Semmems Et Al 2007

RESEARCH PAPER

Approaches to resolving cephalopod movement andmigration patterns

Jayson M. Semmens Æ Gretta T. Pecl Æ Bronwyn M. Gillanders ÆClaire M. Waluda Æ Elizabeth K. Shea Æ Didier Jouffre Æ Taro Ichii ÆKarsten Zumholz Æ Oleg N. Katugin Æ Stephen C. Leporati Æ 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

influenced by the prevalence and scale of their

movements. Environmental parameters, such as

sea temperature and oceanographic processes,

have a large influence 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 fished. 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. LeporatiMarine Research Laboratories, TasmanianAquaculture and Fisheries Institute, University ofTasmania, Private Bag 49, Hobart, TAS 7001,Australiae-mail: [email protected]

B. M. GillandersSouthern Seas Ecology Laboratories, School of Earthand Environmental Sciences, University of Adelaide,Adelaide, SA 5005, Australia

C. M. WaludaBiological Sciences Division, British Antarctic Survey,High Cross, Madingley Road, Cambridge CB3 0ET,UK

E. K. SheaDelaware Museum of Natural History, P.O. Box 3937,Wilmington , DE 19807, USA

D. JouffreUnite OSIRIS, IRD, BP 1386, Dakar, Senegal

T. IchiiNational Research Institute of Far Seas Fisheries,2-12-4 Fukuura, Kanazawa-ward, Yokohama-City236-8648, Japan

K. ZumholzLeibniz-Institute of Marine Sciences, IFM-GEOMAR, Dusternbrooker Weg 20, D-24105 Kiel,Germany

O. N. KatuginPacific Fisheries Research Centre, 4 ShevchenkoAlley, Vladivostok 690950, Russia

P. W. ShawSchool of Biological Sciences, Royal HollowayUniversity of London, Egham TW20 0EX, UK

123

Rev Fish Biol Fisheries (2007) 17:401–423

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 fish.

Geographic differences in parasite fauna have

also been used to indirectly provide movement

information, however, explicit movement studies

require detailed information on parasite-host

specificity 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 identification of mi-

grants. To date genetic studies indicate that

migration in squids is extensive but can be

blocked by major oceanographic features, and in

cuttlefish and octopus migration is more locally

restricted than predictions from life history

parameters would suggest. Satellite data showing

the location of fishing lights have been increas-

ingly used to examine the movement of squid

fishing 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 (O’Dor 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 (O’Dor 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 influencing population size, abun-

dance and distribution. One of the major factors

influencing 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 influence the

response of cephalopods to environmental

change, and the abundance and location of

cephalopod populations and associated fisheries

is strongly influenced by the prevalence and scale

of their movements (Boyle and Boletzky 1996).

Those populations which undertake the largest

migrations are prone to the largest fluctuations in

population abundance (O’Dor 1992; Dawe et al.

2000). Particularly in ommastrephid squid, annual

fluctuations 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 beneficial 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/migrationspatterns/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 fish.

These methods are divided into five 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 fishing fleets.

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) 17:401–423

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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 influenced by factors such as level and extent

of fishing (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,

fisher apathy, resentment of research/manage-

ment and insufficient rewards.

Extensive studies of the annual spawning

migrations of the ommastrephid squid, Todarodes

pacificus, one of the largest single species ceph-

alopod fisheries in the world, has seen over 1

million squid tagged in the Sea of Japan and the

North Pacific 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 fished in large offshore fishing

zones (e.g., 0% for Illex illecebrosus in New-

foundland, Hurley and Dawe 1981; 2.5% for T.

pacificus, Nagasawa et al. 1993), whereas recap-

ture rates are generally much higher in inshore

waters (e.g., 19–32% 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 fishery is important

for tag-recapture studies if the migration routes of

the various species/populations are to be correctly

defined (e.g., T. pacificus, Nakamura and Mori

1998; Mori and Nakamura 2001). This spatial

coverage is only possible if the fishery 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 fishing effort in the Southern Gulf and

Pacific Ocean (Markaida et al. 2005).

The Japanese T. pacificus 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. pacificus,

where 20,000–30,000 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 officinalis, 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 1974–1985 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) 17:401–423 403

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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 cuttlefish (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-fishing fleet. The percentage of

recaptures varied from 0% to 49% depending on

the tagging location along the shelf, with low

recapture rates where few professional fishermen

were present (Domain et al. 2002), again high-

lighting the link between the success of tag-

recapture programs and the spatial coverage of

the fishery (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

dofleini 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 fisheries sam-

pling demonstrated that E. dofleini 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.

dofleini 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

difficult 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.

Cuttlefish (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 officinalis (approximately

10 cm ML) using fluorescent 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 fluorescent 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 field (Replinger and Wood in

press), and may have potential for tag-recapture

of paralarval cephalopods, as small fish have been

tagged and recaptured using VIE tags (e.g., 8 mm

TL reef fish, Frederick 1997).

Electronic tags

These are generally electronic devices that are

implanted or attached to the animal and have


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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 fixed 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 1950’s to study behaviour and physiol-

ogy, particularly in fish (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 fisheries 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 20–100 mm, however, the technology

is getting smaller all the time, with the new

generation of tags being significantly 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 cuttlefish 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. dofleini 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 fish, 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 fish 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 100’s

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


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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 Pacific 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 benefit to inshore species, such as

loliginids, sepioids and octopods.

There have been relatively few acoustic telem-

etry studies of oceanic squid, due to the difficul-

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 Pacific, 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 fishing fleets 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 fish

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 identified automat-

ically. However, the tag has to pass close by a

reader for the animal to be identified, 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 fishways (Castro-Santos

et al. 1996) or ‘flat-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

field (in lairs) and captive Octopus tetricus and

captive Octopus maorum. All octopus retained

the tags for the life of the study (captive:

14 months; field: 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 fishing vessels and fish processors able to

be provided with automatic detectors that record

tag ID’s 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. pacificus, to increase the

tag reporting rate. These tags and auto-readers

have recently been trialled in the southern rock

lobster fishery 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 field 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


123

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 (30–80 mm) and relatively expensive.

However, an advantage is that like acoustic tags

they provide fishery 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 fish

and sharks (see Arnold and Dewar 2001).

Only three published studies have used archi-

val tags on cephalopods (O’Dor et al. 2002;

Jackson et al. 2005; Gilly et al. 2006). Interest-

ingly, the first 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., fluorescent chemicals, elements and iso-

topes) into calcified 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 sacrifice

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 fluorescent markers to exam-

ine movement, however, squid statoliths have

been routinely marked with the fluorescent 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


123

immersion of the animals in solutions of alizarin

complexone. Subadult octopus showed the fluo-

rescent mark on their statoliths when recaptured

after 31 days (Sakaguchi et al. 2000). These stud-

ies suggest that fluorescent 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 fish

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 15–60% of juveniles

return to the natal population.

Elements and isotopes

Besides fluorescent 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. unpublished data) have also been used

to successfully mark fish via immersion. Strontium

is the element most commonly used to mark fish

(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 artificial Sr marks. This problem may 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 SrCl2solution (Hurley et al. 1985). Other elements

occurring in low concentrations (e.g., rare earth

elements) have had variable success in producing

marks in fish 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 fish 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 fish, 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 ablation ICP-MS) can be used to analyse

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

fingerlings 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 fingerlings 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 artifi-

cially mass marking fish larvae, transgenerational

marking, has been described (Thorrold et al.

2006). Briefly, fish 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 fish 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 cuttlefish, 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


123

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

difficult to read and/or interpret.

Parasites

Parasites have long been used as biological tags or

markers in fishes (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 influence the

host’s health or behaviour (Williams et al 1992).

After examining 2000 individuals from 10 species

of cephalopods in Galician waters, Gonzalez

et al. (2003) identified 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 identified for a number of

Atlantic ommastrephid species (Gaevskaya 1977,

in Gonzalez et al. 2003; Gaevskaya and Nigma-

tullin 1978; Bargov 1982; Nigmatullin and Shu-

khgalter 1990, in Gonzalez 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 specificity 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 fishes at their

nursery grounds but not adults at their feeding or

spawning grounds are used to understand recruit-

ment migration in fishes (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

identified 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 flow among

populations averaged over long timescales, and

so are relevant to long-term changes in popula-

tion demographics and distributions. Theoreti-

cally, gene flow 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 significant

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).


123

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 identification

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 cuttlefish 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, Triantafillos and

Adams 2001; Loligo gahi, Shaw et al. 2004) and

oegopsid squid (e.g., T. pacificus, 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 significant genetic

divergence indicating breakdown of gene flow.

For example, gene frequencies in loliginid squid

are significantly 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 (Triantafillos and Adams 2001) and

L. forbesi (Shaw et al. 1999), which otherwise

exhibit panmixia across large geographical

ranges. Other barriers to gene flow in squid

include physical subdivision of species ranges

(Doryteuthis pealeii, Herke and Folz 2002), river

flumes (Loligo plei, Herke and Folz 2002),

different water mass boundaries (separating the

genetically distinct ‘peripheral form’ of S. aus-

tralis, Triantafillos and Adams 2001), and semi-

isolated marine basins (B. magister, Katugin

2000).

Extensive population genetic studies of cuttle-

fish are limited to two species, Sepia officinalis 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 flow (i.e. generation-

on-generation movement) over surprisingly small

scales (<300 km) for such mobile species (Perez

Losada et al. 1999, 2002; Kassahn et al. 2003). Both

species also exhibit evidence of phylogeographic

discontinuities associated with specific geographi-

cal features of either current (Almeria-Oran and

Ionian/Aegean Sea hydrographic front systems in

the Mediterranean, Perez Losada et al. 2002, 2007)

or historical importance (Bass Strait, Kassahn

et al. 2003; Gibraltar Strait and Siculo-Tunisian

Strait, Perez Losada et al. 2007). The important

point concerning such historical genetic patterns

for the consideration of migration is the fact that

historical subdivision of cuttlefish 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 flow is occurring in these

species: effective population movement/migration


123

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 conspecific populations from adja-

cent areas of the Northwest Pacific) 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 flow 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 flow 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 identification 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 cuttlefish 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; Perez Losada et al. 2002, 2007).

Elemental signatures: statoliths as

environmental recorders

Chemical analyses of the naturally occurring

elemental and/or isotopic signatures of fish otoliths

are widely used and have been a useful tool for

reconstructing a fish’s 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 field 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 grow through-

out the life of the organism, and that the chemical

and physical environment in which the organism is

found is reflected 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-specific information on the

movements of fishes/cephalopods.

Calcified 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 fish

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 officinalis 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 field 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-


123

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 field

studies have not been able to find 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 fish see Gillanders and Kingsford

1996; Gillanders 2002). Before such analyses can

proceed it is first 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-specific 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 fishing fleets

Since the late 1990s the use of satellite data

showing the location of fishing lights have been

increasingly used to examine the distribution and

abundance of squid fisheries, 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

difficult to study. The disadvantages are this

technique monitors the movement of the fishing

fleet, not that of the squid directly, and it is only

applicable to those fisheries that use light to

attract squid, however, these fisheries are the

largest and therefore often of the most interest.

The majority of these are far seas jig fisheries for

ommastrephid squid, with the fishing fleets 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 fishing vessels

is detectable using imagery from the United

States Air Force Defence Meteorological Satel-


123

lite Program—Operational Linescan System

(DMSP-OLS) (Rodhouse et al. 2001; Maxwell

et al. 2004) which allows the spatial distribution

of fishing fleets 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 fishing

vessels with synoptic data from aerial surveys

(Maxwell et al. 2004) and Platform Transmitter

Terminals fixed to fishing vessels (Waluda et al.

2004). Using DMSP-OLS data fleet distribution

can be tracked on a daily basis if required, and

several studies have found that changes in fleet

distribution can be indicative of the fleet tracking

squid as they undertake migrations (e.g., I.

argentinus, Haimovici et al. 1998; Waluda et al

2002; T. pacificus, Kiyofuji and Saitoh 2004).

Whilst high intensity fishing lights are visible

from space, ordinary deck lights from fishing

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 fisheries using small boats

with weaker lights and hand-jigging methods,

such as the artisanal fishery for Dosidicus gigas in

the Gulf of California (Morales-Bojorquez et al.

2001), or the fishery 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 influence of environmental variability onmovement 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 (O’Dor 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 specific 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

(O’Dor 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

influence 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; Schon et al.

2002), solar flux, 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 influencing 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 specific water masses. For example, the

strength of the Atlantic currents entering

the English Channel and North Sea can influence

the timing of S. officinalis (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


123

Table 1 The influence of oceanographic processes on cephalopod migration and fisheries

Species Region Oceanographicprocess

Effect References

Octopusvulgaris

CentralEastAtlantic

Retention ofeggs/juveniles

Increased retention with increased upwelling atArguin Bank, Mauritania

Faure et al. (2000)

Dosidicusgigas

EasternPacific


Increased retention with increased upwelling offPeru and Central America

Vecchione (1999) andWaluda et al. (2006)

Illexillecebrosus

NorthwestAtlantic


Increased retention via transport processes inthe Gulf Stream and slope water

Perez and O’Dor (1998)and Dawe et al. (2000)

Illexargentinus

SouthwestAtlantic


Retention related to mesoscale variability atconfluence of Falkland (Malvinas) and BrazilCurrents

Brunetti and Ivanovic(1992), Leta (1992) andWaluda et al. (2001a)

Doryteuthisopalescens

NortheastPacific


Increased retention via tidally reversing currentsand inshore entrainment in SouthernCalifornia Bight

Zeidberg and Hamner(2002)

Octopusvulgaris

NortheastAtlantic


Increased retention with increased upwelling,Ria of Vigo, Spain

Gonzalez et al. (2005)

Loligovulgaris

NortheastAtlantic


Increased retention with increased upwelling,Ria of Vigo, Spain

Gonzalez et al. (2005)

Illexargentinus

SouthwestAtlantic

Frontalprocesses atthe shelf edge

Paralarval distribution related to strong thermalgradients between Brazil Current and theconvergence front

Leta (1992) and Bazzinoet al. (2005)

Todarodespacificus

NorthwestPacific


Paralarvae/juveniles transported via theKuroshio Extension to Sea of Japan

Sakurai et al. (2000) andKawabata et al. (2006)

Illexillecebrosus

NorthwestAtlantic


Enhanced shoreward transport of paralarvae/juveniles due to increased meandering of theGulf Stream

Rowell et al. (1985),Vecchione and Roper(1986) and Dawe et al.(2000)

Thysanoteuthisrhombus

NorthwestPacific


Transport of juveniles through the TsushimaStrait via Tsushima current

Bower and Miyahara(2005)

Todarodespacificus

NorthwestPacific

Fisheryaggregationsat frontalregions

Fishery located at boundary between Kuroshioand Oyashio currents

Cho et al. (1999)

Illexargentinus

SouthwestAtlantic


Fishery located at frontal regions betweenFalkland current and coastal shelf waters

Waluda et al. (2001b)

Ommastrephesbartramii

NorthPacific


Increased catches associated with strongthermal gradient at Subarctic boundary

Ichii et al. (2004), Bowerand Ichii (2005)

Ommastrephesbartramii

NorthwestPacific

Rings,meanders,streamers

Fishery occurs in streamers shed from theKuroshio, Oyashio and Tsushima-TsugaruCurrent systems

Sugimoto and Tameishi(1992)

Pterygioteuthisgiardi

SouthwestPacific


Squid associated with a warm core eddy of EastAustralia Current, Tasman Sea

Brandt (1983)

Brachioteuthisriisei

SouthwestPacific


Squid associated with a warm core eddy of EastAustralia Current, Tasman Sea

Brandt (1983)

Martialiahyadesi

SouthernOcean


Squid associated with warm core ring atNortheast Georgia Rise, Antarctic PolarFrontal Zone

Rodhouse et al. (1996)


123

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 (O’Dor 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 influenced 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 (Schon et al.

2002), and to influence the distribution of Sthe-

noteuthis pteropus around the coast of western

Africa (Zuyev et al. 2002).

Frontal regions (defined 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

influence of mesoscale processes at fronts such as

the formation of rings, meanders and streamers

also shown to influence 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 influence of the El Nino-La Nina, Southern

Oscillation Index (SOI), North Atlantic Oscilla-

tion (NAO) and Trans-Polar Index (TPI) have

been shown to influence the movement and

migration of cephalopod populations in various

locations around the globe, and the influence of

these phenomena can be seen in locations far

removed from the source of variability, mediated

by teleconnections influencing local oceanogra-

phy (Waluda et al. 1999).

Variability in environment related to the

Southern Oscillation and TPI were shown to

have a large influence on cephalopod species of

importance to fisheries, 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 Pacific, the

influence of El Nino variability has been observed

in fisheries 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


123

et al. 2002; Waluda et al. 2006). Warming (El

Nino) events are generally seen to lead to a

reduction in squid abundance in common fishery

areas coupled with an increase in catches outside

these areas (Pearcy 2002; Zeidberg et al. 2006),

suggesting El Nino events could potentially cause

a shift in distribution rather than a decline in

overall population size.

Interest in the influence of environmental

parameters on cephalopod movement/migration

at the various life cycle stages is increasing. Much

work has been done examining environmental

influences on the abundance and distribution of

cephalopods (particularly those which form sig-

nificant fisheries), 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 influenc-

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 pacific 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 influence 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 influences, par-

ticularly temperature and food fluctuations.

‘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 first to define 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 first required to determine if this

technique is viable for cephalopods.

Acknowledgements This review came about as a resultof discussions held at the Cephalopod Movement andMigration Workshop held as part of the 2006 CIACConference in Hobart. The authors would like to thank allthe participants for their valuable contribution to thediscussion. We are also grateful to Hideaki Kidokoro, KenMori, Yoshikazu Nakamura, Kazuya Nagasawa, andMitsuo Sakai for providing information on recent taggingexperiments in Japan. Thanks also to Stephanie Semmensfor editing the manuscript. Funding to JMS and GTP tostudy cephalopod movement and migration comes fromAustralian Research Council Linkage grants andPostdoctoral Fellowships (C00107233 and LP0347556respectively). KZ was funded by the DeutscheForschungesgemeinschaft (DFG PI 203/11-1, 11-2, 11-3,HA 2100/9-1). Travel to CIAC by PWS was supported bythe Royal Society of London.

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