Marine Biology (1997) 129: 113±122
Ó Springer-Verlag 1997
R. Villanueva á M. Segonzac á A. Guerra
Locomotion modes of deep-sea cirrate octopods (Cephalopoda) based
on observations from video recordings on the Mid-Atlantic Ridge
Received: 27 November 1996 / Accepted: 9 December 1996
Abstract The behaviour of cirrate octopods of the
genera Cirroteuthis and Grimpoteuthis in their natural
habitat was studied using video recordings. Sequences
were ®lmed during the French cruise ``Faranaut'', from
the manned submersible ``Nautile'' at depths between
2702 and 4527 m, in two zones in the Fifteen-Twenty
Fracture Zone on the Mid-Atlantic Ridge. Four di€erent modes of active locomotion, namely crawling, takeo€, ®n-swimming, and pumping, and one apparently
passive mode of locomotion, umbrella-style drifting,
were observed. Jet-propulsion, a characteristic mode of
locomotion typically employed by cephalopods, was not
observed in the cirrate octopods ®lmed, although
breathing movements of the mantle to aerate the gills
were assumed to generate some slight propulsion
through the funnel. Fin-swimming was the mode of active locomotion most frequently observed. Neutral
buoyancy was con®rmed in one individual after capture.
This buoyancy enables passive drifting in the umbrellastyle attitude observed in Cirroteuthis spp., possibly
using near-bottom ocean currents. Pumping, a mode of
slow locomotion generated by peristaltic waves in the
primary and intermediate webs, also observed in Cirroteuthis sp., is described here for the ®rst time. The
take-o€ mode of locomotion, a sudden, single contraction of the brachial crown and web, is also described; it
was always followed by ®n-swimming. No medusoid
swimming of the type previously described for
opisthoteuthid cirrates was observed. A ¯ight response
Communicated by A. RodrõÂ guez, Puerto Real
R. Villanueva (&)
Institut de CieÁncies del Mar (CSIC), Paseo Juan de BorboÂn s/n,
E-08039 Barcelona, Spain
M. Segonzac
IFREMER/CENTOB, BP 70, F-29280 Plouzane Cedex,
France
A. Guerra
Instituto de Investigaciones Marinas (CSIC), Eduardo Cabello 6,
E-36208 Vigo, Spain
to the approach of or contact with a strange object, i.e.
the submersible, using the crawling, take-o€, or ®nswimming modes was observed. A ballooning response
was observed in a high-stress situation when a C. magna
individual was captured.
Introduction
In situ studies of animal behaviour in deep-sea habitats
are extremely dicult to carry out, in large measure
because of hostile environmental conditions such as
pressure and darkness. In recent years, the development
of new technologies such as manned submersibles has
opened up new horizons for the observation of the organisms dwelling in these regions. These organisms include deep-sea octopuses of the order Cirroctopoda
(Young 1989), commonly known as cirrate octopods.
This is one of the least understood groups of cephalopods, partly because its members tend to be highly
adapted to deep-sea environments. Cirrate octopods
include some of the largest invertebrate organisms in the
bathyal and abyssal megafauna (Gage and Tyler 1991),
and range from 10 to 130 cm in total length (Roper and
Brundage 1972; Nesis 1987; Guerra et al. 1997); they
occur down to depths of 7279 m in the hadal zone
(Aldred et al. 1983; Voss 1988). The anatomy (Young
1977, 1989; Aldred et al. 1983), feeding (Villanueva and
Guerra 1991), and reproductive strategies (Boletzky
1982; Villanueva 1992a) of this group are clearly distinct
from those of other groups of cephalopods. Cirrate
octopods are gelatinous in consistency, with soft, watery
¯esh and neutral buoyancy, and tend to be particularly
susceptible to damage by conventional methods of
capture such as trawl nets; very few specimens in reference collections are in good condition. As a consequence
mainly of the paucity of specimens and the poor condition of those specimens that are available, the systematics of this group is unsettled (Nesis 1987; Voss
1988; Hochberg et al. 1992). The capture of cirrate
octopods by submersibles has recently provided speci-
114
mens in excellent condition (Vecchione and Roper
1991), and pioneering studies based on serial photographs have furnished the ®rst information on the behaviour of cirrate octopods in their natural environment
(Jahn 1971; Roper and Brundage 1972; Pearcy and Beal
1973). In recent years, video recordings from manned
submersibles in the bathyal zone (Vecchione and Roper
1991; Boletzky et al. 1992; Roux 1994; Vecchione and
Young 1997) have made it possible to perform studies
on the behaviour of these cephalopods that would
probably not have been feasible using any other procedures ± partly because cephalopods are highly mobile.
Video recordings made by remotely operated vehicles
(ROVs) capable of moving along the bottom of the
continental shelf and slope (Vecchione and Gaston 1985;
Vecchione 1988; Felley and Vecchione 1995) and manned submersibles (Moiseev 1991) have been used for in
situ investigations into the behaviour of other groups of
cephalopods. However, a recent study has demonstrated
the impact of ROVs on the behaviour of the American
lobster Homarus americanus (Spanier et al. 1994). Similarly, the presence of manned submersibles can be assumed to a€ect the behaviour of species in the abyssal
zone. Local conditions may vary as a result of the
spotlights, sounds, and turbulence of the submersible as
well as the physical presence of a large object. Nevertheless, video recordings, photographs, and direct observations using manned submersibles are the best
means available to date for in situ research on the behaviour of typically bathyal and abyssal animals such as
cirrate octopods. Earlier studies on the behaviour of
other groups of bathyal benthic organisms on the MidAtlantic Ridge demonstrated the usefulness of manned
submersibles (Segonzac et al. 1993). The present study
reports the observations of the behaviour of cirrate
octopods based on video recordings and photographs
made from the manned submersible ``Nautile'' in the
bathyal and abyssal zones on the Mid-Atlantic Ridge in
the North Atlantic Ocean.
Materials and methods
IFREMER conducted the ``Faranaut'' geological research cruise,
on board the research vessel ``L'Atalante'', equipped with the
manned submersible ``Nautile'', from 15 March to 15 April 1992.
The main objectives of the cruise were to investigate hydrothermal
events associated with ultrabasic rocks and the geological structure
at two junctions in the Fifteen-Twenty Fracture Zone on the MidAtlantic Ridge located at 15°20¢N. In all, 23 dives were carried out
in adjacent zones (A and B; Table 1, Fig. 1). The average distance
travelled was '4 km per dive.
Zone A is a basalt rise located in the median rift valley in the
ridge south of the junction with the axial valley at 15°05'N,
45°20'W at depths between 2450 and 4668 m. Nine dives (FR01 to
FR09) were carried out in that zone. Zone B comprises the western
and eastern walls of the median valley north of the junction with
the axial valley at 15°30¢N, 46°35¢W at depths between 2630 and
4638 m. Fourteen dives (FR10 to FR23) were carried out in that
zone.
The general topography in both zones constitutes a succession
of rising plains covered by globigerina ooze in a series of terraces
Table 1 Twenty-three dives by manned submersible ``Nautile'' on
``Faranaut'' cruise to Mid-Atlantic Ridge in North Atlantic Ocean
in March and April 1992
Dive
Zone
Starting position
Depth (m)
Date
FR01
FR02
FR03
FR04
FR05
FR06
FR07
FR08
FR09
FR10
FR11
FR12
FR13
FR14
FR15
FR16
FR17
FR18
FR19
FR20
FR21
FR22
FR23
A
A
A
A
A
A
A
A
A
B
B
B
B
B
B
B
B
B
B
B
B
B
B
15°04.52¢N;
15°06.18¢N;
15°04.27¢N;
15°04.57¢N;
15°07.43¢N;
15°05.26¢N;
15°01.42¢N;
15°07.07¢N;
15°03.65¢N;
15°35.33¢N;
15°34.85¢N;
15°37.14¢N;
15°28.56¢N;
15°28.75¢N;
15°26.28¢N;
15°29.00¢N;
15°30.74¢N;
15°30.85¢N;
15°34.12¢N;
15°32.86¢N;
15°37.00¢N;
15°30.57¢N;
15°36.54¢N;
2615±2450
3389±2518
3685±2500
2855±2585
4087±2780
2899±2587
4022±3360
4668±3416
3870±3590
3947±3375
4638±3900
3990±3110
3967±2935
3570±2630
4597±3330
4431±3300
3720±3028
4633±3900
3452±3148
4013±3112
4282±3238
3629±3354
4211±3477
19
20
21
22
23
24
25
26
27
28
29
30
31
01
02
03
04
05
06
07
08
09
10
44°58.52¢W
44°56.29¢W
44°56.64¢W
44°57.63¢W
44°57.03¢W
44°57.62¢W
44°55.50¢W
44°50.64¢W
44°55.95¢W
46°45.06¢W
46°37.10¢W
46°32.80¢W
46°34.15¢W
46°33.56¢W
46°36.07¢W
46°39.60¢W
46°40¢74¢W
46°38.24¢W
46°41.74¢W
46°41.22¢W
46°39.97¢W
46°40.77¢W
46°35.29¢W
Mar
Mar
Mar
Mar
Mar
Mar
Mar
Mar
Mar
Mar
Mar
Mar
Mar
Apr
Apr
Apr
Apr
Apr
Apr
Apr
Apr
Apr
Apr
separated by dike-like structures from the valley to the summit.
Accumulations of pteropod shells and molluscan Calyptogena sp.
valve fragments were observed in some areas, where megafauna
consisting of sponges (Hyalonema spp.), pennatulaceans (Umbellula
spp.), octocorallia (Chrysogorgia spp.), asteroids (Brisingidae),
holothurians (Enypniastes spp., Benthodytes spp., and Psychropotes
spp); decapod crustaceans (Polycheles spp. and Munidopsis spp.),
and shrimps (Nematocarcinus spp. and Plesiopenaeus spp.) were
collected. Fish of the families Moridae, Halosauridae, Ipnopidae,
and Bythitidae were also observed and identi®ed from the video
sequences. Water temperature was between 2 and 3 °C.
The submersible ``Nautile'' is equipped with two video cameras
for recording images, one ®xed-focus 15-mm lens tri-CCD camera,
and an adjustable-focus pan and tilt camera with a 6 ´ 48 mm
zoom lens. The date, depth, distance from bottom, and dive
number were printed on the VHS ®lm, and some sequences were
taken from the U-matic ®lm. One of the authors (MS) participated
in the cruise and selected the video sequences. Cirrate octopods
appeared in a total of 27 min 04 s of the video recordings. In addition, 68 still photographs were also taken of those individuals
that had been ®lmed. Individual behaviour was studied in the
laboratory by means of careful examination of the video recordings, photographs, and direct observations made from the submersible. Terminology previously de®ned and illustrated in the
literature has been used to describe the behaviour of the cirrates
whenever possible, e.g. umbrella-style drifting (Roper and Brundage 1972), ®n-swimming (Aldred et al. 1983) and ballooningresponse (Boletzky et al. 1992). New terminology has been coined
when necessary.
Results
Systematic identi®cation posed a problem. Speci®c
systematic characters of cirrate octopods have been
based chie¯y on internal structures (shell, genital apparatus, gills), along with some external features (intermediate web, number and position of enlarged
115
Fig. 1 Geographic location of
Zones A and B, the study area
where dives by manned submersible ``Nautile'' on ``Faranaut'' Cruise were carried out
(F.Z. fracture zone on MidAtlantic Ridge)
suckers, cirrus length, eyes). These characters were not
distinguishable for most individuals ®lmed, which all
had an elongate body, prominent head and eyes, long
arms and ®ns and (when observed) narrow funnel and
long cirri. The cirrates observed did not include the
genera Cirrothauma and Opisthoteuthis (since all the
individuals recorded had well-developed eyes and
elongate body), and the typical ``bell-like'' posture of
the genus Stauroteuthis was not observed (Vecchione
and Young 1997). The individuals observed were tentatively classi®ed as Cirroteuthis spp. (Individuals Nos.
1, 2, 3, and 10) and Grimpoteuthis spp. (Individuals
Nos. 4, 6, 8 and 9, see subsection ``Individuals observed'' below). One individual observed (No. 5) was
captured and identi®ed as Cirroteuthis magna Hoyle
(Guerra et al. 1997).
Cirrates were ®lmed or observed on 8 of the 23 dives
completed. No cephalopods belonging to any other
group were recorded. In all, 10 individuals were observed. When the cirrates were surprised (at the start of
®lming), they were resting on the bottom or swimming at
a distance of <8 m from the bottom. They were observed over very ®ne globigerina ooze, and in one case
an individual was observed 1 m above a lava pillow
(Individual No. 10, see subsection ``Individuals observed'' below). Using the methods described, it was not
possible to estimate either densities or swimming speed
in linear units of distance. The videotapes revealed a
variety of di€erent attitudes and behaviours, some not
previously described.
Attitudes and modes of locomotion observed
Bottom-resting
This was observed in four Grimpoteuthis spp. individuals
(Nos. 4, 6, 8, and 9; Figs. 2a, 3a). They were surprised
while apparently resting with their oral surface on the
bottom. Their mantles were erect and pointing backwards at a slight angle. The arms and web were outspread, with the distal ends curved inwards towards the
oral surface. Fins were extended parallel to the bottom.
Eyes were open. When bu€eted by turbulence from the
submersible, they used their ®ns to hold themselves
steady and in their original position.
Crawling
Crawling was observed in one Grimpoteuthis sp. individual (No. 4; Figs. 2b,c; 3b±e), starting from an attitude
of bottom-resting. Motion was backwards, away from
the disturbance caused by the submersible's presence. At
®rst the cirrate crawled away very slowly, with all arms
extended; it was not observed to bear its weight preferentially on any of the arms. On gaining speed, it supported itself mainly on its ventral and ventrolateral
arms, with the dorsal and dorsolateral arms pulled in at
each stroke of the former. Movement of the right and
left arms during the more rapid crawling was symmetrical.
116
117
Fig. 3 Grimpoteuthis sp. Linedrawings based on video recordings of individuals observed in present study,
depicting a bottom-resting;
b±e crawling; f take-o€; g ®nswimming
b
Fig. 2 Cirrate octopods. Photographs of some individuals ®lmed on
Mid-Atlantic Ridge from manned submersible ``Nautile'' during
``Faranaut'' cruise, showing di€erent behaviours and modes of
locomotion (see ``Results ± Attitudes and modes of locomotion
observed'' for detailed explanation). a Grimpoteuthis sp. (Individual
No. 8), surprised in bottom-resting attitude at depth of 3452 m; b, c
Grimpoteuthis sp. (Individual No. 4) crawling at depth of 3361 m;
d Cirroteuthis sp. (Individual No. 10) surprised while drifting in
umbrella style followed by take-o€ (e) and ®n-swimming (f ) at depth
of 3534 m; g±i, Grimpoteuthis sp. (Individual No. 8) ®n-swimming at
depth of 3452 m; j Cirroteuthis sp. (Individual No. 1) surprised while
umbrella-style drifting and same individual 50 s later near submersible
(k) and displaying long cirri when taking-o€ after touching
submersible (l); m, n same individual (No. 1) swimming by pumping
from umbrella-style position at depth of 2702 m; o Cirroteuthis magna
(Individual No. 5) being manoeuvred into sample box at depth of
3351 m, showing ballooning response in three web sectors
Take-o€
This behaviour was observed in Cirroteuthis spp.
(Individuals Nos. 1, 5 and 10; Fig. 2e, l) and Grimpoteuthis spp. (Individuals Nos. 4, 6, 8, 9; Fig. 3f ). In
these individuals, this mode of locomotion always took
the form of a sudden escape reaction in response to the
disturbance generated by the submersible. Take-o€ took
place from the bottom-resting and crawling (in Grimpoteuthis spp.), and from the umbrella-style (in Cirroteuthis spp.) modes. Just before take-o€, the distal tips
of the arms were curved slightly back upon their aboral
surfaces. Take-o€ comprised a single, strong pulsation
generated by contraction of the brachial crown. This
single, rapid pulsation was sometimes accompanied by a
118
forceful stroke of the ®ns. The cirrate pulled its body
into a hydrodynamic fusiform shape to maximize the
abrupt thrust provided by the single pulse. After takeo€, locomotion was continued by ®n-swimming in all
individuals observed to use this behaviour. No second
pulsation, jet-propulsion through the funnel, or contractions of the mantle were observed during such subsequent ®n-swimming.
Umbrella-style drifting
This was observed in two Cirroteuthis spp. individuals
(Nos. 1 and 10; Fig. 2d, j, k). They were surprised in a
posture like an open umbrella, with arms and web outspread, distal ends slightly curved upon the aboral surface. The oral surface was pointed towards the sea
surface or towards the submersible. Cirri were erect.
Fins were folded in against the mantle. No rhythmic
motion was observed during this attitude, and the cirrates remained apparently motionless, drifting, always at
a slow rate. The posture appears to be designed to take
advantage of bottom currents and the cirrates' neutral
buoyancy to enable passive drifting. This behaviour was
®rst described from photographs by Roper and Brundage (1972).
Pumping
Pumping was observed in one Cirroteuthis sp. individual
(No. 1) from a position near the sea ¯oor (Fig. 4) and
from the umbrella-style posture (Fig. 2m, n). The cirrate
was near the bottom, with the mantle erect, the ®ns
folded in against the mantle, and the arms and web
outspread. The cirrate pumped water by means of peristaltic waves running from the proximal interumbrellar
region to the margin of the web, aparently by using
primary and intermediate webs. The waves took from 11
to 13 s to reach the edge of the web, propelling the cirrate
in the opposite direction. Motion was by slow propulsion of the peristaltic waves pushing against the water.
Time between waves was 22 to 24 s. The pumping mode
was also observed from the umbrella-style position, with
the peristaltic waves taking 16 to 18 s to reach the distal
margin of the web. Pumping seems to make use of the
same system of alternate ®lling and expulsion of water
used in the ballooning-response, with the water contained in the interumbrellar cavity being expelled slowly
out through the distal margin of the web by the peristaltic waves, propelling the cirrate in a pumping motion.
Ballooning seems to be take place when the cirrate
contracts the distal edge of the web, retaining the water.
Ballooning-response
Fin-swimming
Fin-swimming was observed in Cirroteuthis spp.
(Individuals Nos. 1, 2, 3, 5, and 10) and Grimpoteuthis
spp. (Individuals Nos. 4 and 8; Figs. 2g±i and 3 g). The
cirrates swam by moving their ®ns a few metres o€ the
bottom. The direction of motion was always backwards, with the cirrate taking on a fusiform shape,
mantle ®rst, with the arms trailing behind. In most
cases the direction of motion was with the longitudinal
axis of the body parallel to the bottom, with the ventral
side downwards and the dorsal side towards the sea
surface. Individual No. 3 was observed swimming towards the sea surface, perpendicular to the sea ¯oor.
Movement of both ®ns was symmetrical during ®nswimming. From a position in which the ®ns were extended at right angles to the anterior±posterior axis of
the body, the stroke began with a rise starting in the
posterior margins of the ®ns. The posterior ®n margins
were then pushed vigorously downwards, meeting the
water at an angle and beginning the stroke. During the
stroke, the ®ns moved ventrally until they nearly
crossed beneath the cirrate's ventral region. The ®ns
were then brought back to the starting position to
complete one full stroke-cycle. Stroke-cycles were
rhythmic. The number of ®n strokes min)1 ranged from
4 to 30. This mode of locomotion was ®rst described by
Aldred et al. (1983).
This response was observed in Cirroteuthis magna
(Individual No. 5; Fig. 2o), 6 min 4 s after being captured and held by the submersible's claw. As a result of
the complicated handling while attempting to manoeuvre the cirrate into the sample box, ballooning was
observed to take place separately in each of the eight
sectors of the web; consequently, while some web sectors were empty others, in ballooning form, were full of
water. The web sectors emptied when struck against the
sample box, while sectors that had not been struck
remained distended with water. The ballooning-response, ®rst described by Boletzky et al. (1992), takes
place when all sectors of the web ®ll with water simultaneously.
Neither jet-propulsion nor active participation by the
mantle or funnel was observed in any mode of locomotion of the cirrate octopods examined. Movements by
the mantle to aerate the gills were assumed to expel water
through the narrow funnel characteristic of this group of
cephalopods, and thus to give rise to propulsion of unknown, although presumably very low, intensity.
The approach of and contact by the submersible always induced a ¯ight reaction. In no case did the cirrates
exhibit aggressive behaviour or adhere to the surface of
the submersible with their suckers. The behaviours observed in response to the intrusion by a strange object in
the habitat and the possible resulting disturbance are
described below.
119
Fig. 4 Cirroteuthis sp. Linedrawings depicting pumping
locomotion of Individual No. 1,
located close to ocean bottom
Unmodi®ed behaviours. These occurred at the start of
®lming, as the submersible approached from afar, and
any disturbance was assumed to be minimal. These behaviours included bottom-resting, umbrella-style drifting, and ®n-swimming.
Locomotive responses to disturbance. Such responses
were observed on close approach of or contact by the
submersible and included crawling, ®n-swimming, takeo€, and pumping.
Postural responses to disturbance. Such responses were
observed on capture of an individual, i.e., the ballooning-response. The diagram in Fig. 5 depicts the changes
in mode of locomotion or type of behaviour observed in
Cirroteuthis spp. and Grimpoteuthis spp. Bottom-resting
and crawling were observed only in Grimpoteuthis spp.
individuals, a genus that seems to be more associated
with the bottom than Cirroteuthis. In contrast, the umbrella-style, pumping and ballooning modes observed in
cirroteuthids, are due to their well-developed intermediate web.
Individuals observed
Individual No. 1: Cirroteuthis sp., Dive No. FR03. Film
time, was 4 min 7 s, starting time 15:04 hrs, starting
depth 2702 m. Behaviour: this individual was surprised
drifting umbrella-style 3 m above the bottom for 56 s
(Fig. 2j). In that position it touched the submersible
(Fig. 2k) with the oral surface of the web and cirri; this
was followed by take-o€ (Fig. 2l) and then ®n-swimming at 30 ®n strokes min)1 until it disappeared from
view. Ten seconds later it reappeared near the submersible 3.5 m above the bottom, again drifting umbrella-style; this was followed by pumping behaviour
(Fig. 2m, n). It once more touched the submersible with
its oral surface, again followed by take-o€ and then ®nswimming. The cirrate reappeared 43 s later very close
to the bottom, although apparently not on it, pumping
(Fig. 4) for 1 min 12 s until it disappeared from view.
Individual No. 2: Cirroteuthis sp., Dive No. FR05. Film
time was 36 s, starting time 12:15 hrs, starting depth
3837 m. Behaviour: this individual was surprised 5 m o€
the bottom, moving by ®n-swimming at 12 ®n strokes
min)1 until it disappeared from view.
Individual No. 3: Cirroteuthis sp., Dive No. FR11. Film
time was 1 min 32 s, starting time 11:38 hrs, starting
depth 4527 m. Behaviour: when surprised, the Individual
No. 3 was ®n-swimming 7.5 m from the bottom, some
distance away from the submersible, at 19 ®n strokes
120
handling with the submersible's claw, ballooning was
observed to take place separately in each of the eight
web sectors, with the individual web sectors taking
about 6 s to swell, quickly ®lling up with water or
emptying out, and resembling orange segments in appearance (Fig. 2o). The cirrate died on being placed in
the sample box, and upon its removal from the box, its
buoyancy was observed to be neutral. The anatomy of
this specimen is fully described by Guerra et al. (1997).
Individual No. 6: Grimpoteuthis sp., Dive No. FR14. Film
time was 1 min 57 s, starting time 14:12 hrs, starting
depth 3356 m. Behaviour: Individual No. 6 was resting
on the bottom when surprised. When bu€eted by turbulence from the submersible, it kept itself steady by
¯apping its ®ns at the rate of 12 to 30 ®n strokes min)1
without leaving the bottom. Twice it rose slightly o€ the
bottom, only to lower itself back down again, until it
®nally executed take-o€ and disappeared from view.
Individual No. 7: Unidenti®ed cirrate octopod, Dive No.
FR17. This individual not ®lmed. Observation time was
at 13:15 hrs, starting depth 3706 m.
Fig. 5 Cirroteuthis spp. and Grimpoteuthis spp. Diagram showing
relationships between di€erent attitudes and modes of locomotion
observed in cirrate octopods during present study. For detailed
explanation see ``Results ± Attitudes and modes of locomotion
observed''
min)1. It rose to 14 m from the bottom and disappeared
from view.
Individual No. 4: Grimpoteuthis sp., Dive No. FR14. Film
time was 3 min 50 s, starting time 12:57 hrs, starting
depth 3361 m. Behaviour: when surprised, Individual
No. 4 was resting on the bottom, and it remained in that
position, lit by the submersible's spotlights, without any
apparent reaction for 2 min. At the approach of the
submersible's claw, it moved away in crawling mode for
50 s (Fig. 2b, c). When struck on the distal portion of
the mantle by the submersible claw, it closed its eyes and
used its ®ns to hold itself steady on the bottom for a
further 68 s. An attempt to capture the individual using
the claw elicited take-o€ followed by ®n-swimming until
it disappeared from view.
Individual No. 5: Cirroteuthis magna, mature male,
mantle length 220 mm and 1300 mm total length, Dive
No. FR14. Film time was 10 min 34 s, starting time
13:47 hrs, starting depth 3351 m. Behaviour: when surprised, the individual was ®n-swimming near the submersible at 4 ®n strokes min)1. It was captured using the
submersible's claw, which gripped the distal end of
Right Arm IV. The cirrate endeavoured to escape by
continued ®n-swimming (at between 20 and 24 ®n
strokes min)1) and by 11 take-o€ events in 6 min 23 s.
After this time, the ballooning response was observed on
attempting to place the cirrate in the sample box. During
Individual No. 8: Grimpoteuthis sp., Dive No. FR19. Film
time was 3 min 25 s, starting time, 13:10 hrs, starting
depth 3452 m. Behaviour: when surprised, it was resting
on the bottom (Fig. 2a), where it remained for 1 min
05 s. It reacted to the approach of the submersible's claw
with take-o€ followed by ®n-swimming (Fig. 2g±i) a few
metres above the bottom for 2 min 15 s at 17.5 ®n
strokes min)1, until it disappeared from view.
Individual No. 9: Grimpoteuthis sp., Dive No. FR20. Film
time was 40 s, starting time 11:55 hrs, starting depth
3563 m. Behaviour: this individual was resting on the
bottom when surprised. It remained in that position for
44 s while the submersible approached. On being touched by the submersible's claw, it reacted with take-o€
and disappeared from view.
Individual No. 10: Cirroteuthis sp., Dive No. FR22. Film
time was 23 s, starting time, 15:24 hrs, starting depth
3534 m. Behaviour: this cirrate was surprised while
drifting umbrella-style <1m from the bottom (Fig. 2d).
It reacted to the submersible's approach with take-o€
(Fig. 2e), and then moved away by ®n-swimming
(Fig. 2f) at 22.5 ®n strokes min)1 until it disappeared
from view.
Discussion
As in previous studies (Roper and Brundage 1972; Pearcy
and Beal 1973), only solitary individuals were encountered in the present work. The literature contains no reports of school formations by cirrate octopods, although
there are reports of the formation of loose aggregations
(Vecchione 1987; Villanueva 1992b). The video sequences
121
analysed here show that cirrates employ di€erent modes
of locomotion, namely, crawling, umbrella-style drifting,
take-o€, ®n-swimming, and pumping. These modes of
locomotion must be viewed from the perspective of the
advantages and disadvantages conferred by these octopods' neutral buoyancy (Denton 1974; Clarke et al. 1979;
and present results) resulting from the presence of numerous vacuolate cells (Aldred et al. 1983) and the gelatinous consistency of these cirrates.
Crawling along the bottom is known to be the main
mode of locomotion employed by benthic incirrate
octopods (i.e. Octopus spp.). This mode of locomotion
is, overall, similar to the crawling mode observed in the
Grimpoteuthis spp. individuals discussed here. However,
cirrate arms do not have the strong musculature of
benthic incirrate octopods, and their suckers are comparatively smaller (Nixon and Dilly 1977; Young 1977;
Villanueva and Guerra 1991). The term ``crawling'' has
been used here for cirrates on a tentative basis only, and
may have to be changed later, following study of the
suction and adherence functions of cirrate suckers which
are presently not understood. Bottom-resting and
crawling was not observed in Cirroteuthis spp., which do
not display as close an association with the bottom as do
Grimpoteuthis spp. (Fig. 5).
Umbrella-style drifting appears to be a passive mode
of locomotion. Cirroteuthids may take advantage of
their neutral buoyancy to use the umbrella-style mode to
drift with near-bottom water currents. Modes of locomotion that require low energy-expenditure may be extremely useful in regions such as the abyssal zone, where
energy-transfer rates are low. In addition, in the umbrella-style posture, the cirri are fully extended and exposed (as opposed to ®n-swimming), which may enhance
their responsiveness to environmental stimulation. This
mode of locomotion was not observed in Grimpoteuthis
spp. Gentle expulsion of water between the primary and
intermediate webs may be used by cirroteuthids for slow,
placid movement, thanks to their buoyancy. This mode
of locomotion has been termed ``pumping'' and was
unknown before the present study. The observations
reported here have also demonstrated that each of the
individual sectors of the web can undergo a separate
ballooning response. Consequently, by employing different combinations, these cirrate octopods, appear to
enjoy a greater range of modes of locomotion than has
hitherto been observed, and additional modes of locomotion are likely to be discovered in the near future.
Fin-swimming was the mode of locomotion most
frequently observed in the present study. This agrees
with the reports on the mode of locomotion of other
cirrates observed from manned submersibles (Aldred
et al. 1983; Boletzky et al. 1992; Vecchione and Young
1997). Most of the individuals observed during the dives
reported in the present study used this mode of locomotion, and ®n-swimming always followed take-o€.
Using photographs, Roper and Brundage (1972)
described a mode of locomotion in cirrates which they
termed ``water-ejection or jet propulsion''. As in other
kinds of cephalopods, the source of this mode of locomotion was assumed to consist of forced expulsion
of water through the funnel by contractions of the
pallial muscles, the function of the ®ns being complementary or for the purpose of stabilization only. The
present video recordings have not demonstrated jet
propulsion in cirrates. The attribution of jet-propulsion
by Roper and Brundage (their Figs. 7, 8, and 13), was
probably incorrect, although fully understandable
bearing in mind that the material with which they
worked consisted of still-photographs taken at 10 to
30 s intervals, which thus did not record continuous
motion. The mode of locomotion in the photographs
which they interpreted as water ejection was probably
®n-swimming. It seems likely that the breathing
movements of the mantle to aerate the gills and ®n
motion may allow water to enter the mantle cavity, and
that water may be expelled through the narrow funnel.
However, any propulsion that may be derived from this
process would appear to be complementary to ®nswimming, which thus seems to be the main mode of
active locomotion in cirrates. Earlier, Bidder (1970)
expressed the view that ``the mantle-funnel complex or
jet propulsion plays a minimal part in the locomotion
of these organisms''.
Locomotion consisting of cycles of medusoid pulsations, the ``pulsating style'' suggested by Roper and
Brundage (1972; their Figs. 16 to 18) in cirrates, was not
observed in any of the ®lm sequences examined in the
present study. The ®rst direct observations of cirrate
behaviour, in individuals of Opisthoteuthis californiana
recently captured by bottom trawl and held in an onboard aquarium, were reported by Pereyra (1965), who
reported a pulsating style ``analogous to that of a jelly®sh''. The photographs of the individuals in question
show multiple wounds and abrasions in the skin (Pereyra 1965, his Fig. 3). In our opinion, the said ``pulsating
style'' may have been a repeated escape reaction, i.e.
take-o€, caused by the great stress of capture and preagonal conditions. However, in an individual of
Opisthoteuthis agassizii observed in situ on the bottom,
Vecchione and Roper (1991) and in a juvenile individual
of Grimpoteuthis sp. observed in a shipboard aquarium
(Vecchione and Young 1997), medusoid pulsations
combined with ®n ¯apping were reported. The medusoid
swimming reported in opisthoteuthids ± which are
rounder, with a bell-shape that is hydrodynamically
better adapted to medusoid pulsations ± needs to be
corroborated in cirrates other than cirroteuthids, which
are more elongate animals with large ®ns.
The present results con®rm that the ballooning response is a reaction to disturbance or to high stress and
may constitute a defense mechanism for cirrates (Boletzky et al. 1992). Possible predators on cirrates in the
bathyal and abyssal zones remain unknown. The only
report of beaks of Opisthoteuthis sp. in stomach contents
was in Australian fur-seal stomachs (Gales et al. 1993).
The observed reaction of the cirrates to the approach of
a strange object (the submersible) or even direct contact
122
with that object was always ¯ight, in contrast to the
ballooning-response reaction by the single individual
described by Boletzky et al. (1992). Packard and Sanders
(1971) showed that responses to disturbances in Octopus
vulgaris vary with the intensity of the disturbance. The
¯ight response, preceded by take-o€, was the most frequently observed reaction to disturbance in the present
series. Future studies on cirrate octopods will be needed
to elucidate the full range of behavioural responses and
their adaptation to the abyssal zone, such as the periods
of activity and relative use of each mode of locomotion.
Acknowledgements The authors wish to express their appreciation
to Dr. H. Bougault (IFREMER, Brest), Chief Scientist on the
``Faranaut'' Cruise, for the facilities provided and to all the participants on the cruise for their cooperation. Drs. E. Spanier and
M. Vecchione reviewed the manuscript, improving the ®nal version. Mr. J. Corbera made the ink drawings, Mrs. M.T. FernaÂndez
provided technical support, and Mr. R.B Sacks improved the English text.
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