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RESEARCH PAPER

Approaches to resolving cephalopod movement and


migration patterns
Jayson M. Semmens Gretta T. Pecl Bronwyn M. Gillanders
Claire M. Waluda Elizabeth K. Shea Didier Jouffre Taro Ichii
Karsten Zumholz Oleg N. Katugin Stephen C. Leporati Paul W. Shaw
Received: 2 January 2007 / Accepted: 1 February 2007 / Published online: 16 March 2007
Springer Science+Business Media B.V. 2007
Abstract Cephalopod movement occurs during
all phases of the life history, with the abundance
and location of cephalopod populations strongly
inuenced by the prevalence and scale of their
movements. Environmental parameters, such as
sea temperature and oceanographic processes,
have a large inuence on movement at the
various life cycle stages, particularly those of
oceanic squid. Tag recapture studies are the most
common way of directly examining cephalopod
movement, particularly in species which are
heavily shed. Electronic tags, however, are being
more commonly used to track cephalopods,
providing detailed small- and large-scale move-
ment information. Chemical tagging of paralarvae
through maternal transfer may prove to be a
viable technique for tracking this little under-
stood cephalopod life stage, as large numbers of
individuals could be tagged at once. Numerous
indirect methods can also be used to examine
cephalopod movement, such as chemical analyses
of the elemental and/or isotopic signatures of
J. M. Semmens (&) G. T. Pecl S. C. Leporati
Marine Research Laboratories, Tasmanian
Aquaculture and Fisheries Institute, University of
Tasmania, Private Bag 49, Hobart, TAS 7001,
Australia
e-mail: Jayson.semmens@utas.edu.au
B. M. Gillanders
Southern Seas Ecology Laboratories, School of Earth
and Environmental Sciences, University of Adelaide,
Adelaide, SA 5005, Australia
C. M. Waluda
Biological Sciences Division, British Antarctic Survey,
High Cross, Madingley Road, Cambridge CB3 0ET,
UK
E. K. Shea
Delaware Museum of Natural History, P.O. Box 3937,
Wilmington , DE 19807, USA
D. Jouffre
Unite OSIRIS, IRD, BP 1386, Dakar, Senegal
T. Ichii
National Research Institute of Far Seas Fisheries,
2-12-4 Fukuura, Kanazawa-ward, Yokohama-City
236-8648, Japan
K. Zumholz
Leibniz-Institute of Marine Sciences, IFM-
GEOMAR, Du sternbrooker Weg 20, D-24105 Kiel,
Germany
O. N. Katugin
Pacic Fisheries Research Centre, 4 Shevchenko
Alley, Vladivostok 690950, Russia
P. W. Shaw
School of Biological Sciences, Royal Holloway
University of London, Egham TW20 0EX, UK
1 3
Rev Fish Biol Fisheries (2007) 17:401423
DOI 10.1007/s11160-007-9048-8
cephalopod hard parts, with growing interest in
utilising these techniques for elucidating migra-
tion pathways, as is commonly done for sh.
Geographic differences in parasite fauna have
also been used to indirectly provide movement
information, however, explicit movement studies
require detailed information on parasite-host
specicity and parasite geographic distribution,
which is yet to be determined for cephalopods.
Molecular genetics offers a powerful approach to
estimating realised effective migration rates
among populations, and continuing developments
in markers and analytical techniques hold the
promise of more detailed identication of mi-
grants. To date genetic studies indicate that
migration in squids is extensive but can be
blocked by major oceanographic features, and in
cuttlesh and octopus migration is more locally
restricted than predictions from life history
parameters would suggest. Satellite data showing
the location of shing lights have been increas-
ingly used to examine the movement of squid
shing vessels, as a proxy for monitoring the
movement of the squid populations themselves,
allowing for the remote monitoring of oceanic
species.
Keywords Cephalopods Movement
Migration Environmental variability
Introduction
Movement of cephalopod populations takes place
during all phases of the life history, from the
passive drifting of egg masses (ODor and Balch
1985) and paralarvae to the daily vertical migra-
tions of many oceanic species (Roper and Young
1975) and large-scale migrations (thousands of
kilometres) of adult animals from feeding to
spawning grounds (ODor 1992). Cephalopods
are short lived, and exhibit a high level of
plasticity in their life history strategies where
changes in environmental conditions have a large
part to play in inuencing population size, abun-
dance and distribution. One of the major factors
inuencing the active movement of cephalopods
is likely to be the availability and movement of
food supplies (Rodhouse and Nigmatullin 1996),
and many cephalopod populations have evolved
their migratory strategies to maximise high feed-
ing rates. Movement patterns can inuence the
response of cephalopods to environmental
change, and the abundance and location of
cephalopod populations and associated sheries
is strongly inuenced by the prevalence and scale
of their movements (Boyle and Boletzky 1996).
Those populations which undertake the largest
migrations are prone to the largest uctuations in
population abundance (ODor 1992; Dawe et al.
2000). Particularly in ommastrephid squid, annual
uctuations in catch can vary between 2 and 5
orders of magnitude for an individual species
(FAO 2000).
This review seeks to clarify our understanding
of cephalopod movement and migration and
determine where future research investment will
be most benecial in terms of increasing our
understanding and providing effective tools for
resolving movement patterns. We appraise meth-
ods for resolving movement and migration pat-
terns of cephalopod species and examine the
strong relationship between movement in cepha-
lopods and environmental parameters.
Methods for resolving movement/migrations
patterns/processes
The various methods used to examine cephalopod
movement/migration will be explored in this
section, using relevant examples, along with
potential methods currently being developed or
to date only used for other groups, such as sh.
These methods are divided into ve broad cate-
gories: tag recapture methods, which involve
marking and releasing animals; electronic tags;
chemical tags; natural tags (which includes para-
sites, molecular genetics and elemental signa-
tures) and tracking shing eets.
Tag-recapture
External tags
External tags which are attached to the study
animal and identify individuals or groups of
402 Rev Fish Biol Fisheries (2007) 17:401423
1 3
animals, along with instructions for reporting, are
the most widely used technique to examine the
movement patterns of cephalopods (see Nagasa-
wa et al. 1993 for an excellent review and
description of the types of external tags com-
monly used), and other marine organisms in
general. This wide-spread use is due to their
relatively low cost and ease of application, which
allows for large number of individuals to be
tagged. There are several potential disadvantages
to using these tags, however, including damage to
the tagged animal from the tag rubbing against
the muscle/skin, (e.g., Kanamaru and Yamashita
1966; Sauer et al. 2000), tag loss (e.g., Kanamaru
and Yamashita 1966; Tsuchiya et al. 1986, in
Nagasawa et al. 1993), and the relatively large tag
and applicator meaning that in general juveniles
can not be tagged. Recapture rates are variable
and inuenced by factors such as level and extent
of shing (e.g., Mokrin 1988; Markaida et al.
2005), tag colour (e.g., Nagasawa et al. 1993;
Sauer et al. 2000), tag type (e.g., Mokrin 1993;
Nagasawa et al. 1993) and tag placement (e.g.,
Nagasawa et al. 1993; Sauer et al. 2000). Report-
ing rates for external tags can also be highly
variable for a wide variety of reasons such as,
sher apathy, resentment of research/manage-
ment and insufcient rewards.
Extensive studies of the annual spawning
migrations of the ommastrephid squid, Todarodes
pacicus, one of the largest single species ceph-
alopod sheries in the world, has seen over 1
million squid tagged in the Sea of Japan and the
North Pacic with various types of external tags
(see Nagasawa et al. 1993; Kidokoro, pers.
comm.), most commonly T-bar (or anchor) tags
with a pentagonal pennant (Shevtsov 1973, 1978;
Skalkin 1973; Mokrin 1988, 1993, pers. comm.;
Nagasawa et al. 1993). Such large numbers are
required as low recapture rates are common for
ommastrephids shed in large offshore shing
zones (e.g., 0% for Illex illecebrosus in New-
foundland, Hurley and Dawe 1981; 2.5% for T.
pacicus, Nagasawa et al. 1993), whereas recap-
ture rates are generally much higher in inshore
waters (e.g., 1932% I. illecebrosus, Hurley and
Dawe 1981; 8% Dosidicus gigas in the Gulf of
California, Markaida et al. 2005; 10% Sepioteu-
this australis in Tasmania, Australia, Pecl et al.
2006). Interestingly, several studies suggest that
recaptures rates may be size and/or sex dependent
(e.g., D. gigas, Markaida et al. 2005; S. australis,
Pecl unpublished data).
As well as high release numbers, spatial cov-
erage of the full extent of the shery is important
for tag-recapture studies if the migration routes of
the various species/populations are to be correctly
dened (e.g., T. pacicus, Nakamura and Mori
1998; Mori and Nakamura 2001). This spatial
coverage is only possible if the shery operates
throughout the migratory route, for example the
movement of D. gigas into and out of the Gulf of
California is unknown due to the much lower
level of shing effort in the Southern Gulf and
Pacic Ocean (Markaida et al. 2005).
The Japanese T. pacicus tag-recapture pro-
grams demonstrate a major advantage of external
tags, with their relatively low cost and ease of
application making them well suited to creating
long-term data sets to examine temporal trends in
migration patterns. Analysis of long-term tag-
recapture data for autumn spawning T. pacicus,
where 20,00030,000 individuals have been tagged
annually since the 1950s (Nagasawa et al. 1993;
Kidokoro pers. comm.) suggest that within the
Sea of Japan, the southward migratory route to
the spawning area changes in response to climate
shifts caused by variations in the southward
meandering of the Subarctic Front (Kidokoro
et al. 2004).
Unlike ommastrephid squids, coastal cephalo-
pod species such as octopods, loliginids and sepi-
oids, generally undertake relatively small scale
(tens to hundreds of kilometres) migrations,
between spawning and feeding grounds (e.g.,
Loligo forbesi, Holme 1974; Waluda and Pierce
1998, Sepia ofcinalis, Wang et al. 2003; Royer
et al. 2006, Octopus vulgaris, Sobrino et al. 2002).
Long-term tag-recapture studies of the loliginid
squids Uroteuthis edulis and Heterololigo bleekeri
in the Sea of Japan between 19741985 and 1960
1989 respectively (see Nagasawa et al. 1993),
showed that despite favouring open coastal waters,
these squid do not move beyond the continental
shelf (Natsukari and Tashiro 1991). Tag-recapture
studies of Loligo reynaudii on the southeast coast
of South Africa showed that loliginids can move
relatively large distances within a spawning area,
Rev Fish Biol Fisheries (2007) 17:401423 403
1 3
with an average movement of around three km/day
and a maximum of almost 15 km/day during their
spawning period of a month or more (Sauer et al.
2000), which may be in response to changing
environmental conditions (see Roberts and Sauer
1994) and food availability.
External tagging experiments on octopuses
present additional challenges to those for squid
and cuttlesh (see examples in Nagasawa et al.
1993; Bakhayokho 1986), as their dexterity and
strength allows them to easily remove external
tags (e.g., O. vulgaris, FAO 1979; Tsuchiya et al.
1986, in Nagasawa et al. 1993). Despite this,
Domain et al. (2000, 2002) successfully tagged
4245 O. vulgaris on the Senegalese shelf using
Petersen discs attached to the base of an arm,
including individuals as small as 200 g (Domain
et al. 2002), with 1,019 recaptured (24%) by the
commercial line-shing eet. The percentage of
recaptures varied from 0% to 49% depending on
the tagging location along the shelf, with low
recapture rates where few professional shermen
were present (Domain et al. 2002), again high-
lighting the link between the success of tag-
recapture programs and the spatial coverage of
the shery (Markaida et al. 2005). Despite the
success of the tagging method, all recaptured
individuals were captured in the area they were
released (Domain et al. 2002), suggesting that O.
vulgaris may not undertake migrations on the
Senegalese coast, unlike the seasonal inshore-
offshore migrations made by this species in the
Mediterranean Sea (Mangold 1983), however,
octopus were only at large for 100 days maximum
and all stages of the life cycle were not examined.
External tags attached to the base of the arms
have proved effective for tagging Enteroctopus
doeini in Japan (see Nagasawa et al. 1993) and
North America (e.g., Hartwick et al. 1984a, b;
Robinson and Hartwick 1986; Hartwick et al.
1988). Tag-recapture studies and sheries sam-
pling demonstrated that E. doeini undertakes
two seasonal inshore-offshore migrations per year
in the northern Sea of Japan (Kanamura and
Yamashita 1966, 1969, in Nagasawa et al. 1993;
Kanamura and Yamashita 1967, in Mottet
(1975)). A similar pattern was not found for E.
doeini in British Columbia, Canada (Hartwick
et al. 1984b, 1988), and electronic or natural
tagging techniques may be more applicable for
elucidating an inshore/offshore migratory pattern
(see below).
Tattooing and branding
Tattooing and branding techniques have been
trialled on several cephalopods, predominately
octopus, but with limited success (see Nagasawa
et al. 1993). Although these approaches over-
come the problem of tag removal and allow for
juveniles to be tagged, they are often technically
difcult to undertake and can cause severe stress
and damage to the animal. However, Tsuchiya
et al. (1986, in Nagasawa et al. 1993) compared
various external tagging techniques with tattooing
for O. vulgaris, and found tattooing dye spots in
the mantle musculature to be the most successful,
in terms of tags retention and minimising damage/
stress to the animal.
Cuttlesh (Sepia latimanus) have also been
tagged using a similar technique, namely injecting
red latex between the skin and cuttlebone. How-
ever there were few recaptures (two from 450
individuals tagged), marks lasted only a short
time (2 months) and wounds led to mortality
(Oka 1990b, in Nagasawa et al. 1993). Forsythe
(pers. comm.), however, successfully tagged juve-
nile cultured Sepia ofcinalis (approximately
10 cm ML) using uorescent injectable micro-
spheres, with at least one individual growing
through to maturity, with its tag still visible after
six months; however these animals were never
released from captivity. Similarly, visible implant
elastomer (VIE) tags (Northwest Marine Tech-
nology, Shaw Island, USA, www.nmt.us), which
are uorescent silicon tags injected under the
skin, have been used successfully to tag and
recapture Sepioteuthis sepioidea juveniles as small
as 19 mm ML in the eld (Replinger and Wood in
press), and may have potential for tag-recapture
of paralarval cephalopods, as small sh have been
tagged and recaptured using VIE tags (e.g., 8 mm
TL reef sh, Frederick 1997).
Electronic tags
These are generally electronic devices that are
implanted or attached to the animal and have
404 Rev Fish Biol Fisheries (2007) 17:401423
1 3
either a unique code or frequency, which is
transmitted to a recording device, or record envi-
ronmental information as the animal swims
around. There are several different classes of tag
(see below).
Acoustic transmitters
Acoustic telemetry, where an aquatic organism is
tagged with a high-frequency transmitter that can
be heard by a mobile or xed hydrophone linked
to a receiver that provides either a presence/
absence record, a geographical position, or the
relative direction of the animal, has been used
since the 1950s to study behaviour and physiol-
ogy, particularly in sh (Arnold and Dewar 2001;
Sibert 2001). Development of this technology has
increased rapidly in recent years matching that of
electronics and technology in general, but also in
response to a trend towards spatial management
of sheries worldwide (Sibert 2001). The advan-
tage of this type of tag is that individuals do not
need to be recaptured to gain movement infor-
mation, and unlike tag-recapture studies, you gain
much more detailed information rather than just
a capture and recapture position. A disadvantage
of these tags is that they have typically been quite
large, often 20100 mm, however, the technology
is getting smaller all the time, with the new
generation of tags being signicantly smaller
(15 mm and 0.5 g in water, Vemco, Halifax,
Canada, www.vemco.com). Cost is also a disad-
vantage, as releasing large numbers of acoustic
tags is an expensive exercise and the receiving
equipment, which also can be relatively expen-
sive, is also required. As such, these studies may
be done in conjunction with tag-recapture pro-
grams (e.g., S. australis, Pecl et al. 2006) with
traditional tag-recapture providing minimal data
on a large number of animals and acoustic tagging
providing much more detailed information on
fewer individuals. A further disadvantage comes
where moored automatic tracking systems are not
available or practical, meaning tagged animals
have to be manually followed in vessels using
directional hydrophones which can generally only
be done for short periods of time.
Three of the most interesting acoustic tagging
studies on cephalopods use a Radio-Acoustic
Positioning and Telemetry system (RAPT, Vem-
co) to triangulate the position of tagged animals
and track them in near real-time (see Klimley
et al. 2001 for details on RAPT); this system has
provided previously unavailable insights into the
behaviour of inshore cephalopods. Loligo rey-
naudii was tracked in South Africa using RAPT,
revealing their mating system to be unexpectedly
complex (Sauer et al. 1997). RAPT was used to
examine small-scale movement of Sepia apama in
Port Lincoln, South Australia, demonstrating that
the cuttlesh spent more than 95% of the day
resting, which suggests that these are sit and wait
predators and make few excursions in pursuit of
food (Aitken et al. 2005). Unique vertical move-
ments of E. doeini tagged with depth (absolute
pressure)-position tags in Northern Japan, which
were observed to be out of sequence with the
tides, were detected using RAPT (Rigby and
Sakurai 2005). Observations using SCUBA re-
vealed these octopuses were moving towards a
gill net and scaling the net to remove sh, thus
producing the unusual vertical movements.
Recently, underwater curtains of acoustic
listening stations (Vemco VR2 acoustic receivers,
see Heupel et al. 2006 for a review of this
technology) have been used to examine move-
ment of cephalopods (Stark et al. 2005; Pecl et al.
2006). This technology is becoming increasingly
popular for examining the movement of a wide
variety of sh and shark species (see Heupel et al.
2006). Pecl et al. (2006) assessed the relationship
between two S. australis spawning areas on the
east coast of Tasmania, Australia separated by
approximately 30 km. Although individuals were
spawning over several months and travelled 100s
of km within the spawning areas during this time,
movement between the two areas or out of each
area was not detected. Interestingly, these results
contrast in some respects with the preliminary
external tagging experiment carried out by Molts-
chaniwskyj and Pecl (this volume), where 90% of
S. australis individuals tagged with T-bar tags on
the spawning grounds were later caught within
1 km of the tagging site, suggesting no movement.
This appears to highlight one of the main advan-
tages acoustic monitoring has over tag-recapture
studies, that more detailed movements can be
detected in a well designed study i.e., careful
Rev Fish Biol Fisheries (2007) 17:401423 405
1 3
placement of receivers, not just the release and
capture points. The use of acoustic curtains, may
become more commonly used to examine med-
ium to large-scale movements of cephalopods,
with several countries establishing permanent
arrays of these listening stations for tracking a
wide range of marine animals, and users needing
only to purchase tags (e.g., the Pacic Ocean
Shelf Tracking (POST) project, www.post-
coml.org). These arrays will, however, only
extend as far as the continental shelf and so will
be of greatest benet to inshore species, such as
loliginids, sepioids and octopods.
There have been relatively few acoustic telem-
etry studies of oceanic squid, due to the difcul-
ties of tracking in this environment, however,
Nakamura (1991, 1993), Yatsu et al. (1999) and
Yano et al. (2000) actively tracked mature female
Ommastrephes bartramii in the North Pacic, D.
gigas off Peru and Thysanoteuthis rhombus in
Okinawa, Japan respectively, using depth-posi-
tion tags. All species showed clear daily patterns
of vertical movement, with D. gigas migrating to
below 1000 m and O. bartramii and T. rhombus
moving deeper during the night, perhaps to avoid
predators (Nakamura 1993) or follow prey (Yano
et al. 2000), with the vertical movement of T.
rhombus matching that of the deep scattering
layer. As active-tracking technology develops,
these oceanic studies may become more common,
with the potential for shing eets to automati-
cally upload data from tagged squids, using
vessel-mounted receivers.
PIT tags
Passive Internal Transponder (PIT) tags are elec-
tromagnetically coded tags that are injected under
the skin of various animals, including many sh
species; particularly salmonids (see Prentice et al.
1990). The advantage of these tags is they are
relatively small (typically 10 mm and 0.1 g), inex-
pensive, and individuals can be identied automat-
ically. However, the tag has to pass close by a
reader for the animal to be identied, meaning the
tagged animal needs to be recaptured and read
with a portable tag reader (e.g., Roussel et al.
2000), or in some situations electronic gates can
be established, such as in shways (Castro-Santos
et al. 1996) or at-bed antennae can be used to
monitor small-scale behaviour in streams (e.g.,
Armstrong et al. 1996).
Only one published study has used these tags
for cephalopods (Anderson and Babcock 1999).
PIT tags were implanted in the base of the arm of
eld (in lairs) and captive Octopus tetricus and
captive Octopus maorum. All octopus retained
the tags for the life of the study (captive:
14 months; eld: 13 weeks), with no signs of
damage or deterioration from the tags, and
individuals demonstrating normal growth. As
such, PIT tagging could be a useful tool for
providing long-term recognition of octopuses,
with shing vessels and sh processors able to
be provided with automatic detectors that record
tag IDs as the animals are dropped into holding
tanks/bins, eliminating the reporting problems
associated with external tags. Recently, Hallprint
(South Australia, www.hallprint.com) began pro-
ducing PIT tags imbedded within conventional T-
bar external tags, allowing for both vessels with/
without auto-readers to record tag numbers, with
these tags perhaps suited to the large-scale
tagging programs for T. pacicus, to increase the
tag reporting rate. These tags and auto-readers
have recently been trialled in the southern rock
lobster shery in Tasmania, with the concept
proving to be worth pursuing (see www.hall-
print.com). A limitation of these tags is, however,
the need to pass close to the tag reader and
therefore aside from the utility mentioned above,
they are likely to only be useful in eld situations
for small-scale movement.
Coded micro-wire tags
Coded micro-wire tags (Northwest Marine Tech-
nology) are a small length of stainless steel wire
(1 0.25 mm), which is magnetised and injected
into the animal. Tags are detected using a manual
or automatic magnetic detector and an etched
identifying number can be read with a micro-
scope. The advantage of these tags is that they are
relatively cheap (although the auto-readers are
relatively expensive), cause minimum harm, and
very small animals can be tagged (e.g., Arctic char
Salvelinus alpinus 22 mm total length, Champi-
gneulle et al. 1987). The disadvantage is the small
406 Rev Fish Biol Fisheries (2007) 17:401423
1 3
tag needs to be removed from the animal for its
individual code to be read. These tags have not
been used on cephalopods, but may have promise
for tagging paralarvae/juveniles, and are widely
used on small salmonids in the USA.
Archival tags
Archival (or data storage) tags record and store
environmental data, typically light intensity for
estimating geoposition, pressure for estimating
depth, and water and body temperature (see
Arnold and Dewar 2001 for a review). One major
disadvantage of these tags is that they have to be
recovered to download the data; they are also
quite large (3080 mm) and relatively expensive.
However, an advantage is that like acoustic tags
they provide shery independent data and can
provide a wide variety of ecological data over
large distances and time-scales. New types of
archival tags have been designed to overcome the
recovery issue, with pop-up archival transmitting
(PAT) tags (Wildlife computers, Washington,
USA, www.wildlifecomputers.com) detaching
from the animal at set times and up-loading
summaries of their data to satellites once they are
on the surface. Communicating history acoustic
transponder (CHAT) tags (Vemco), download
their data, and in the case of so-called business
card tags data from other tags encountered along
the way is also downloaded, to moored or mobile
acoustic receivers (Voegeli et al. 2001, Vemco
pers. comm.). However, the current size of these
tags limits the use of this technology to large
species (e.g., D. gigas, Gilly et al. 2006).
Although, with the technology steadily getting
smaller and automatic down-loading versions
being developed, it is envisaged that these types
of tags will become more common in cephalopod
movement/migration studies, as they are for sh
and sharks (see Arnold and Dewar 2001).
Only three published studies have used archi-
val tags on cephalopods (ODor et al. 2002;
Jackson et al. 2005; Gilly et al. 2006). Interest-
ingly, the rst two studies both employed hybrid
acoustic/archival tags to maximise the amount/
type of data collected and the ability to recover
the archival tags, although the latter was only
partially successful. Most notably, Gilly et al.
(2006) tagged D. gigas in the Gulf of California
using 96 archival tags (Lotek, Ontario, Canada,
www.lotek.com) and 10 PAT tags, with only one
of the archival tags recovered. Of the 10 PAT
tags, seven up-loaded data and provided temper-
ature, depth and horizontal movement (deter-
mined from light intensity) data. The PAT tag
data demonstrated that during seasonal migra-
tions D. gigas can travel almost 100 km in around
3 days, with the direction of the migration
matching prevailing currents. Most interestingly,
D. gigas spent most of the daylight hours and
some of the night in a midwater hypoxic zone
below 250 m, the oxygen minimum layer (OML),
with Gilly et al. (2006) suggesting that the squid
were foraging in this layer as it overlapped with
the prey-rich deep scattering layer. Laboratory
experiments showed that D. gigas has physiolog-
ical adaptations that allow it to actively forage in
the OML (Gilly et al. 2006)
Chemical tags
This type of tagging incorporates compounds
(e.g., uorescent chemicals, elements and iso-
topes) into calcied tissues. The advantages of
this type of tagging are that you can mark large
numbers of animals simultaneously with minimal
handling, all life history stages can be marked, the
compounds do not affect growth and mortality,
and the marks can be detected for a considerable
time. Disadvantages include the need to sacrice
the organism to detect the mark, often there are a
limited number of unique marks possible, and
detection may be limited to analytical methods
(at least for elemental and isotopic tags).
Fluorescent markers
There have been very few published studies on
cephalopods using uorescent markers to exam-
ine movement, however, squid statoliths have
been routinely marked with the uorescent com-
pounds tetracycline and calcein in order to
validate their age (see review by Jackson
(1994)). Statoliths of hatchling (Fuentes et al.
2000) and subadult (100 g) (Sakaguchi et al.
2000) O. vulgaris were successfully stained by
Rev Fish Biol Fisheries (2007) 17:401423 407
1 3
immersion of the animals in solutions of alizarin
complexone. Subadult octopus showed the uo-
rescent mark on their statoliths when recaptured
after 31 days (Sakaguchi et al. 2000). These stud-
ies suggest that uorescent marking of statoliths
could be a viable technique for mass labelling of
paralarval cephalopods to examine movement
throughout their life history. As an example of
the potential of this type of tagging, Jones et al.
(1999) marked >10 million embryos of a reef sh
with tetracycline to determine how far the larvae
disperse. They examined 5000 juveniles to obtain
15 marked individuals. The authors estimated
that they had marked between 0.5% and 2% of
all embryos and therefore 1560% of juveniles
return to the natal population.
Elements and isotopes
Besides uorescent compounds, a range of ele-
ments (e.g., Sr, rare earth elements, Ennevor and
Beames 1993; Giles and Attas 1993; Ennevor 1994)
and isotopes (e.g., enriched isotopes of Ba and Sr,
Munro et al. unpublisheddata) have alsobeen used
to successfully mark sh via immersion. Strontium
is the element most commonly used to mark sh
(Brown and Harris 1995), but Sr:Ca ratios of
freshwater can be as much as that of marine waters
or higher (Kraus and Secor 2004) and therefore
potential exists to confuse natural Sr signatures
with articial Sr marks. This problemmay not be as
great for cephalopods found in marine environ-
ments since Sr:Ca of marine waters is relatively
constant. Only one study has used Sr to mark
cephalopod statoliths, but the objective was to
validate growth increments rather then determine
movement (Hurley et al. 1985). Squid (Illex illece-
brosus) statoliths were marked by feeding the
squid shrimp that had been soaked in a SrCl
2
solution (Hurley et al. 1985). Other elements
occurring in low concentrations (e.g., rare earth
elements) have had variable success in producing
marks in sh especially over short time scales
(Munro et al. unpublished data), but have not been
applied to cephalopods. Enriched stable isotopes
can be used to create unequivocal marks that
cannot be mistaken for a natural signature since
there is no way that a wild sh could have a similar
signature (Munro et al. unpublished data). Other
advantages of enriched stable isotope marking
include that it is stress-free to the sh, the isotopes
are naturally occurring and are stable (i.e. non-
radiogenic) and therefore pose no environmental
or human health risks, the method can be applied
to any life history stage, and standard equipment
(e.g., laser ablationICP-MS) canbe usedtoanalyse
the otoliths since the isotope ratios are shifted so
drastically (Munro et al. unpublished data). Whilst
enriched stable isotopes are expensive, small con-
centrations (e.g. 15 lg/l Ba and 100 lg/l Sr) are
required to produce clear shifts in isotopic ratios
(Munro et al. unpublished data). The work of
Munro et al. (unpublished data) was focused on
ngerlings of golden perch (Macquaria ambigua),
but there is potential for the technique to be used
on larvae. Presumably, this technique could also be
used to mark cephalopods, and then questions
related to movement and metapopulation dynam-
ics could be addressed.
The previous techniques described all require
marking of thousands of ngerlings via immer-
sion. A potentially easier method may be to mark
the mother in an effort to mark her subsequent
offspring. Recently, a new technique for arti-
cially mass marking sh larvae, transgenerational
marking, has been described (Thorrold et al.
2006). Briey, sh larvae are marked after gravid
females injected with enriched isotopes transfer
the isotope spike to the embryonic otoliths of
their offspring (Thorrold et al. 2006). Thorrold
et al. (2006) demonstrated that both a benthic-
spawning and a pelagic-spawning sh had
unequivocal isotope signatures over a range of
dose rates and that marked larvae were found for
at least 90 days after a single injection. This
method may also have potential for use on
cephalopods, but further work is required to
determine this. If the method is applicable to
cephalopods, then potential exists to mark indi-
viduals that form part of breeding aggregations
(e.g., giant Australian cuttlesh, Sepia apama)
and determine the degree of natal homing.
Natural tags
Natural tags are organisms, compounds or phys-
ical marks (e.g., colour patterns) that naturally
408 Rev Fish Biol Fisheries (2007) 17:401423
1 3
occur in the animal of interest and there is
variability in their occurrence between regions,
seasons, depth etc. The main advantage of these
types of tags is that all animals are tagged and
thus all specimens that are captured, regardless of
size, represent a recovery. Furthermore natural
behaviour is guaranteed throughout the entire
tagging-period. The disadvantage, however, is
the information stored in natural tags can be
difcult to read and/or interpret.
Parasites
Parasites have long been used as biological tags or
markers in shes (e.g., Sindermann 1983; Wil-
liams et al. 1992; MacKenzie and Abaunza 1998)
and can be used to examine movement/migration,
providing there is variability in degrees of host
infection or parasite genetics across the study
area, the parasite is easily found and recognized
in the host, and the parasite does not inuence the
hosts health or behaviour (Williams et al 1992).
After examining 2000 individuals from 10 species
of cephalopods in Galician waters, Gonza lez
et al. (2003) identied three ecological groupings
of parasite fauna, coastal, intermediate and neri-
to-oceanic, suggesting that the ecological niche of
a cephalopod species is more important in deter-
mining its parasite fauna than its phylogeny.
Similarly, distinct coastal and oceanic parasite
communities have been identied for a number of
Atlantic ommastrephid species (Gaevskaya 1977,
in Gonza lez et al. 2003; Gaevskaya and Nigma-
tullin 1978; Bargov 1982; Nigmatullin and Shu-
khgalter 1990, in Gonza lez et al. 2003).
Geographic differences in parasite fauna made
stock discrimination possible in the oceanic squid
O. bartramii (Bower and Margolis 1991) and T.
rhombus (Bower and Miyahara 2005), and indi-
rectly provided information on movement. How-
ever, explicit movement and migration studies
require more detailed information on parasite-
host specicity and parasite geographic distribu-
tion (Nagasawa and Moravec 2002). Variation in
infection by dicyemid mesozoans is found within
cephalopod families, species, and individuals,
with these parasites found in tropical, subtropical,
temperate and polar regions, making them poten-
tially useful for large-scale migration studies of
benthic or epibenthic species (Finn et al. 2005).
Parasites that infect juvenile shes at their
nursery grounds but not adults at their feeding or
spawning grounds are used to understand recruit-
ment migration in shes (Williams et al. 1992).
However, there is an almost complete lack of
information on parasites of cephalopod paralar-
vae (Vidal and Haimovici 1999), with parasites
identied in paralarvae of only two species (I.
argentinus, Vidal and Haimovici 1999; Sthenoteu-
this oualaniensis, Vecchione 1991), and the
method of infection not known in either case.
Much more research into the parasite fauna of
cephalopods is needed before parasites can be
reliably used as natural tags, however, there may
be the potential for parasites to provide a tagging
technique for paralarval cephalopods, which is
currently lacking.
Molecular approaches
Molecular genetic methods can be used to
estimate migration rates of individuals between
and among populations, but the estimates pro-
duced are fundamentally different from those
produced by physical tagging studies or direct
observation. Genetic methods cannot estimate
absolute numbers for contemporary migration,
but they do offer a very powerful approach for
estimating relative rates of gene ow among
populations averaged over long timescales, and
so are relevant to long-term changes in popula-
tion demographics and distributions. Theoreti-
cally, gene ow rates of only a few individuals per
generation (i.e. migration rates <1%) are high
enough to maintain genetic homogeneity among
populations. So the detection of signicant
genetic differences between areas or populations
indicates that very low rates of effective migration
are occurring, and the degree of genetic differen-
tiation gives an estimate of relative rates. Molec-
ular genetic approaches have been applied to a
wide variety of species for the estimation of
population connectivity and the inference of
migration rates (e.g., Palumbi 2003), although to
date their application to cephalopods has been
limited (see below).
Rev Fish Biol Fisheries (2007) 17:401423 409
1 3
Recent developments in genetic marker meth-
odologies (e.g., microsatellite DNA regions) and
analytical procedures (coalescent-based ap-
proaches and maximum likelihood e.g., MI-
GRATE, Beerli and Felsenstein 2001, or
Bayesian e.g., BAYESASS+, Wilson and Rannala
2003) to estimate long-term or contemporary
migration (respectively), hold the prospect of
more relevant estimates of migration rates gen-
erated from genetic data. These developments
also have taken the molecular genetic approach
closer to the direct observation and identication
of migration at the individual level. Improved
methods of estimating migration, identifying
clusters of individuals, and identifying the popu-
lation of origin of individuals are now available
(see review by Pearse and Crandall 2004). These
techniques have unravelled the complex dynamics
of migration, dispersal and the spatial and/or
temporal integrity of populations (Buonaccorsi
et al. 2005; Weetman et al. 2006), but their
potential contribution to understanding cephalo-
pod biology may be limited to those cephalopods
with patchy distributions, association of individ-
uals with small home ranges, and limited adult
migration or juvenile dispersal, such as reef-
associated squid and Nautilus, octopus species
with patchy distributions, and cuttlesh species
with restricted dispersal.
The large majority of genetic studies of ceph-
alopods conducted to date have involved squid
and these studies have shown that where no major
barriers to migration occur (such as land masses,
major hydrographic fronts, deep water, etc), squid
exhibit very low or no genetic differentiation
among populations throughout their geographical
range. Such a pattern is common to both myopsid
(e.g., Sepioteuthis australis, Triantallos and
Adams 2001; Loligo gahi, Shaw et al. 2004) and
oegopsid squid (e.g., T. pacicus, Kim 1993;
Katugin 2002; Ommastrephes bartramii, Katugin,
2002; Illex argentinus, Adcock et al. 1999; Berry-
teuthis magister, Katugin 1999).
Genetic homogeneity suggests that there is
effective dispersal/movement and interbreeding
across large geographical areas, at least on time-
scales of tens of generations. Where barriers to
adult and/or paralarval migration/movement do
occur, populations exhibit signicant genetic
divergence indicating breakdown of gene ow.
For example, gene frequencies in loliginid squid
are signicantly different among populations to
either side of cold upwelling systems on the
western coasts of both South America (L. gahi,
Shaw et al. 2004) and southern Africa (Loligo
reynaudii, Shaw et al., unpublished data), indicat-
ing that the upwelling is a complete barrier to
both adult and paralarval movement. Similarly,
stretches of deep water are indicated as barriers
to migration and dispersal of neritic species such
as S. australis (Triantallos and Adams 2001) and
L. forbesi (Shaw et al. 1999), which otherwise
exhibit panmixia across large geographical
ranges. Other barriers to gene ow in squid
include physical subdivision of species ranges
(Doryteuthis pealeii, Herke and Folz 2002), river
umes (Loligo plei, Herke and Folz 2002),
different water mass boundaries (separating the
genetically distinct peripheral form of S. aus-
tralis, Triantallos and Adams 2001), and semi-
isolated marine basins (B. magister, Katugin
2000).
Extensive population genetic studies of cuttle-
sh are limited to two species, Sepia ofcinalis and
S. apama. Both species exhibit the same genetic
pattern of isolation-by-distance (IBD), where
populations show increasing genetic differentia-
tion with increasing geographical distance, indi-
cating locally restricted gene ow (i.e. generation-
on-generation movement) over surprisingly small
scales (<300 km) for such mobile species (Pe rez
Losada et al. 1999, 2002; Kassahnet al. 2003). Both
species also exhibit evidence of phylogeographic
discontinuities associated with specic geographi-
cal features of either current (Almeria-Oran and
Ionian/Aegean Sea hydrographic front systems in
the Mediterranean, Pe rez Losada et al. 2002, 2007)
or historical importance (Bass Strait, Kassahn
et al. 2003; Gibraltar Strait and Siculo-Tunisian
Strait, Pe rez Losada et al. 2007). The important
point concerning such historical genetic patterns
for the consideration of migration is the fact that
historical subdivision of cuttlesh populations
caused by sea level changes during Pleistocene
glaciations are still evident in the genetic structur-
ing of present day populations indicating the slow
timescale on which gene ow is occurring in these
species: effective population movement/migration
410 Rev Fish Biol Fisheries (2007) 17:401423
1 3
rates along coasts must be very low. Low sea levels
during the Pleistocene period also resulted in the
isolation of demersal deep-water B. magister pop-
ulations within the Sea of Japan basin so that they
have accumulated notable genetic differences
(compared to conspecic populations from adja-
cent areas of the Northwest Pacic) and evolved
into a separate subspecies (Katugin 2000).
The few genetic studies of octopus to date, all
involving Octopus vulgaris, indicate genetic
homogeneity over large areas (many 100s of
km) but with some evidence of differentiation at
large geographical scales, for example between
the western and eastern Mediterranean (Casu
et al. 2002; Maltagliati et al. 2002). The microsat-
ellite DNA study by Murphy et al. (2002) also
described differentiation at more local scales
(100s of km), associated with discontinuities in
population distributions. These results indicate
that the extensive gene ow and widespread
genetic homogeneity predicted from the posses-
sion of a pelagic paralarval dispersal stage in O.
vulgaris may not necessarily be realised in natural
populations, and that gene ow and paralarval
dispersal may be locally restricted.
Molecular genetics offers a powerful approach
to estimating realised effective migration rates
among populations, and continuing developments
in markers and analytical techniques hold the
promise of more detailed identication of mi-
grants. However the biological and life history
characteristics of many cephalopod species mean
that assignment and migration estimation meth-
ods may have limited success, and careful consid-
eration is needed in matching species with
suitable genetic techniques. To date genetic
studies indicate that migration/dispersal in squids
is extensive but can be blocked by major ocean-
ographic features, and in cuttlesh and octopus
migration/dispersal is more locally restricted than
predictions from life history parameters would
suggest (e.g., Shaw et al. 1999, 2004; Murphy
et al. 2002; Pe rez Losada et al. 2002, 2007).
Elemental signatures: statoliths as
environmental recorders
Chemical analyses of the naturally occurring
elemental and/or isotopic signatures of sh otoliths
are widely used and have been a useful tool for
reconstructing a shs life history, including eluci-
dating migration pathways (e.g., Tsukamoto et al.
1998; Campana 1999; Elsdon and Gillanders 2005,
2006). Chemical investigations on cephalopod
statoliths are few, but there is growing interest in
this eld of research. One study has also analysed
C and N isotopes of the beak, primarily to infer
trophic relationships, but also to indicate life long
residency in the same water mass or migration
between different areas (Cherel and Hobson 2005;
see also Takai et al. 2000 for example using muscle
tissue). Such analyses are based on the assump-
tions that once deposited the otolith/statolith
material is not resorbed or reworked over time,
the structure of interest continues to growthrough-
out the life of the organism, and that the chemical
and physical environment in which the organism is
found is reected in the chemistry of the otolith/
statolith (Campana 1999). The chemical informa-
tion together with the growth increments found in
these structures can be coupled to provide unprec-
edented life stage-specic information on the
movements of shes/cephalopods.
Calcied structures can provide an accurate
chronology of exposure to particular environ-
mental conditions, including salinity, temperature
and composition of ambient water, therefore
providing information on movement between
different water masses (for reviews regarding sh
and sampling and analyses issues see Campana
1999; Elsdon and Gillanders 2003a; Gillanders
2005a, b). Although a number of studies have
investigated how otolith chemistry changes with
different environmental parameters (e.g., Elsdon
and Gillanders 2002, 2003b, 2004), relatively few
studies have focused on statoliths (but see Ikeda
et al. 1997; Zacherl et al. 2003a, b; Arkhipkin
et al. 2004; Landman et al. 2004; Zumholz et al.
2006, this issue, in press a, b). A negative
relationship between levels of barium in the
statoliths of Sepia ofcinalis and environmental
temperature was found in a laboratory study
(Zumholz et al. in press a), and a negative
relationship between water temperature and
Sr:Ca in statoliths of eld caught squid has also
been determined (Ikeda et al. 1998; Arkhipkin
et al. 2004). These results suggest that changes in
Sr:Ca and/or Ba:Ca (and potentially other ele-
Rev Fish Biol Fisheries (2007) 17:401423 411
1 3
ments such as U:Ca) may indicate movement to
colder or warmer waters. For example, an
increase in Sr:Ca, Ba:Ca (and U:Ca) in the outer
region of G. fabricii statoliths is suggestive of
movement to cooler water (Zumholtz et al. in
press b). It should be noted that some other eld
studies have not been able to nd a relationship
between statolith chemical composition and tem-
perature (e.g., Ikeda et al. 2003) and therefore
further laboratory experiments on other species
are needed. Lack of a relationship also highlights
the need to have data on water chemistry to
properly interpret such analyses. Likewise, oxy-
gen isotopes have also been used to infer move-
ment (e.g., Landman et al. 2004).
Besides relating elemental analyses to environ-
mental parameters, which typically requires
experimental work to validate such relationships,
it is also possible to determine natal origins of
sub-adults/adults. Such an analysis requires using
known origin hatchlings as a baseline data set and
then retrospectively determining the natal origin
of adults by analysing the region of the statolith
formed during its paralarval/early juvenile life
(e.g., S. australis, Pecl unpublished data) (for
examples using sh see Gillanders and Kingsford
1996; Gillanders 2002). Before such analyses can
proceed it is rst necessary to demonstrate that
spatial differences in elemental signatures of
hatchlings are found, which may not necessarily
be the case (e.g., Sepia apama, Gillanders unpub-
lished data). Several other assumptions also exist,
namely that all source populations have been
sampled (this assumption is also necessary for
molecular methods) and that the temporal stabil-
ity of elemental signatures is known or alterna-
tively that adults are matched to the appropriate
year class of paralarvae/juveniles (see Gillanders
2005b for further details).
Spatially resolved statolith analyses have great
potential to provide information on life history,
habitat use and migrations of cephalopods. How-
ever, due to their lack of growth increments (Tait
1980) octopus statoliths, unlike other cephalopod
statoliths, are of little use for time-specic trace
element studies. Stylets (also known as vestigial
shells) are a little known structure unique to the
octopoda and are thought to represent a remnant
shell. Their composition is currently unknown,
however, the stylet microstructure of Octopus
pallidus has been found to have distinct concen-
tric regions, a visible pre-hatch nucleus and age-
related growth (daily growth increments) (Dou-
bleday et al. 2006). Due to this microstructure,
stylets are likely to incorporate elements from the
environment on a chronological basis and there-
fore have the potential to address questions on
the dispersal patterns of both juveniles, including
paralarvae, and adults.
For studies using trace elements to reconstruct
the life-history of individuals the main restric-
tion at present is the lack of experimental
laboratory data examining the relationship be-
tween statolith (or stylet) chemistry and a range
of environmental parameters. Such information is
required for each species of interest since there
are likely to be different responses for different
species. However, for those studies that only aim
to assign adults to their natal origin, there is no
need to understand why elements vary, only that
they do and this allows individuals to be assigned
back to their natal habitat.
Tracking shing eets
Since the late 1990s the use of satellite data
showing the location of shing lights have been
increasingly used to examine the distribution and
abundance of squid sheries, which use lights to
attract squid, operating in various regions around
the globe. The advantage of this technique is it
allows for remote monitoring of species, which
migrate in oceanic waters, and as such can be
difcult to study. The disadvantages are this
technique monitors the movement of the shing
eet, not that of the squid directly, and it is only
applicable to those sheries that use light to
attract squid, however, these sheries are the
largest and therefore often of the most interest.
The majority of these are far seas jig sheries for
ommastrephid squid, with the shing eets con-
sisting of as many as 20,000 vessels (Kiyofuji and
Saitoh 2004) each using up to 300 kW for light
production (Rodhouse et al. 2001).
The emission of light from squid shing vessels
is detectable using imagery from the United
States Air Force Defence Meteorological Satel-
412 Rev Fish Biol Fisheries (2007) 17:401423
1 3
lite ProgramOperational Linescan System
(DMSP-OLS) (Rodhouse et al. 2001; Maxwell
et al. 2004) which allows the spatial distribution
of shing eets to be observed at a high level of
resolution, at around 2.7 km (Cho et al. 1999).
DMSP-OLS data have been successfully ground-
truthed by comparing the location of shing
vessels with synoptic data from aerial surveys
(Maxwell et al. 2004) and Platform Transmitter
Terminals xed to shing vessels (Waluda et al.
2004). Using DMSP-OLS data eet distribution
can be tracked on a daily basis if required, and
several studies have found that changes in eet
distribution can be indicative of the eet tracking
squid as they undertake migrations (e.g., I.
argentinus, Haimovici et al. 1998; Waluda et al
2002; T. pacicus, Kiyofuji and Saitoh 2004).
Whilst high intensity shing lights are visible
from space, ordinary deck lights from shing
vessels are generally not detected using DMSP-
OLS (Maxwell et al. 2004) at the current level of
image resolution. Perhaps, as satellite resolution
improves, those squid sheries using small boats
with weaker lights and hand-jigging methods,
such as the artisanal shery for Dosidicus gigas in
the Gulf of California (Morales-Bojo rquez et al.
2001), or the shery targeting Loligo reynaudii off
the coast of South Africa (Roberts and Sauer
1994) will be observed in satellite imagery in the
future, thus greatly expanding the use of this
method.
The inuence of environmental variability on
movement and migration
The embryonic development of many cephalo-
pods has been shown to be highly temperature
dependent, with eggs generally developing faster
in warmer waters (ODor et al. 1982; Boyle et al.
1995; Forsythe et al. 2001). Spawning regions and
the distribution of egg masses have been shown to
be linked to specic temperature zones (Roberts
and Sauer 1994; Ichii et al. 2004; Bower and Ichii
2005), with the distribution of many paralarval
and juvenile squid linked to local regional ocean-
ography (Vecchione 1999; Dawe et al. 2000;
Sakurai et al. 2000; Waluda et al. 2001b; Ander-
son and Rodhouse 2002). Pelagically spawning
ommastrephid squid appear to utilise water
masses in which density increases with depth
(due to decreasing temperature or increasing
salinity), allowing neutrally buoyant egg masses
to be held within the mesopelagic zone and
transported to suitable areas for hatching
(ODor and Balch 1985; Bakun and Csirke
1998). Even in the deep sea, brooding deep-sea
octopus Graneledone spp. have been observed in
association with cold seep regions (Drazen et al.
2003).
Various studies have linked environmental
conditions during the spawning and hatching of
cephalopods with recruitment success or failure,
with availability of thermal resources shown to
inuence population size in the following season
(Bower 1996; Sakurai et al. 2000; Yatsu et al.
2000; Waluda et al. 2001a; Waluda and Rodhouse
2006). Sea surface temperature is the most easily
obtained, and therefore the most common param-
eter used to assess links between cephalopod
distribution and environment, providing an easily
obtained proxy for oceanographic variability.
Other factors such as rainfall, river discharge
(Sobrino et al. 2002), water turbidity (Roberts
and Sauer 1994; Faure et al. 2000; Scho n et al.
2002), solar ux, sea level pressure, wind speed,
wind direction (Denis et al. 2002) sea level
variability (Miyahara et al. 2005) and salinity
(Laughlin and Livingston 1982) may also be
important in inuencing the distribution and
migration of various cephalopod populations.
Local oceanographic processes during the early
life history stages may be particularly important
in retaining paralarval squid in areas of high food
availability. Retention processes have been
shown to favour the recruitment of many ceph-
alopod species (Table 1). Oceanographic vari-
ability has also been shown to alter the patterns
and timing of the migrations of some coastal
species, such as octopods, loliginids and sepioids,
suggesting that migration patterns may be linked
to specic water masses. For example, the
strength of the Atlantic currents entering
the English Channel and North Sea can inuence
the timing of S. ofcinalis (Wang et al. 2003) and
L. forbesi migrations (Holme 1974; Waluda and
Pierce 1998; Robin and Denis 1999), with the
migration of L. forbesi into the English Channel
Rev Fish Biol Fisheries (2007) 17:401423 413
1 3
Table 1 The inuence of oceanographic processes on cephalopod migration and sheries
Species Region Oceanographic
process
Effect References
Octopus
vulgaris
Central
East
Atlantic
Retention of
eggs/
juveniles
Increased retention with increased upwelling at
Arguin Bank, Mauritania
Faure et al. (2000)
Dosidicus
gigas
Eastern
Pacic
Retention of
eggs/juveniles
Increased retention with increased upwelling off
Peru and Central America
Vecchione (1999) and
Waluda et al. (2006)
Illex
illecebrosus
Northwest
Atlantic
Retention of
eggs/juveniles
Increased retention via transport processes in
the Gulf Stream and slope water
Perez and ODor (1998)
and Dawe et al. (2000)
Illex
argentinus
Southwest
Atlantic
Retention of
eggs/juveniles
Retention related to mesoscale variability at
conuence of Falkland (Malvinas) and Brazil
Currents
Brunetti and Ivanovic
(1992), Leta (1992) and
Waluda et al. (2001a)
Doryteuthis
opalescens
Northeast
Pacic
Retention of
eggs/juveniles
Increased retention via tidally reversing currents
and inshore entrainment in Southern
California Bight
Zeidberg and Hamner
(2002)
Octopus
vulgaris
Northeast
Atlantic
Retention of
eggs/juveniles
Increased retention with increased upwelling,
Ria of Vigo, Spain
Gonza lez et al. (2005)
Loligo
vulgaris
Northeast
Atlantic
Retention of
eggs/juveniles
Increased retention with increased upwelling,
Ria of Vigo, Spain
Gonza lez et al. (2005)
Illex
argentinus
Southwest
Atlantic
Frontal
processes at
the shelf edge
Paralarval distribution related to strong thermal
gradients between Brazil Current and the
convergence front
Leta (1992) and Bazzino
et al. (2005)
Todarodes
pacicus
Northwest
Pacic
Frontal
processes at
the shelf edge
Paralarvae/juveniles transported via the
Kuroshio Extension to Sea of Japan
Sakurai et al. (2000) and
Kawabata et al. (2006)
Illex
illecebrosus
Northwest
Atlantic
Frontal
processes at
the shelf edge
Enhanced shoreward transport of paralarvae/
juveniles due to increased meandering of the
Gulf Stream
Rowell et al. (1985),
Vecchione and Roper
(1986) and Dawe et al.
(2000)
Thysanoteuthis
rhombus
Northwest
Pacic
Frontal
processes at
the shelf edge
Transport of juveniles through the Tsushima
Strait via Tsushima current
Bower and Miyahara
(2005)
Todarodes
pacicus
Northwest
Pacic
Fishery
aggregations
at frontal
regions
Fishery located at boundary between Kuroshio
and Oyashio currents
Cho et al. (1999)
Illex
argentinus
Southwest
Atlantic
Fishery
aggregations
at frontal
regions
Fishery located at frontal regions between
Falkland current and coastal shelf waters
Waluda et al. (2001b)
Ommastrephes
bartramii
North
Pacic
Fishery
aggregations
at frontal
regions
Increased catches associated with strong
thermal gradient at Subarctic boundary
Ichii et al. (2004), Bower
and Ichii (2005)
Ommastrephes
bartramii
Northwest
Pacic
Rings,
meanders,
streamers
Fishery occurs in streamers shed from the
Kuroshio, Oyashio and Tsushima-Tsugaru
Current systems
Sugimoto and Tameishi
(1992)
Pterygioteuthis
giardi
Southwest
Pacic
Rings,
meanders,
streamers
Squid associated with a warm core eddy of East
Australia Current, Tasman Sea
Brandt (1983)
Brachioteuthis
riisei
Southwest
Pacic
Rings,
meanders,
streamers
Squid associated with a warm core eddy of East
Australia Current, Tasman Sea
Brandt (1983)
Martialia
hyadesi
Southern
Ocean
Rings,
meanders,
streamers
Squid associated with warm core ring at
Northeast Georgia Rise, Antarctic Polar
Frontal Zone
Rodhouse et al. (1996)
414 Rev Fish Biol Fisheries (2007) 17:401423
1 3
occurring earlier in years of higher than average
temperature (Sims et al. 2001). Variability in
current systems may also shift squid from their
usual feeding areas. In the south Atlantic,
westward shifting of the Falkland Current has
been shown to displace part of the L. gahi
population to a region north of the usual feeding
area (Arkhipkin et al. 2006), whereas in the north
Atlantic a southward shift in the position of the
Gulf Stream (coupled with increased meandering
and thus improved paralarval retention) has been
shown to favour high abundance of I. illecebrosus
in Canadian waters, at the north of the species
range (Dawe et al. 2000).
Those cephalopods that undertake the longest
migrations, spanning several thousands of kilo-
metres are generally large oceanic ommastrephids
associated with high-energy western boundary
current systems. Large boundary current systems
provide both a highly productive environment
and an environment where appropriate tempera-
tures are available at all life stages (ODor and
Coelho 1993), however, they are environmentally
unpredictable areas. As such, the adult squid
migrate from these boundary current systems to
areas with lower productivity but more environ-
mentally stability in order to spawn (Rodhouse
and Nigmatullin 1996). The migration of young
stages of many species is facilitated by their
association with current systems, with paralarval
or juvenile squid often associated with frontal
processes at the shelf edge (Sakurai et al. 2000)
(see Table 1 for examples). Thus, juvenile squid
take advantage of high-speed transport systems to
assist their migration to feeding areas. Current
systems such as the Gulf Stream provide a rapid
transport system, of up to 1,000 km per week for
juvenile squid (Rowell et al. 1985). The further
poleward the young squid travel, the larger they
grow, the longer they take to return to spawning
grounds and the greater their fecundity.
Cephalopod abundance and distribution can be
strongly inuenced by upwelling, which are areas
of high productivity, with populations apparently
shifting to less common parts of their species
range during periods of extreme warming and
reduced upwelling (Ichii et al. 2002; Zeidberg and
Hamner 2002; Waluda and Rodhouse 2006).
Variability in upwelling has also been found to
restrict the movement of L. reynaudii to spawning
areas off the coast of South Africa (Scho n et al.
2002), and to inuence the distribution of Sthe-
noteuthis pteropus around the coast of western
Africa (Zuyev et al. 2002).
Frontal regions (dened by large temperature
changes over a small distance) may be important
for the accumulation of large concentrations of
cephalopods (see Table 1 for examples), with the
inuence of mesoscale processes at fronts such as
the formation of rings, meanders and streamers
also shown to inuence the distribution of om-
mastrephid squid (see Table 1 for examples).
Large-scale environmental variability may
change the distribution patterns of squid species,
and effect shifts in timing of seasonal movements
and migrations, probably by altering the avail-
ability of thermal resources (Sims et al. 2001).
The inuence of the El Nin o-La Nin a, Southern
Oscillation Index (SOI), North Atlantic Oscilla-
tion (NAO) and Trans-Polar Index (TPI) have
been shown to inuence the movement and
migration of cephalopod populations in various
locations around the globe, and the inuence of
these phenomena can be seen in locations far
removed from the source of variability, mediated
by teleconnections inuencing local oceanogra-
phy (Waluda et al. 1999).
Variability in environment related to the
Southern Oscillation and TPI were shown to
have a large inuence on cephalopod species of
importance to sheries, particularly during the
juvenile and adult phases of the life cycle respec-
tively (Waluda et al. 2004). In the Northern
Hemisphere, interannual variability in the timing
of L. forbesi migrations has been shown to be
related to variability in the strength of the NAO
(Sims et al. 2001). Higher abundances of I.
illecebrosus were shown to be associated with a
negative NAO index (Dawe et al. 2000), and the
summer biomass of Eledone cirrhosa in the
Ligurian Sea was shown to be related to the
NAO index during the previous winter (Orsi
Relini et al. 2006). In the eastern Pacic, the
inuence of El Nin o variability has been observed
in sheries for Doryteuthis opalescens off Califor-
nia (Jackson and Domeier 2003; Maxwell et al.
2004; Reiss et al. 2004; Zeidberg et al. 2006) and
D. gigas off Central and South America (Ichii
Rev Fish Biol Fisheries (2007) 17:401423 415
1 3
et al. 2002; Waluda et al. 2006). Warming (El
Nin o) events are generally seen to lead to a
reduction in squid abundance in common shery
areas coupled with an increase in catches outside
these areas (Pearcy 2002; Zeidberg et al. 2006),
suggesting El Nin o events could potentially cause
a shift in distribution rather than a decline in
overall population size.
Interest in the inuence of environmental
parameters on cephalopod movement/migration
at the various life cycle stages is increasing. Much
work has been done examining environmental
inuences on the abundance and distribution of
cephalopods (particularly those which form sig-
nicant sheries), and the development of models
utilising some of the observations described here
to predict abundance and distributions are
becoming more common (Roberts et al. 1998;
Waluda et al. 1999; Agnew et al. 2002; Denis
et al. 2002; Ichii et al. 2002; Pierce and Boyle
2003; Reiss et al. 2004; Zuur and Pierce 2004;
Miyahara et al. 2005; Sacau et al. 2005), enabling
a better understanding of the processes inuenc-
ing cephalopod population variability. Under-
standing these patterns will become increasingly
important, with increased ocean temperatures
predicted as a consequence of global warming,
which could disrupt or change migration patterns
for some cephalopod species, as is predicted for
migrating pacic salmon (Welch et al. 1998).
Conclusion
In summary, over recent years we have seen many
exciting developments in terms of our increasing
ability to examine movement and migration of
cephalopods, and understanding the inuence of
environmental processes on this movement. Still
many challenges lie ahead and it is hoped that this
review can spark some interest in tackling the key
questions that remain. One of the major questions
that needs addressing is how to tag and track
paralarval cephalopods, as our knowledge of this
life stage is far less than that of adults. This is
particularly important; as it is this stage which is
most affected by environmental inuences, par-
ticularly temperature and food uctuations.
Natural tags, such as parasites or elemental
signatures, hold promise for tracking paralarval
cephalopods, as each animal caught is a recap-
ture, however, large numbers of paralarvae need
to be examined rst to dene the parasitic and
elemental characteristics of various populations
before these techniques could be used routinely.
Perhaps, chemical tagging of paralarvae through
maternal transfer will prove to be a successful
technique, as large numbers of offspring could be
tagged at once. However, extensive laboratory
studies are rst required to determine if this
technique is viable for cephalopods.
Acknowledgements This review came about as a result
of discussions held at the Cephalopod Movement and
Migration Workshop held as part of the 2006 CIAC
Conference in Hobart. The authors would like to thank all
the participants for their valuable contribution to the
discussion. We are also grateful to Hideaki Kidokoro, Ken
Mori, Yoshikazu Nakamura, Kazuya Nagasawa, and
Mitsuo Sakai for providing information on recent tagging
experiments in Japan. Thanks also to Stephanie Semmens
for editing the manuscript. Funding to JMS and GTP to
study cephalopod movement and migration comes from
Australian Research Council Linkage grants and
Postdoctoral Fellowships (C00107233 and LP0347556
respectively). KZ was funded by the Deutsche
Forschungesgemeinschaft (DFG PI 203/11-1, 11-2, 11-3,
HA 2100/9-1). Travel to CIAC by PWS was supported by
the Royal Society of London.
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