Navigation and seasonal migratory orientation in juvenile sea turtles
1 Department of Biology, University of North Carolina, Chapel Hill, NC
27599-3280, USA
2 NOAA Fisheries, Beaufort, NC 28516-9722, USA
* Author for correspondence (e-mail: larisa.avens{at}noaa.gov)
Accepted 17 February 2004
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Summary |
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Key words: sea turtle, orientation, navigation, migration, map, loggerhead, green turtle, Caretta caretta, Chelonia mydas
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Introduction |
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Loggerheads and green turtles that occupy temperate and sub-tropical
regions often undertake seasonal migrations, presumably to avoid lethal water
temperatures that occur during winter months
(Morreale et al., 1992;
Shoop and Kenney, 1992
;
Epperly et al.,
1995a
,b
).
For example, turtles from inshore waters in North Carolina, Virginia and New
York migrate south/southeast during autumn months to reach warmer, coastal
waters or the Gulf Stream (Shoop and
Kenney, 1992
; Keinath,
1993
; Morreale and Standora,
1995
; NOAA Beaufort Laboratory, unpublished data). In the spring,
some of these juveniles migrate back to the same specific northern feeding
sites that they inhabited during the warm months of the previous year
(Byles, 1988
;
Avens et al., 2003
).
Little is known about the mechanisms of orientation and navigation that
enable juvenile and adult sea turtles to navigate to specific targets, such as
feeding areas, or to complete long, seasonal migrations. The guidance
mechanisms of hatchling turtles have been studied extensively (reviewed by
Lohmann et al., 1997;
Lohmann and Lohmann, 2003
),
but ontogenetic changes in orientation and navigation are known to occur in
many animals (Wiltschko, 1983
;
Baker, 1984
;
Able and Bingman, 1987
;
Rodda and Phillips, 1992
;
Able and Able, 1996
). Thus, the
strategies and mechanisms used by large, juvenile turtles, as well as by
adults, may differ significantly from those used by hatchlings beginning their
first migration.
As a first step towards investigating mechanisms of orientation and navigation in older turtles, we have adapted techniques used to study hatchlings for use with juvenile turtles captured in inshore waters. The results indicate that both homing behavior and seasonal migratory orientation can be elicited in an experimental arena under conditions in which environmental variables can be carefully controlled. In addition, the results provide strong evidence that juvenile turtles can assess their position relative to a destination using cues available at the test site and are therefore capable of map-based navigation.
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Materials and methods |
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Although specific age estimates are not available for the turtles used in
this study, current estimates of pelagic stage duration for loggerheads
recruiting to the benthic environment at 4664 cm SCL range from 7.0 to
11.5 years (Bjorndal et al.,
2003). Thus, the majority of loggerheads used for these
experiments were probably at least 7 years old. Estimates of ages for juvenile
green turtles inhabiting inshore waters in Florida range from 2 years at 21 cm
to 7 years at 44 cm,indicating that the green turtles obtained for our study
were at least 2 years of age (Zug and
Glor, 1998
).
All turtles were first transported by boat to land and then by vehicle to
the testing site at the National Oceanic and Atmospheric Administration (NOAA)
Laboratory in Beaufort, North Carolina
(Fig. 1). Turtles caught during
fishing operations were typically held in the boat for 13 h before
being taken to shore. During this time, turtles were prevented from viewing
their surroundings and the sky, and the boat moved along indirect, circuitous
routes that typically involved multiple detours to different fishing nets.
Loggerheads captured at the nuclear power plant intake canal were transported
uncovered, first by boat and then in a truck, to a temporary holding facility
approximately 2 km away, where they were held for less than 6 h before being
transported to the NOAA lab. All overland transport to the lab occurred during
daylight hours. During these trips, turtles from all capture sites were kept
inside the vehicle, where they were unable to view their surroundings, and
transported to the test site by indirect routes along winding coastal roads.
The test site was approximately 30 km (straight-line distance) from capture
locations in Core Sound, 4574 km from capture sites in Pamlico Sound
and 65167 km from capture areas outside of Core and Pamlico Sounds.
At the laboratory, each turtle was placed into an outdoor, circular, holding tank measuring 2 m in diameter that was partially covered to provide shade. The walls of each tank blocked the view of the horizon and any natural landmarks; however, turtles were able to view the sky directly above and might have glimpsed the tops of nearby buildings and trees. Sea water was continuously circulated through the tanks and water depth was maintained at 0.75 m. Turtles were allowed to acclimate to captive conditions for approximately 24 h before being used in experiments.
Orientation arena and data acquisition
Juvenile turtles were tested in an experimental arena
(Fig. 2) consisting of a
circular, fiberglass tank that was 6 m in diameter and 1.5 m high (Red Ewald,
Karnes City, TX, USA). The arena, which was filled with seawater to a depth of
0.75 m, was located outdoors and was uncovered, allowing the turtles to view
the sky. However, the walls of the tank blocked the turtles' view of the
natural horizon and surroundings.
|
During testing, each turtle was outfitted with a nylonLycraTM harness that encircled the carapace. The turtle was then tethered to a rotatable arm mounted at the center of the arena (Fig. 2). As the turtle swam, the tether pulled the arm so that the arm tracked the turtle's swimming direction continuously. A digital encoder coupled to the arm was wired to a nearby computer so that headings could be recorded to the nearest 1.4° at intervals of 30 s.
Immediately before and after each trial, the tracking system was checked to ensure that data were recorded accurately relative to magnetic north (0°). In addition, the water was stirred prior to each trial to ensure that no chemical gradients existed in the tank.
Testing procedure
All experiments were conducted between May and November, months when
turtles inhabit coastal waters of North Carolina or migrate through them
(Epperly et al.,
1995a,b
).
Trials were conducted during daylight hours, between 12:30 h and 17:00 h,
under diverse weather conditions.
To minimize the possibility that the orientation of a turtle upon release might influence the direction it subsequently swam, green turtles were released in the center of the arena facing random directions. To release loggerheads (which were much larger and heavier than the green turtles), it was necessary to stand on a low platform, which was located just outside the northern edge of the arena. Thus, all loggerheads were released in the north, but successive animals were released facing east and west.
After a turtle was tethered to the arm and released in the tank, it was
allowed a 5-min acclimation period before the trial was initiated. The data
acquisition computer then recorded the turtle's directional headings for the
next 10 min, resulting in 20 measurements of headings. At the end of the
10-min trial, the computer calculated a mean angle on the basis of the 20 data
points. This angle represented the average direction that the turtle swam
(Batschelet, 1981).
Trials were observed from a raised platform located approximately 5 m from
the perimeter of the tank. Previous tests have demonstrated that the presence
of observers at this distance does not influence the orientation of turtles
swimming in the arena (Avens and Lohmann,
2003). These observations are consistent with similar findings
involving hatchling turtles (Salmon and
Lohmann, 1989
; Witherington,
1991
). Animals were monitored to ensure that they swam
consistently at the end of the tether. Turtles were eliminated from the study
if, during three or more computer readings, they either did not swim (i.e.
they floated motionless or sat on the bottom of the tank) or they moved
backwards or otherwise swam erratically so that the direction of the rotatable
arm did not accurately reflect the turtle's orientation.
Data analysis
In North Carolina, sea turtles occupy inshore waters from approximately
April through September and begin to migrate when water temperatures decrease
during October and November (Epperly et
al., 1995a). Data obtained between May and September (`summer')
were therefore analyzed to determine whether turtles exhibited orientation
that might represent homing to the feeding areas where they were captured. By
contrast, data collected during October and November (`autumn') were analyzed
to determine whether turtles exhibited seasonally appropriate migratory
orientation. Because turtles were obtained from Pamlico Sound only during the
autumn, no data for turtles caught in this area were used in the homing
analysis.
The distributions of headings for turtles tested during the summer were
analyzed using the V-test in conjunction with the 95% confidence
interval for the mean angle. This was done to determine whether turtles in
each group were significantly oriented in a direction that was consistent with
the direction of their capture location
(Batschelet, 1981). The
`homeward' direction for loggerhead and green turtles captured in Core Sound,
to the eastnortheast of the testing site, was 74°. Because
loggerheads obtained to the westsouthwest of the testing site were
caught at several different locations (Fig.
1), a mean homeward bearing (255°) was calculated for these
turtles and this bearing was used for the V-test analysis. Watson's
U2 test was used to determine whether the headings of
loggerheads obtained to the eastnortheast and to the
westsouthwest were significantly different
(Batschelet, 1981
).
Data obtained from turtles tested during the autumn were analyzed using the
Rayleigh test to determine whether the turtles were significantly oriented
(Batschelet, 1981). The
V-test was not used in this case because the precise direction of the
migration (e.g. south vs southeast) could not be predicted. Watson's
U2 test was used to determine whether the orientation of
loggerhead and green turtles in the autumn was significantly different from
that observed for each species during the summer
(Batschelet, 1981
).
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Results |
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Juvenile green turtles obtained to the eastnortheast during the summer were also significantly oriented towards their capture area (mean angle=50°, P<0.0025, V-test, 95% confidence interval ±37°; Fig. 4A).
|
Autumn orientation
Juvenile loggerheads captured eastnortheast of the testing site
during October and November (`autumn') were significantly oriented with a mean
heading of 190° (P<0.005; Rayleigh test, 95% confidence
interval ±33°; Fig.
3C). This direction of orientation was significantly different
from that observed for loggerheads captured to the eastnortheast and
tested during the summer (P<0.001, Watson's U2
test). Similarly, green turtles tested during the autumn were significantly
oriented with a mean heading of 199° (P<0.02; Rayleigh test,
95% confidence interval ±39°;
Fig. 4B). The orientation of
green turtles during summer months differed significantly from orientation
during autumn (P<0.02; Watson's U2 test).
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Discussion |
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Animals capable of homing are thought to possess both a positional sense to
determine geographic location (or at least the direction to the goal) and a
directional or compass sense to maintain a heading towards the appropriate
homeward direction (Kramer,
1961; Able, 2001
).
Sea turtles are known to have a magnetic compass sense
(Lohmann, 1991
;
Lohmann and Lohmann, 1996a
),
and results of recent experiments have provided evidence that juvenile turtles
possess a second mechanism for maintaining headings, possibly based on a sun
compass or on patterns of skylight polarization
(Avens and Lohmann, 2003
).
By contrast, little is known about the position-finding system of juvenile and adult sea turtles. In principle, displaced turtles in our experiments might have determined the direction to the capture site in at least two different ways: by monitoring the outward path to the test site or by detecting positional cues available at the test site.
Map-based navigation
One possibility is that the turtles monitored the outward journey to the
test site with sufficient resolution to set a course back towards the capture
area. However, most turtles remained on fishing boats for at least 13 h
after capture, during which time the turtles were deprived of visual cues and
the boat changed direction and location almost continuously. Turtles were then
transported by vehicle for an additional period of 30200 min along
winding, circuitous routes to the test site.
Thus, to determine the direction towards the capture site using information obtained during the outward journey, turtles would have had to monitor closely the direction and distance of different parts of the trip over both water and land for a period of several hours, in the absence of visual cues, and with little or no information about the velocity of the boat or vehicles. Although such a possibility cannot be excluded with certainty, we consider it unlikely.
An alternative explanation is that turtles determined their position
relative to the capture area, or at least the general direction towards the
capture area, using cues available at the testing location. Such an ability is
known to exist in several animals, including birds
(Wiltschko and Wiltschko,
2003), amphibians (Phillips, 1995) and lobsters
(Boles and Lohmann, 2003
). Our
data suggest that sea turtles also possess this ability and are therefore
capable of map-based navigation as defined by Able
(2001
).
The cue or cues that turtles used to assess their position relative to the
capture site cannot be determined from these initial experiments. Visual
landmarks could not have provided the basis for the positional assessment
because no natural landmarks were available in the test arena or holding
tanks. Among several potential sources of positional information are
location-specific chemical cues (Grassman
et al., 1984), if such cues existed in the water in which the
turtles were tested, and information from the Earth's magnetic field (Lohmann
and Lohmann, 1994
,
1996b
;
Lohmann et al., 2001
).
Although positional information is also potentially available from celestial
cues such as the elevation (height above the horizon) of the sun at specific
times of the day, there is presently no evidence that any animal exploits this
information in navigation (Gould,
1998
).
Homing in the ocean
In several previous studies, juvenile or adult sea turtles were displaced
and released at various distances away from capture sites
(Ireland, 1980;
Murphy and Hopkins-Murphy,
1990
; Ryder, 1995
;
Standora et al., 1995
;
Avens et al., 2003
). In each
case, many returned to the capture area, implying that the turtles have
navigational mechanisms that enable them to compensate for displacements and
to home to specific locations. These findings are consistent with the
observations of Carr (1967
),
who reported that turtles displaced approximately 50 km from feeding grounds
in the Gulf of Mexico often returned rapidly to the sites where they had been
captured. They are also consistent with several published anecdotes in which
marked turtles displaced from Nicaragua to Florida
(Carr, 1956
), from Nicaragua
to the Cayman Islands (Carr,
1956
), and from Ascension Island to the English Channel
(Cornelius, 1865
) also
returned to their original capture sites.
Not all turtle displacements have resulted in clear homing behavior (Luschi
et al., 2001,
2003
). In general, however,
studies in which little or no homing has been reported have involved unusually
long displacements, displacement of nesting turtles during the internesting
interval when turtles are normally inactive, or placement of satellite
transmitters directly on the turtles' heads
(Luschi et al., 2001
). Because
transmitters produce magnetic fields, this last treatment may impair the
turtles' ability to perceive magnetic information in the same way that magnets
placed on turtles disrupt magnetic orientation
(Avens and Lohmann, 2003
;
Irwin and Lohmann, 2003
;
Grocott, 2003
). Regardless of
these considerations, however, our results are consistent with the hypothesis
that turtles are capable of map-based navigation.
Migratory orientation
Whereas turtles tested during summer months oriented in directions that
coincided with routes towards their capture areas (Figs
3A,B,
4A), turtles tested during the
autumn migration oriented southward (Figs
3C,
4B), a direction consistent
with the seasonal movements of North Carolina turtles at this time of year
(Shoop and Kenney, 1992;
Keinath, 1993
;
Morreale and Standora, 1995
;
NOAA Beaufort Laboratory, unpublished data). These results demonstrate for the
first time that seasonal migratory orientation can be elicited in juvenile
loggerhead and green turtles under controlled conditions.
The orientation behavior of the turtles during the migratory season closely
parallels the restlessness exhibited by captive, migratory birds
(Wiltschko and Wiltschko,
1991). Avian researchers have been able to exploit this behavior
to investigate a number of factors related to bird migration, including the
cues used to orient and navigate (Munro et
al., 1997
; Wiltschko et al.,
1998
), the genetic basis of migratory orientation
(Helbig, 1996
;
Pulido et al., 2001
) and the
circannual rhythms involved in migration
(Gwinner, 1996
). Similar
topics can now be studied in sea turtles using the techniques described in
this study.
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Acknowledgments |
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