anti-predator responses of the intertidal crab heterozius rotundifrons (brachyura: belliidae) in air...

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Anti-predator responses of theintertidal crab Heterozius rotundifrons(Brachyura: Belliidae) in air and waterBrian A. Hazlett a & Colin L. Mclay ba Department of Ecology and Evolutionary Biology , University ofMichigan , Ann Arbor, MI, 48109, USAb School of Biological Sciences , University of Canterbury ,Christchurch, New ZealandPublished online: 31 Jan 2007.

To cite this article: Brian A. Hazlett & Colin L. Mclay (2005) Anti-predator responses of theintertidal crab Heterozius rotundifrons (Brachyura: Belliidae) in air and water, Marine andFreshwater Behaviour and Physiology, 38:2, 95-103

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Marine and Freshwater Behaviour and Physiology

June 2005; 38(2): 95–103

Anti-predator responses of the intertidal crab Heterozius

rotundifrons (Brachyura: Belliidae) in air and water

BRIAN A. HAZLETT1 & COLIN L. MCLAY2

1Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor,

MI, 48109 USA and 2School of Biological Sciences, University of Canterbury, Christchurch,

New Zealand

(Received 15 October 2004; in final form 24 January 2005)

AbstractThe intertidal crab Heterozius rotundifrons responds to tactile input, as occurs during a predationattempt, by hyper-extending all of its limbs and remaining in that posture for a variable length oftime. We compared the duration of this anti-predator response: (1) in the day versus night (2) intwo fluid media (air versus water) (3) after exposure to additional predator cues in one medium (airor water) and testing in the other medium (4) for crabs from different parts of the tidal range and(5) for females with and without eggs on their pleopods.Crabs showed the posture at night as well as during the day. They also executed the posture

when tested in air and extended the duration of the posture in air when they detected an additionalpredation-risk cue, shadows passing overhead. When crabs experienced input in one medium therewas no effect on the duration of behavior shown in the other medium. Crabs from the lower portionof the intertidal showed a markedly longer duration of the limb-extended posture compared to crabsfrom the higher end of the tidal range of this crab. Berried females responded the same as femaleswithout eggs in both air and in water. Thus, crabs show this anti-predator behavior under a widevariety of conditions, but do not appear to transfer information received in one medium to behaviorshown in the other media.

Keywords: Anti-predator behavior, fluid media, intertidal, crab, brachyura

Introduction

The marine intertidal zone presents an environment in which animals are faced with regular

marked changes in the fluid environment as well as many other environmental conditions.

While some marine species move regularly to avoid the change from an aquatic to aerial

environment (Chelazzi et al. 1988), many others remain approximately in place and

must deal with living and behaving in both water and air, albeit moist air in a low-tide

Correspondence: Brian A. Hazlett, Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor,

MI, 48109 USA. Fax: 734-763-0544. E-mail: [email protected]

ISSN 1023–6244 print/ISSN 1029–0362 online/00/000095–103 # 2005 Taylor & Francis Group Ltd

DOI: 10.1080/10236240500078339

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hiding place. A survey of the shores at the Lough Hyne Marine Nature Reserve, Ireland

showed that the number of mobile taxa outnumbered sessile taxa by approximately 2 : 1

(Davidson et al. 2004).

Intertidal animals commonly move to a refuge from the extremes of terrestrial conditions

during low-tide periods. Some animals, such as barnacles, are specialized to form a refuge by

closure of parts of the animal to create a secure shelter (Barnes & Reese 1960). A more gen-

eral pattern is to move to a crevice (Bovbjerg 1960), into a burrow (Ansell 1988), or under a

rock in the intertidal (e.g. Heterozius rotundifrons) for the duration of the low-tide/aerial con-

ditions. However, even in refuge, animals must receive and respond to sensory input. For

example, if they can receive input indicating increased predation risk, animals should

respond to this even in the context of refuge occupation. We would expect that intertidal

animals should behave in an adaptive fashion in both fluid worlds.

Heterozius rotundifrons is a New Zealand endemic brachyuran crab that lives in the inter-

tidal zone (McLay 1988). It has an unusual anti-predator defense of fully extending all

appendages in a ‘‘frozen’’ posture for many seconds or minutes when disturbed by tactile

input (Field 1990). This posture is an effective anti-predator behavior (Hazlett & McLay

2000), greatly increasing the fish gape size needed to eat a given size crab. This catatonic

response occurs both in water and in air. The time spent in this posture following tactile

induction is increased by additional predation risk cues such as the odor of crushed conspe-

cifics (Hazlett & McLay 2000), the odor of some related crabs when crushed (Hazlett &

McLay 2005a), and visual cues simulating a predator swimming overhead (Hazlett &

McLay 2000). That is, crabs respond to odors from crushed conspecifics and to the

visual input of shadows passed overhead as danger cues (Hazlett & McLay 2000). When

both visual cues and chemical cues are presented at the same time, the crabs switch strategy

and rather than spend more time they spend less time in the limb-extended posture (Hazlett

& McLay 2005b). However, in all of the experimental results mentioned above, crabs were

exposed to different conditions and tested only during the day, in water, and we avoided

using berried females.

Individuals of H. rotundifrons of course face potential predation risk at times other than

daylight hours, in air as well as in water, during different phases of the tidal cycle, and,

for females, whether they are carrying eggs or not. In this study we examine the duration

of the crab’s anti-predator response under a wide variety of relevant environmental condi-

tions, paying special attention to transference of effects experienced in one fluid medium

to the behavior shown in the other fluid medium. We addressed five questions concerning

the anti-predator responses of individuals of H. rotundifrons. First, we asked if animals

behave differently in the dark compared to illuminated conditions. Second, we asked if indi-

viduals of H. rotundifrons would execute the limb-extended posture in air and was the dura-

tion of the posture similar to that shown when placed in water. Third, we asked if

experiences in water affected behaviors shown in air and vice versa. Fourth, we asked if con-

ditions associated with location within the tidal range of this species affected anti-predator

behavior duration. And finally, we asked if females behaved differently depending upon

whether they were carrying eggs or not.

Methods

General methods

In all of the tests described here, animals were collected from the vicinity of the Edward

Percival Field Station in Kaikoura, New Zealand. They were tested either in the field, at the

96 B. A. Hazlett & C. L. McLay

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Field Station in Kaikoura, or in the facilities of the School of Biological Sciences, University

of Canterbury, Christchurch, NZ. Tests were conducted in February, March and May of

2003. In every test, the limb-extended posture was induced by picking up a crab, holding it

in air, turning it upside-down, and then turning it back right-side-up and placing it on a

substrate (Field 1990). The duration of the ‘‘frozen’’ limb-extended posture was recorded as

the time from initial induction to the time of the first movement of an ambulatory leg or

cheliped. Individuals were tested just once and sample sizes varied from 20–24 in each kind

of test. Some treatments involved exposing the crabs to two types of additional predation

risk cues. These cues were exposure to chemical cues from crushed conspecifics and the

visual cue of a shadow passing overhead, identical to the cues used in earlier studies (Hazlett

& McLay 2000). The chemical cue was prepared by crushing two medium-size individuals

of H. rotundifrons in 150mL of sea water, letting them soak for 10min and then filtering with

coarse filter paper. Twenty-five mL of this solution were added to containers with 150mL

of sea water containing a test crab. The shadow presentations were done by passing a 15 cm

wide black posterboard by hand, 10 cm above a treatment container at the speed of

15 cm s�1 every 15 s for 10min.

Day–night

Individuals were tested in the facilities of the School of Biological Sciences in Christchurch.

Crabs were tested in water, in one of three situations: (a) during the day (10:00–14:00 hrs)

with tactile induction (b) during the night (20:30–21:30 hrs) with tactile induction, and (c)

during the night (20:30–21:30 hrs) with conspecific alarm odor added to the test container

prior to tactile induction. For the night experiments, the crabs were moved from the salt-

water holding facility and moved to the testing lab in a light-tight container. Observations

were made with a red light source, which crabs cannot detect.

Air–water

To test responses in air compared to water, a series of four experiments were conducted.

First, we needed to establish that crabs would show the limb-extended posture in air in order

to compare the duration of the response in the two media. Experiment #1 (Response in

water versus air) involved tactile induction followed by placing the crabs either in control sea

water in a container with sand in the bottom or placing the crabs on the surface of moist

sand with no standing water in the container.

Next, we needed to establish if an additional predator cue detected in air had an effect on

the duration of the response in air. In Experiment #2 of this series (Treat in air, test in air),

crabs were held in a container with moist sand for 10min prior to tactile induction and then

placed on moist sand. During the 10min period, control animals received no other treat-

ment while the experimental animals had a shadow passed over them every 15 s while

resting on moist sand. The shadow treatment is the same as that used in earlier studies

(Hazlett & McLay 2000, 2005b) where crabs were treated and tested in water.

Given the results of the first two tests, we examined possible transference of effects of

treatment in one medium to behavior shown in the other medium (Experiments #3 and

#4). Experiment #3 (Treat in water, test in air) involved exposing crabs for 10min to

one of four conditions while in water followed by testing them in air. The four treatments

were (a) control (b) a shadow being passed overhead every 15 s for 10min (c) 25mL of

alarm odor added to the water prior to placement of the crabs in the container and (d) the

combination of shadow treatment þ the addition of alarm odor. Following the

Behaving in two environments 97

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treatment in water, crabs were picked up, the tactile induction of the limb-extended posture

was effected and the crabs were placed right-side-up on moist sand and the duration of the

posture was recorded.

In Experiment #4 (Treat in air, test in water), crabs were exposed to one of two treat-

ments in air for 10min, while resting on moist sand, prior to induction of the limb-extended

posture and placement in water. The two conditions were (a) no special treatment in air

(control) and (b) a shadow was passed over in air once every 15 s for 10min. Pilot tests

failed to demonstrate that crabs could detect alarm odor in air, thus testing for transference

from air to water for a chemical cue associated with increased predation risk was not

possible.

Tidal cycle effects

While individuals of H. rotundifrons experience alternating periods of submersion and

exposure to moist air conditions, the extent of the tidally generated periods differ, given the

location of the crabs within the intertidal zone. We tested animals to see if location within

the intertidal range affected the duration of anti-predator behavior. We collected animals

from the highest and lowest regions of the species’ range within the intertidal from Keane

Pt., Kaikoura peninsula, Kaikoura, NZ. In the first experiment (#1), following tactile

induction of the limb-extended posture, we placed the collected crabs in water and recorded

the duration of the posture. In Experiment #2, we placed the collected crabs on moist sand

following tactile induction.

Female reproductive conditions

Female H. rotundifrons were tested for the duration of the limb-extended posture under

two environmental conditions (air and water) and two reproductive conditions (bearing

eggs on the pleopods or not bearing eggs on the pleopods). The standard tactile

induction of the posture was effected on females that were either berried or not and

placed either in control water or on moist sand and the duration of the limb-extended

posture recorded.

In all of the above experiments, the number of seconds spent by crabs in the limb-

extended posture under different conditions was compared by either t-test or ANOVA

depending on the number of experimental conditions being compared. In the case of experi-

ments analyzed with ANOVA, pair-wise comparisons were made with Tukey tests. Where

means are presented in the text, they are followed by standard errors of the mean.

Results

Day–night

As shown in Figure 1, individuals of H. rotundifrons responded to the standard tactile

induction by assuming the limb-extended posture at night and the duration of the posture

was not significantly different than during the day (Tukey p¼ 0.140). The response duration

under the three conditions varied significantly (F¼ 3.45, df¼ 2, 57, p¼ 0.039). As was the

case for tests during the day (Hazlett & McLay 2000), the addition of conspecific alarm odor

at night resulted in an increase in the duration of the posture at night compared to tactile

induction alone (Tukey p¼ 0.040).


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Air–water

The results of Experiment #1 (Response in water versus air) showed that there was no

difference in the duration of the limb-extended posture following simple tactile induction

depending upon whether the crabs were placed in water ( �xx¼ 194.9� 26.2 s) or in air

( �xx¼ 202.7� 20.3 s) (t¼ 0.53, df¼ 39, p¼ 0.644).

In Experiment #2 (Treat in air, test in air), crabs that experienced the additional preda-

tion risk cue of a shadow passing over them in air prior to tactile induction remained in the

limb-extended posture in air longer (�xx¼ 294.1� 31.5 s) than those that did not experience

the visual cue (�xx¼ 199.8� 30.4) (t¼ 2.93, df¼ 39, p¼ 0.009). Experience in air affected

response in air in a fashion similar to experiences in water affecting responses in water

(Hazlett & McLay 2000).

In Experiment #3 (Treat in water, test in air), there was an overall effect of treatment

(F¼ 6.7, df¼ 3, 76, p<0.0001). However, crabs that had experienced the shadow treatment

in water tended to remain in the limb-extended posture for a similar duration as controls

(Tukey p¼ 0.108) (Figure 2) and those crabs experiencing the alarm odor chemical cues

in water showed no effect compared to control conditions when tested in air (Tukey

p¼ 1.000) (Figure 2). The combination of shadow þ alarm in water tended to effect

a reduction of the duration of the posture when tested in air, but the difference between

control and SþA was not significant (Tukey p¼ 0.13). The comparison of the shadow

alone treatment and shadow þ alarm was significantly different (Tukey p< 0.0001), the

shadow þ alarm duration being shorter.

In Experiment #4 of the air–water series (Treat in air, test in water), responses of crabs

that experienced a shadow in air and were placed in water (�xx¼ 167.5� 32.2) did not

differ significantly from crabs that experienced no shadow treatment in air and were

tested in water (�xx¼ 176.7� 32.2) (t¼ 0.20, df¼ 38, p¼ 0.84).

Day Night Night + Alarm Odor0

50

100

150

200

250

CCCCoooonnnnddddiiiittttiiiioooonnnn

MM MMee ee aa aa

nn nn nn nn uu uu

mm mmbb bb ee ee

rr rr oo oo ff ff

ss ssee ee cc cc

oo oo nn nndd dd ss ss

Figure 1. Mean (s.e.) number of seconds spent in the limb-extended posture by individuals ofH. rotundifrons when tested during the day and at night. Night tests included exposure to conspecificalarm odor as well as placement in water without any added cues.


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Tidal cycle effects

Responses of animals tested in the field in water showed that crabs from the lowest portion

of the tidal range had significantly longer response durations compared to the crabs

collected from the highest portion of the tidal range (t¼ 34.5, df¼ 19, p<0.0001)(Figure 3).

When animals were tested in air there was no difference in response duration between

collection locations (t¼ 0.09, df¼ 19, p¼ 0.923).

Female reproductive condition

As shown in Figure 4, there was a strong effect of the fluid medium female crabs were placed

in, with the duration of the posture being longer in air than in water (ANOVA main effect

F¼ 10.88, df¼ 1, 77, p¼ 0.001). However, there was no effect of female reproductive

condition either as a main effect (F¼ 0.001, p¼ 0.972) or an interaction term between

female condition and fluid medium (F¼ 0.008, p¼ 0.929). The berried and non-berried

females responded to the two fluid conditions in almost exactly the same way (Figure 4).

Discussion

The limb-extended posture adopted by individuals of H. rotundifrons when handled by a

potential predator is an effective anti-predation behavior in both water (Hazlett & McLay

2000) and in air (Field 1990). Given that predation risk can occur under a variety of

circumstances, it is not too surprising that these crabs showed this response under a variety

of conditions. Fish predators could attack crabs during day or night when tidal conditions

Control Shadow Alarm Odor Shadow + Alarm0

50

100

150

200

250

TTTTrrrreeeeaaaattttmmmmeeeennnntttt iiiinnnn wwwwaaaatttteeeerrrr

MM MMee ee aa aa

nn nn nn nn uu uu

mm mmbb bb ee ee

rr rr oo oo ff ff

ss ssee ee cc cc

oo oo nn nndd dd ss ss

(( ((tt tt ee ee

ss ss tt ttee ee dd dd

ii ii nn nn aa aa

ii ii rr rr)) ))

Figure 2. Mean (s.e.) number of seconds spent in the limb-extended posture by individuals ofH. rotundifrons when exposed to conditions in water and tested in air. The conditions in water were(a) control (b) a shadow passed over the crabs every 15 s for 10min (c) 25mL of conspecific alarmodor solution added to the pre-test container and (d) exposure to both shadow and conspecificalarm odor.


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allow, bird predators could attack crabs stranded on moist sand, and both males and females

could be attacked no matter what their reproductive status is.

It is interesting that the duration of the limb-extended posture, resulting from tactile

induction, tended to be shorter at night than during the day. This may be associated with

Water Air0

50

100

150

200

250

300 Non-berriedBerried

Testing environmentTesting environment

Mea

n nu

mbe

r of

sec

onds

Mea

n nu

mbe

r of

sec

onds

Figure 4. Mean (s.e.) number of seconds spent in the limb-extended posture by females ofH. rotundifrons when tested in water or air for non-egg-bearing (solid bars) and egg-bearing (stippledbars) females.

Water Air0

100

200

300

400

500

Low intertidalHigh intertidal

Testing environmentTesting environment

Mea

n nu

mbe

r of s

econ

dsM

ean

num

ber o

f sec

onds

Figure 3. Mean (s.e.) number of seconds spent in the limb-extended posture by individuals ofH. rotundifrons collected from the low and high intertidal when tested in water and in air.


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larger fish predators being active at night and the effectiveness of the limb-extended posture

being reduced under those circumstances, thus less time in the immobile posture before

utilizing locomotion to find a refuge as an alternative strategy (Hazlett & McLay 2005b).

The detection of an additional predation risk cue, alarm odor, resulting in an increase in

the duration of the posture at night is very similar to the results reported earlier for tests con-

ducted during the day (Hazlett & McLay 2000). Or course, the other additional risk cue

used in our earlier study, shadows passing overhead, is not applicable at night.

While individuals of H. rotundifrons would usually be under a rock at low tide and

thus sheltered from aerial predators such as birds, they could be subject to such predation

risk on occasion if they failed to return to a rock shelter before the tide went out. Thus it

was not surprising that they showed the limb-extended posture following tactile induction

and being placed on moist sand. The fact that the duration of the posture was almost

identical in air and water may indicate that predation in air and water may be equally

efficiently deterred by the posture in both situations, even though the predators in the

two situations could be different. The observation that the duration of the posture was

just as long in air as in water is somewhat surprising, given that the crabs placed on moist

sand are in an unfavorable environment, subject to desiccation and thermal stress. The

fact that detection of an additional danger cue (shadows passing overhead) in air extended

the duration of the anti-predator posture in air is similar to the responses reported earlier for

the crabs experiencing that kind of signal in water and being tested in water (Hazlett &

McLay 2000).

The results of the tests in which crabs experienced a danger cue (shadows passing over-

head, alarm odor) in one medium and were tested in the other medium showed little

evidence of transference of effects from one medium to the other. In most tests there

seemed to be no effect of experience in air on behavior in water and vice-versa. This may

very well indicate a strategy which ignores cues received in one fluid medium when the

posture is induced in the other because the two media represent different sets of predation

risks. Detection of alarm odor, indicating recent successful nearby predation in water, may

be irrelevant to the level of predation risk in air by different predators.

The tidal cycle tests clearly showed that crabs from a location lower in the tidal range

remained in the limb-extended posture for a longer period of time than crabs from higher

in the intertidal when tested in water. The longer duration of the anti-predator behavior

in the lower tidal location seems intuitive since the lower tidal location would subject the

crabs to larger fish predators, given the greater depth of water in such locations. Since the

same aerial predators, i.e. birds (Field 1990), would be present in the lower or upper

tidal regions, the lack of a difference in anti-predator behavior in air by animals from the

different tidal locations also seems reasonable.

Berried females behaved the same in both air and water as females that were not carrying

eggs. This result was surprising especially when the crabs were tested in air since the eggs,

along with the female bearing them, are subject to desiccation and the eggs would seem

particularly subject to the negative effects of exposure to air. The presumed positive effects

of adopting the limb extended anti-predator posture for the female appears to take

precedence over any negative effects that behavior might have on egg survival.

Overall, our results point to the utilization of a similar effective anti-predation behavior

under a wide variety of conditions by these crabs. One would expect there to be different

responses in air compared to water because in air crabs are subject to the additional

hazard of desiccation. The similarity of responses in a variety of environmental conditions

would indicate that this anti-predator behavior is effective for these crabs in all portions

of their environment.


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Acknowledgements

This study was made possible by support for BAH as a Visiting Erskine Fellow funded by the

Erskine Foundation, University of Canterbury. We wish to thank Jack Van Berkel for his

assistance at the Percival Field Station, Kaikoura and thanks to Catherine Bach and Dan

Rittschof for their comments on the manuscript.

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with special reference to its ecology and distribution. J. Anim. Ecol. 29:169–185.

Bovbjerg RV. 1960. Behavioral ecology of the crab. Pachygrapsus crassipes. Ecology 41:785–790.

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anti-predator responses of the intertidal crab heterozius rotundifrons (brachyura: belliidae) in air...

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