Migratory Reed Warblers Need Intact Trigeminal Nerves to Correct for a 1,000 km Eastward Displacement

Abstract

Several studies have shown that experienced night-migratory songbirds can determine their position, but it has remained a mystery which cues and sensory mechanisms they use, in particular, those used to determine longitude (east-west position). One potential solution would be to use a magnetic map or signpost mechanism like the one documented in sea turtles. Night-migratory songbirds have a magnetic compass in their eyes and a second magnetic sense with unknown biological function involving the ophthalmic branch of the trigeminal nerve (V1). Could V1 be involved in determining east-west position? We displaced 57 Eurasian reed warblers (Acrocephalus scirpaceus) with or without sectioned V1. Sham operated birds corrected their orientation towards the breeding area after displacement like the untreated controls did. In contrast, V1-sectioned birds did not correct for the displacement. They oriented in the same direction after the displacement as they had done at the capture site. Thus, an intact ophthalmic branch of the trigeminal nerve is necessary for detecting the 1,000 km eastward displacement in this night-migratory songbird. Our results suggest that V1 carries map-related information used in a large-scale map or signpost sense that the reed warblers needed to determine their approximate geographical position and/or an east-west coordinate.

Figure 1. Results of our previous displacement study with intact Eurasian reed warblers (re-drawn after [4]).

(A) Orientation of birds at the capture site (Rybachy). (C) Orientation of the same birds after the 1,000 km eastward translocation at the displacement site (Zvenigorod). On A and C, pooled data for 2004, 2005 and 2007 are shown. Each dot at the circular diagram periphery indicates the mean orientation of one individual bird. The arrows show group mean directions and vector lengths. The dashed circles indicate the length of the group mean vector needed for significance (5% and 1% level for inner and outer dashed circle, correspondingly) according to the Rayleigh test . The lines flanking group mean vectors give 95% confidence intervals. gN – geographic North. On (B), a map of the displacement is shown. The shaded light gray zone represents the breeding range of the Eurasian reed warbler. Visual observations by local ornithologists (e.g. [22]) confirm that there are no regular breeding populations of Eurasian reed warblers further east than indicated on the map. The black filled circle represents the single known recovery of a reed warbler ringed in Rybachy and re-captured as a breeding bird , . The dashed line vector from the capture site at Rybachy shows the mean migratory direction of the given species according to our previous study (, α = 42°). The solid line circle represents a proposed area where transit Eurasian reed warblers are heading to based on our previous study combined with ringing recoveries (the goal). The solid line vector from Rybachy to Zvenigorod shows the direction and distance of the displacement. The two dashed line vectors from Zvenigorod represent our expectations for V1-sectioned and sham-sectioned birds, respectively: (1): no compensation, (2): compensation towards the eastern part of the breeding range.

Figure 2. Orientation of birds at the capture and displacement site.

(A, C) Results for sham-sectioned birds, before sham-surgery at the capture site (A) and after sham-surgery and translocation to the displacement site (C). (E, G) Results for V1-sectioned birds before V1-sectioning at the capture site (E) and after V1-sectioning surgery and translocation to the displacement site (G). For description of the circular diagrams and the map (D), see Figure 1. The schemes of real V1-section (F) and sham section (B) show the approximate locations of the three branches of the trigeminal nerve. The ophthalmic branch (V1) is shown in bold. The crosses on F indicate the approximate locations at which the nerve was sectioned and a piece of the nerve was removed. For details about the surgeries, see Methods.

Figure 3. Differences of the geomagnetic field parameters between capture site, displacement site and a putative goal area.

(A) Difference in total intensity; (B) Difference in inclination; (C) Difference in declination. The measured geomagnetic field parameters at Rybachy (the left dot) were the following: total intensity 50,688 nT, inclination 70.3°, declination 5.6°. The measured geomagnetic field parameters at Zvenigorod (the right dot) were the following: total intensity 52,175 nT, inclination 71.2°, declination 10.1°. As a goal site (the upper dot), the centroid of “the goal” shown on Figure 1 (60° 30′N, 27° 51′E) was taken. Computation of the Earth’s magnetic field parameters for the goal site was done with the calculator of IGRF Model 11 in the website of the National Geophysical Data Center (http://www.ngdc.noaa.gov/geomag/geomag.shtml). The calculated geomagnetic field parameters at the goal site were the following: total intensity 52,172 nT, inclination 73.7°, declination 8.9°. The charts with the isolines of the geomagnetic field parameters are taken from http://pubs.usgs.gov/sim/2007/2964 with modifications.