Polarized light cues underlie compass calibration in migratory songbirds.

Abstract

Migratory songbirds use the geomagnetic field, stars, the Sun, and polarized light patterns to determine their migratory direction. To prevent navigational errors, it is necessary to calibrate all of these compass systems to a common reference. We show that migratory Savannah sparrows use polarized light cues from the region of sky near the horizon to recalibrate the magnetic compass at both sunrise and sunset. We suggest that skylight polarization patterns are used to derive an absolute (i.e., geographic) directional system that provides the primary calibration reference for all of the compasses of migratory songbirds.

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DOI: 10.1126/science.1129709
, 837 (2006);
313
Science
et al.Rachel Muheim,
in Migratory Songbirds
Polarized Light Cues Underlie Compass Calibration

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Polarized Light Cues Underlie
Compass Calibration in
Migratory Songbirds
Rachel Muheim,1,2* John B. Phillips,2Susanne A˚kesson1
Migratory songbirds use the geomagnetic field, stars, the Sun, and polarized light patterns to
determine their migratory direction. To prevent navigational errors, it is necessary to calibrate all of
these compass systems to a common reference. We show that migratory Savannah sparrows use
polarized light cues from the region of sky near the horizon to recalibrate the magnetic compass at
both sunrise and sunset. We suggest that skylight polarization patterns are used to derive an
absolute (i.e., geographic) directional system that provides the primary calibration reference for all
of the compasses of migratory songbirds.
S
modal directional cues is poorly understood.
Although many species of songbirds have been
shown to have an innate sense of migratory
direction derived from magnetic (6–8) and/or
celestial (9–11) cues, these compass systems
are Brecalibrated[ when exposed to conflicting
directional information. Such conflicts occur
naturally when magnetic declination changes;
this change is especially pronounced at high
latitudes (12). When cue availability changes
with time of day and/or weather conditions,
avoiding navigational errors requires that infor-
mation from all of the compasses be calibrated
with respect to a common reference (13). Here,
we show that the primary calibration reference
is derived from horizon-polarized light cues at
sunrise (SR) and sunset (SS).
Research on the integration of compass in-
formation by migratory songbirds has focused
on experiments in which birds were given con-
flicting directional information from two or
more cues to determine which of the cues is
given greater saliency and whether the con-
flict results in recalibration of one or more of
the compass systems. Such experiments have
produced variable and sometimes contradictory
findings. Most studies suggest that birds give
precedence to celestial light cues and use these
cues to recalibrate the magnetic compass before
the onset of migration (6, 7, 14–16) but that
the reverse is true once birds begin migration;
that is, the magnetic compass takes precedence
over and is used to calibrate celestial light cues
(17–19). However, two studies demonstrated
recalibration of the magnetic compass with
respect to SS cues during migration (i.e., the
cue hierarchy normally observed during the
premigratory period) (20, 21). In a recent re-
tudies of migratory songbirds provide
evidencethattheyusemultiplecompasses
(1–5), but the integration of these multi-
view (13), we found that recalibration of the
magnetic compass with respect to SS (or SR)
cues occurred during both the premigratory and
migratory periods when birds exposed to con-
flicting information were able to see celestial
polarized light cues from the horizon sky. In
studies carried out during migration that failed
to show magnetic compass recalibration, birds
were exposed to cue conflicts in orientation
cages/funnels that blocked a view of the sky
near the horizon (13). When deprived of polar-
ized light cues from this region of sky, birds
gave precedence to magnetic cues and second-
arily calibrated other celestial cues (e.g., star
patterns and/or overhead polarized light cues)
with respect to the magnetic field (22–29).
To clarify the role of polarized light cues
in calibration of the magnetic compass, we
tested whether wild-caught Savannah spar-
rows, Passerculus sandwichensis, recalibrated
their magnetic compass when exposed to con-
flicting magnetic and polarized light cues near
the horizon at SR or SS. We captured juvenile
and adult birds in the Yukon Delta National
Wildlife Refuge, Alaska, during autumn 2005.
The birds were held indoors under the natu-
ral photoperiod without access to natural visual
cues (30). All orientation experiments were
started at around SS and carried out indoors in
the ambient magnetic field in the absence of
celestial cues, thus requiring the birds to use
their magnetic compass for orientation (30). The
magnetic orientation of individual birds selected
for experimental exposures is shown in Fig. 1B
(see also table S1). They were given a single
exposure for 60 min around SR or SS to a cue
conflict between the ambient magnetic field
and an artificial polarization pattern rotated
by T90- relative to the natural polarization
pattern at that time of day (Fig. 1C). During
exposure, the birds had a full view of the
surroundings, including the horizon, through
the polarization filters that produced the
artificial pattern (30).
After exposure to the cue conflict, the mag-
netic compass orientation of the birds was again
tested indoors. The distribution of bearings was
indistinguishable from random (SR, mean bear-
ingoraxisa0 138-/318-,r 0 0.08, P 0 0.82, N 0
30; SS, a 0 309-, r 0 0.17, P 0 0.59, N 0 20;
Fig. 1D and table S1) and was significantly
different from the birds_ initial responses (Fig.
1B; nonparametric two-sample Watson U2test:
SR, U20 0.33, P G 0.005; SS, U20 0.42, P G
0.001). The absence of significant clustering of
bearings after cue-conflict exposure suggests that
the birds did not orient in a consistent direction
or axis relative to the magnetic field. Thus, the
birds had not calibrated the magnetic compass in
a fixed relationship (e.g., perpendicular or
parallel) to the polarization pattern or to the
Sun_s position, which was visible to some birds
during the cue-conflict exposure (Fig. 1, D and
E, open symbols; table S1). However, when
each bird_s response after cue-conflict exposure
(Fig. 1D) was plotted as a deviation from its
initial response (Fig. 1B), the deviations were
bimodally distributed along an axis perpendic-
ular to their earlier response (SR, a 0 85-/265-,
r 0 0.54, P G 0.001, N 0 30; SS, a 0 94-/274-,
r 0 0.58, P G 0.001, N 0 20; Fig. 1E and
table S1).
These findings indicate that the birds had
shifted their orientation relative to the magnetic
field by T90-, corresponding to the rotation of
the artificial polarization pattern relative to the
natural pattern at the same time of day (i.e., SR
or SS; Fig. 1E). The alternative hypothesis that
calibration of the magnetic compass occurs
only at SS or only at SR is excluded by the data
(Fig. 1E, triangles outside circle) (30). More-
over, both juvenile and adult birds recalibrated
their magnetic compass (adult birds were ex-
posed and tested only at SR) (30) (table S1).
Birds that recalibrated the magnetic compass at
SR subsequently did so again at SS, and vice
versa (30) (table S1).
A small sample of birds exposed to a rotated
polarization axis that did not include the horizon
exhibited orientation that was indistinguishable
from their responses before exposure, indicating
that the magnetic compass had not been re-
calibrated (fig. S1E and table S2) (30).
Our findings support the following conclu-
sions: (i) The magnetic compass is recalibrated
with respect to polarized light cues at both SR
and SS; a conflict between magnetic and po-
larizedlightcuesateithertimeofdayresultedin
recalibration of the magnetic compass. (ii) This
recalibration occurs both before Eas shown by
previous investigators, reviewed in (13)^ and
during migration, and in both juvenile and adult
birds. (iii) A view of the polarization patterns
from the sky near the horizon is required for
magnetic compass recalibration. Thus, the fail-
ure to observe magnetic compass recalibration
in many studies carried out during migration is
probably the result of exposure to the cue
conflict in cages/funnels that obscured the
natural horizon (13). In conjunction with earlier
work showing that Sun and star compass cali-
brations are secondarily derived from magnet-
ic and polarized light cues (23, 24, 31), these
1Department of Animal Ecology, Lund University, Ecology
Building, SE-223 62 Lund, Sweden.
Biological Sciences, Virginia Polytechnic Institute and State
University, Derring Hall, Blacksburg, VA 24061, USA.
2Department of
*To whom correspondence should be addressed. E-mail:
rmuheim@vt.edu
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findings suggest that horizon polarization pat-
terns at SR and SS provide the primary cali-
bration reference for all the compass systems
of migratory songbirds.
At SR and SS, the band of maximum polar-
ization (BMP) passes directly through the zenith
(32, 33) and, along with the e-vector (electrical
vector) of polarized light, is aligned vertically on
the horizon (30) (fig. S2, A and B). In contrast to
Sun position, therefore, the intersections of the
BMP with the horizon at SR and SS are inde-
pendent of topography (i.e., horizon height). In
addition, because the BMP and e-vector are
vertically aligned only at SR and SS, their use as
a calibration reference would not require a time
compensation mechanism (34). Averaging the
intersections of the BMP with the horizon during
a successive SR and SS would enable migratory
birds to derive an absolute reference system that
is Bfixed[ with respect to the north-south
meridian at any location on Earth and thus
independent of latitude and time of year (30, 34)
(fig. S2C). Periodic updating of the relationship
between the polarization patterns at SR and SS
(i.e., their angular Bsplit[ on either side of the
meridian) would make it possible to use either
the SR or SS pattern to estimate the reference
direction and calibrate other compass systems
(30) (fig. S2, D and E).
Changes in latitude and time of year produce
oppositeshiftsinthealignmentsoftheBMPatSR
and SS (fig. S3). Consequently, use of the polar-
ization pattern at either SR or SS alone as an
independentcalibrationreference(i.e.,withoutav-
eraging) can result in a gradually curving mi-
gratory route that may under some conditions be
adaptive (30) (fig. S3). However, such routes
depend on the timing of migration and would
therefore be altered by delays such as those
caused by extended periods of inclement weather.
InspecieslikeourSavannahsparrowsthatuse
both SR- and SS-polarized light patterns (Fig. 1),
failure to integrate the information from these
two times of day would produce an unpredict-
able Bzig-zagging[ migratory path depending on
whether the clear skies necessary to see the
polarization pattern occurred most recently at SR
or at SS (30). Thus, not only does averaging of
SR- and SS-polarized light cues provide a cal-
ibration reference that is unaffected by changes
in latitude and time of year, but failure to do so
would decrease the accuracy and increase the
distance of migration. In species that use both
SR- and SS-polarized light cues to calibrate
other compass systems, therefore, both curving
migratory routes and abrupt changes in migrato-
ry direction associated with major topographic
features (such as oceans and mountain ranges)
are likely to involve secondary adaptations rather
than properties of the underlying calibration
reference system (12, 30, 35–37).
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(SR; left) and sunset (SS; right). (A and C) 360- view of sky under natural and experimental conditions
(gN, geographic north; mN, magnetic north). Purple and orange bars indicate mean position of band of
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Fish and Wildlife Service (permit 05-YDNWR-02).
Supported by the Swedish Science Research Council
(S.A˚.), a Swiss National Science Foundation postdoctoral
fellowship (R.M.), and NSF grants IBN04-25712 and
IBN02-16957 (J.B.P.).
Supporting Online Material
www.sciencemag.org/cgi/content/full/313/5788/837/DC1
Materials and Methods
SOM Text
Figs. S1 to S3
Tables S1 and S2
References
9 May 2006; accepted 4 July 2006
10.1126/science.1129709
Requirement for Coronin 1 in
T Lymphocyte Trafficking and
Cellular Homeostasis
Niko Fo ¨ger,1Linda Rangell,2Dimitry M. Danilenko,2Andrew C. Chan1*
The evolutionarily conserved actin-related protein (Arp2/3) complex is a key component of actin filament
networks that is dynamically regulated by nucleation-promoting and inhibitory factors. Although much is
known about actin assembly, the physiologic functions of inhibitory proteins are unclear. We generated
coronin 1j/jmice and found that coronin 1 exerted an inhibitory effect on cellular steady-state F-actin
formation via an Arp2/3-dependent mechanism. Whereas coronin 1 was required for chemokine-
mediated migration, it was dispensable for T cell antigen receptor functions in T cells. Moreover, actin
dynamics, through a mitochondrial pathway, was linked to lymphocyte homeostasis.
T
regulated by a cohort of actin-associated pro-
teins. The Wiskott-Aldrich syndrome (WAS)
and the suppressor of cyclic adenosine mono-
phosphate (cAMP) receptor (SCAR) proteins
promote actin nucleation and assembly via the
Arp2/3 complex (1–3), whereas inhibitory pro-
teins, which include coronin, tropomysosin, and
caldesmon, oppose Arp2/3 function (4–6). The
evolutionarily conserved coronin family of
actin-binding proteins has been implicated in
the regulation of multiple actin-mediated cellular
functions, including cell migration, cytokinesis,
and cell growth of Dictyostelium discoideum and
Saccharomyces cerevisiae (7–12). Among the
seven mammalian coronin family members,
he integrity of the actin cytoskeletal
network is critical for a diverse range of
biological processes and is dynamically
coronin 1 (also known as coro1a, TACO, or
p57) is preferentially expressed in cells of
hematopoietic origin, where it is coexpressed
with other more widely expressed coronin family
members that include coronins 2, 3, and 7 (fig.
S1A) (13). In mammals, coronin 1 colocalizes
with F-actin surrounding phagocytic vesicles in
neutrophils and macrophages and F-actin–rich
membranes in activated T cells (14–16).
To investigate the physiological role of
coronin 1, we generated coronin 1j/jmice (fig.
S1, B and C). No coronin 1 protein was detected
in thymocytes, splenocytes, or bone marrow–
derived cells isolated from coronin 1j/jmice,
and expression of coronins 2 and 3 was not
altered (fig. S1D). Analysis of lymphoid tissues
revealed normal segregation of T and B cells but
a paucity of T cells in spleens and lymph nodes
of coronin 1j/jmice (Fig. 1A). Both CD4þand
CD8þT cells were decreased in the blood,
spleen, and lymph nodes (Fig. 1B). NaBve, but
not memory/effector, splenic T cells were de-
creased, although both were reduced in the blood
and lymph nodes of coronin 1j/jmice. Thymic
cellularity and subpopulations were similar
between coronin 1j/jand coronin 1þ/þmice,
although a small reduction in mature CD4þand
CD8þ(CD69–) coronin 1j/jthymocytes was
observed (Fig. 1C and fig. S1, I to J). An anal-
ysis of coronin 1j/jmice bearing either major
histocompatibility complex (MHC) class 1 re-
stricted H-Y or class II restricted DO11.10 trans-
genic T cell antigen receptors (TCRs) revealed
normal thymic development and decreased naBve
T cells in lymph nodes (Fig. 1D).
The requirement for coronin in cell motili-
ty in D. discoideum prompted us to examine
whether coronin 1 may play a role in thymic
emigration and homing to secondary lymphoid
organs. CD4þcoronin 1j/jthymocytes dem-
onstrated reduced spontaneous migration and
transwell migration to CCL19, CXCL12, and
CCL25 (Fig. 2A). Defects in chemotaxis were
also observed in splenic CD4þnaBve and
effector/memory coronin 1j/jT cells (fig. S2B).
Coronin 1j/jT cells also demonstrated com-
promised migration in whole-organ thymic
cultures and in vivo thymic egress (fig. S2, C
and D). Lastly, adoptive transfer of differen-
tially labeled coronin 1j/jand coronin 1þ/þ
CD4þthymocytes revealed È60% decreased
homing of coronin 1j/jcells to lymph nodes
(Fig. 3A). Thus, coronin 1 plays important func-
tional roles in cell motility and chemokine-
mediated homing of T lymphocytes to secondary
lymphocyte organs.
Because the actin cytoskeleton is required
for cellular polarization and lymphocyte migra-
tion, we analyzed the morphologic changes
induced by CCL19. Whereas stimulated coronin
1þ/þT cells acquired a polarized phenotype
with unipolar accumulation of talin beneath
the cell membrane opposite of the uropod,
coronin 1j/jT cells failed to develop a uro-
pod and formed multiple patch-like talin-rich
1Department of Immunology,
Genentech, Incorporated, 1 DNA Way, South San Francisco,
CA 94080, USA.
2Department of Pathology,
*To whom correspondence should be addressed. E-mail:
acc@gene.com
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