The sun compass of the sandhopper Talitrus saltator: the speed of the chronometric mechanism depends on the hours of light
1 Dipartimento di Biologia Animale e Genetica, Università di Firenze,
Via Romana 17, 50125 Firenze, Italy
2 Istituto Nazionale di Ottica Applicata, Firenze, Italy
3 Dipartimento di Sanità Pubblica, Università di Firenze,
Italy
* Author for correspondence (e-mail: ugolini_alb{at}dbag.unifi.it)
Accepted 8 July 2002
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Summary |
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Key words: orientation, sun compass, chronometric mechanism, sandhopper, Talitrus saltator
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Introduction |
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The sun compass mechanism in sandhoppers has been the subject of thorough
investigations (Papi and Pardi,
1953; Pardi and Papi,
1953
; Papi, 1955
;
Pardi and Grassi, 1955
). These
revealed the mechanism's chronometric basis, which results in compensation for
the azimuthal variation of the sun. Experiments utilising photoperiod
phase-shifting (Pardi and Grassi,
1955
; Marchionni,
1958
) and the `longitudinal jump' (i.e. Italian sandhoppers tested
in Argentina; Papi, 1955
)
showed that the ability to compensate for apparent solar motion is not due to
local orientation factors. On the basis of experimental observations made on
freshly collected individuals, Pardi and Papi
(1953
) hypothesized that this
mechanism compensates precisely for the azimuthal variation of the sun (=
differential compensation). However, it should be remembered that the
azimuthal speed of the sun varies during the day and the year depending on its
height above the horizon. These variations could affect the accuracy of
sandhopper orientation (for example, see
Ugolini, 2001
).
It has been hypothesised (Ugolini and
Frittelli, 1998) that compensation for apparent solar motion does
not vary during the day but is based on the mean speed of the sun (determined
on the basis of the sun's daily azimuthal variation and the number of hours of
light).
We have therefore carried out experiments to test the two hypotheses of sun compensation in T. saltator. In particular, we tested whether the light:dark (L:D) ratio affects the speed of compensation of the sun compass chronometric mechanism.
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Materials and methods |
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The experiments were conducted from August to October in 1998 and 1999 in Florence in conditions of natural sun and sky. The tests were performed every 15-30 min throughout the animals' subjective day or night.
The sandhoppers were released into an apparatus described previously
(Ugolini and Macchi, 1988;
Ugolini, 2001
) composed of a
transparent Plexiglas bowl (diameter 18 cm) set on a transparent Plexiglas
plate placed horizontally on a tripod. A cylindrical white Plexiglas screen (3
cm high) around the bowl prevented the sandhoppers from viewing the
surrounding landscape but allowed them to see the sun and sky. Groups of
approximately five individuals were released into the bowl containing
approximately 1 cm of seawater. Each individual was tested only once, and a
single direction per individual was recorded 2 min after release by means of a
video camera under the bowl.
Statistical analyses of the circular distributions deriving from each
release were performed using the procedure reported by Batschelet
(1981). For each distribution,
we calculated the mean resultant vector. Rao's test was applied to assess
whether the distribution differed from uniformity (P
0.05). The
bimodality of each distribution was assessed by the possible increase in
length of the mean vector using the method of doubling angles
(Batschelet, 1981
). In cases of
bimodality, only the landward resultant was considered. Uniform distributions
were excluded from further analysis. We chose the two-dimensional Cartesian
axes form rather than the circular form to represent the results because we
believed it would describe the results more effectively.
To test the time course of variation in compensation for apparent solar motion, we used least-squares polynomial regression, testing the successive powers of the independent variable (time) as separate predictor variables. The fit of functions to the data was quantified both by adjusted r2 (i.e. the adjusted coefficient of determination, the percentage of the total variability explained by the particular function taking account of the fact that the parameters are estimated from the data) and by testing the highest term in the polynomial for significance by Student's t-test. From the different polynomials tested for the same values, the one with maximum r2 and the lowest t probability was chosen.
To compare the fitting of the selected curves in
Fig. 2C, we chose the following
method. For each curve, we calculated the sum-of-squared differences between
the mean angle and the corresponding value on the curve; we then divided this
sum by the degrees of freedom to obtain a variance value quantifying the
variability about the regression. To compare these variabilities with the
variability about the polynomial regression, we calculated the variance ratio:
the variance about the regression for a single curve divided by the variance
about the regression for the polynomial regression; the result was compared
with the F table for N-1 and N-3 degrees of
freedom. The F-probability gives a measure of similarity between
curves, the highest probability indicating the greatest similarity (see
Armitage et al., 2002).
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Tests of the slopes and intercepts and of whether the regression lines were parallel were carried out with the usual Student's t-test methods.
Theoretical models of the sandhoppers' sun compass chronometric
mechanism
The theoretical variation in the angle of orientation that individuals
should assume with respect to the sun to maintain a constant direction was
calculated according to the following criteria. For individuals tested when
their subjective day corresponds to the natural day, we considered the model
proposed by Ugolini and Frittelli
(1998), i.e. that the
mechanism of compensation for the movement of the sun has a constant speed
during the period of light (or dark) and that its speed is regulated by the
duration of the photoperiod of the previous day (or a few days) and the
azimuthal variation of the sun in that period of the year. Obviously, a
constant speed during the same time period will cause theoretically
predictable orientation `errors' by the animals, as a result of the
discrepancy between the speed of the internal chronometric mechanism and the
azimuthal speed of the sun (which is not constant during the day or year).
This can be represented by the following expression, given that the mean
direction of orientation of the sandhoppers and the solar azimuth at the time
of the release are parameters that derive from the experiment itself:
![]() | (1) |
![]() | (2) |
To simplify interpretation of the experiments in which the tests occurred
during the sandhoppers' subjective night (inverted photoperiod), it should be
remembered that there are two models of compensation for apparent solar motion
at night: (i) the `Apis mellifera model' (Lindauer,
1954,
1957
): at night, the sun passes
from west through north to its position in the east in the morning
(Fig. 1A); and (ii) the
`Talitrus model' proposed by Pardi
(1954
) and not since tested in
amphipods, although confirmed in other riparian or littoral arthropods
(Birukow, 1957
;
Ercolini and Scapini, 1976
;
Pardi, 1958
): compensation for
the sun in the nocturnal period of solar orientation occurs as if the sun,
once it has set in the west, retraces the path covered during the day, i.e.
passing from west to south to east at sunrise
(Fig. 1B). It should be
emphasised that, during the subjective night, the sandhoppers were tested
under the natural sun (which appears to move from east to west). Therefore,
the expected direction of orientation will necessarily be different from that
of the home beach (Fig.
1C).
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Results |
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Tests with individuals kept under an artificial L:D cycle corresponding to the natural photoperiod, during the subjective night (Fig. 2B), gave the best fit to the regression line (adjusted r2=0.335). The slope, which is positive and statistically significant (P=0.029), is significantly different from that of the expected direction (P<0.0001). In fact, there is a tendency for the animals to assume angles of orientation that are constantly less than the expected ones.
Fig. 2C,D illustrates the results of experiments with sandhoppers subjected to 4h:20h L:D and 20h:4h L:D inverted (i.e. tested under the natural sun during the 4h of subjective night).
To determine the degree of the polynomial model for the regression of Fig. 2C, we used the method described above. The second-degree polynomial gave the best fit: adjusted r2=0.548; residual sum of squares=11940 (d.f.=14); F=10.7; P(F)=0.0015; t for the highest term=-2.61; P(t)=0.020. Comparisons of the fitting of the curves to the second-degree polynomial are reported in Table 2. The highest F-probability indicates the highest similarity between the model and the second-degree polynomial. The final model chosen (curve c) was the second-degree polynomial (Fig. 2C).
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For sandhoppers subjected to 20h:4h L:D inverted (Fig. 2D), the fit to the regression line is given by r2 adjusted=0.597; the slope, which is positive and significant (P<0.0005), is not significantly different from that of the expected direction (P=0.109).
The slopes of the regression lines in Fig. 2B,D are significantly different (t=4.18; d.f.=28; P=0.0003).
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Discussion |
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It is well documented that sunrise is an important Zeitgeber for
sandhoppers (Williams, 1980).
Therefore, it should be emphasised that in our experiments the imposed time of
sunrise does not cause a deviation in the mean directions of orientation
corresponding to the theoretically predicted deviation in the case of a
clock-shifting of 6 h and 17 min with respect to the natural sunrise, which
affects the subjective noon; in this case, the mean directions represented in
Fig. 2C should correspond to
lines d or e but not to line b.
Therefore, the relationship between the number of hours of light and the
number of hours of dark influences the speed of the chronometric mechanism of
compensation for apparent solar motion. However, this implies that the
sandhoppers use information about the total azimuthal variation in the sun in
that particular period of the year but not about the daily variation in the
sun's azimuthal speed. In other words, the speed of the solar compensation
mechanism is independent of the height of the sun above the horizon. Although
experiments on this topic were not conducted in the present study, this
hypothesis is supported by the results of previous experiments in which the
solar azimuth was deflected with a mirror: the height of the reflected sun had
no influence on the sandhoppers' choice of direction (see
Pardi, 1957;
Pardi and Ercolini, 1986
).
We do not wish to enter the debate about the existence of an ephemerid's
function in crustaceans, as demonstrated for insects and birds (see
Wehner and Lanfranconi, 1981;
Neuss and Wallraff, 1988
;
Schmidt-Koenig et al., 1991
;
Wehner and Müller, 1993
;
Dyer and Dickinson, 1994
;
Towne and Kirchner, 1998
;
Wiltschko et al., 2000
).
However, we would like to emphasize that sandhoppers are neither `homers' nor
`central place foragers'; instead, they use a unidirectional, nonvectorial
orientation in their zonal recovery (i.e. to return as quickly as possible to
the belt of damp sand near the sea). Therefore, it would not be surprising if
they used a chronometric system for sun compensation that differed somewhat
from (i.e. was simpler than) that used by other animals with different
spatio-temporal problems to solve.
Moreover, the present study shows that a single chronometric mechanism
provides for compensation for apparent solar motion both during the day and at
night. Concerning nocturnal compensation for the movement of the sun, our
results do not fully confirm the `Talitrus model' proposed by Pardi
(1954); a larger number of
releases is necessary to clarify the matter of sun compensation at night.
However, for the purposes of the present research, it is sufficient to note
the difference between Fig. 2B
and Fig. 2D: the slope of the
regression line in Fig. 2D is
significantly different from that in Fig.
2B, in agreement with the expected effect of a reduction in the
number of hours of dark.
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Acknowledgments |
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