Burrow surveillance in fiddler crabs I. Description of behaviour
Visual Sciences, Research School of Biological Sciences, Australian National University, GPO Box 475, Canberra, ACT 2600, Australia
* Author for correspondence (e-mail: jan.hemmi{at}anu.edu.au)
Accepted 30 July 2003
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Fiddler crabs [Uca vomeris (McNeill)] operate from burrows that they guard and defend vigorously against other crabs. The crabs live in dense populations, with many animals inhabiting one square metre of mudflat. We describe here the behavioural responses of foraging crabs to repeated presentations of small crab-like dummies approaching their burrows. We explore the relationship between the probability and the timing of burrow defence responses, the crab's behavioural state, and the visual appearance and direction of approach of the dummies. We find that the probability of response of resident crabs is independent of the relative position of crab and dummy but is strongly affected by the dummy's position and movement direction relative to the crab's burrow. The critical stimuli are the dummy's distance from the crab's burrow and whether the dummy is moving towards the burrow or not. The response distance (dummy-burrow distance) increases with the crab's own distance from the burrow, indicating that the crabs modify their assessment of threat depending on their own distance away from the burrow. Differences in dummy size and brightness do not affect the probability or the timing of the response.
We discuss these results in the context of fiddler crab social life and, in a companion paper, identify the visual and non-visual cues involved in burrow defence.
Key words: resource defence, burrow defence, visual behaviour, competitor, territory, fiddler crab, Uca vomeris
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Fiddler crab societies are an interesting model system in which such
questions can be addressed experimentally within the animals' natural social
context. The crabs live in high-density colonies and occupy small, overlapping
home ranges that are centred around the important resource of their burrow. In
this and a companion paper (Hemmi and
Zeil, 2003a), we describe the `knowledge base' of burrow
surveillance and defence in fiddler crabs (Uca vomeris). We ask what
aspects of a threatening situation the crabs take into account when they
decide whether to respond to an intruder and what sensory cues they use to
make this assessment. Our main focus is on the use of vision in these crabs
and how they exploit the particular geometry of the flat world they inhabit to
organise behaviour.
Fiddler crabs are small, semi-terrestrial crabs that are active during low
tide on the inter-tidal mudflats and sandflats of tropical and subtropical
estuaries. Most species are diurnal and work to a tight schedule of a few
hours a day with most of their time spent feeding, while the remaining time is
divided between burrow maintenance, social interactions, grooming and predator
avoidance (e.g. Caravello and Cameron,
1987; Crane, 1975
;
Wolfrath, 1993
). Each crab
operates from its own burrow, which it defends vigorously against other crabs.
Among males, burrow ownership is contested in partially ritualised, and often
drawn-out, fights (e.g. Crane,
1975
; Hyatt and Salmon,
1978
; Jennions and Backwell,
1996
; Jones, 1980
;
Pratt et al., 2003
).
The burrow is a very important resource for the crabs (for reviews, see
Crane, 1975;
Montaque, 1980
;
Zeil and Layne, 2002
). It
offers protection from aquatic predators during high tide and from aerial and
terrestrial predators during low tide, when the crabs are active on the
surface. It provides a safe refuge for moulting animals and for females while
incubating their eggs. The burrow protects the crabs from desiccation during
their activity on the surface by offering them access to water, which is
needed for respiration and feeding. How crucial burrows are as the only
protection against predators is illustrated by the behaviour of crabs that
have lost their burrow and are wandering through the colony in search of a new
home. These wanderers are vulnerable to predation and protect themselves by
approaching burrow owners. Although they are reliably chased away by resident
crabs, wanderers remain oriented towards the foreign burrow and, in case of
danger, are able to use it as a temporary refuge by following the resident
crab down into its burrow (Crane,
1975
; Ens et al.,
1993
; Zeil and Layne,
2002
).
In addition, the location of a fiddler crab burrow plays a significant role
in determining the owner's social environment and its access to food. The
burrow serves as a central hub from where the crabs venture out on their
feeding excursions, which, in the case of our study species (U.
vomeris), take them rarely more than 1 m away from the burrow. The crabs
repeatedly return to their burrow to defend it against other crabs, to take
refuge from predators or to replenish their water supply
(Zeil, 1998).
The degree of burrow fidelity appears to vary considerably, both between
and within species, depending on predation levels, social system, food
availability and possibly also on the substratum properties affecting the
stability of burrows (deRivera and
Vehrencamp, 2001; Ens et al.,
1993
; Genoni, 1991
;
Hyatt and Salmon, 1978
;
Koga et al., 1998
;
Montaque, 1980
; Salmon,
1984
,
1987
;
Wolfrath, 1993
). In Uca
vocans, a species closely related to U. vomeris, burrow fidelity
appears to be very weak (Altevogt,
1955
), and in some populations of U. vomeris only females
remain with their burrow for extended periods of time
(Salmon, 1984
). By contrast,
in our study population, both males and females appear strongly attached to
their burrows, at least within one activity period. Burrow fidelity is
possibly enhanced by the fact that the burrows are deep and that unoccupied
burrows are destroyed by the incoming tide, due to the soft ground. Such a
high-density, shelter-based, central foraging system must exert immense
pressure on burrow owners to not only guard their resource against
conspecifics but also to be efficient in avoiding over-responding to the
presence of burrow-owning, non-threatening neighbours. A crab that would not
be able to distinguish between resident neighbours and potential burrow
snatchers would spend a large part of its time guarding its burrow.
Here, we describe the circumstances that trigger burrow defence in foraging
fiddler crabs. We moved small, simple, dummy crabs (see also
von Hagen, 1962;
Hyatt and Salmon, 1978
;
Land and Layne, 1995a
;
Salmon and Stout, 1962
) across
the substrate towards the burrows of resident crabs and determined if and when
the crabs responded to the approaching dummy by rushing back to the burrow
entrance. The sensory cues that fiddler crabs use to make their assessment are
explored in a companion paper (Hemmi and
Zeil, 2003a
). A brief report on some of our results has been
published elsewhere (Hemmi and Zeil,
2003b
).
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The crab dummies consisted of small plastic cylinders, mounted on a Perspex
sled, which was slightly larger than the dummies themselves. The dummies were
black or white and were one of seven different sizes
(Fig. 1A). Most experiments
(484 of the total 633 experiments analysed) were performed with a dummy size
of 2.25 cmx1.2 cm. The dummy was attached to a monofilament line, which
was fed around two tent pegs that were 3-4 m apart and allowed the dummy
to be moved along a straight line, which we will call the `dummy track', by
manually pulling on the monofilament line
(Fig. 1B). With this
arrangement, the observer could control the dummy while sitting about 5-6 m
away. The dummy was moved with an approximately constant velocity. Due to the
nature of the substrate and the fact that dummies were moved by hand, some
variations in speed within each run could not be avoided. The mean velocity
ranged from 3 cm s-1 to 14 cm s-1 between experiments
(mean ± S.D. = 7.8±1.9 cm s-1).
|
The dummy track was arranged such that it passed the burrow of the focal
crab at a closest distance of about 10 cm (`track distance'). The distance of
the dummy track from the burrows of peripheral crabs was not controlled and
ranged from 5 cm to 55 cm. In a typical experiment, the dummy would approach
the burrow of the focal crab from 1-1.5 m away, move past the closest
point to the burrow for a short distance and then return to its original
position. In a small number of trials, the dummy did not reverse its direction
but left the area on the opposite side of the burrow from where it approached.
Each dummy approach was filmed for later analysis.
Video analysis
The film sequences were digitised at 240 ms frame intervals via an
IEEE 1394 card in a computer running a Linux/Slackware operating system. The
x and y coordinates of crabs and dummies were determined
using a video analysis program written by Jan Hemmi in C and Matlab and
corrected for optical and perspective distortions. The program automatically
tracks all crabs in a sequence. Because crabs can leave the recording area,
disappear by entering their burrows or become cryptic against the mottled
mudflat background, the operator had to manually track the crabs when the
program failed to do so. Based on the x and y coordinates of
the crabs, the dummy and the burrow, a response was considered to have started
in a given frame if a crab moved at least 0.66 cm towards its burrow during
the 240 ms time interval preceding this frame and at least 2 cm over a
three-frame interval (720 ms) starting at the previous frame. Responses were
not counted as such if the crab responded after the dummy had reached its
closest point to the burrow for the first time (74 of the 493 cases in which
crabs responded or 15%). This was necessary as most of these late responses
(60) occurred after the dummy turned around at the end of the track to move
back to its starting position and therefore completely changed the geometry of
the particular experiment. A special analysis, however, concentrates on these
late responses (Fig. 9). The
position of the dummy and the crab in the last frame before a crab reached the
response criterion was then taken as their position at the time of response.
This response criterion is used in the probability analysis outlined below. In
addition, we calculated a relative measure for the crab's response strength
based on the entire path of the crab (Fig.
1C). This measure expresses as a percentage how far a crab moved
towards its burrow during an experiment. The reference distance is the largest
crab-burrow distance before the crab responded.
|
Selection of trials for the final analysis
As we worked in the natural setting, the crabs not only responded to the
dummy but also to other crabs, to predatory birds or to other events beyond
our control. The data set thus contains a number of responses that were
unrelated to the dummy's movements. In order to keep such responses to a
minimum, and to make sure that all experiments used in the analysis were as
homogeneous and unbiased as possible with respect to variables of interest, we
used the following criteria to include trials into the final analysis: (1)
there was no bird or crab interference during the trial; (2) the dummy
approached to at least 1 cm of its closest point to the burrow; (3) crabs were
at least 5 cm away from their burrow at the start of the experiment; (4) the
crabs were within the recording area when the dummy entered the recording area
and (5) for each crab only the first 50 dummy presentations were included. A
total of 633 experiments met these criteria and were subsequently analysed.
Excluded experiments were still used to calculate the number of dummy
presentations a crab had been exposed to prior to a particular experiment,
except where the crab was underground during the entire trial and did not see
the dummy.
Statistical analysis
As we took repeated measurements for each crab, the statistics used needed
to take possible crab-to-crab variation into account. This was done in the
framework of a Generalised Linear Mixed Model (GLMM) to analyse the
probability of a response (GenStat,
2000; Schall,
1991
), while response distance, the response speed and the
response strength were analysed in a Linear Mixed Model (REML;
GenStat, 2000
). By fitting crab
identity as a random term, all these analyses take repeated measures on
individual crabs into account and adjust the probability calculations
accordingly. As the values of the response strength are limited in range
between 0% and 100%, we first applied a logit transformation. A statistical
model was constructed by sequentially testing terms of interest. The final
model included only those terms that reached significance at the 5% level. The
significance of an individual term was tested by calculating the
Wald-statistic associated with dropping the term from the full model. We then
checked for some of the interactions between the final terms and also for some
interactions between these terms and other previously excluded terms if we had
a good reason to believe that they might be important. The final models are
described in the Results section. All REML models were checked graphically for
outliers and for a normal error distribution. Where fitted values were
calculated for a certain variable, all other variables were set to their mean
values.
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
In most cases, the crabs responded strongly to the approaching dummy. The
strength exceeded 80% in 72% of the responses
(Fig. 3). In fact, in more than
93% of all responses the crabs made sure they ended up closer to the burrow
than the dummy. However, even though more than half of the crabs (54%)
returned to within 2 cm of their burrow (solid black line in
Fig. 3), in only 27 cases (6%)
did the crab enter its burrow and disappear below ground. Their usual
behaviour was to sit at or near the burrow while the dummy was in the
vicinity. While sitting in the burrow entrance, the crabs often pivot around
to track the dummy as it moves past, threatening it with their claws.
Occasionally, males wave their enlarged claw while retreating and even attack
the dummy, hitting it with their claw, or try to block the dummy's path. These
responses are very different from the crabs' responses to an approaching bird
predator or a bird dummy. Confronted with a bird dummy (a 2 cm black ball
moving 10-30 cm above ground), the crabs respond earlier and run towards their
burrow at a higher speed and in many cases disappear underground. The
responses to dummies moving on the substrate, by contrast, are usually slower
and coordinated with the movement of the dummy, as if the crabs are trying to
make sure they always stay closer to the burrow than the dummy. In a display
of parallel processing, the crabs often continue feeding while they slowly
retreat to their burrows and therefore appear to minimise the impact the
response has on their feeding time. Both male and female U. vomeris
respond with burrow defence to the approaching dummy. This is in contrast to
Uca pugnax and Uca pugilator, in which males - who try to
attract females into their burrows for underground mating - take dummies
lacking an enlarged claw to be females
(Aspey, 1971;
Crane, 1975
;
von Hagen, 1962
). Uca
vomeris, however, mate on the surface at the entrance of the female
burrow (Crane, 1975
;
Salmon, 1984
), and females or
female-like dummies are not tolerated near male burrows.
|
We summarize the data set to be used in the following analysis in Figs4,5 and define the variables `track angle', `track distance' and `crab side', which are needed to describe the geometry between the crab, the dummy and the burrow in Fig. 6.
|
|
|
The dummy paths in Figs4, 5 are shown in a coordinate system defined by the crabs' home vectors. The data have been split in three ways: (1) Fig. 4 shows all the trials where the dummy's extended track intersects the vertical line defined by the home vector on the crab side of the burrow (crab side = 1; Fig. 4B, inset), while Fig. 5 shows all the trials where the dummy track intersects the line of the home vector beyond the burrow (crab side = 0; Fig. 5B, inset); (2) the data set within each figure is split according to the starting distance of the crabs from their burrows (panels A,D: 5-15 cm; B,E: 15-25 cm; C,F: 25-55 cm) and according to (3) whether the crabs responded (panels A-C) or not (panels D-F; see the figure legends and methods for additional details). Because the data in Figs4 and 5 are shown in a coordinate system defined by the crabs' home vectors, a crab that moved during the dummy presentation produces a change in direction of the dummy path. Most dummy paths are straight, however, indicating that in the vast majority of our experiments the crabs did not move significantly prior to responding to the dummy.
What Determines Whether A Crab Responds?
The crabs do not respond to every dummy approach. Crabs outside the 1
m2 of recording area almost never responded to the dummy. The crabs
only take note of the dummy when it approaches their own burrow. This can be
verified by inspecting the dummy paths in
Figs 4 and
5. Panels D-F of both figures
show the paths when the crabs did not respond; in these cases, clearly more
tracks passed the burrow at a distance of >20 cm compared with those in
which the crabs responded (panels A-C). The `response panels' show
predominantly radial paths pointing towards the burrow. As we show below, the
particular geometry of a trial, i.e. the relationship between a crab, its
burrow and the dummy's direction of approach, is indeed an important factor
determining the probability of response.
We used a GLMM to test for the influence of a variety of factors on the crabs' probability of response when faced with the approaching dummy. Since no interactions reached significance, the final model contained four significant terms:
Logit(P) ß0 + ß1(track
distance) + ß2(track angle) + ß3(crab side) +
ß4(presentation repeat) + error.
Random term: crab identity; N=633; logit=log[P/(1-P)].
Table 1 lists the statistical output for these terms, for some of the interactions and for other terms of interest that failed to achieve significance. Three of the four significant terms in the final statistical model - (burrow) track distance, track angle and crab side - describe the geometrical situation of each experiment (Fig. 6).
|
Track distance
As expected, the distance of the dummy track to the crab's burrow is the
single most important factor determining the response probability
(Table 1A). The probability
decreases sharply with increasing distance, by about 80% over a range of 60 cm
(Fig. 7A).
|
The (burrow) track distance, the closest distance between the crab's burrow
and the dummy track, is a measure of how directly the dummy approaches a
crab's burrow, but it also measures how closely a dummy can approach the
crab's burrow. The effect of track distance therefore suggests that the crabs
are either sensitive to the dummy's position or motion relative to the burrow.
At this point, it is not possible to test for the influence of the
dummy-burrow distance directly because this distance is not defined for trials
where the crabs did not respond. However, a special analysis presented below
will distinguish between the influence of the dummy's direction of motion and
its distance from the burrow. To make sure that the relevant variable is
indeed the distance between the track and the burrow and not between the track
and the crab, we removed the (burrow) track distance from the model and fitted
the (crab) track distance instead. (Crab) track distance is clearly not
significant (Table 1E), even
when we allow for a difference in response depending on whether the dummy
approaches from the crab side of the burrow or not
(Table 1F). The crabs thus
assess the dummy's position or its path relative to their burrow and not
relative to themselves. In other words, the crabs make their decision to
respond not in an egocentric frame of reference but in one that is centred on
the burrow (Hemmi and Zeil,
2003b). The dummy paths in Figs
4 and
5A-C strongly support this
conjecture in a qualitative way. Whenever the dummy approaches from the crab
side of the burrow (i.e. from the top in the figures), the crabs usually allow
the dummy to come very close but respond when it threatens to overtake them.
When the dummy approaches from the opposite side of the burrow, however, the
distance between the crab and the dummy at the time of response is much
larger. Note that the dummy's distance to the burrow is similar in both cases.
Below, we will provide further evidence that the crabs initiate their response
independent of their own distance from the dummy
(Fig. 11B).
|
Track angle and crab side
The dummy's approach direction relative to the crabs' home vector (track
angle) strongly affects the probability of responses
(Table 1B). For statistical
purposes, track angles were sorted into 20° bins from 0° to 180°
and fitted as a categorical variable (d.f.=8). The probability is high
whenever the dummy approaches from the crab side of the burrow; that is, for
track angles larger than 100° (Fig.
7B). The probability drops off sharply towards smaller approach
angles and reaches its lowest probability when the dummy approaches the burrow
from directly opposite the crab (track angle <20°).
Crab side is a measure of whether the dummy track crosses the extended home vector on the crab side of the burrow or on the opposite side. Crab side has two values, 0 and 1, and was needed to achieve a complete geometrical description of each trial. Each track angle can have either value of crab side. The influence of crab side (Table 1C) on the probability of response is weak and only just significant. The crabs are more likely to respond to the dummy when it crosses the home vector on the side of the burrow occupied by the crabs themselves (Fig. 7B).
The effect of repeated dummy presentations
The variable `presentation repeat'
(Table 1D) counts the number of
dummy approaches a given crab has already been exposed to before a given
experiment and can therefore be used as a measure of how the probability of
response is affected by the repeated presentations. Since the time course of
this effect was not known, presentation repeat was fitted as a categorical
variable with degrees of freedom (1-5, 6-10, 11-20, 21-30, 31-40, 41-50;
Fig. 7C). The first two bins
were kept smaller, because habituation is more likely to have an effect early
on in a series of experiments. The estimated response probability of crabs
decreases monotonically with increasing presentation repeat (solid black
line).
Crab characteristics
Neither crab sex (Table 1G)
nor size (Table 1H) influenced
the probability of response, which was also independent of the distance the
crabs were away from their burrows at the start of an experiment
(Table 1I).
The role of intrinsic dummy characteristics
So far, we have mainly analysed variables that describe the way the dummy
moved with respect to the crab and its burrow during a trial. Are there any
intrinsic dummy characteristics that affect the crabs' probability of
response? Neither the dummy's size (Table
1J), brightness (i.e. whether it was black or white;
Table 1K) nor speed
(Table 1L) affected the crabs'
probability of response. However, as the dummy track was fixed for each
experimental set-up, the compass bearing from which the dummy approached a
crab's burrow was always the same. To test whether the crabs associate the
repeatedly approaching dummy with a certain compass direction, we changed the
dummy's approach direction by rotating the track 90° around the burrow of
the focal crab in 17 experiments. This was done after the crabs had had
extensive exposure to the dummy approaching from the initial direction (at
least 14 experiments per crab). While the change in direction did not affect
the crabs' probability of response (Table
1M), it did increase the response strength from a mean of 83% to
96% (REML; N=419, d.f.=1, Wald/d.f.=7.48, P=0.006). This
increase is consistent with the interpretation that the dummy approaching from
a new direction was perceived as being different from the initial dummy, even
though the two were physically identical. This indicates again that the crabs
do not simply evaluate the dummy in an egocentric frame of reference. While
the dummy always approached from the same external compass direction during
the initial habituation period, the crabs themselves frequently changed the
direction in which they foraged and thus would have seen the dummy approach
from a number of different directions relative to their own home vector. As
the crabs keep their longitudinal body axis always approximately aligned with
their burrow (Ens et al., 1993;
Land and Layne, 1995b
;
Zeil, 1998
), the dummy would
have been seen in different parts of their visual field.
We also tested whether a change in the size of the dummy during the course of the experiment had a similar effect. There was no difference in the response probability or of the response strength regardless of whether we used all available trials for the statistical analysis (N=31) or only the first two trials with a new dummy size per crab (N=12) (all P>0.35).
The critical parameters: the distance from the burrow or the
direction of travel?
As mentioned earlier, the (burrow) track distance influences two different
parameters: how close to the burrow the dummy can get (minimal dummy-burrow
distance) and how directly the dummy moves towards the burrow (see
Fig. 6). The strong influence
of the (burrow) track distance on the probability of response of the crabs may
therefore either indicate that the crabs are sensitive to the distance between
the dummy and their burrow or that they are sensitive to the direction of the
dummy's path. For large track distances, for instance, the dummy can never
come very close to the burrow, but its path also never points directly at the
burrow. If distance were the main factor, we would expect that, for a given
dummy-burrow distance, the probability that a crab responds should be
independent of the track's direction relative to the burrow. If, on the other
hand, the crabs were sensitive to the direction of the dummy path, we would
expect that for a given dummy-burrow distance, the probability of response
should be higher for tracks that have a trajectory that points more directly
at the burrow (small burrow track distance). This difference should increase
as the dummy gets closer to the burrow, because it should then be easier for
the crabs to assess the direction of the dummy's path relative to the burrow.
Fig. 8 shows the relationship
between the probability of response and the dummy's distance from the burrow
for three ranges of track distances. The overall shape of the three curves is
very similar: all three curves show a strong increase in the probability of
response as the dummy gets closer to the burrow, with only a slightly lower
probability for larger track distances.
|
For a statistical test of these differences, we used a GLMM model identical to the one presented above, but this time we only counted responses if they occurred before the dummy reached a distance of 20 cm to the burrow. In essence, we now check whether the (burrow) track distance affects the probability that a crab responds before the dummy reaches a burrow distance of 20 cm (cumulative probability of the three curves over the distances marked by the grey area in Fig. 8). The previous model checked for the influence of track distance on the cumulative probability of the entire curves. In order to do this in an unbiased way, we had to limit the data set to track distances below 20 cm, such that each included track allowed the dummy to approach to within 20 cm of the burrow. This limitation on its own did not affect the statistical model. However, the probability that a crab responds before the dummy reaches a distance of 20 cm from the burrow is independent of the track distance (GLMM; N=558, d.f.=1, Wald/d.f.=0.85, P=0.356). The significance of the other three parameters in the model remained unchanged. The result of this analysis is not affected by the exact response cut-off used (e.g. 20 cm). We cannot categorically rule out a small influence of the dummy's path direction, due to the limited number of data points at large and very small (<5 cm) track distances. However, the analysis shows that the dummy's distance to the burrow is the dominating factor that determines the response probability of burrow owners and not the direction of the dummy's path relative to the burrow.
There is yet another way to approach the question of whether the crabs are sensitive to the direction in which the dummy is moving. It became very clear during the experiments that the crabs responded almost exclusively as the dummy approached the burrow but ignored it when it moved away. To test this, we used a subset of our experiments in which the dummy moved at least 5 cm past the burrow (Fig. 9A). The selection criterion was chosen in such a way that the dummy had to move more than 5 cm beyond the closest point to the burrow (CP) before reversing direction at the return point (RP), including all experiments where the crabs did not respond, or responded late, after the dummy had moved past CP (Fig. 9A). Based on the distance that the dummy had moved past CP we then defined four equal length segments on the dummy's path (Fig. 9A). Experiments in which a crab responded to the dummy before the dummy reached segment 1 were excluded and only the first response of a crab was counted. All remaining experiments were analysed regardless of whether the crabs reacted or not. If a crab responded to the dummy during a given segment, the remainder of that experiment was then ignored in the probability calculations for the subsequent segments. This selection process left us with 232, 176, 162 and 123 trials to compare the probability of response for segments 1-4, respectively. We can state the following, non-exclusive hypotheses: (1) The probability of response should decline from segment 1 to segment 4 because sensitive crabs would respond early, and we should see an accumulation of insensitive crabs towards later segments. (2) If the crabs are sensitive to the direction of movement of the dummy, we would expect the probability of response to be higher when the dummy approaches the burrow (segments 1 and 3) compared with when the dummy moves away from the burrow (segments 2 and 4). Otherwise, the probability of response should be the same for all segments.
The number of responses is clearly much higher for track segments 1 and 3 than for segments 2 and 4 (Fig. 9B), and the response probability is significantly different for the four segments (GLMM; d.f.=3, Wald/d.f.=11.95, P<0.001; Fig. 9B). In fact, the crabs respond much more often when the dummies move through segments 1 and 3 than through segments 2 and 4. An inspection of the pair-wise standard errors of the linear transformation of the model shows that all four segments differ significantly from each other. Two of these comparisons are especially interesting. Segment 3 has a higher probability of response than segment 2, demonstrating that the crabs distinguish between an approaching and a retreating dummy. On such a coarse scale, therefore, the crabs are sensitive to the dummy's direction of movement relative to the burrow. It is important to keep in mind that if there were a general decrease in the probability of response towards later segments, we would actually expect segment 3 to show a lower probability of response than segment 2. The second interesting comparison is between segments 1 and 3. The fact that the probability of response is higher in segment 3 suggests that the crabs are somehow sensitised by the directional change in movement direction of the dummy at the return point. The crabs often responded almost immediately as the dummy changed direction, especially if the dummy was still close to the burrow. This is not obvious in Fig. 9B because the return points fall into different bins along the histogram.
What determines the response distance?
The previous analysis has shown that the distance between the dummy and the
crab's burrow and the geometry of the dummy approach are the most important
predictors of whether or not a crab responds. In the following analysis, we
investigate what parameters determine the response distance, which we define
as the distance between the dummy and the burrow at the time the crabs
initiate their response. An inspection of
Figs 4 and
5 suggests that crabs respond
when the dummy has reached a certain distance from the burrow, irrespective of
the dummy's approach direction. The median response distance is 24.5 cm, and
75% of the responses occur when the dummy is between 14.2 cm and 42.4 cm
(upper and lower 12.5th percentile) away from the burrow
(Fig. 10).
|
To test which factors affect the response distance, we performed an REML
(Table 2). The response
distance was log transformed to achieve a satisfactory error distribution. The
final model had the following form: loge(dummy-burrow distance)
ß0 + ß1(track distance) +
ß2[(crab) burrow distance] + ß3[track distance
x (crab) burrow distance] + ß4(trial index) +
ß5(track angle) + ß6(crab side) + error.
|
Random term: crab identity; N=419.
The effect of the crab's distance from its burrow
The main parameters affecting the response distance are the track's
distance from the crab's burrow (Table
2A) and the crab's distance from its own burrow at the time of
response (Table 2B). Also
significant is the interaction between these two variables
(Table 2C). The relationship
between the response distance and the (crab) burrow distance depends on the
(burrow) track distance and vice versa. The larger the track
distance, the smaller the effect of the (crab) burrow distance. For small
track distances (i.e. larger dummy-burrow distances, when they are further
away from the burrow), the crabs respond earlier
[Fig. 11A; dashed line (track
distance = 10 cm) and open dots]. However, when the track is 20 cm away
from the burrow (solid line and filled dots), the crab-burrow distance has no
influence on the response distance (dummy-burrow distance).
Track angle and crab side
Track angle has a very weak effect, which is statistically only just
significant, on the timing of the response
(Table 2E). The effect of crab
side just fails to be significant (Table
2F). Dummies that would intersect the extended home vector on the
crab side of the burrow (crab side = 1) trigger a response slightly
earlier, and dummies that approach on a low track angle are allowed slightly
closer to the burrow. However, the response distance is remarkably constant,
no matter where the dummy comes from. Fig.
11B shows that the crabs respond at a roughly equal dummy-burrow
distance, irrespective of the dummy's approach direction, which is
irrespective of where relative to the home vector the crabs see the dummy. The
statistical difference between the track angles is mainly based on the fact
that if the dummy approaches from across the burrow, as seen from the crab's
perspective, the crabs respond late, allowing the dummy to come slightly
closer to the burrow than for the other approach directions
[Fig. 11B, lightest grey lines
(track angles <20°)].
The effect of repeated presentations on the timing of the
response
The crabs adjust their behaviour to repeated dummy presentation by allowing
later dummies to approach the burrow more closely before they respond
(Table 2D). The effect is
surprisingly small, however (Fig.
11C): over the course of 50 trials, the dummy-burrow distance
at the moment of response decreased by only 30%.
Crab and intrinsic dummy characteristics
As in the case of the response probability, neither the sex nor size of the
crabs (Table 2G,H) nor the size
nor speed of the dummies influenced the response distance
(Table 2I,J).
The most striking result of the analysis of the response timing is that the crabs retreat towards their burrows when the dummy has reached a certain distance from the burrow, irrespective of its approach direction. In addition, the crabs adjust this response distance according to their own distance from the burrow: they respond earlier when they are further away from their own burrow.
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
On the most general level, our results show that the crabs took our
simplistic dummies very seriously, even though they did not resemble real
crabs in attributes other than their size and their position in the visual
field of a crab observer (von Hagen,
1962; Land and Layne,
1995a
). The crabs' overall probability of response is very high
(Fig. 7C) and most responses
are strong in that in the majority of trials the crabs retreat all the way
back to their burrows when they become aware of a dummy
(Fig. 3). The crabs habituate
little to repeated dummy approaches, with over 60% of the crabs continuing to
respond even after 30 dummy presentations. This is in spite of the fact that
the time pressure the crabs were subjected to during our experiments was
severe. The crabs involved spent a significant amount of their time responding
to the dummy. Burrow surveillance is of such significance to these crabs that
each event is taken seriously, independent of the recent history. The decline
we observed in the probability of response during the course of the
experiments - rather than being based on sensory habituation - is probably
indicating a change in the crabs' perceived balance between the burrow's
resource value and the cost associated with its surveillance and defence.
Indeed, for some crabs it proved too much: many of them stopped participating
in our experiments by disappearing below ground, while most other crabs were
still active on the surface. A few crabs even abandoned their burrows and
wandered off in search of a new one.
Our analysis identified the dummy's distance to the burrow of a crab as the
single most important parameter that determines the crab's probability of
responding by rushing back to the burrow. The probability of response declines
sharply with increasing dummy-burrow distance
(Figs8, 10). The
decision that the burrow needs defending is thus not made in an egocentric
frame of reference but in one that is centred on the burrow. The crabs
evaluate the dummy's movements relative to their burrow and not relative to
themselves. This is also evident in Fig.
11B, where the mean distance between the dummy and the burrow at
response time varies little for the different approach directions, but the
distance between the dummy and the crab depends very strongly on where the
dummy comes from. The ability of fiddler crabs to judge the distance between
the burrow and an approaching dummy regardless of their own distance from the
burrow is quite an astonishing feat of information processing. We will devote
a companion paper to a detailed analysis of this problem
(Hemmi and Zeil, 2003a).
While the dummy's distance from the burrow is clearly very important, the crabs are also sensitive to the general direction in which these crab-like dummies move. The probability that a crab responds to a dummy that is close to its burrow is about three times higher when the dummy moves towards the burrow than when it moves away from it (Fig. 9). Our results also reveal that the crabs use knowledge of their own distance from the burrow to modify their behaviour. The crabs respond earlier to an approaching dummy if they themselves are further away from the burrow (Fig. 11A).
Our dummies clearly do not look like real crabs, yet they were very
successful in eliciting burrow defence. The reason for this is likely to be
related to the limits of resolution of fiddler crab compound eyes. In the
context of burrow defence, the crabs simply cannot afford to be choosy. They
often need to respond to intruders at a large distance. At a mean crab-dummy
distance of 30 cm at the time of the response, the angular size of our dummies
was so small that they would be seen by, at most, a few ommatidia. This is
clearly not enough to make sophisticated visual discriminations. Indeed,
despite the male's massively enlarged claw, fiddler crabs are only able to
distinguish between a male and a female crab at distances of 10-15 cm
(Aspey, 1971;
Land and Layne, 1995a
). This
might also be the reason why we failed to find differences in the response
probability or response distance between male and female crabs or between
crabs of different sizes. Similarly, intrinsic dummy characteristics, such as
its size and the sign of its contrast against the mudflat background (white or
black dummy), do not influence the crabs' probability of response or the
response timing. Burrow surveillance responses are initiated at distances at
which the crabs do not have sufficient information to distinguish between an
intruder's size and sex or between a crab and a simple dummy. The responses we
observed are therefore only based on the dummy's position and motion. Our
dummies not only didn't look like real crabs but they also moved differently.
Burrow-less, wandering crabs frequently change direction and often approach
other crabs (Zeil and Layne,
2002
), whereas our dummies moved along a predictable straight
line. We might therefore expect to see even higher probabilities of responses
towards real crab intruders than the ones we found with dummies.
The observation that the crabs' probability of response actually increased when the dummy changed direction after passing the burrow, compared with the initial approach (Fig. 9), suggests that the crabs are indeed sensitive to such changes in motion direction. These changes might be another way in which the crabs attempt to distinguish between neighbouring resident crabs and potentially dangerous intruders.
Interestingly, the crabs respond more strongly when the same dummy
approaches the burrow from a new compass direction, as if it was perceived as
a new threat. It may be important to note in this context that resident crabs
are able to remember the locations of the burrows of at least some of their
neighbours based on path integration (Zeil
and Layne, 2002). The direction from which a crab approaches might
thus contain information on its identity. Keeping track of the approach
direction of another crab with which a burrow owner has interacted before
could therefore be part of a mechanism that allows fiddler crabs to avoid
unnecessary interactions with their neighbours.
Our results show that the crabs are able to adjust their response behaviour
according to the particular situation during which a conspecific approaches
their burrow. They are sensitive to the intruder's distance
(Fig. 8) and motion
(Fig. 9) relative to their
burrow, to changes in the direction of motion
(Fig. 9), to the compass
direction from where the intruder approaches and to their own distance from
the burrow (Fig.11A). The
effects of all these factors are consistent with the hypothesis that the crabs
try to minimise the time lost during burrow defence without increasing the
risk of losing their burrow. It is not clear at this point why the crabs
respond less often to dummies that approach from beyond the burrow
(Fig. 7B). Two non-exclusive
hypotheses that could explain this difference are based on strategic or
perceptual considerations. Wandering crabs initially approach the burrow
owners rather than the burrows themselves because the burrow entrances are not
normally visible to the crabs from a distance of >15 cm
(Zeil, 1998;
Zeil and Layne, 2002
). Burrow
owners might therefore be more responsive to crabs approaching or overtaking
them as mimicked by dummies approaching from the crab's side of the burrow.
The result could also indicate that the crabs find it more difficult to make a
judgement on the position and direction of movement of dummies that approach
from beyond the burrow. The mean distance between the crab and the dummy at
the time of the response is much larger when the dummy approaches from beyond
the burrow (Fig. 11B). In
fact, the crabs clearly respond to dummies that are up to 80 cm away. At such
a distance, the apparent size of the dummy is only 1.6° wide and
<1° high, and the crabs would clearly find it difficult to accurately
determine its position and motion relative to the burrow. Such a detection
problem would lead to a higher percentage of crabs not responding to dummies
approaching from these directions.
In summary, fiddler crabs protect their burrow against conspecifics by
returning to its entrance whenever another crab approaches to within a certain
distance of the burrow. Foraging crabs evidently know how far away they are
from their burrows because the further away they are from home, the earlier
and faster they respond to an approaching dummy. We know that crabs do not see
their own burrows from more than 15 cm away, so their path integration system
needs to provide them with information about the direction and distance in
which their burrow lies (Cannicci et al.,
1999; von Hagen,
1967
; Zeil, 1998
;
Zeil and Layne, 2002
).
Burrow-surveying crabs thus need to be able to integrate visual information
and information from the path integration system to assess another crab's
position and movement relative to the burrow. Exploring how they are able to
do this and unravelling how they could achieve the necessary `sensor fusion'
is the subject of the following paper
(Hemmi and Zeil, 2003a
).
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Altevogt, R. (1955). Some studies on two species of Indian fiddler crabs, Uca marionis nitidus (Dana) and U. annulipes (Latr.). J. Bombay Nat. Hist. Soc. 52,702 -716.
Aspey, W. (1971). Inter-species sexual discrimination and approach avoidance conflict in two species of fiddler crabs, Uca pugnax and Uca pugilator. Anim. Behav. 19,669 -676.
Cannicci, S., Fratini, S. and Vannini, M. (1999). Short-range homing in fiddler crabs (Ocypodidae, genus Uca): a homing mechanism not based on local visual landmarks. Ethology 105,867 -880.[CrossRef]
Caravello, H. E. and Cameron, G. N. (1987). Foraging time allocation in relation to sex by the gulf coast fiddler crab (Uca panacea). Oecologia 72,123 -126.
Crane, J. (1975). Fiddler Crabs of the World (Ocypodidae: genus Uca). Princeton, NJ: Princeton University Press.
deRivera, C. E. and Vehrencamp, S. L. (2001).
Male versus female mate searching in fiddler crabs: a comparative analysis.
Behav. Ecol. 12,182
-191.
Ens, B. J., Klaassen, M. and Zwarts, L. (1993). Flocking and feeding in the fiddler crab (Uca tangeri): prey availability as risk-taking behaviour. Neth. J. Sea Res. 31,477 -494.[CrossRef]
Genoni, G. P. (1991). Increased burrowing by fiddler crabs Uca rapax (Smith) (Decapoda: Ocypodidae) in response to low food supply. J. Exp. Mar. Biol. Ecol. 147,267 -285.[CrossRef]
GenStat (2000). GenStat for Windows Release 4.2. Fifth Edition. Oxford: VSN International Ltd.
Hemmi, J. M. and Zeil, J. (2003a). Burrow
surveillance in fiddler crabs. 2. The sensory cues. J. Exp.
Biol. 206,3951
-3961.
Hemmi, J. M. and Zeil, J. (2003b). Robust judgement of inter-object distance by an arthropod. Nature 421,160 -163.[CrossRef][Medline]
Huntingford, F. A. and Turner, A. K. (1987). Animal Conflict and Fighting Behaviour. London: Chapman and Hall.
Hyatt, G. W. and Salmon, M. (1978). Combat in the fiddler crabs Uca pugilator and U. pugnax: a quantitative analysis. Behaviour 65,182 -211.
Jennions, M. D. and Backwell, P. R. Y. (1996). Residency and size affect fight duration and outcome in the fiddler crab Uca annulipes. Biol. J. Linn. Soc. 57,293 -306.[CrossRef]
Jones, A. R. (1980). Chela injuries in the fiddler crab, Uca burgersi Holthuis. Mar. Behav. Physiol. 7,47 -56.
Koga, T., Backwell, P. R. Y., Jennions, M. D. and Christy, J. H. (1998). Elevated predation risk changes mating behaviour and courtship in a fiddler crab. Proc. R. Soc. Lond. Ser. B 265,1385 -1390.[CrossRef]
Land, M. F. and Layne, J. (1995a). The visual control of behaviour in fiddler crabs. I. Resolution, thresholds and the role of the horizon. J. Comp. Physiol. A 177, 81-90.
Land, M. F. and Layne, J. (1995b). The visual control of behaviour in fiddler crabs. II. Tracking control systems in courtship and defence. J. Comp. Physiol. A 177,91 -103.
Maynard Smith, J. and Parker, G. A. (1976). The logic of asymmetric contests. Anim. Behav. 24,159 -175.
Montaque, C. L. (1980). A natural history of temperate western Atlantic fiddler crabs (Genus Uca) with reference to their impact on the salt marsh. Contrib. Mar. Sci. 23, 25-55.
Parker, G. A. (1974). Assessment strategy and the evolution of animal conflicts. J. Theor. Biol. 47,223 -243.[Medline]
Pratt, A. E., McLain, D. K. and Lathrop, G. R. (2003). The assessment game in sand fiddler crab contests for breeding burrows. Anim. Behav. 65,945 -955.[CrossRef]
Salmon, M. (1984). The courtship, aggression and mating system of a "primitive" fiddler crab (Uca vocans: Ocypodidae). Trans. Zool. Soc. Lond. 37, 1-50.
Salmon, M. (1987). On the reproductive behaviour of the fiddler crab Uca thayeri, with comparisons to U. pugilator and U. vocans: evidence for behavioural convergence. J. Crust. Biol. 7,25 -44.
Salmon, M. and Stout, J. F. (1962). Sexual discrimination and sound production in Uca pugilator Bosc. Zoologica 47,15 -20.
Schall, R. (1991). Estimation in generalized linear models with random effects. Biometrika 78,719 -727.
von Hagen, H.-O. (1962). Freilandstudien zur Sexual- und Fortpflanzungsbiologie von Uca tangeri in Andalusien. Z. Morphol. Ökol. Tiere 51,611 -725.
von Hagen, H.-O. (1967). Nachweis einer kinästhetischen Orientierung bei Uca rapax. Z. Morphol. Ökol. Tiere 58,301 -320.
von Hagen, H.-O. (1993). Waving display in females of Uca polita and of other Australian fiddler crabs. Ethology 93,3 -20.
Wolfrath, B. (1993). Observations on the behaviour of the European fiddler crab Uca tangeri. Mar. Ecol. Prog. Ser. 100,111 -118.
Zeil, J. (1998). Homing in fiddler crabs (Uca lactea annulipes and Uca vomeris, Ocypodidae). J. Comp. Physiol. A 183,367 -377.
Zeil, J. and Layne, J. (2002). Path integration in fiddler crabs and its relation to habitat and social life. In Crustacean Experimental Systems in Neurobiology (ed. K. Wiese), pp. 227-246. Heidelberg: Springer Verlag.
Related articles in JEB: