--
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This paper riot to be eited ..\ithout referenee to the authors
International Council for
the Exploitation of the Sea
..
Shellfish cOmrIUttee
C.l\L 19951K:40 Ref: F
The Azorean squid L'!lig() jorbesi (Cephalopoda: Loliginidae) m
captivity: reproductive behaviour
Filipe M. Porteiro. Joao M. Gon~ves. Frooerieo Carcligos & Helen R.
MartinS
Departarnento de Oceanognma e PescaS da Universidade dos A~ores. PT 9900 Hortl
Abstract
Reproductive beha\iour of L. förbesi in captivity iS described. Male·riiate agonistic internctions
increaS'ed when a female is introduced between triaIes. Mate pair formation is quickly established with
acorisequent hier.irchy of dominance bet\veen males. During such beha\iour the male coristrained the
female againstthe tank wall. isolating her from theother maIe present Exchange of the partnerS
in~olved in courtship was fe,,, times observed. A chromatic pattern associated with courtship was
diSi>layed continuously by the dominant male. Thfee females laid eggs on the tank PVC walls. One of
them SUI'\ived 12 days after spanning. Tbe reproductive orgails of post·spa,..ning feInales bad mature.
m:uuring :md immature oOc)1e. Spa,..ning b7haviour :ind :i briefdescnption of the si:iaWn is presented.
An update ofthe components ofbeba..iour is provided.
Introduction
Squid ai-e schooIing soeial invene1>cites
..\ith
high developed system' of
comniimicacion :uid camouflage. They ure
able to exhibit many ritualised beha\icumI
patterns tbat can be described as a
coinbinatiori of chromatic. postumI and
mcvement componerits (Packard &
Sanders, 1971; Packard and Hcehberg,
1977;
Haßlon.
1982).
Chromatic
componentS, rriade up by seleetive nervous
e~eiciticn of units cf chromatcphores and
iridophores (P~ekard. 1982) are the eore of
the
visual
commumcation
amcng
cephalopods. Body patterns are associated
with specific behaviour as feedirig,
predator avoidarice. courtship. ete. and
they can alter during the omogeny of one
spccies (e.g.• Hanlcn & Woltering, 1989).
The accurate descripticn of the eomponents
of pattemmg is required for several
biologieal approaehes as quantitative
ethOIcgy. b~haviotimI taxcnomy and
phylogem:tic analysis (see Hanlcn. 1988
a
and Hanlon et. al. 1994). However, the
description of tbe behaviour is somewhat
complicate due .to the multiplicity arid
ambivalence of the sigrials combined with
the dependence cf their expression on
extemaJ. environment (Moynihan &
Rodaniche. 1982). Obviously, observations
in the field ure the ideal when this is
possible. but when squid gi-ounds ure
unkno\\n or not accessible. studies in
capti\;ty are an alt~n1ative. Also. the
proximity to the squid and the confuted
space can turn some behavioural patterns
conpiscous.
.
Oetopods and sepiids were the cephalopods
preferred for beha\ioural sriidies, both in
situ and in labor.ltory. Nevertheless, the
behaviours of some myopsid were
extensively investigated (in field e.g.•
:\Ioymhan & Rodaniche. 1982~ Sauer &
Srßale. 1993: Hanlon er al. 1994 and iIi
capcivity e.g.. Hanlon 1982, Anlold, 1990).
Lvligo forhesi is the oilly loliginid species '.
lhing arourid the Azores islands. It inhabits
inshore water from the surfuce. ai night.
--
-
--
----
.,
·"
dO\\n to 400 meters during da)time. A
daylight squid jigging fishery was kno\\n
sinee the last eentury (Drouet, 1858).
Mainly maturing and mature squid are
caught (Martins, 1982). However, the
spa\\ning grounds of this population and
spa\\ning migrations bave never been
deteeted. Naturallaid eggs have been found
only once (porteiro & Martins, 1982) in
the Azares.
The Azorean L. forbesi proved to be
effieient for culture e:<:perirnents, at least
for maintenance and reanng (sensus
Boletzky & Hanlon, 1983). Squid embryos
(laid by captive females) were transported
to Marine Biomedical Institute, Texas arid
two successful reanng. trials were carried"
out (Forsythe et al., 1989; Hanlon et al.,
1989). During maintenance preliminary
studies of adult squid behaviour" were
condueted (Porteiro et al., 1990). There,
17 chromatic, 6 poStural and j movement
components were described as weil as
feeding arid agonistic behaViour. Ho\vever,
reproductive behaviour was not extensively
emphasised.
Presently, we bave a closed sea-water
system designed specifically for squid
culture (see Gon~ves et al., 1995) which
allow to maintairi simultrineously' a
signifieant number oflarge squid.
In this study we present additional
qualitative information of the behaviour of
captive squid mainly related with courtship
and spa\\nmg.
recorded daily and several ..vater
parameters controlled regularly (see
Gon~ves et al. 1995, for a complete
description ofthe system).
The number of squid inside eaeh tank was
variable (1 to 7) and different combinations
of sexes were mamtained (e.g., 1 female
and two males, 2 feIriaIe and 2 lna1es, 1
female"and 4 males, etc.). Individual squid
were· distinguished thrOught natural skin
rilarks cr artificial tags
Observations v."ere performed during day
time, from the top of the tanks and laSted
from 10 minutes to ca. 2 haurs. While
observing, the black plastic cover was
partially elevated and the exterior light held
at minimum to avoid major disturbance.
The water influx was, also, suspended.
Squid were fed once or twice a day.
\\-:lS
Trachurus picturatus, Pagellus bogaraveo
and Scoinber japonicus were the main food
items. Feeding took place in the marning
and atnoon.
The hierarchical oi-ganisation of bemiviouf
as described by PackaCd & Sanders (1971),
Packard & Hochberg (1977), and Hanlon
(1982) arid the behavioUraI components
terminology previously established for"
loliginids (Hanlon, 1982, 1988; Porteiro et
aL, 1990;SaueretaL~ 1992, 1993;Hanlon
al., 1994) were adoptoo.
er
Results
Ari
Material aod :\'Iethods
Several squid were rriainciined during t\Vo
sets of experiments (16 Oetober to 27
December 1994 and 2 February to 18
April). The squid size ranged was between
275 to 639
DML. Squid were eaught
by jigging, tr.l.nsported ashore ::md kept in a
elose sea water system. Basically this
arrangement consist af three circular t:lnks
(3.6 m 0 arid 0.90
high: ca 80001 of
natural sea \\-ater) painted with verrical
dark stripes on the \\-alls and ca. ..lern of
gravel an bartom Light was kept at dim
during all the experiments. temperature
mm
m
average of 7.6 squid were maintained
simultaneously in captiviiy and the avernge
survival waS 17.7 days (up to 46 days) in
the first experiment. During the second
trial the average survival \\-:lS longer (22.8
days) niainly due to the preferential
maintenance of mature, maturing squid
and sexual segregation in same tanks.
Behaviour
.Wale-male ü1teractions
~[ale-male
agamsttc be.'taviour was
observed many times. In the tanks a
hierarchy af domirumce was eSt:lblished.
~crmaIly, the weal<er male die with major
damaged areas after few d::i.ys in captivity
2
1
and successively all squid but the dominant
male die. The most obvious damaged areas
were usually the same: the latero anterior
part of the mantle, funnel and head.
Injuries on ehe fins and on ehe posterior tip
of mantle were caused by abrasion and
collision on the tank walls, respeetively.
Lesions on the anterior dorsal tip of the
mantle were commonly observed but eould
not be related with any type of eontaec.
Agonistie interactions oceured between
male of markedly different sizes are
maintained together and between males of
the same size or of different size when
competing for reproductive dominanee,.
Fig. 1 - Dorsal view of counship body pattern of adult male squid Loligo forbesi in capnvlty.
Composed by the chromatie components, White arm tip. Accentuated tesris and .rlccentuaced digestive
gland.
All the movement eomponents preVlous
deseribed for the speeies (Parallel
posirioning, Fin hearing, Forward rosh,
Chase and Flee) were observed. Some
variation on Forward rosh was reeorded:
the aggressor eharges ehe subordinate male
by jetting against him the tentacles
resulting often in eontaer. TItis component
was preeeded by Chase (by the dominant
male) and culminate with Flee by th~
subordinate male). All dark is the common
body pattern in th se intemctions (Dark
flashing was ::Uso observed several times).
Perpendic:liar
positiomng,
a
new
movement componenr.. was recorded dunng
low stress situations. TItis is characterised
by the presence of several males elose
together moving on different vertic::u levels
mainuining between them perpendicular
positions. The chronie chromatlc pattern
was predominantly observed during such
behaviour (Clear. Dorsal scripe).
lvfaie- emale courtshiv behavlOur (mare
paIr/ormanon
Mature male-femaie inter:lctiv~ benaviour
expressed
by
captlve
squid
was
characterised by Pair formation. When a
female was in a tank with males, one of the
latter would shortly afterwards change his
behaviour.
The male exhibits his
dominance isolating the female from the
other male squid. He constrained her
against the tank wall limiting her
'swimming space. A short distance was
maintained continuously between the two
and prolonged fin to fin contaet occurred.
A circular motion around the tank wall was
prevalent. in opposition to the normal
forward backward radial trajectory.
It was always the male who ~nforced ehe
pair jormation behaviour. However, the
preservation of the eouple depends of the
male aptitude to ;lvoid the evasive action of
the female (unhealthy males are unable to
maincain a pair with a hea1th female).
Sometimes
male
sexual
dominance
exchange was observed (i. e.. , the dominant
male is replaced by another). Also, the
dominant male may change his partner
preference (observed when a new female
was introduced in the tank). Most of ehe
pairs were suble for se'/eral days.
Jockeying J.lld Parrymg (sensus Hanlon et
ai. 1994) were observed several tunes and
often culminated in violent male-male
3
agonistic behaviour (see above). Stress also
inereased in the tank also when a male
interfered with the trajeetory of the pair.
Subordinate squid tend to avoid such
................................
..
Figure 2.Top plan of the tank and detail of the area selected by squid to lay eggs (see text).
interactions whieh is diffieult given the
eonfined space ofthe tanks.
The courrship behaviour is characterised
by a specific chromatic pattern. That
pattern is more obvious in the male. At
least, three dorsal chromatic components
are ~xpressed to fonn the Courtship body
pattern (Fig. 1): Accentuated testis,
Accentuated digestive gland and White
arm tips. Strong green iridescence on the
dorsal mantle areas was exhibited. During
all watehing periods the dominant male
frequently showed this pattern (it ean
pt:rsist during a long time). However. it
was more conspieuous when another male
was in the proximity of the pair. The
female display was of a less obvious
chromatic pattern. but also some distinet
components were consistently present (e.g..
Don'al stripe. Ivfantle spots, Dark fin
fine). Whlte arm fips (as in males).
Accentuated
ovary,
Accennlated
nidamental oalands and Asvmmetric
ocular
•
spot (on the male side) were also observed
duling
more
intense
interactions.
As....m metrv of the ehromatic eomponems
w~ 5ho~ (stronger on the adjacent squid
side} by the MO parmers.
Spawning behaviour
Three spawns were laid by captive females
during the period of observation (Tablel.).
All squid initiated spawning during
aftemoon and continued through the night.
Two of the females (Al, B2) that started
egg-Iaying, finished one day 1ater and then
died. One female (B 1) lived for 12 days
after spawning. During that period she ate
4 small meals (average daily feeding rate of
2.1 % against 6.5% before spawning). The
female Al bad paired with a dominant
male (two male squid were in the tank) and
B 1 forrned a stable pair with a sole male in
the tank. The squid 82 were all the time
alone.
Sinee light seemed [0 influence behaviour
of the squid, observations of the spawning
process were gready limited by the dark
condition in the tank. However, some
postural and movement components were
observed. The female approached the egg
mass (previously laid) with eonie arms and
when in contact with them she spiayed the
arm tips and attached a new str.lI1d (Esg
holding). This activity took around _0
seconds or less. During this operation the
squid unduiated the fins vigorously in a
forward movement. The body was kejJt
parallel to the substrarum.
4
..
{
am
Frequently,the female sW
fast to theegg
strands handled them and jetted ,water
violently toward the spa\\n in back",..ard
mo\'ement. This beha\iour Y,as observed
manv tirries. Male also made such
be~viour, but less frequently. ThemaIe
was alwavs swimming elose to the fernale,
showing the courtship body pattern ~ith
high iridescence (Mate guarding) .
At least the first strands laid by the squid
were fixed elose to the surfaee on the tank
wallover a PVC liner, (fig.2). The squid
B2 iaid eggs on the same place where the
prrnous strandS were laid by BI. Water
flow WaS at a maxm'l1.uu at spa\\n location
(oxrsen level \Vas, elose to saturation
unifonnly in the tmks). Later some
capsures were disperse and others were in a
burich, throughout the gcivel bottom. Few
of thern were cemented on the basalt
gravel. It was not cIear to wh::ii extent these
strings v,'ere displaced from the PVC wall
by the jenmg and manipulation behaviour
of the female.
Spawn
The spa\\ns were eomposed by well-sh:iped
egg strands (normal strands) and by a few
with redueed dimensions and with fewer
eggs or none (balloon Strands). Fourtythree common strands were laid by both
squid Al arid BI. The squid B2 lay
significandy less (15) of whieh 50% of
them were empty. The remairiderS were
shorter and bad fe\v eggs thanthose from
the other. squid. The norIDal sti':inds. bad
bet\~,een 25 and 90 eggs and the percentage
of fertilisation was 64%.
balloon
strands bad a lower percent:age of
fertilisation.
Reeentlv fixed strings, (during the fust 2-3
houes), • were more siretchilble, thin and
long, but afterwards they decrease in size,
and the gelatinous ninics became more
finii
The.
Table 1. Refereneeof L. jorhesi female squid timt spa,\n in captivity. DML, i - I?0rsai man~e i~gth
when captured; BW i-Total body weight when captured; OVW f - Ov:uy welght after spawnmg;
ODPW r- Proximal oviduet weighl after spawning.
.Ref.
Date of
capture
Days
captive
before
Days fram DMLi
sp'a\Vnmg , (nun)
to dead
B\Vi
OVW
(g)
f
f
(g)
(g)
ODPW
spawnimz.
AI
BI
B2
05.11.94
16
09.02.95
03.03.95
8
7
Reproducti....e organs
/emales
0/
1
12
1
31
330
993.0
279
835.0
607.9
33.7
16.8
55.4
56.9
0,8
6.0
post-spawning
Post-spa"ning ferilales still had ~ture,
maturing and immature eggs m the
proxinial oviduct and ovary (see Tabl~ 1)~
All had rnatcd but fe,v sperm were in the
bursa colmlatr:x. The ovary of the fe=nale
BZ lud a high quantity of ocC:.1e c!C:,~ to
rnaturation but less few eggs in the
oviducJ.1 comple::.. The ferI1aIe BI bad i
few hundredS mature eggs in the oviduct
and ooc:-te in v::l.nous devdcpm.:nul .rt::l.ges
in the ovar)'.
Discussion
Agonistic behaviour be:'veen males ~~ ~e
main reason for mortallty both by colliSlon
and abrasion on the tank walls or by direet
charge. This behaviour \vas.obs,erved ,in
several species kept in captiVlty but bodily
contact has oDly been rarely observed (see
Arnold. 1990; Hanlon et al. 1983).
Prcbablv. the coniined space in the tanks
ccmbin~d \\;th the big size ?f the squid
:l2!!1"::l.v::l.te .menistie interactiens ccmpared
t;-animals in
the wild. In the wild the
5
,
,
subordinate squid can run away before
being touched during an attack. These
interactions are more evident when
different sizes male squid are mairitained
together or when males compete for
females
(see Hanlon,
1990). No
cannibalism was recorded probably due to
small differences bet\veen the size of
captive squid.
Pair formation 'was observed for the firsi
time for L. forbesi. HO\vever, it has been
described for several other squid held in
captivity (e.g.• L opaleseens by Hurley,
1977; L. pealei by Amold, 1990; L (D.)
plei by Hanlon, 1981) as weIl as in the
natural
spa\\ning
grounds
(e.g.•
Sepioteuthis sepioidea by Moynihan &
RodaIiiche, 1982; L. v. reynaudii by Sauer
& Smale, 1993). During our observations,
captive pairs seem 10 be quite stable and
male dominant, except when a weak ll1a1e
is not abte to contain the evaSive behaviour
of the female. Tbe latter behaviour can
support the assumption by Hanlon (1994)
that female choice and evaluation of the
partner is an iritPOrtaIlt reproductive
str.:i.tegy bet\veen squid. However, llla1e
dominance has been described by several
authors based on the displacenierit of ari
intruder male by the paired male and the
maintenance of the originill pair. Pair
stability on field is not kno\\n but it
probably split during riight (see Sauer &
Smale. 1993). The long duration of the
pairs obsenoed in this stUdy can be an
arrifice due to thecaptive condition.
Although, we did not observe ccpulation,
we know that sperm is stored only in the
bursa copulatnx (Porteiro & Martins.
1994) which indicate that just head-to-head
mating occurs. Very little sperm was found
in the bursa copularnx of post-spa\Vnmg
females. This suggests that the amount of
sperm in this organ is not enough for
fertilisation if a prolonged spa\\ning period
occur or if one intensive sp:mning is l1lade.
We :lgree with HanIcn (1994) that squid
reprcductive tactics would be better
understood if anaIysed in a sperin
competition contest. The existence of small
mature r"sneaker'') males \"ithin this
spec:es (Martins. 1982: Boyle & Pierce.
as
1994)
weIl as Jockey;ng and Parrying
movernent componenis cari indicate an
alternative reproduCtive str3.tegy, aS
observed for L v. reyruludii (Hanlon et al.
1994). The meclUiriiSiris of sperm
competition are not lciIö,,,n for the majority
of cephalopodS.
Arnold (1990) suggest thai L. pealei pair
formation and consequently reproductive
doininaßce by the Iriale. is established by a
visUa1 Stimulus (i.e.•. the presenee of egg
masses m the aquarium). Hurley (1977)
found some evidence that egg deposition is
visually Stirriulated by the preSence of
preVious spa\Vns but he could not ioelate the
male reproduCtive dominance 10 presence
of eggs. In our case pair formation
occurred without any visua! externaI
stizllulus,
it
eStablished
soon as a
feIriale was mtrOduced among ritales.
Male chromatie eomponents related 10
reprOductive dOßUnance behaviour have not
been deseribed previously for this species.
White arm tips cOuld be associated 10 the
importance .of the arms in rrlating and egg
mass h3ndling. The Accentuated testis is a
component very common arnong 10liginidS
and interpreted as a sign of mature
coridition. Tbe component Accentuated
digestive gland is described hen: for the
tirst time alld it could be a sign related to
theeondition of the squid. since this organ
is used as storage resen'e. Similaicourtship body pattern is not found iri the
literatUre.
Is accepted that acute body patterns
(expressed during few seeondS or minutes)
are more useful for behavioural ta.'conomy
and phylogenetie approaches tfcin chrome
patterns (whieh can be displa):ed during
lang periods). However. courtship body
pattern (as, a chrome pattern) is
stereotyped, species-specific and orie whieh
proVide more information about the species
chafaeteristies (Hanlon, 1988). It would
have ethological interest to compare the
behaviour between Azorean and Europe::m
populations of L. for~esi smce they are
genetically separated (Brierley et al. 1993;
Pierce et aI.• 1994) and body patterns c::m
be used probably as a eharaeter which
shows variations at the population or sub-
as was
as
6
•
.
(
•
species level (Hanlon, 1988; Hanlon et al.
1994). One example of different
reproduetive behaviour benveen these nvo
populations is show in the nurnber of eggs
within each str:md. Lurn-Kong (1993),
reported a mean vaIue of 109 eggs per
string against less than 90 found by us in
several spa\'fns. Also, the percenmge of
mated immature females in Azores seems
to be higher than L. forbesi from elsewhere
(Porteiro & Martins, 1994). In order to
provide basic information for further
ethologic::u companson it is presented an
update of body components recorded for
the Azorean population of L. forbesi
(Table 3).
Table 3. Update of the behavioural components recorded for Lo/igo forbesi (based on Hanlon, 1988;
Poneiro et al., 1990; this scudy; and unpublish observations).
Chromatic components:
Dark components:
•
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
'J,,: All
dark
Later::l1 mantle streaks
Ring
Fin and mantle spots
Infraocular spot
Dark fust or third arms
Darkarms
Mid-ventr.ll ridge
Later::l1 mantle stripe
Dark fin line
Mantle margin stripe
Dorsal stripe
Shaded eye
Postur::l1 components:
1.
2.
...
.J.
4.
5.
6.
7.
3.
Two raised arms
DO\mward curling
Extended tentac!es
Splayed arms
Ellipsoidal eyes
Bottom sitting
Egg holding
Perpendicular positioning
Fresh laid egg strings were sirnilar to those
described for L. pealei by Roper (1965)
(leng :md soft). The duration ef softness ef
the string tunics can presumably be rehlted
\"ith the fertilisation process. Tnis
me::..:..:mism remains co be studied.
Variation in the way that squid make their
sp:l\\ning bed is knC\\n (see Vechicne.
1983: Sauer er al. 1992). From our
Light components:
1.
2.
3.
4.
5.
6.
7.
8.
9.
Clear
Dorsal mantle eollar iridophores
Dorsal iridophores splotches
Gold irideseent sheen
Aceentuated testis
Accentuated nidamental gland
Accentuated ovary
Accentuated digestive gIand
White tip ofarms
Movement eomponents
1.
2.
...
~.
4.
5.
6.
7.
3.
9.
Par::l1lel positioning
Fin beating
Forward rush
Chase
Flee
Inking
Jetting
Jocking and Parrymg
Mate guarding
observations it is difficult to say how this
species makes their spa\'.ns in nature. The
loeation where the squid fi.'ced their eggs in
the tanks is probably related to the water
current or to the existenee of a PVC fold
(see Fig.l). The later supposition. if
correct. can suggest that cre"lices or smaIl
caves are used fcr spa\ming as discussed
before by Porteiro & ~[artins (1992). L.
7
vulgaris in Madeira spa\..n in such bottom
1--
structures (p. Winz. pers. comm.)
Death of captive squid after spa\..ning haS
been recorded by several sttidies and
accepted as a natural behaviour. The
presence of mature, maturing and
immature eggs in the reproduetive system
of post-spa\'.ning females and the survival
of one female for several days (12) after
egg- laying could support the assumption
of a prolonged intermittent spa\..ning
before exfuluStion. Several questions arise
when this problem is examined: v,'hy does
the squid die befoIe all the eggs are laid? is
this ecologically justified? have the "üd
femaIe the same behaviour or is it
influenced. by captive condition? does she
need high food input after spa\..ning one
batch of eggs? This should be investigated
carefully to 6stablish the reproductive
behaviour ofthis loliginid.
a
AcknowledgementS
This work could not be done ",ithout the assistance of Paulo Martins. Thanks to Ricardo S.
Santos, to commentS and revision of the manuscript.
.
This ?''ork was funded by the European Commission within the frame of EC research
programme in the Agriculture and Fisheries seetor(AIR. Contract No. AIR l-CT92-573). We
also thank to the Region::U. Secretariat of Agriculture and Fisheries of the Azores Government
who gave us permission to use their installations at Porto Pim beach (Rorta) and supported its
running costs.
References
Arnold. I. M 1990. Squid mating beruivior. Pp 65-75, in: Squid as Experimental Animals, D.L.
Gilbert, W. I. Adelman Ir &. I. M AInold (Eds). New York. Plenum Press, 516pp
Brierley, A. S. ,. 1. P. Thorpe. M. R.. Clarke &. H. R. Martins, 1993. A preliminary biochemic:ll
genetic investigation of population stnleture of Loligo förbesi Steenstrup. 1856 frOm British Isles
'and the Azores. Pp, 61-69, in: Recent Advances in Cephalopod Fisheries Biology, T. Okutani.
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