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ANIMAL BEHAVIOUR, 2005, 69, 615–625doi:10.1016/j.anbehav.2004.06.019

Predator avoidance in fiddler crabs: 2. The visual cues

JAN M. HEMMI

Centre for Visual Sciences, Research School of Biological Sciences, Australian National University

(Received 16 December 2003; initial acceptance 16 March 2004;

final acceptance 18 June 2004; published online 7 December 2004; MS. number: 7948)

The efficiency of predator avoidance strategies depends on the availability and accuracy of sensoryinformation. Although vision can in principle provide instant information on a predator’s position,direction of approach and identity, prey animals that face fast predators have to respond so early (close tothe limits of detection) that visual cues are unreliable predictors of actual risk. This is a major problem forprey animals that have to balance predation risk with the cost of antipredator action. I investigated thevisual cues fiddler crabs Uca vomeris use to decide when to run towards their burrow in response to anapproaching (dummy) predator by running towards their burrow. The crabs did not always escapeimmediately when they first detected the dummy, but continued to monitor and assess its approach. Thecrabs relied on retinal image speed to trigger a home run. Retinal speed did not correlate well with theactual risk of predation because it confounded a predator’s direction of approach with its speed andproximity. In an attempt to reconcile what is known about predator avoidance in semiterrestrial crabs, Ipropose a two-tier antipredator response system and discuss the crabs’ multistage response strategy in thecontext of the associated costs and the availability of information. Multistage predator avoidance, which iscommon among prey animals, appears to be designed to improve the quality of information in an attemptto minimize the costs associated with predator avoidance responses.

� 2004 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

In many predator–prey interactions vision plays an im-portant role. The high information content of vision interms of temporal and spatial resolution makes it an idealsense to detect and localize objects in the world (Curio1993; Cronin, in press). Both predators and prey shownumerous visual adaptations concerned with improvingthe detection and recognition of each other (Land &Nilsson 2002). However, there are fundamental con-straints on eye design and the different uses of visionhave competing demands on the acquisition and process-ing of visual information. The information that preyanimals have available to make decisions is limited bythese constraints with far-reaching consequences fortheir behavioural options and their lifestyles (Bouskila &Blumstein 1992; Sih 1992; Koops & Abrahams 1998;Lima 1998; Martin & Lopez 1999; Luttbeg & Schmitz2000; Luttbeg 2002; Welton et al. 2003; Fernandez-Juricicet al. 2004; Koops 2004). To understand and predict whyprey animals use particular strategies to avoid predatorswe therefore need to find ways to measure the quality ofinformation on which animals base their decisions.

Correspondence: J. M. Hemmi, Centre for Visual Sciences, ResearchSchool of Biological Sciences, Australian National University,G.P.O. Box 475, Canberra ACT 2600, Australia (email: jan.hemmi@anu.edu.au).

61003–3472/04/$30.00/0 � 2004 The Association for the S

Animals constantly have to make decisions aboutwhether, how and when to respond to events in theirenvironment. Fiddler crabs, for instance, are an importantfood source for a large variety of bird predators withdifferent and versatile hunting techniques (e.g. Zwarts1985; Ens et al. 1993; Iribarne &Martinez 1999). The crabsrespond to birds by retreating to their burrow entranceand, if the threat persists, they disappear below ground(Nalbach 1990; Land & Layne 1995; Jennions et al. 2003;Hugie 2004). Their antipredator responses are exclusivelybased on visual information (Nalbach 1990; Land & Layne1995). My previous analysis of crab responses to dummypredators simulating a hunting tern (Hemmi 2005)showed that the crabs are sensitive to the speed, the size,the height above ground and the approach direction ofa dummy. Against expectations, the crabs responded later,the more directly the dummy approached, even thougha directly approaching predator would appear to presenta higher risk (see also Nalbach 1990; Land & Layne 1995).In addition, the crabs evaluated the information they hadabout the dummy predator relative to themselves ratherthan relative to their refuge, contradicting model predic-tions of optimal escape behaviour (Kramer & Bonenfant1997; Hemmi 2005). These unexpected results can beexplained by the fact that fiddler crabs, like many smallanimals, initially cannot measure the distance, the size

5tudy of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

ANIMAL BEHAVIOUR, 69, 3616

and the approach direction of a predator. I investigatedthe visual cues that fiddler crabs use to decide when torespond to an approaching predator, discuss the informa-tion content of these cues in relation to the risk ofpredation and ask how the availability of informationinfluences the crabs’ response strategy.Two studies have addressed the question of how semi-

terrestrial crabs decide when to respond to a predator (seealso Cannicci et al. 2002). In field and laboratory experi-ments, Nalbach (1987, 1990) directly approached crabs(Heloecius cordiformis and Pachygrapsus marmoratus) witha range of objects under varying conditions. The crabsresponded whenever the apparent size of the approachingobjects (more precisely their solid angle, Nalbach 1990)had increased by a threshold amount (5.6 � for H. cordi-formis). This threshold change in angular size was in-dependent of the objects’ initial angular size and of theobjects’ approach speed.The second study investigated the same question in

a fiddler crab Uca pugilator with a focus on the limits ofvisual resolution (Land & Layne 1995): how small couldan object be, in terms of its apparent size, and still triggera response? Land & Layne (1995) exposed large groups ofcrabs to a variety of danger stimuli and for each stimulusrecorded the largest distance at which a crab responded.The crabs responded to nonapproaching objects whenthey were just 1 � in apparent size, which is close to theresolution limit of their eyes. Like Heloecius (Nalbach1987), fiddler crabs respond later when approached di-rectly. Land & Layne (1995) suggested that, in this case,the limiting factor is the apparent speed of the object.Their two measurements (1 and 1.4 �/s) correspond ap-proximately to a positional change of the retinal image ofabout one ommatidium/s.The three experiments reported in this paper were

designed to address the question of what informationfiddler crabs have available when they need to initiateevasive action. I monitored the second stage of thepredator avoidance response, the home run, which isthe same stage on which both previous studies focused.The elevation experiment was designed to clarify howresponse timing depends on the dummy’s retinal eleva-tion. The speed experiment explored the effect of thedummy’s speed on the response distance and the loomingexperiment addressed the specific contribution of loom-ing to the response timing.

METHODS

Apparatus

The experimental procedures of the present study wereidentical to those described in Hemmi (2005) with theexception of the stimulus apparatus. The dummies in theelevation and speed experiments consisted of small,round, black styrofoam balls with a diameter of 5 cm(elevation experiment) or 2, 3 or 5 cm (speed experiment).The dummies were threaded on two parallel monofila-ment lines which were tightly strung between two stain-less steel poles about 6 m apart and allowed the dummy tobe moved along a straight line, the dummy track, while

minimizing wind-driven vibration (Fig. 1a, b). The dum-my was moved along the track by a nonstretch polyfila-ment line, which was attached to both sides of thedummy and then looped around a small wheel (diameter5 cm). The rotation of the wheel was recorded with thesame video camera that recorded the crabs’behaviour. Thisallowed me to reconstruct the dummy’s exact positionrelative to the crab even when the dummy itself was notvisible in the video image. The dummy track was arrangedsuch that it passed approximately through the middle ofthe recording area (1.1 m2) with several resident crabs. Foradditional details see Hemmi (2005).

The looming stimuli of the last experiment consisted ofthree black pieces of cloth which were, starting in theirmiddle, rolled up on to either a diagonal, a horizontal ora vertically oriented bar (Fig. 1c). The cloth could beunwound by pulling on a fishing line from a distance. Thethree versions of the stimulus were mounted behind eachother in a fixed Perspex frame, in the following order asseen from the viewpoint of a crab: diagonal, vertical,horizontal. The back of the cloth was a very light grey toreduce the contrast to the sky while the cloth was wrappedaround the pole. Fully unrolled, the final size of the clothwas 45 ! 45 cm for all three stimuli, or approximately 5 �

in angular size (depending on a crab’s distance). Thecentre of the cloth was 75 cm above the ground. Thethree versions of the cloth differed in the direction ofexpansion. The horizontally oriented cloth expandedonly along the vertical dimension and the horizontalcloth along the vertical dimension. The diagonal clothproduced looming along both dimensions and was un-rolled slightly faster such that it took approximately thesame time to reach full size.

Video Analysis

The video analysis followed the same procedures andrules as described before (Hemmi 2005) with the excep-tion that frames were digitized at 200-ms intervals. Basedon the X and Y coordinates of the crabs, the dummy andthe burrow, a response was considered to have started ina given frame if a crab moved at least 0.7 cm towards itsburrow during the 200-ms interval preceding this frameand at least 2 cm over a three-frame interval (600 ms)starting at the previous frame. If the crabs responded afterthe dummy had reached its closest point to the crab, theywere considered not to have responded at all. Thishappened twice in the elevation experiment, and neverin the speed and the looming experiments. For theanalysis of the response timing, I defined the position ofthe dummy and the crab in the last frame before a crabreached the response criteria as their position at the timeof response. The analysis produced a full three-dimen-sional description of the dummy’s position relative to thecrabs and their burrows, for the entire dummy approach.

Experimental Design and Analysis

Data were collected in defined experimental settings (aset-up) where the camera and the dummy apparatus were

HEMMI: PREDATOR AVOIDANCE: 2. VISION 617

Observer

Observer

Diameter: 5 cm

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Figure 1. The experimental set-up. (a) A bird’s-eye view, showing the spatial relationship between the observer, the crabs, the camera’s field of

view and the stimulus apparatus. (b) Three different track slopes were used to measure the effect of stimulus elevation. The vertical crab–track

distance (dvertical) is given by dvertical2 Z dtotal

2 � dhorizontal2 . (c) The looming apparatus. The frontal view (top row) shows the apparatus, as it

would appear to the crabs during the three stimulus conditions. The three sails were housed in the same frame with the diagonally expandingstimulus facing the crab and the vertically expanding sail in the middle. For details, see text.

placed in a particular location on the mudflat to film theresponses of several crabs to repeated dummy presenta-tions. Within each set-up the presentations of different, ordifferently moving, dummies were organized in random-ized blocks (see below). In the elevation experiment, Iinterspersed dummies that approached horizontally(20 cm above the ground) with dummies that approachedalong a descending track that was inclined downwards byeither 10 � or 20 � (Fig. 1b). The randomized block size wasnine trials. Each block consisted of a randomized pre-sentation of the three track angles (0 �, �10 � and �20 �)and within each track angle, a randomized presentation ofthree starting distances. Starting distance was nestedwithin track angle to minimize the disturbance to thecrabs required by changing the track angle. As the closerstarting distance turned out to be too short and somecrabs responded as soon as the dummy started to move,only the longest starting distance was analysed. In thespeed experiment, all dummies approached along a hori-zontal dummy track 20 cm above the ground. Random-ized blocks of six runs with two speed classes (means: 19.3and 54.6 cm/s) and three sizes (2, 3, 5 cm) were presented

sequentially. In the looming experiment, randomizedblocks of three runs, one of each orientation (horizontal,vertical and diagonal looming), were presented sequen-tially.As these were field experiments, I did not have full

control over all variables. To achieve a homogeneous andcomparable data set, I used the following criteria to selectthe trials for the analysis: (1) there was no bird or crabinterference during the trial; (2) crabs were at least 5 cmfrom their burrow at the start of the trial; (3) the crabs hadto be within the recording area when they responded to thedummy. At most, the first 50 dummy presentations wereanalysed for each crab. A total of 135 dummy presentationsmet these criteria for the elevation experiment, 110 for thespeed experiment and 81 for the looming experiment.Excluded dummy presentations were used to calculate thenumber of presentations a crab had seen, except where thecrab was underground during the entire trial.A lack of orthogonality in the data precluded the use of

an ANOVA for the statistical analysis. Instead, I followeda mixed model approach (Schall 1991; McCulloch &Searle 2001). A linear mixed model (REML, GenStat

ANIMAL BEHAVIOUR, 69, 3618

2002) was used to analyse the response distance (three-dimensional-crab–dummy distance) for the elevation andspeed experiments. Because the crab–dummy distance wasfixed in the looming experiment, I used apparent size asthe response measure. The individual components ofvariation between and within crabs (crab identity), be-tween set-ups (set-up identity) and between dummypresentations (experimental identity) were accounted forby treating them as random factors. Random factors inmixed models are equivalent to the block structure in theanalysis of variance. To analyse the probability of responsein the looming experiment, I used a generalized linearmixed model, with crab identity as the random factor(GLMM, GenStat 2002). A final model was constructedincluding only those terms that reached significance atthe 5% level. The Wald statistic is a large sample approx-imation of the F test used in the analysis of variance. Itwas used to test the statistical significance of the in-dividual model parameters (McCulloch & Searle 2001). AllREMLmodels were checked graphically for outliers and fora normal error distribution.I addressed the question of how the apparent size, the

apparent speed and the retinal position of the dummypredators affect the crab’s response timing. It is, however,not possible to test directly for the influence of thesevariables, because they are, for basic geometrical reasons,highly correlated with the response distance. Experimen-tally manipulated variables, such as track angle, dummysize and dummy speed, are not a priori correlated with the

response distance, but are highly correlated with themeasures of interest, namely the retinal position, apparentsize and apparent speed.

RESULTS

Elevation Experiment

My previous experiments have shown that the crabs’response distance is influenced by the dummy’s heightabove ground: higher dummies produce earlier responses(Hemmi 2005). This suggests that the crabs adjust theirresponse timing according to the elevation at which anapproaching predator is seen. However, a change in heightchanges not only the elevation at which a dummy is seen,a positional effect, but also the rate at which the dummy’simage moves across a crab’s visual field, because heightinfluences the (vertical) distance between the crab and thedummy track. To tease these two factors apart, I comparedthe responses to dummies moving on two descendingtracks (descent angle: �10 � and �20 �) and one movinghorizontally (0 � descent angle, 20 cm height). The ratio-nale is the following. From the crabs’ point of view, thethree tracks differed in two important ways. First, theydiffered in how directly the dummy approached the crabsas measured by the vertical crab–track distance (Fig. 1b),which, for this experiment, was significantly larger for thehorizontal track than for the descending tracks (Fig. 2a).

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Figure 2. The elevation experiment. (a) Distributions of the vertical crab–track distance (Fig. 1b). (b) Distribution of the change in dummyelevation between the start of each trial and the time of response for three track angles. (c) Distribution of the dummy’s elevation at the time of

response for three track angles. (d) The response distance as a function of track slope. LSD: least significant difference.

HEMMI: PREDATOR AVOIDANCE: 2. VISION 619

This in turn led to larger and faster elevation changesduring the dummy’s approach for the horizontally mov-ing dummy (Fig. 2b). The change in elevation was notonly smaller for the descending tracks, but also predom-inantly negative, meaning that the dummy moved down-wards in the visual field. In contrast, the horizontallyapproaching dummies were always seen at increasinglyhigher elevations (Fig. 2b). Since crabs responded earlierwhen the crab–track distance was larger (Hemmi 2005), Ipredicted, that crabs should respond earlier to the hori-zontally moving dummies if the rate of change ofelevation or its sign, which are both determined by thecrab–track distance, were important. If, on the other hand,crabs responded earlier to higher dummies because higherdummies are on average seen at higher elevations, crabsshould respond earliest to the dummies moving along the�20 � track because they were seen at significantly higherelevations (Fig. 2c).The results are clearly consistent with the second

hypothesis. The crabs responded significantly earlier tothe dummy that approached on a �20 � slope (Table 1,Fig. 2d). The significance of the variable track angle isindependent of whether the three-dimensional crab–trackdistance (Table 1) or the vertical crab–track distance(Fig. 1b) is included in the statistical model. The effect oftrack angle is therefore not a result of it changing thethree-dimensional crab–track distances. The vertical crab–track distance itself had no significant effect on theresponse distance (REML: Wald1 Z 1.28, NZ 135;PZ 0.255). The experiment also confirmed that the re-sponse distance increased with crab–burrow distance(Table 1).

Speed Experiment

Crabs responded significantly earlier when the dummymoved faster (Fig. 3, Table 2). A change in the averagedummy speed from 19.3 cm/s to 54.6 cm/s increased theaverage response distance by 36.5 cm. The crab–burrowdistance again influenced the response distance (Table 2).For every centimetre the crabs moved away from theirburrow, they responded earlier by a mean G SE of0.85 G 0.37 cm. Crab–track distance and dummy sizehad no effect on the response distance, which is in

Table 1. Elevation experiment: results of the Linear Mixed Modelanalysis*

Termy df Wald P

Crab–burrow distance 1 9.79 0.002Track anglez 2 13.17 0.001Three-dimensional crab–track distance 1 2.80 0.094

*(REML; NZ 135): random model: set-up identity C crab identity Ctrial identity.yVariables were measured at the time a crab initiated its firstresponse.

zThe track angle measures the angle of the dummy track relative tothe horizontal (Fig. 1b) and was fitted as a factor with three levels(0, �10, �20 �).

contrast to their significant effect in previous experiments(Hemmi 2005). The absence of a size effect is probablycaused by the relatively small N (110 compared to 459; seealso Discussion). There are two reasons why crab–trackdistance may have had less influence in this experiment.First, the overall response distances were much largerbecause the dummy was on average larger, higher andfaster than in the previous experiment. The same absolutechange in crab–track distance therefore produced a muchsmaller angular change in the dummy’s approach di-rection. Second, in the current experiment, the dummyalways moved at a height of 20 cm above the ground. Theeffect of the crab–track distance was much less pro-nounced for higher tracks (Hemmi 2005). Two previouslyundetected variables affected the response distance in thisexperiment: group size and crab size. The more crabs wereon the surface at the time the dummy approached, theearlier the crabs tended to respond (Table 2). The responsedistance was on average G SE 7.9 G 3.04 cm larger forevery other crab on the surface in the 1.1-m2 recordingarea. Second, larger crabs responded earlier than smallercrabs (Table 2).

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Figure 3. Response distance as a function of dummy speed. The grey

lines show the predictions of the statistical model (Table 1).

Table 2. Speed experiment: results of the Linear Mixed Modelanalysis*

Termy df Wald P

Dummy speedz 1 22.75 !0.001Crab–burrow distance 1 6.99 0.008Group size 1 6.68 0.01Crab size 1 14.75 !0.001Dummy size 1 2.81 0.093Crab–track distance 1 0.00 0.967

*(REML; NZ 110): random model: set-up identity C crab identity Ctrial identity.yVariables were measured at the start of each trial.

zDummy speed: implemented as a factor with two levels, slow orfast.

ANIMAL BEHAVIOUR, 69, 3620

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Figure 4. The looming experiment. (a) The probability of responseas a function of the looming direction. NZ 26. (b) Apparent sail size

at the time of response, measured along the shorter dimension.

NZ 27. (c) Retinal speed at the time of response as a function oflooming direction. NZ 28.

Looming Experiment

The crabs responded very strongly and reliably to thevertically and diagonally expanding dummies, but failedto respond consistently to the horizontally expanding one(GLMM: Wald1 Z 15.28, N Z 81, P! 0.001; Fig. 4a).They seemed most sensitive to the vertically expandingdummy for which the response probability was 100% andfor which the apparent size at the time of response, asmeasured along its smallest dimension, was smallest(REML: Wald1 Z 4.87, N Z 58, P Z 0.008; Fig. 4b). Thecrabs responded latest to the horizontally expandingcloth, which consequently had the largest apparent sizeat the time of response. The results for the diagonallyexpanding cloth were intermediate (Fig. 4a, b).

DISCUSSION

Visual Cues and Predator Avoidance

What triggers an escape run?My experiments were designed to identify the visual

stimuli that trigger fiddler crabs to initiate the secondstage of their avoidance response, the run home. In thefollowing I distinguish between the detection of a dummypredator and the ‘decision’ to initiate a response. Aresponse may be triggered as soon as the predator isdetected, as was implied by Land & Layne (1995).However, while detection is obviously a prerequisite fora response, it is not necessarily sufficient. Crabs could,after detecting the dummy, monitor the changes of itsretinal image and respond only after certain criteria weremet.

My results provide two pieces of evidence that fiddlercrabs often do not respond immediately after they havedetected the dummy. First, crabs were unlikely to see thedummy earlier or later depending on how far away theywere from their burrow, yet their distance from the burrowstrongly affected the timing of their response. Crabs thatresponded later because they were closer to their burrowtherefore must have ‘decided’ to delay their response,presumably because they needed less time to reach safety.Second, the crabs responded earlier to dummies that wereseen at higher elevations, even though their visual acuitydecreases with increasing elevation (Zeil et al. 1986), againsuggesting that crabs selectively delayed their responses todummies seen at lower elevations. In addition, the merefact that the crabs’ home runs are usually preceded byfreezing (Nalbach 1990; Land & Layne 1995; Hemmi2005) indicates that they are not automatically triggeredby detection, although the crabs are certainly capable ofomitting the ‘freeze’ and running straight home (Layne1998, personal observations).

The crabs’ detection threshold can be estimated byconsidering the earliest responses, assuming that at leastsome crabs ran home as soon as they detected the dummy.My data set indicates a distinct threshold of just under 1 �

for angular size (Fig. 5a) and of approximately 0.5–1 �/s forapparent speed (Fig. 5b). The dummy’s image thus needsto move by at least 0.5–1 �/s before the crabs are able to

HEMMI: PREDATOR AVOIDANCE: 2. VISION 621

detect a movement. Crabs are known to be capable ofperceiving such low angular velocities, even for very smallstimuli (Horridge & Sandeman 1964; Sandeman & Erber1976; Nalbach 1989). These thresholds agree well withthose determined by others (Land & Layne 1995; Layne1998) and mark the limiting case, or the best the crabs cando. In most situations, however, the crabs initiated theirrun home at much larger apparent sizes and speeds(Fig. 5).

Response Criteria

After they have detected a predator, how do the crabsdecide when to initiate a home run? Their closely set, low-resolution eyes do not provide fiddler crabs with directinformation on a predator’s distance and absolute size(Collett & Harkness 1982; Zeil et al. 1986). The crabs thushave to rely on other predator-related visual cues to assessrisk. Crabs could, for instance, monitor the speed withwhich the image of a predator moves and respond whenits apparent speed reaches a certain threshold. Responsedecisions may also be based on the predator’s apparentsize. Nalbach (1990), for example, showed that H. cordi-formis respond to a fixed change in apparent size, in-dependent of the absolute size, speed or starting positionof an object. Alternatively, escape responses could betriggered when the apparent size has reached a certainthreshold value, or when it increases (looms) at a certainthreshold rate (e.g. Dill 1974). Time to contact and othervisual cues that carry information on approaching objectsare computationally more demanding and, in the case ofcrabs, can easily be ruled out.The observation that crabs respond later when ap-

proached more directly has a direct bearing on the

Retinal speed (degrees/s)

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Figure 5. (a) Apparent size and (b) speed of dummy spheres at thetime of response. -: Data from the speed experiment (dummy size:

2, 3 or 5 cm); : data from an earlier experiment (Hemmi 2005)

where the dummy was 1.6, 2.4 or 3 cm in size.

question of whether fiddler crabs base their responses onmeasures of apparent size or apparent speed. A distantpredator that approaches directly produces a slowlychanging image on the crabs’ eyes. Although the imagegrows larger as the predator comes closer, it does notchange its retinal position, making it difficult for a crab todetect that the predator is actually moving. On the otherhand, the retinal image of a predator moving alonga tangential path has a very small looming componentat all, but is easier to detect, because it has a much higherretinal speed. The fact that the crabs responded earlierwhen approached less directly therefore suggests that thespeed with which the retinal image moves across the eye,rather than its apparent size, determines when the crabsrespond. The observation that crabs also responded earlierwhen the dummy moved faster (Fig. 3) is consistent withthis conclusion and directly contradicts the hypothesisthat the home run is triggered by a fixed change inapparent size (Nalbach 1987, 1990), a response criterionthat is independent of approach speed.Now, if the speed of the retinal image of the predator is

indeed the critical variable that triggers a home run, itfollows that the retinal speed at the time of responseshould be approximately independent of the dummy’slinear speed (Fig. 6a). The dummy’s translational speedhad indeed no significant effect on its apparent speed atthe time of the response (REML: Wald1 Z 2.59, NZ 107,PZ 0.11; three outliers with large retinal speeds wereomitted), even though the approach speeds differed byalmost a factor of three (Fig. 6b). The strength of this resultis demonstrated by asking what retinal velocities the fastdummy class (mean: 56.4 cm/s) would have produced, ifthe crabs responded to them at the same distances as theydid to the slow dummies or vice versa (Fig. 6c). Clearly,neither of these hypothetical distributions looks anythinglike the corresponding distributions in Fig. 6a. The crabs,therefore, did not respond 36.5 cm earlier to the fasterdummies (Fig. 3), but they responded to both fast andslow dummies when their retinal speed had reacheda certain value. The faster dummies reached this speedjust 36.5 cm earlier.The crabs responded earlier to larger dummies (Hemmi

2005), which shows that they are not insensitive to thesize of the approaching predator. The influence of dummysize on the response distance was, however, clearly smallerthan would be expected if the crabs responded when thedummy reached a specified angular size (Fig. 7, dashedline), or even a specified change in angular size, assuggested by Nalbach (1987, 1990; Fig. 7, dotted line).Because a dummy’s size does not affect its retinal speed,this result indicates either that the crabs take the dummy’sapparent size into account when they decide to respond,for instance by adjusting the speed threshold dependingon apparent size, or that the mechanism with which thecrabs measure retinal speed is sensitive to size.Image motion as it is generated by the dummy is

measured by local elementary motion detectors (EMDs)in the crab’s visual system (e.g. Egelhaaf & Borst 1993). Atsmall apparent sizes, such EMDs confound the speed andthe size of moving objects (e.g. O’Carroll et al. 1996) andan EMD’s output increases with the angular size of the

ANIMAL BEHAVIOUR, 69, 3622

object. The influence of size on the EMD responsestrength, however, decreases with increasing size. Thismight explain why dummy size was not significant in thespeed experiment, where, at the time of response, thedummies were significantly larger, both in their absoluteand in their apparent size, than those in my previousexperiment (Hemmi 2005; Fig. 6a). One consequence ofthe conclusion that the crabs’ responses to predators are

Retinal speed (degrees/s)

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Figure 6. (a) The dummy’s retinal speed at the time of response. (b)

The dummy’s actual speed for the two speed classes. (c) Two

hypothetical distributions. The dark grey bars show what the retinalspeed of the slower dummies would have been had the crabs

responded to them at the same distance as they did to the faster

dummies. Light grey bars show the corresponding prediction for the

fast dummies.

triggered by the output of EMDs is that for a small dummyto imitate a much larger bird, its distance and speed needto be scaled to its size. For a 3-cm dummy that flies 20 cmpast the crab to be directly comparable to a 30-cm birdflying 2m past the crab, the dummy needs to move 10times slower for the output of EMDs to be exactly thesame.

One or Two Predator Avoidance Systems?

The above results are at odds with the extensive work ofNalbach (1987, 1990), but agree with the finding of Land& Layne (1995) that looming is not necessary to elicitescape responses in semiterrestrial crabs. In addition, mylooming experiment showed that fiddler crabs are muchmore sensitive to vertical than to horizontal expansion,which again contradicts Nalbach (1990) who found nosuch difference. However, this second discrepancy canprobably be explained by the fact that my looming stimuliwere so fast that the travelling edges of the cloths reachedretinal speeds comparable to those of the horizontallymoving dummies (Figs 4c and 6a). The crabs in the loom-ing experiment thus probably responded to the retinalspeed of the travelling edge rather than to the cloths’increase in apparent size. The difference in responses tohorizontal and vertically expanding cloths (Fig. 4a) isprobably due to the crabs’ high sensitivity to verticalangular velocities. Fiddler crab eyes have a higher resolu-tion in the vertical direction (Zeil et al. 1986, 1989; Land& Layne 1995; Zeil & Al-Mutairi 1996).

I suggest that the remaining discrepancy between myand Nalbach’s results is due to differences in the approachgeometry of our respective dummy predators. Nalbachalways approached the crabs directly, so that his stimuli

Cra

b–d

um

my

dis

tan

ce (

cm)

Dummy size (cm)

60

80

100

120

1.6 2.4

LSD

3.0

Figure 7. The effect of dummy size on the timing of the response(data from Hemmi 2005). The black line shows the prediction of the

statistical model. Dashed line: the predicted response distances if

the crabs had responded at a threshold angular size. Dotted line: thepredicted distances if the crabs had responded after the apparent

size of the dummy had increased by a fixed threshold amount. LSD:

least significant difference.

HEMMI: PREDATOR AVOIDANCE: 2. VISION 623

consistently had a high looming component and pro-duced little retinal image motion. For instance, whenHeloecius responded to an approaching human, the retinalmotion at the mean response distance (13m) was justunder 0.4 �/s, but the apparent size was already above 7 �,an increase of 5.6 � from the initial size (Nalbach 1987). Aretinal speed of 0.4 �/s is less than the limiting speed Ifound (0.5–1 �/s; Fig. 5b). The crabs in Nalbach’s experi-ments therefore responded before the predator’s apparentmotion even reached the speed threshold values. Thereverse is also true: at the higher speed/size ratio of mydummies (ca. 20 cm/s, 3 cm diameter) a dummy thatwould miss a crab by only 9 cm already produces a retinalspeed of over 1 �/s at a distance of 1 m, when it is only 2.8 �

in size. A study done on H. cordiformis using the dummysystem described in this paper (Jensma 2002) producedresults similar to mine, arguing against a difference be-tween species as a possible explanation for the divergentresults.Rather than contradicting each other, Nalbach’s and my

studies appear to have investigated two different, butcomplementary, predator response systems. Which sys-tem is triggered first depends on a predator’s speed relativeto its size and on its approach direction. Based on thisdual-system hypothesis we can make three testable pre-dictions. (1) the response distance should depend on thepredator’s approach speed at high but not at low retinalspeeds (!1 �/s) for which responses should be triggered byan increase in apparent size only. (2) Nonlooming stimuliwith a retinal speed of less than 1 �/s should not producea response. (3) Pure looming stimuli should triggerresponses after their apparent size has increased by a setamount, independent of the size, speed and the startingposition of the stimulus.

Sensory Information and AntipredatorResponses

From theory, we expect animals to time their responsesto predators depending on the risk they pose (e.g. Yden-berg & Dill 1986), which in this context is defined by thedistance and movement of the predator relative to theprey. However, fiddler crabs, like most small animals,including lizards and fish (Dill 1974), cannot know theidentity, distance and movement direction of a predatorand have only limited information on its approach.Binocular stereopsis as a distance cue, for instance, is oflimited use to small animals and, even for larger animals,is restricted to the frontal, binocular visual field and givesaccurate information only at close range (e.g. Collett &Harkness 1982). How then do animals assess the risk ofpredation? And how should a prey animal respond toa predator if it has incomplete information?In the absence of accurate information on risk, crabs are

forced to rely on retinal speed, which is a nonspecific cuethat only weakly correlates with real risk. Not only is thecorrelation weak, but in many situations it is also actuallymisleading. Retinal speed confounds speed, distance andapproach direction, which means that a predator couldlearn to circumvent a response system based on retinal

speed alone. A slowly moving, directly approachingpredator would remain below threshold until it is withinstriking distance, forcing the crabs to use a second visualalarm system based on apparent size (Nalbach 1990). Thesame slowly approaching predator could not avoid in-creasing in apparent size. Looming is a more robustindicator of risk, because it faithfully indicates that anobject is approaching. Responding when an object’sapparent size has increased by a certain amount wouldthus save a crab from becoming a meal. To rely on changesin apparent size alone, however, is also risky. Apparent sizeis ambiguous in relation to size and distance, and changesin apparent size are difficult to measure for small angularsizes, allowing small but fast predators, such as birds orghost crabs, to approach dangerously close.In the absence of more accurate information on the

approach of the predator, the crabs are forced to respondas early as possible, in order not to get caught out by caseswhere the visual cues underrepresent risk. Retinal speed isa fundamental and easily measured cue, which allows thecrabs to respond to approaching predators at large andsafe distances despite their limited visual capacity. Appar-ent size changes are much more difficult to determineaccurately at long range and I would predict that, in thecontext of the home run, they provide a backup systemfor approaching predators that do not produce significantretinal motion.An early warning system based on retinal speed,

however, is necessarily nonspecific and crabs respond toalmost anything that moves above the visual horizon(Layne et al. 1997; Layne 1998), whether it is small orlarge or whether it approaches them or not. Fiddler crabsrun for protection from butterflies, high-flying kites oreven leaves blowing in the wind, none of which is a realthreat. I suggest that the predator avoidance strategy offiddler crabs has to be seen as an attempt to gatherinformation in order to minimize the costs of falseresponses, without taking significant risks. The crabs, likea wide variety of animals, respond to a predator inthree distinct stages: freeze, home run and, finally, refugeentry. Each successive stage is characterized by highersecurity, but also higher cost in terms of lost opportunityor energy. However, the first two stages improve thecrab’s ability to gather reliable information on a potentialthreat.Freeze, the first stage, is triggered upon detecting an

object that moves in the upper visual field: the crabs stopfeeding and remain still. This has two effects. Still crabs aremuch harder to detect and at the same time can gathermore reliable information about the predator by eliminat-ing self-induced image motion. Freezing thus improvesthe crabs’ ability to assess predator-related visual cues suchas apparent size and retinal speed.The second stage of the crabs’ response sequence, the

home run, is triggered very early, often close to thedetection threshold, by retinal speed, or a change inapparent size. The home run clearly has a higher costthan the freeze, but the costs would still appear relativelylow, because the crabs can continue feeding near therefuge and can immediately continue whatever they weredoing before, once the threat has passed. The return to

ANIMAL BEHAVIOUR, 69, 3624

their refuge greatly increases the crab’s safety. They now sitdirectly at or in the burrow entrance and any uncertaintyabout the burrow’s location or the burrow’s availability hasbeen removed. Most importantly, however, the crabs cannow continue to assess the situation from a relatively safeposition, giving them access to more reliable indicators ofpredation risk.The third stage of predator evasion is the descent into

the burrow, which essentially eliminates the risk of pre-dation, at least for U. vomeris, which builds relatively deepburrows. However, upon burrow entry, the crabs lose sightof the predator and therefore suffer a significant loss ofinformation. The crabs have to decide when to resurfacewithout further information on the predator’s locationand therefore run the risk of encountering a new ora waiting predator, a risky and costly waiting game (Hugie2003, 2004; Jennions et al. 2003). The decrease in risk andthe difference in the available information between thesecond and the third stage of the escape response suggestthat the crabs should use different cues to decide when toinitiate each of these actions. In the case of burrow entry,crabs would be expected to monitor more selective cuesthat more accurately reflect actual risk. We do not knowwhat triggers burrow descent (Nalbach 1987; Koga et al.2001), but I would predict that apparent size or loomingare likely candidates, as they convey more risk-relatedinformation than retinal speed. Indeed, looming has beenshown to be the critical stimulus of the escape response inmany fish species (e.g. Dill 1974). Fiddler crabs couldachieve higher response selectivity at this stage with thesame two response systems by changing their thresholds,such that most responses would now be triggered byapparent size changes rather than apparent speed. Beingclose to their burrow, the crabs can afford to let thepredator approach closer before triggering the third andmost costly stage of the response.In conclusion, fiddler crabs lack accurate information

on the risk posed by a predator and are forced to rely onunreliable sensory correlates of risk. The crabs cope withthis dilemma by using a three-stage response strategy,which allows them to update and increase the quality ofinformation without exposing themselves to significantrisk. The sequential response strategy also helps crabs tominimize false responses and therefore reduces the overallcost of their predator avoidance behaviour. The fiddlercrab example shows that the availability of information isan important constraint that can strongly affect optimaldecision making strategies.

Acknowledgments

The work was supported by postdoctoral fellowships fromthe Swiss National Foundation and the Centre for VisualSciences at the Australian National University. Manythanks to Jochen Zeil for his input at all stages to DavidO’Carroll for his advice on motion detectors and JeffWood from the Statistical Consulting Unit for his help. Iam also grateful to Paul Dixon, Lindsay Trott and LizHowlett at the Australian Institute of Marine Sciences formaking it possible for me to work there. The manuscript

was greatly improved by the comments of two anony-mous referees.

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