Ethological studies of the Veined Octopus Amphioctopus marginatus (Taki)
(Cephalopoda: Octopodidae)
in captivity, Kerala, India
V. Sreeja1 & A. Bijukumar 2
1,2 Department
of Aquatic Biology & Fisheries, University of Kerala, Thiruvananthapuram, Kerala
695581, India
1 sreejaaqb@gmail.com, 2 abiju@rediffmail.com
(corresponding author)
doi: http://dx.doi.org/10.11609/JoTT.o3256.4492-7 | ZooBank:urn:lsid:zoobank.org:pub:C0815DD9-67A5-4A45-9573-D05D89F3E23F
Editor: Anonymity requested. Date of publication: 26 June 2013
(online & print)
Manuscript details: Ms #
o3256 | Received 16 July 2012 | Final received 09 May 2013 | Finally accepted
04 June 2013
Citation: Sreeja,
V. & A. Bijukumar (2013).Ethological studies of the Veined Octopus Amphioctopus marginatus(Taki) (Cephalopoda: Octopodidae) in captivity, Kerala, India. Journal
of Threatened Taxa 5(10): 4492–4497; http://dx.doi.org/10.11609/JoTT.o3256.4492-7
Copyright: © Sreeja& Bijukumar 2013. Creative
Commons Attribution 3.0 Unported License. JoTT allows unrestricted use of this article in any medium,
reproduction and distribution by providing adequate credit to the authors and
the source of publication.
Funding: Department of Biotechnology,
Government of India and Kerala State Council for Science and Technology
(student fellowship)
Competing Interest: None.
Acknowledgements: Sreeja thank Kerala State Council for Science,
Technology and Environment for the taxonomy fellowship. Bijukumaracknowledges the support of Department of Biotechnology, Government of India
for funding a project on Biodiversity and DNA barcoding of Marine Molluscs of India.
Abstract: Five Veined Octopus Amphioctopus marginatus (Taki),
collected from Vizhinjam Bay in the
Thiruvananthapuram District of Kerala, India were kept in aquariums to study
their behaviour in captivity. Primary and secondary defence mechanisms studied included crypsis,
hiding and escape behaviour. Deimatic behaviour was used by captive animalswhen camouflage failed and they were threatened. Crawling behaviourto escape from the aquarium was observed in all specimens. Stilt walking and bi-pedal locomotion
were also observed. As a defence behaviour,A. marginatus used aquarium rocks to protect
the soft underside of their bodies. A. marginatus demonstrated
tool use of coconut shells to make protective shelters, carrying the shells for
future use. A female specimen also
selected a coconut shell for egg laying and performed parental care by
continuously cleaning and aerating her eggs with her arms and by squirting jets
of water over the eggs.
Keywords: Behaviour, crypsis, India,
octopus, tool use.
For images, videos -- click here
Octopuses are solitary
animals that are considered advanced among invertebrates because of their
demonstrated learning abilities (Nixon & Young 2003) and complex nervous
system, including a central brain with areas associated with learning and
complex personality behaviours (Sinn et al.
2001). The discovery of playful
octopuses (Mather & Anderson 1999; Kuba et al.
2003) is an important step towards understanding the phylogenetic origin and
function of play, as well as the cognitive abilities of invertebrates. The report on existence of personalities
in octopuses (Mather & Anderson 1993) is further proof of their complex behaviour. The
octopus is the only invertebrate which has been shown to use tools and is
considered as a benchmark for cognitive sophistication (Finn et al. 2009).
Octopuses are dioecious animals with internal fertilization. Breeding occurs seasonally. Mating has been considered
opportunistic, indiscriminate and almost devoid of complex behaviour(Hanlon & Messenger 1996). Mating occurs when the male transfers sperm into the body cavity of the
female using a specialized hectocotylized arm. Eggs are usually
protected by the female. The
female usually attaches egg strings to substrates on rocky shores, in a hole,
den or sheltered place. During the
incubation period the female ventilates and protects the eggs until they
hatch. During this time she usually
remains sessile, starves and dies. Through the study of captive Veined Octopus Amphioctopus marginatus, we aimed to undertake a
quantitative analysis of locomotory patterns and
characterize: (i) defensive responses under
controlled conditions, (ii) tool use behaviour, and
(iii) breeding behaviour in captivity.
Materials and Methods
Amphioctopus marginatus (Image 1) is
a medium-sized octopus found in the tropical western Pacific and coastal waters
of the Indian Ocean. Two female and
three male specimens of A. marginatus (ML
110–113 mm; TL 340–345 mm; weight 200–250 g) were collected
live from Vizhinjam Bay (8022’N & 76015’E),
Thiruvananthapuram District, Kerala State, India. The specimens were collected with the
help of local fishermen from a depth of approximately 2m. The collected octopuses were transported live to the laboratory
and kept individually in fully set glass tanks of 120x60x60 cm size. An escape proof plexiglas lid was used to cover the tanks. The substrate used was sea sand with
plenty of building materials and rocks so that the octopuses could establish
their dens at a place of their choice. The tank water was filtered using protein-skimmers and biological
filters. Observations were made for
a period of six months. Behavioural responses, locomotorypatterns, tool use behaviour and breeding behaviour were recorded in captivity and documented with
the help of videos (videos 1–3) and photographs.
Results
Locomotion: Observation
on the locomotory patterns of Amphioctopus marginatus in captivity showed stilt
walking and bipedal locomotion (Images 2, 3). In bipedal locomotion the octopuses used
two arms for locomotion and the remaining arms to provide camouflage. In stilt
walking the arms were used as rigid limbs. These movements are distinctly
different from their normal crawling, which usually involves several arms
sprawling around the body, using the suckers to push and pull the animal along.
Defence: A. marginatus showed primary and secondary
defensive mechanisms in captivity. In their natural environment the defensive behaviour is used for predator avoidance. Primary defensive behaviours shown by the animal in captivity included
camouflage (chromatophore based skin display) and crypsis in motion. Crypsis in
motion is the phenomenon whereby an animal’s colourpattern, behaviour, or other features help it blend
in with the background (Huffard et al. 2005). The main primary defenceof the octopuses recorded in captivity was hiding; they hid in small, tight
places, made possible by the absence of exoskeleton. The primary defenceof escaping from the aquarium was observed in all specimens.
In captivity A. marginatus showed secondary defences,
while agitated by objects presented to them. The secondary defencesexhibited included flight (swimming/burial responses), jet propulsion (fast
escape) and flashing of colour (contrasting colours white and dark brown) (Image 4). The most common secondary defence was fast escape. The defensive behaviouralstudy also revealed that A. marginatus used
aquarium rocks to protect the soft underside of their bodies (Image 5).
Tool use: Observations
on the tool use behaviour (advanced cognitive
abilities) recorded the use of coconut shells kept in the aquarium by the
octopuses as portable armour, protective shelters and
homes (Images 6–8). They
manipulated two coconut shell pieces to make perfect homes and resided within them as other hiding devices were not made available for
them in the aquarium. We observed
that they also use coconut shells for egg laying (Images 9,10).
Breeding Behaviour: A. marginatuslaid eggs as festoons (Image 11) and throughout the brooding period, the female
never let go off the egg cluster which was held close
to the body on the aboral side. The female became more active and
vigilant during brooding and took extreme care to remove anything that came
near the spawn. The octopus squatted
directly over the eggs, holding the coconut shell firmly with few suckers and
waving free arms across the egg sheet, thus constantly aerating the eggs. Usually, two or more arms were
continuously swept over the eggs with slow, radial sweeps and with slow
undulating movement of the arms. The octopus also tended to keep particles of debris and micro-organisms from aggregating on the eggs by using the
arms and water jets created by the funnel. When the eggs and shell were removed, the octopus was observed to
release ink (Image 12). The octopus
also attempted to repel approaching objects by darting strong jets of water
through the funnel.
On the first day of egg
laying the octopus accepted food, whereas it avoided food subsequently. A small
part of the egg mass was removed from the coconut shell and kept in separate
troughs with filtered and aerated sea water to study
the development of the eggs. The brooding octopus died on the eighth day after
egg laying. The eggs consisted of an ovoid egg capsule, moderately long stalk and a bulb which attach the egg with the substratum. The eggs were laid by intertwining and
cementing the long chorion stalks of the egg capsules
together to form a string, or festoon, of eggs (Image 11). Each festoon is cemented at one end to
the substratum. A total of about 22
festoons were collected from the coconut shell after the death of the octopus
and the total number of eggs was estimated at around 20,000. The number of eggs present in each
string ranged from 33–45/ cm of string. The size of the eggs ranged from
3.3–3.7 mm in length.
Release of a few hatchlings
was noticed by the 16th day and the paralarvaewere observed to lead a planktonic existence. Hatchlings resembled adult octopuses in
general body pattern (Image 13). The
larvae were fed with Artemia nauplii. Further developmental stages were not obtained in this study.
Discussion
The Coconut or Veined
Octopus Amphioctopus marginatus,is an under-studied, medium-sized cephalopod common in the coastal
waters of India. In natural waters
elsewhere in the world, A. marginatus is
reported to display unusual behaviour, including
bipedal walking and gathering and using coconut shells and seashells
for shelter (Finn et al. 2009). This study revealed that these behavioural patterns
are also exhibited by A. marginatus collected
in India, when maintained in captivity.
Amphioctopus marginatus achieves
bipedal locomotion despite having only a hydrostatic skeleton, although this
mode of locomotion has often been thought to require the opposition of muscles
against a rigid skeleton (Huffard 2006). Amphioctopus marginatus and Abdopus aculeatus are the only species of octopods
reported to show bipedal behaviour. This behaviour was first recorded in
Sulawesi, Indonesia, where the sandy bottom was littered with coconut
shells and it was reported to be to mimic a floating coconut (Huffard et al. 2005).
An octopuses’ camouflage is
aided by certain specialized cells which can change
apparent colour, opacity, and reflectiveness of the
epidermis; the colour changing ability can also be
used to communicate with or warn other octopuses (Wells 1978). Amphioctopus marginatus made themselves cryptic by modifying
their physical appearance while in captivity.
Crypsis, which can be achieved in a variety
of ways, is the primary defence against predators
used by most shallow-water octopuses, although there is some evidence that
whether they choose to make themselves cryptic by modifying their physical
appearance and/or behaviour may depend on their assessment
of the level of threat in their environment (Hanlon 1999). Octopuses are able to modify their
appearance and behaviour in such a way that they
seem, at least to human observers, to resemble swimming fish, rocks, or other
familiar objects in their habitat (Hanlon 1999). In captivity Amphioctopus marginatus were observed to use two arms for
locomotion and the remaining six arms to provide camouflage.
The coconut shell carrying behaviour is likely to have evolved using large empty
bivalve shells prior to the relatively recent supply of the clean and light
coconut shell halves discarded by the coastal human communities adjacent to the
marine habitat of this species (Finn et al. 2009). The present study shows that A. marginatus may also employ this behaviour in captivity in addition to using coconut shells
for brooding, reported here for the first time. While examining A. marginatus in natural waters Norman (2000) observed
that individuals of this species often carry around coconut shell halves, assembling
them as a shelter only when needed. Finn et al. (2009) recorded that these
shells offer no protection while being carried and, in fact, appear to be a
burden as they force the octopus to use a novel and awkward form of locomotion
which the authors describe as “stilt-walking”. They argued that this is the first known
example of tool use by an invertebrate, if part of the definition of a tool is
that it provides no benefit until it is used for a specific purpose. They further propose the fact that the
shell is carried for future use rather than as part of a specific task which differentiates this behaviour from other examples of
object manipulation by octopuses, such as rocks being used to barricade
lair entrances. Furthermore, the
necessity to correctly assemble the separate parts (when transporting two
shells) in order to create a single functioning tool sets this example of tool
use apart from most or all examples previously known for invertebrates.
The embryonic development of A.marginatus is recorded for the first time during
the present study. Data on
fecundity of octopuses is limited in scientific literature. The available data
shows that the octopuses inhabiting benthic, littoral waters fall into three
categories: (i) species that produce large eggs
(>10mm) and benthic young; (ii) species that produce small eggs (<6mm)
and long duration planktonic young (Boletzky 1974);
and (iii) species that produce medium-sized eggs (6–10 mm) and short
duration planktonic young. This
result showed that A. marginatus falls into
the second category. It is noted
that the species having a planktonic phase in their life cycle have a more
widespread distribution than those with benthic young. This is true in the case of A. marginatus, which enjoys a wide distribution from Japan
to India. While this study revealed that the egg development time of this
species is short, 17 days, data on the period of planktonic existence could not
be collected during this study.
Octopuses inhabit many
diverse regions of the ocean and play a critical role in marine ecosystem
functioning. Moreover, they are
economically important as a preferred item in marine fisheries export from
India. Despite the burgeoning
demand for octopuses, not much information is available on the reproduction and
embryonic development of octopods inhabiting the coastal waters of India. Research to update present knowledge on
the reproductive biology of octopods should be given priority status, because
of their increasing exploitation, high economic value and importance as a key
element in marine biodiversity.
REFERENCES
Boletzky, S.V. (1974). The “larvae” of Cephalopoda: a review. Thalassia Jugosl 10: 45–76.
Finn, J.K., T. Tregenza & M.D. Norman (2009). Defensive
tool use in a coconut-carrying octopus. Current Biology 19:
1069-1070; http://dx.doi.org/10.1016/j.cub.2009.10.052
Hanlon, R.T. (1999). Crypsis,
conspicuousness, mimicry and polyphenism as antipredator defences of foraging
octopuses on Indo-Pacific coral reefs, with a method of quantifying crypsis from video tapes. Biological Journal of the
Linnaean Society 66: 1–22; http://dx.doi.org/10.1111/j.1095-8312.1999.tb01914.x
Hanlon,
R.T. & B.J. Messenger (1996). Cephalopod Behaviour. Cambridge University Press, Cambridge, 232pp.
Huffard, C.L. (2006). Locomotion by Abdopus aculeatus (Cephalopoda: Octopodidae):
walking the line between primary and secondary defences.Journal of Experimental Biology 209: 3697–3707; http://dx.doi.org/10.1242/jeb.02435
Huffard, C.L., F. Boneka & R.J. Full (2005). Underwater
bipedal locomotion by octopuses in disguise. Science307: 1927. http://dx.doi.org/10.1126/science.1109616
Kuba, M., D.V. Meisel, R.A. Byrne, U. Griebel& J.A. Mather (2003). Looking at play in Octopus vulgaris. BerlinerPalaontologische Abhandlungen3: 163–169.
Mather, J.A. & R.C.
Anderson (1993). Personalities of octopuses (Octopus rubescens). Journal of Comparative Psychology107(3): 336–340; http://dx.doi.org/10.1037/0735-7036.107.3.336
Mather, J.A. & R.C.
Anderson (1999). Exploration, play, and habituation in octopuses
(Octopus dofleini). Journal
of Comparative Psychology 113: 333–338.
Nixon,
M. & J.Z. Young (2003). The Brains and Lives of Cephalopods. Oxford
University Press, New York, 392pp.
Norman, M.D. (2000). Cephalopods: A World
Guide. Conch Books. Hackenheim, Germany, 320pp.
Sinn, D.L., N.A. Perrin, R.C.
Anderson & J.A. Mather (2001). Early temperamental traits in an octopus (Octopusbimaculoides). Journal of Comparative
Psychology 115(4): 351-364; http://dx.doi.org/10.1037//0735-7036.115.4351
Wells, M.J. (1978). Octopus: Physiology and Behaviourof an Advanced Invertebrate. Chapman and Hall, London,
417pp.