis under long-wavelength (>500nm) light. (K) When tested under full-spectrum light, newts with caps transmitting short-wavelength light exhibited significant orientation along the shoreward axis. (L) When tested under long-wavelength light (550–650nm, indicated in yellow), however, these newts failed to exhibit significant shoreward orientation. (Parts A-J of this figure are modified from Deutschlander et al., 1999a; Deutschlander et al., 1999b, in which all original data and statistical analyses can be found.)

View larger version (19K): [in a new window]   Fig. 2. Comparison of the wavelength-dependence of light-dependent magnetic compass orientation and polarized light responses. (A) Wavelength-dependence of shoreward magnetic compass orientation in newts (data from Phillips and Borland, 1992a). The shoreward components (filled symbols, y axis on left) and 90°-shifted components (open symbols, y axis on right) of mean vector bearings were calculated from the distributions of magnetic bearings of newts tested under different wavelengths of light (x axis) and plotted relative to the magnetic direction of shore (0°). The shoreward components were highest under 400 and 450nm light, whereas the 90°-shifted (90–270°) components were highest under 500, 550 and 600nm light. Under 475nm light, both components were close to zero, indicating that the newts failed to exhibit a consistent direction of magnetic orientation. Shoreward component=cosine(mean vector bearing)x(mean vector length). 90°-shifted component=-sine(mean vector bearing)x(mean vector length). (B) Wavelength-dependence of sensitivity to the alignment of the e-vector of plane polarized light in the optic nerve of rainbow trout Oncorhynchus mykiss (from Parkyn and Hawryhsyn, 1993). Parkyn and Hawryshyn determined sensitivity by extracellular recordings from the optic nerve in which individual cone mechanisms were isolated by spectral adaptation (Parkyn and Hawryhsyn, 1993). Sensitivity to each e-vector alignment was calculated as log10 of the reciprocal of irradiance at a criterion response of 30µV. Data taken from Fig.5 in Parkyn and Hawryshyn, 1993 were used to calculate a mean axis of response by vector addition, from which the components of the response to vertically aligned e-vectors (0–180° component, y axis on left, filled squares) and to horizontally aligned e-vectors (90–270° component, y axis on right, open squares) were calculated. The component of the response to vertically aligned e-vectors was highest in the ‘ultraviolet’ mechanism stimulated by 380nm light, while the component of response to horizontally aligned e-vectors was highest in the ‘green’ mechanism stimulated by 540nm light and the ‘red’ mechanism stimulated by 660nm light. The ‘blue’ mechanism stimulated by 440nm light was insensitive to e-vector alignment. The mean axes of the response were calculated by the present authors using vector addition on the relative sensitivities (the antilogarithm of the responses measured from Fig.5 in Parkyn and Hawryshyn, 1993) after first doubling the e-vector angles; the mean axis of the response was obtained by dividing the mean vector bearing of the distribution of doubled angles by 2. 0–180° component=|cosine(deviation of mean axis from vertical)x(mean axis length)|. 90–270° component=|sine(deviation of mean axis from vertical)x(mean axis length)|. Absolute values were used because there was no basis for distinguishing between clockwise and anticlockwise deviations from vertical. So, for example, the vertical component of the response to an e-vector of 60–240° is the same as that of a comparable response to an e-vector of 120–300°. (C) Wavelength-dependence of sensitivity to the alignment of the e-vector of plane polarized light in goldfish Carassius auratus (from Hawryshyn and McFarland, 1987). Hawryshyn and McFarland determined polarization sensitivity by measuring increment thresholds obtained by heart-rate conditioning while using spectral adaptation to isolate individual cone mechanisms (Hawryshyn and McFarland, 1987). Sensitivity to each e-vector alignment was calculated as log10 of the reciprocal of irradiance at threshold. Data taken from Fig.4 in Hawryshyn and McFarland, 1987, were used to calculate a mean axis of response by vector addition, from which the components of response to vertically aligned e-vectors (0–180° component, y axis on left) and to horizontally aligned e-vectors (90–270° component, y axis on right) were calculated. The component of response to vertically aligned e-vectors was highest in the ‘ultraviolet’ mechanism stimulated by 380nm light, while the component of response to horizontally aligned e-vectors was highest in the ‘green’ mechanism stimulated by 540nm light and the ‘red’ mechanism stimulated by 660nm light. The ‘blue’ mechanism stimulated by 460nm light was insensitive to e-vector alignment. Mean axes of response were calculated as in B.

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