Prey capture by the cuttlefish (Sepia officinalis L): An experimental study of two strategies

Behavioural Processes, 9 (1984) 13-21 Elsevier

PREY CAPTURE BY THE CUTTLEFISH STUDY OF TWO STRATEGIES

PIERRE

DUVAL+,

Laboratoire

MARIE-PAULE

(SEPIA OFFICINALIS

CHICHERY

de Psychophysiologie;

and Laboratoire (Accepted

13

maritime

4 August

AND RAYMOND

Universite

de Luc-sur-Mer,

L): AN EXPERIMENTAL

CHICHERY++

de Caen,

14032 Caen Cedex, FRANCE

14530 Luc-sur-Mer,

FRANCE

1984)

ABSTRACT Duval, P., Chichery, M.P. and Chichery, R., 1983. Prey capture by the cuttlefish (Sepia officinalis L): an experimental study of two strategies. Behav. Processes 9: 13-21. This study shows that the size of the prey (Carcinus maenas) relative to the predator (Sepia officinalis) is of importance in the choice between two types of attack: either capture by ejection of the two extensible tentacles, captured or capture by jumping on the prey. Small crabs are preferentially by the first method and large crabs by the second. Other factors which may explain the observed variations, include previous experience of the predator and the behaviour of the prey.

INTRODUCTION The cuttlefish, catch comparatively studies

(Wilson,

large living prey:

1946; Boulet,

there are two methods the prehensile

of attack:

tentacles

shrimps,

1964; Messenger, an attack

1964) think that each type of capture

kind of prey. Messenger

as regards

to study thoroughly to answer

(swimming,

Some authors

the ejection

However,

and we thought

once

1946;

of a certain

of capture

creeping,

his observations

(Chichery,

linked to the locomotory

moving

and to try

1980):

characteristics

fast or slowly) or is it related

P.DUVAL: Present address: ISTPM, centre de Ouistreham, 67 rue Gambetta 14150 OUISTREHAM. FRANCE ++ : Reprint requests: R.CHICHERY, Laboratoire de Psychophysiologie, Universite de Caen. 14032 CABN CEDEX. FRANCE

0 1984 Elsevier

Science

Publishers

B.V.

remain

it would be interesting

set by the choice of capture method

+

0376-6357/84/%03.00

of

the tentacles (Wilson,

is characteristic

which have been asked lately

- Is the choice of method of the prey

of capture.

this question,

the problem

two questions

either

(1968) was the first to show that crabs could be sei-

zed by either of these two methods fragmentary

1968, 1977) have shown that

involves

("jump").

able to

fishes and crabs. Various

or the use of all the arms without

the animal has jumped upon its prey Boulet,

L., is a very active predator

Sepia officinalis

14

simply to the size of the predator - Does an individual

and the size of the prey?

animal preferentially

use one method

of capture or the

other?

MATERIAL

AND METHODS

The animals used in this study had been caught by local fishermen miles away from Luc-sur-Mer 140 to 1700 g according months

to thirty months).

months.

The floating

were never

vidual

The captivity

life varies

The animals

ranged

individuals

from

(from eight

from few days to ten

animals do not take preys any more and are moribund.

considered

tory of Luc-sur-Mer

between May and October.

to the age of the different

few

in our study. We also used animals

and weighing

animals was followed

from 30 to 70 g. The behaviour

over several weeks

They

bred in the labora-

to see whether

of some indi-

their strategies

changed with experience. The observations containing

were made through an aquarium made of glass (80x45~30

filtered

fresh circulating

Several

seawater.

cm)

series of experiments

were carried out: - In the first, different natural

conditions.

types of prey were caught by the cuttlefish

Thus, we used crabs

(Carcinus maenas)

each crab the surface of the cephalothorax length).

270 captures were observed

camera for a detailed the weight

gnates the weight

is R, the bigger

studied

179 attacks

(young Mugil

cephalothorax

to the Sepia,

we altered

whether

RcO.3)

very quickly

allowed

of the tentacles.

avoids a positive

characteristics

the type of catch. Large

system. This apparatus

part of the

allowed us to move

at the beginning

of the "jump" or at

At the end of four trials the cuttlefish

was

the last type of capture attempt used. This

reinforcement

- The third series of experiments ratory. These experiments

the locomotory

this changed

(8 cm in about 200 ms). The time of the displa-

to eat the crab, whatever

procedure

We also

sp.) and observed

were fixed by the anterior

cement was selected by the experimenter the ejection

size-

sp.).

to an electromechanical

the crab backwards

relation

R which desi-

to the cuttlefish.

(Crangon crangon, Palaemonetes

of the prey (crab) to determine (relative

between

divided by the surface of the crab. The

- In the second series of experiments

crabs

(width x

the relation

1971). We use the quotient

is the crab, compared

on shrimps

11 attacks on fishes

We calculated

and the exponential

for *,

(Richard,

of the cuttlefish

smaller

approximately

(in g) and the size of the crab (in mm'). Weight

easy to measure

is now well known

in nearly sizes. For

and 197 of them were filmed with a video-

study of the capture.

of the cuttlefish

is a parameter weight

was measured

of various

of one or other type of capture.

included

were specifically

only young cuttlefish designed

bred in labo-

to study the factors in-

15 volved

in the attack on shrimps.

called "clubs"

Ten animals aged 8 months

(which are the only parts with suckers)

ved under alcohol

anaesthesia

mals were regularly

(2% alcohol

fed with shrimps.

mals for four weeks,

in seawater).

We followed

had the extremities

of both tentacles Afterwards

the behaviour

remo-

these ani-

of all ten ani-

and 4 of them for eight weeks.

RESULTS (1) Rate of successful Our results

captures

indicate

that the rate of success of the captures

attempt

(87.7%) can be compared with

those obtained

capture

of shrimps by the prehensile

tentacles.

The analysis has allowed

of the catches

us to reckon

of crabs

higher

(2) The importance

-0.5

of tentacles;

for the "jump" strategy, of prey size (quotient

(a) Choice of capture method

0

attacks

on the first attempt.

the "jump" seems to be more efficient

the "jump" and 84.6% for the ejection gnificantly

at the first (1968) for the

(n = 197) recorded with a videotape

the rate of successful

Of the two types of capture,

by Messenger

0.51-1.00

accuracy

(96.2% for

of attacks was si-

X2 = 6.71, P,
R)

for crabs in relation

1.01 -1.50

to R (Fig.l)

>1.51

R

Fig.1. Choice of the capture method for crabs in relation to prey size: quotient R (R is a measure of the relation between crab size and cuttlefish size - a small R means that the prey is large compared with the predator). tentacles &\p : “jud’

im:

16

Fig.1 represents the different

the frequencies

observed

for both types of capture

classes of R over the whole of the population

studied

for

(270 cap-

tures). We can note: - on the one hand, a reduction

of the frequency

crease of R; crabs which are small in relation are preferentially

captured

by the ejection

- on the other hand, the existence 0.5 and 1.5) where

the frequencies

of the "jump" with

the in-

to the size of the cuttlefish

of the tentacles.

of a central area (R values between

of the two types of capture

seem to be ba-

lanced. (b) Study of some individual We were able to observe diagrams

in the frequency

of captures

duals

of results

(Fig.2)

some animals over a period of a few weeks.

dy of individual

absence

diagrams

shows, just as for the whole population, using the tentacles

with an increase

The stu-

an increase of R. The

in the high classes of R for the small cuttlefish

(indivi-

1 and 2) may be explained by the fact that they do not catch crabs which

are too small (carapace width<5 Once we were able to observe

mm); the profitability

an animal

(unfortunately

seemed always to use the tentacles whatever (3) The role of previous

experience

is probably

for only 5 days) which

the value of R.

and the behaviour

of the prey

Because we were able to follow the catches of an individual several weeks we gained an impression (a) Changing

the jumping

too small.

animal over

of the part played by other factors.

strategy

as a result of a quick displacement

of

the crab A temporal

analysis

the intervention

of the "jump" allowed us to develop

of a closed loop control

cution of this behaviour experiments

was undertaken

tained were fragmentary differently

to test this hypothesis.

and although

the six animals

we can still draw one conclusion.

ture a rapidly displaced RC0.3

(with visual

(Chichery, work in progress).

usually

inducing

crab begins

thod of capture

profile.

feedbacks)

of

in the exe-

The second series of

Although

the results

studied behaved

An animal

to use the tentacle

catches by the jumping method).

result with an individual

an hypothesis

ob-

rather

that has failed to capattack

(with a ratio

Fig.3 illustrates

Then, an animal resorts

this

to the tentacle me-

after the "jump" has failed many times.

(b) Changing

the tentacle

strategy

as a result of ablation

of the tentacle

tips We noticed

1359 attempts

- 1123 attempts

to catch shrimps, distributed

by ejection

of the tentacles

as follows:

(failing because

of the lack

of suckers). - 236 attempts

by "jump".

Fig.4 shows the change with time in the rate of "jump" related

to the to-

17

0

4

_

50-

02

I 50,

MALE

2109

03 MALE

50l-

330g

04 MALE 4809

5()-

05 FEMALE 5 O-

Fig. 2.

10709

Indiv&\q

;i;;:;s:

choice

of

the&

e of capture : tentacles.

for

crabs

18

tal attempts

(on the first day after the operation,

week after the operation, Among

the 2nd week,

the 236 jumps we noticed

96 attempts were successful the point priate

3rd, 4 th and 8th week).

100 failures

and 136 successes

that these animals

a very obvious

are perfectly

that the last animals regeneration

suckers just visible tained by Feral

(57.6%); only

at the first try (40.6%). However we must stress able to catch crabs of the appro-

size by the jump technique with a standard

We observed

the average of the first

studied

rate of success.

(8 weeks)

of the extremities

showed, at that time,

of the tentacles,

(but not yet functional).

with

This result confirms

small

those ob-

(1978, 1979).

DISCUSSION Our results on the success rate of capturing (87.7%) confirm

those obtained

91% in grey tanks probably

by Messenger

without

studied.

fishes by ejection

Our results,

obtained

of the tentacles

on only a few captures,

a low rate of success. The small fishes used in this study (w in schools. Neil1 and McCullen the protective of different

The duration

of the ejection

of tentacles

possesses

feedbacks

This difference

in central

the possibility

of the two strategies

reside

The most important

particularly

and R>1.5).

The quotient, of determining

central values portant,

(>lOOms)

noted mistakes

of the attacking

of R relative

as the frequencies

characteri-

adjustments.

dissimilarities of tentacles

in the strategy

distance.

an answer to the two ques-

of the size of the prey in rela-

in the case of extreme

size cuttlefish/size between

the "jump"

allow the use of

corrector

the observed

result of this study affords

part in the process

a closed loop sys-

(84.6% for the ejection

It shows the importance

tion to that of the predator, (R<0.5

of terminal

The more frequently

in an under-estimation

tions posed earlier.

duration

control might explain

and it seems

animal,

of the animal. These stages might

and 96.2% for the "jump"). "tentacles"

of the whole

stage which has a variable

and ensure

in the efficiency

feedback

1968). A study in preparation

control of the "jump" also includes

zed by an active braking visual

(Messenger,

after a very quick displacement

a terminal

study of

to the efficiency

is less than 30ms. The hight

its control by visual

that it is under "open loop" control

tem. Indeed,

show

(Sepia, Loligo).

speed of this motor act precludes

shows that the central

in relation

was

sp.) move

(1974) have already made a thorough

role of these social structures

predators

tank and

reflection.

The rate of success of catching not methodically

shrimps at the first attempt

(1968): 81% in a white

values

prey, plays a definite

the two types of capture.

sizes of predator

For the

and prey appear to be less im-

of the two types of capture

are more equally

19

attempts by

jump

n n,nn fly

n Il. I

attempts

by tentacles 1

I

2

I

3

I

Fig.3. Changing the jumping strategy the crab: an individual profile.

4

I

5

I

6

I weeks

as a result of a quick displacement

of

% rate of jump

60

._

57.6 * 0

20

I

24.4 0

253

16.9

12

3

4

a

weeks

Fig.4. Increasing the jump strategy as a result of ablation tips. * : Result obtained on only four animals.

of the tentacle

20 divided.

Therefore,

factors relating

it is necessary

to take into account

to the prey or to the predator.

viour of individuals cular strategies

over some weeks

the existence

An examination

shows that individuals

of other

of the beha-

do not have parti-

and use the two strategies.

The part of previous

experience

the capture of crabs mechanically

is well demonstrated

displaced.

in the experiment

In spite of a quotient

on

Rt0.3

quickly noted numerous

attempts

the cuttlefish

to the "jump" with a change in the speed of its execu-

returns

tion (Chichery,

to catch the prey with the tentacles.

we

in preparation).

The visual perception

ment of the prey induced by the apparatus resorts

to ejecting

is well known lopods

(Young,

how flexible

1965; Messenger,

the programming

the different individual

diagrams

the method normally are particularly

used for fast prey. It

well developed

1973), and so it is interesting

of the attack

is. This individual the relative

in Cepha-

to see here experience

disparity

and

of the

(cf. Fig.2.).

obtained

support earlier

of the quick displace-

may also explain why the cuttlefish

levels of hunger might explain

The results

tacles"

its tentacles,

that memory processes

Then,

after ablation

interpretations.

induce progressively

of the extremities

The repeated

failures

of the tentacles

of the strategy

more attempts with the alternative

"ten-

"jump". Howe-

ver, two results must be emphasized: - Even after very many tries the cuttlefish attempts

to eject the tentacles.

- The rate of successful inferior

still show very numerous

compared

of tentacles

captures

of shrimps by the "jump" method

on the one hand to those usually

obtained

and on the other hand to those of the catches of crabs. We must

stress that these young cuttlefishes

(about 8 months)

the crabs by jumping on them. The last experimental (considering

is very

by the ejection

the persistence

of the tentacles

of the technique

is particularly

well adapted

are quite able to catch

series shows very well

"tentacles") to catching

that the ejection rapidly escaping

prey. We must stress that the shrimps with their giant fibres and the fishes with the Mauthner slower

cells are able to escape very quickly.

(200-1OOOms)

than the ejection

1968) might not be adapted failures noted In summary

of tentacles

to catching

The "jump" which

(<30ms,

is

cf. Messenger,

such quick prey; hence the numerous

in the last series of experiments. this work shows the importance

of the ratio between

predator

and prey size in the choice of the type of attack on crabs, and presents dence that the type of attack employed riments have also shown decisively always used to capture

may change with experience.

that the ejection

small fast prey.

of tentacles

evi-

Our expeis nearly

21

ACKNOWLEDGEMENTS We are grateful to Dr. J.B. Messenger (Department of Zoology, University of Sheffield, Sheffield, Great Britain) for his critical review of the manuscript.

REFERENCES Boulet, P.C., 1964. La predation chez la Seiche. Actualites marines, 8: 26-32. Chichery, R., 1980. Etude du comportement moteur de la Seiche, Sepia zfficinalis L. Approches neurophysiologique et neuropharmacologique. Th6s.e Doctorat Sci. nat., Universite de Caen. Feral, J.P., 1978. La regeneration des bras de la Seiche Sepia officinalis L. I - Etude morphologique. Cahiers de Biologie marine, 19: 355-361. Feral, J.P., 1979. La regeneration des bras de la Seiche spia officinalis L. II - Etude histologique et cytologique. Cahiers de Biologie marine, -20: 29-42. Messenger, J.B., 1968. The visual attack of the cuttlefish, Sepia officinalis. Anim. Behav., 16: 342-357. Messenger, J.B., 373. Learning in the cuttlefish, Sepia. Anim. Behav., -21: 801-826. Messenger, J.B., 1977. Prey-capture and learning in the cuttlefish, Sepia. In: The Biology of Cephalopods. Symp. 2001. Sot. Lond., 38: 347-376. by Neill, S.R. and McCullen, J.M., 1974. Experiments on whetherschooling their prey affects the hunting behaviour of Cephalopods and fish predators. J. Zool. Lond., 172: 549-569. B l'etude experimentale de la croissance et Richard, A., 1971. Contribxon de la maturation sexuelle de Sepia officinalis L. These Doctorat Sci. nat., Universite de Lille. Wilson, D.P., 1946. A note on the capture of prey by Sepia officinalis L. J. Mar. Biol. Ass. U.K., 26: 421-425. of a memory system. Proc. Roy. Sot., Young, J.Z., 1965. The organiztion B -163: 285-320.