loligo reynaudii, chokka squid - nova science publishers...loligo reynaudi) are found on the west...

In: Advances in Squid Biology, Ecology and Fisheries. Part I ISBN: 978-1-62808-331-6

Editors: Rui Rosa, Ron O'Dor and Graham Pierce © 2013 Nova Science Publishers, Inc.

Chapter II

Loligo reynaudii, Chokka Squid

Warwick H. H. Sauer1

, Nicola J. Downey2,1

, Marek Lipinski1,

Mike J. Roberts3,1

, Malcolm J. Smale4, Paul Shaw

5,1,

Jean Glazer6 and Yolanda Melo

6

1Department of Ichthyology and Fisheries Science

Rhodes University Grahamstown South Africa 2Bayworld Centre for Research and Education, Port Elizabeth/

Rhodes University, Grahamstown, South Africa 3Department of Environmental Affairs, Cape Town, South Africa

4Port Elizabeth Museum, Bayworld, Port Elizabeth, South Africa

5Institute of Biological, Environmental and Rural Sciences (IBERS)

Aberystwyth University Penglais Aberystwyth, UK 6Department of Agriculture, Forestry and Fisheries, Cape Town, South Africa

Abstract

Chokka squid (Loligo reynaudi) occur in the diverse and highly variable shelf

environments between the Great Fish River, on the east coast of South Africa, and the

Orange River on the west coast. A separate stock occurs further north off Southern

Angola, however little information is available from this region. In South African waters,

most of the biomass occurs on the south-east coast. Adults move inshore to spawn in the

relatively sheltered embayments found on the South Coast. Squid mature at about 1 year

of age with a potential fecundity of about 18000 eggs. The spawning behaviour is

particularly complex, and females commonly mate with multiple males over short time

periods. Females have access to sperm from different males and multiple paternity within

the offspring of individual females appears common. Adult squid move up to 200km

between inshore spawning sites, generally in an eastward direction. Spawning

aggregations are targeted by a commercial handline jig fishery operating primarily off the

Eastern Cape of South Africa. Squid are also caught as a bycatch in the commercial

Email: [email protected].

No part of this digital document may be reproduced, stored in a retrieval system or transmitted commercially in any form or by any means. The publisher has taken reasonable care in the preparation of this digital document, but makes no expressed or implied warranty of any kind and assumes no responsibility for any errors or omissions. No liability is assumed for incidental or consequential damages in connection with or arising out of information contained herein. This digital document is sold with the clear understanding that the publisher is not engaged in rendering legal, medical or any other professional services.

Warwick H. H. Sauer, Nicola J. Downey, Marek Lipinski et al. 34

inshore demersal trawl fishery. The chokka squid fishery has the highest variability in

both biomass and catches of all the South African commercial fisheries, with annual

catches varying from 2 000 to 13 000 tons. This variability has largely been attributed to

changes in the environment. The fishery is primarily managed by the capping of effort at

a level which secures the greatest catch without exposing the resource to the threat of

reductions to levels at which recruitment success is compromised or catch rates become

economically unviable. Currently effort is capped at 136 vessels and a maximum of 2 422

crew. In addition, an annual closed season of 5 weeks is implemented during the peak

spawning season (October/November).

1. Introduction

Chokka squid (Loligo reynaudi) occur in one of the most diverse and highly variable

environments found anywhere in the world (Figure 2.1; Lutjeharms et al., 2001). The

oceanography of South Africas’ east coast and outer Agulhas Bank is strongly influenced by

the warm, fast-flowing (~ 2 m s–1

) Agulhas Current, described in detail in Roberts (2005);

“This is a well-defined western boundary current with origins in the Moçambique Channel

(Lutjeharms, 2001). At the southern tip of the Agulhas Bank, the Agulhas Current undergoes

a number of configurations which include retroflection eastwards along the Subtropical

Convergence into the South Indian Ocean, the formation of anticyclonic rings shed into the

South Atlantic (Duncombe-Rae, 1991), or continuous flow along the shelf edge of the

western Bank (Lutjeharms and Cooper, 1996). Large-scale upwelling is common east of Port

Elizabeth, as a result of the divergence between the shelf edge (and Agulhas Current) and the

coast (Lutjeharms et al., 1999). Intense thermoclines induced by shelf-edge upwelling and

insolation are characteristic of the eastern and central Bank (Largier and Swart, 1987). The

inner shelf is influenced by wind-driven coastal upwelling, particularly during summer

(Schumann et al., 1982). Upward doming of the thermocline in an elongated formation is

often found on the central Agulhas Bank. This feature, referred to as a “cold ridge” (Figure

1b), is commonly associated with high levels of primary and secondary production (Boyd and

Shillington, 1994).

The west coast is completely different, dominated by the cold Benguela upwelling system

(Shannon and Nelson, 1996), one of the largest eastern boundary upwelling systems in the

world and primarily driven by the South Atlantic High Pressure (anticyclone) and associated

south-easterly winds (Figure 2.1a). Consequently, the region has abundant primary and

secondary production, frequently leading to low levels of dissolved oxygen in the bottom

layer, and at times almost anoxic conditions (Chapman and Shannon, 1987). The northern

boundary is formed by the Angola-Benguela Front commonly found near the Kunene River at

~ 16° S (border of Angola and Namibia, see Figure 2.1a). This results from a confluence of

the southward flowing warm Angola Current and the northward flowing cold Benguela

Current”.

Much of the variability on the shelf around South Africa is consequently caused by the

dynamics of the Agulhas Current, Benguela Current (and jet), and north–south seasonal

migration of atmospheric high-pressure cells situated over the SE Atlantic and SW Indian

Oceans (Figure 2.1; Tyson and Preston-White, 2000). In winter, the westerly belt expands to

the latitudes of southern Africa, causing strong westerly winds to dominate, with large swells.

Loligo reynaudii, Chokka Squid 35

In summer, the westerly belt contracts south, and the wind field is then largely driven by the

two anticyclones, causing coastal upwelling on the west coast and Agulhas Bank.

Figure 2.1. (a) The complexity and variability of the marine environment around southern Africa is

partly due to the latitude and associated weather. In summer, the oceanic high-pressure cells either side

of southern Africa dominate the windfield, causing southeasterly winds on the west coast and

northeasterly winds on the eastern Agulhas Bank and east coast. In winter, the westerly wind belt

migrates north, moving cold fronts and strong westerly winds to southern Africa. (b) The oceanography

is also dominated by the warm Agulhas and cold Benguela Currents. These drive many of the physical

processes and key features on the shelf. (from Roberts, 2005).


L. reynaudi live within this diverse environment mainly on the shelf between the Orange

River and the Great Fish River (Figure 2.2), and also in relatively large numbers in Southern

Angola (Shaw et al., 2010) where spawning is also known to occur. Few squid have been

found on the Namibian shelf between these distributions. Seldom are squid found deeper than

200 m, and in South African waters most of the biomass is over the Agulhas Bank.

In South Africa fishing occurs mainly in the South Eastern Cape (Figure 2.2) and is

concentrated largely on spawning aggregations but offshore drift fishing using drogue

anchors also occurs. Squid are also caught as a bycatch in the hake directed demersal trawl

fishery.

The fishery in southern Angola is largely artisanal, with hand-line jigs used from small

individual rafts made from floats washed ashore, and occurs close to shore (Sauer

unpublished data).

As with many squid fisheries fluctuations in biomass and catch are characteristic of this

fishery (Figure 2.3).

Variability and uncharacteristic changes in the environment could either weaken or

strengthen the inherent biological advantages, and ultimately impact recruitment. This may

explain, at least in part, the large fluctuation observed.

Figure 2.2. (a) Demersal trawl catches indicate that chokka squid (Loligo reynaudi) are found on the

west coast and Agulhas Bank to a depth of about 300 m. Most of the biomass is on the Agulhas Bank

(insert b). The main spawning grounds in the South eastern Cape are indicated by the shaded area

between Plettenberg Bay and Port Alfred. (Roberts, 2005).


Figure 2.3. (a) The (autumn) chokka squid biomass on the Agulhas Bank is conservatively estimated to

range between 8000 and 28 000 t (no surveys were carried out for 1998-2000). (b) Annual catches

appear to follow a trend similar to that in (a) (Roberts, 2005).

2. Life History and Biology

2.2. Early Stages

The eggs of L. reynaudi are embedded in pods in the shape of “fingers”, around 9 cm

long. Each pod contains just over 100 eggs, which are typically ~2 mm in diameter and yolk-

rich. Blastulation is in the form of a partial, non-spiral cleavage and a discoblastula is subject

to epibolic gastrulation which leads to formation of the yolk sac. The yolk sac allows for

survival of newly hatched paralarvae for 3-5 days depending upon temperature. The

embryonic development of L. reynaudi was first described by Blackburn et al. (1998), and for

comparability with other species, both Naef’s (1928) and Arnold’s (1965) classifications were

used. This was further refined by Oosthuizen et al. (2002), expanding the classification of the

early stages. Figure 2.4 illustrates an early stage of the blastoderm formation and

organogenesis.

Temperature plays a key role in embryological development. It was initially found from

laboratory experiments that paralarvae will not develop or survive well in temperatures >20°C

or <9°C (Oosthuizen, 1999). But more recently Oosthuizen and Roberts (2009) found that

downwelling can extend as deep as 120 m and as far offshore as 20 km, resulting in


temporary intrusions of warmer water >10°C. This possibly explains why successful egg

development has been found on the mid-shelf spawning grounds previously thought to be too

cold (Roberts and Sauer, 1994) and accounts for the fact that a substantial percentage of

successful spawning takes place in relatively deep water (>60 m).

Figure 2.4. (a) stage 15 (Arnold) or V (Naef): Blastoderm covers about on half of the egg. Scale bar: 1

mm; (b): stage 15+ or VI-VII: Blastoderm covers four-fifths of the embryo except for a small arc of

yolk. A shallow girdling depression appears around the equator, forming a boundary between the future

external yolk sac and the future embryonic body. Scale bar 1 mm; (c): stages 16-18 (VII): Nodule of

yolk is barely visible. Major organ primordial evident as thickening in the blastoderm. (Primordia of the

shell gland are visible). Rudimentary primordial of optic vesicles are visible, and the arm primordial are

visible as slight thickening of the blastoderm. Scale bar: 1 mm; (d): stages 19-20 (VIII-IX): Primordia

of statocysts appear, arms and tentacles grow and begin to project. Posterior and anterior fnnel folds

extend toward the midline. Shell gland invagination is progressing and transverse fin folds develop on

the broadening mantle. Other organ primordial become prominent, such as gills and anal knoll. Scale

bar: 1 mm; (e-f): stages 21-22 (XI-XII): Shell gland completely closed, transverse fin folds prominent

on the developing mantle. Anterior and posterior funnel folds lie together but fusion of funnel folds has

not yet begun. First suckers appear on tentacles. Retina is well pigmented. Scale bar: 1 mm. (from

Blackburn et al., 1998).


Ecological information about paralarvae is generally scarce. The distribution of L.

reynaudi paralarvae per month was illustrated in Augustyn et al. (1994, Figure 2.5). In fact,

there are two overlapping loliginid species: L. reynaudi and Afrololigo mercatoris, distributed

between Namibia and the South African south east coast.

Figure 2.5. Distribution of chokka squid hatchlings in South African waters, 1985-91. (a)

January/February, (b) May/June, (c) July/August, (d) September, (e) October-December. (Augustyn et

al., 1994).


Vecchione and Lipinski (1995) have shown paralarval differences between them (Figure

2.6). The largest concentration of L. reynaudi paralarvae was found along the south coast of

South Africa between September and December (data for years 1985-1991). It was

hypothesized that paralarvae may experience substantial losses when transported off the shelf

into open ocean (Roberts and Mullon, 2010). This is mitigated by their negative buoyancy

and vertical migration habits (Martins et al., 2010). Research attempting to determine

dominant prey types for paralarvae on a population scale has so far not been successful

(Hoving et al., 2005; Venter et al., 1999).

Figure 2.6. (a) Loligo reynaudi ventral, dorsal and club; (b) Afrololigo mercatoris, same (Vecchione

and Lipinski, 1995).

2.3. Age and Growth

Techniques that have been developed to age squid on the basis of statolith analysis

(Lipinski, 1978; Spratt, 1978) involving extraction of statoliths, visualization of increments,

enumeration and subsequent interpretation of these readings, have been applied to L.

reynaudi. Augustyn et al. (1994) and Lipinski and Durholtz (1994) found more than 400 daily

increments for largest males (>40 cm) and females (>25 cm). These results were subsequently

validated both in the laboratory and in the field (Durholtz et al., 2002; Lipinski et al., 1998).

On a population scale, Lipinski et al. (unpublished data) have confirmed that on average L.

reynaudi are mature at about one year of age. Figure 2.7 illustrates the visualization of

increments in L. reynaudi statoliths, prepared for light microscopy, and Figure 2.8 illustrates

the validation procedure.

Interpretation of squid growth in general terms is still problematic. Results based on both

field and aquarium analysis suggests fast exponential growth (e.g. Jackson and O’Dor, 2001).

Analysis based on theoretical bioenergetic considerations (Pauly, 1998), however, suggests

much slower growth. Of course growth trajectories are likely to differ between individuals

and the composite trajectories from population samples are likely to vary according to the

seasonal composition of the sampled animals (i.e. proportion of animals from different

microcohorts). Presently either the Gompertz equation (Arkhipkin and Roa-Ureta, 2005) or

multi-phase growth model (e.g. three-phase linear, Lipinski, 2002; Figure 2.9) has been

advocated.


Figure 2.7. Chokka statolith sectioned in the frontal plane. Light microscopy. Black arrows indicate the

axis of observation and counting of increments. W – wing. Scale bar 0.07 mm. (Lipinski et al., 1998).

Figure 2.8. Statolith with good oxytetracycline mark (arrows, and fluorescent band shown above). Scale

bar: 0.05 mm. (Lipinski et al., 1998).


Figure 2.9. Three-phase growth model of cephalopods. (Lipinski et al., 1998).

2.4. Maturation and Fecundity

Studies on the maturation process of chokka squid have been ongoing since the 1970s.

Maturity has been determined histologically (Badenhorst, 1974), morphologically (Augustyn,

1989, 1990; Lipinski and Underhill, 1995) or using a combination of both (Sauer and

Lipinski, 1990). Although these studies led to important advances in our understanding of the

maturation process of the chokka squid, key areas in the life cycle of this species, such as

spawning strategy and fecundity, were still uncertain. Chokka squid were thought to be serial

spawners, based on histological data of oocyte-size frequency distribution from gonads at

various stages of maturity (Sauer and Lipinski, 1990) and on the fact that no mass mortality

has been found on the inshore spawning grounds, despite extensive diving surveys

(Sauer et al., 1992).

To resolve the question of serial spawning in chokka squid a more detailed study on

oogenesis and gonad development was carried out by Melo and Sauer (1999). These authors

corroborated the asynchronous growth of oocytes in the ovaries indicated by Sauer and

Lipinski (1990) and provided additional evidence supporting serial spawning for this species,

namely the presence of partially spent ovaries containing post-ovulatory follicles (indicating

recent ovulation) alongside oocytes at various stages of vitellogenesis for a future spawning.

Histological data also revealed the predominance of small protoplasmatic oocytes in all

maturity stages. This is a characteristic of pelagic fish that spawn frequently but at short

intervals (Melo, 1994; Melo and Armstrong, 1991). Additional indication of serial spawning

is the presence of atresia (oocyte degeneration and resorption) in developing and particularly


in spent ovaries, a feature characteristic of serial spawner (Hunter and Macewicz, 1980).

Atresia was found in all the oocytes stages (unyolked and yolked), being most frequent late in

the spawning season, where 80% of the advanced vitellogenic oocytes were atretic. A low

percentage of atresia (5.9%) was found in mature individuals early in the spawning season

probably indicating the end of one of several spawning bouts. During the spawning season

squid return to a particular spawning site over a number of days (Sauer et al., 1997) and move

between sites over a period of weeks (Sauer et al., 2000). It is therefore assumed that chokka

squid undergo more than one cycle of oocyte maturation, spawning and, presumably atresia

(Melo and Sauer, 1998).

Based in the above observations Melo and Sauer (2007) postulated an ovarian cycle for

chokka squid, which represents a serial spawning strategy for this species (Figure 2.10), with

periods of recovery between spawning, suggesting that squid may be further aligned towards

iteroparity than previously postulated; “The ovarian cycle commences with females entering

the cycle on reaching sexual maturity. After the first batch of advanced yolk stage oocytes is

completed, females enter an inner cycle (spawning phase) where ovaries go through ripe,

partially spent and recovering stages by undergoing a process of maturation, ovulation and

redeveloping, where a new batch of advanced oocytes is recruited”. The cycle typically

appears to last between 12 to 36 hours, with the histological evidence supported by results

from laboratory experiments (Sauer et al., 1999). After a number of spawning bouts the

ovaries undergo a resting stage, indicated by the histological characteristics of the ovaries.

Figure 2.10. The serial spawning strategy of L. reynaudi.

Fecundity of chokka squid was first estimated by Sauer et al. (1999) following the

conventional methods of egg production in loliginid squid. Egg production was estimated

from mature individuals collected from both inshore and offshore. Those collected from

inshore included individuals collected after noting the deposition of an egg strand. Variation

was observed in the fecundity of squid in terms of oocytes in the ovary and the oviducts in the

three groups studied, with fecundity higher on the inshore spawning grounds than offshore.

This may be attributed to resorption. As expected, inshore squid show low number of eggs in

the oviducts, which could imply more frequent spawning on the inshore spawning grounds.

As mature females on the offshore feeding grounds have oviducts filled with mature eggs it is


therefore likely that after a certain minimum fecundity has been achieved, under some

conditions of food availability, part of the energy resources may be redirected to growth

during maturation and squid store mature eggs for extended periods of time without

spawning. This implies that L. reynaudi are not generally forced to empty their oviducts of

eggs in deeper water during periods of unfavorable environmental conditions inshore — a

theory proposed to explain the eggs of L. reynaudi caught in trawl nets in depths of water

greater than 60 m.

Studies on spawning frequency on chokka squid were conducted by Melo and Sauer

(2007) by means of classification and grouping by age of post-ovulatory follicles. Estimation

of this parameter in squid is complicated. The short–lived (about 14 h) nature of the post-

ovulatory follicles precludes the calculation of the exact spawning intervals and does not

allow accurate prediction of the spawning frequency. The fact that spawning periods may

extend over several months and that attainment of maturity is also highly variable (Augustyn,

1989; Sauer and Lipinski, 1991) further complicates spawning frequency estimates.

A realistic estimation of potential fecundity for chokka squid was calculated as 17 809

eggs — the mean value of the number of discernible oocytes in the ovary of squid jigged on

the spawning grounds added to the number of eggs in the oviducts of partially spent squid.

However, aquarium experiment observations showed that females produce an average of 8

140 eggs over 36 hours. It would therefore appear that the estimation of actual fecundity for

this species is between 8 000 and 17 000 eggs. Certainly, follicular atresia lowers the number

of maturing oocytes in the ovary, so the fecundity values reported here may be overestimated.

Nevertheless, the serial spawning strategy of chokka squid makes any single count

conservative, without taking into account the exact number of batches of eggs spawned from

a particular ovary, the number of eggs released per batch and the frequency of the spawning.

In the future acoustic tagging of specific individuals during a stable spawning period,

coupled with long-term observations of mature females under laboratory conditions and a

study of the dynamics of oocyte production, growth and resorption may provide more

certainty on fecundity estimates.

3. Ecology

3.1. Distribution and Abundance

Spatial distribution and variation in yearly abundance has been recognized as a main

driving mechanism in the phylogenetic survival of squid (Lipinski, 1998). Squid, as a

consequence of fast growth (see previous section), do not enjoy the safety net provided by

multi-generational age structure, as most marine fish do. This is compensated by large life-

cycle variations between individuals as well as complicated vertical and horizontal

distribution patterns.

Early published accounts on the distribution of L. reynaudi indicated these animals to be

dispersed and isolated (e.g. Crawford, 1982). However, the first comprehensive review on

distribution, compiled by Augustyn (1989) and based on research demersal trawl data,

demonstrated that this species certainly occupied the shelf between Port Alfred and the


Orange River (Figure 2.2a). It is now understood that L. reynaudi are also found in Southern

Angola (Shaw et al., 2010) but are almost entirely absent on the Nambian shelf (Figure 2a).

In South African waters more than two thirds of the adult biomass is concentrated on the

south east coast (Augustyn, 1989, 1991; Augustyn, et al., 1993, Figure 2b). Although chokka

squid aggregate in dense spawning shoals inshore (Augustyn, 1990), the offshore distribution

is more uniform and widespread (Augustyn, 1989) and squid are caught in most research

trawls at depths shallower than about 200 m. Olyott et al. (2006) found a lack of spatial

variability in GSI values, which was surprising because earlier studies (Augustyn et al., 1994)

indicated that the GSI increased from west to east, and to peak on the preferred spawning

grounds on the eastern Agulhas Bank (see Figure 2.2a for Agulhas Bank divisions). The lack

of spatial variability found by Olyott et al. (2006) suggests that squid from across the Agulhas

Bank have equal reproductive potential, and that some spawning may take place anywhere

across the bank, at least in some years.

Figure 2.11. Schematic overview of the chokka life cycle. Question marks relate to possible feeding

areas in the eastern region (24°-27°E) where squid may grow and mature offshore of the spawning

grounds. Arrows indicate possible migration patterns.

The biomass, distribution, size composition and reproductive data reveal that the

population characteristics of L. reynaudi in the western part of its distribution differ

substantially from that further east, as described by Augustyn (1989). Generally squid from

the western Agulhas Bank grow slower and mature at a larger size (Olyott et al., 2007), than

those on the eastern Agulhas Bank. The size distribution is also much narrower, and gonadal

development is not as far advanced for those on the western Agulhas Bank. On the west coast,

most of the chokka are located south of 34" 30's at depths less than 200 m (Figure 2.2). Few

chokka occupy the narrow steeply sloping shelf between the 200 m isobath and the shelf


break (400 m) in this region. This trend changes north of 33' 00's where the shelf widens and

deepens, with more than 50% of the chokka here being found deeper than 200 m.

Furthermore, it is evident that chokka in this region do not occupy the entire shelf as is the

case on the south coast, but tend to avoid the inshore coastal region and the deeper outer-shelf

first noticed by Roberts and Sauer (1994). Olyott et al. (2006) investigated the possibility of

there being a geographically fragmented stock by examining both historical and recent

biological data from commercial and research sources. Adults were predominately inshore

and in the east with juveniles inshore in the east and offshore in the west and immature squid

showing an intermediate distribution pattern. Size-at-age data are not yet available for L.

reynaudi (Lipinski and Durholtz, 1994). Although results were inconclusive Olyott et al.,

(2006) proposed that there may indeed be separate stocks inhabiting the western and eastern

regions of the Agulhas Bank. Spawning may occur on the western region of the Agulhas

Bank, and juveniles grow and mature on the west coast and central Agulhas Bank. The larger

eastern population, by contrast, matures at a smaller size and spends its life in the inshore and

offshore waters on the eastern regions of the Agulhas Bank. Recent genetic evidence

strengthens this hypothesis (Shaw et al., 2010). On the basis of all available information the

postulated life cycle (Lipinski et al. in prep.) is illustrated in Figure 2.11.

Stratified random sampling surveys, primarily designed to estimate hake biomass, are

currently carried out on the South African south coast in spring and autumn. These surveys

also provide estimates of squid biomass, which are useful in determining shelf biomass trends

(Augustyn, 1992; Augustyn et al., 1993; Sauer et al., 1993). Estimates of absolute abundance

are not currently possible and will require understanding of net avoidance, the vertical

distribution of squid, level of aggregation and inadequate coverage of grounds as a result of

inability to trawl (Augustyn et al., 1993).

Hydroacoustic methodology has been developed to estimate biomass of spawning

concentrations of squid (Lipinski and Soule, 2007) but as yet has not been comprehensively

tested. Preliminary estimates indicate that concentrations at any given time during the main

spawning period (November) may reach a “snap-shot” biomass of ~4 600 t.

3.2. Migration and Horizontal Movements (and Range Expansion)

Although the limits of distribution of chokka are reasonably well known, data on the

temporal and spatial nature of the stock are limited. Offshore vertical movements are known

from simple observations (occurrence in bottom trawls during the day and hunting behaviour

close to surface during the night; Augustyn, 1989) and hydroacoustic research (Lipinski and

Soule, 2007; Roberts et al., 2002; Soule et al., 2010). Roberts et al. (2002) (Figure 2.12)

found evidence of large concentrations present in deeper water in the early mornings.

Inshore, distances of up to 200 km have been measured between tagging (spaghetti tags)

and recapture positions on the inshore spawning grounds, and a generally eastward direction

of migration of adults on the inshore spawning grounds has been established (Augustyn,

1989; Sauer et al., 2000). This suggests that there is an ongoing but varying in intensity,

immigration and emigration cycle by juveniles and small subadults from, and by larger adults

to, the spawning areas on the south east coast (Sauer et al., 2000). The timing, duration and

intensity of immigration determine the biomass at any given time in the area (Augustyn,


1991; Roberts and Sauer, 1994). Within one year it is possible that a squid may remain within

a relatively small area or travel more than 1000 km.

Figure 2.12. Echogram showing deep-water occurrence and characteristic type of the chokka

concentration, known also from shallower water. (Roberts et al., 2002).

The dynamics of spawning concentrations inshore has also been studied using remote

telemetry (Sauer et al., 1997) or hydroacoustics combined with tagging and pelagic trawl

fishing (Lipinski et al., 1998). The hydroacoustic research showed that 0.2 of the

concentration may change per day (i.e. for each 100 individuals, 20 individuals will be

replaced by others per day). Details for this calculation are given in Figure 2.13.

Based on the information given on the distribution and movement information for L.

reynaudi there is no evidence for a range expansion for this species, although the information

on their presence in Angolan waters is fairly recent and it is postulated that movement

between Angola and South African waters may increase in future years due to greater

environmental fluctuations being experienced in the Benguela region.

3.3. Feeding Ecology and Behavior

3.3.1. Diet

In general the diet, feeding ecology and feeding behaviour of L. reynaudi is not well

known and requires further in-depth studies.


Sauer and Lipinski (1991) investigated diet composition of adult L. reynaudi on their

spawning grounds. Squid mainly fed at night (28.5%) compared to day feeding of 6.7%, with

the majority of stomachs examined being empty. Mostly a single prey item was found in the

stomachs (90.8%). Teleosts dominated during the night, while squid dominated during the

day. Dominant species were Bregmaceros sp., L. reynaudi, Betaeus sp. and Nereis sp. The

average stomach mass was 0.6% of the body weight, whereas on the feeding grounds it is

usually around 2%.

Figure 2.13. Principle of estimating the stability of a squid concentration. The total number of

individuals (∑) is estimated hydroacoustically and simultaneously n1+n2 individuals are tagged. After

time t, a catch is made and n1, m1 individuals are counted. The net effect of migration and mortality is

estimated by assessing the difference between n1t expected and observed (Lipinski et al., 1998).

Venter et al. (1999) investigated predation by chokka paralarvae. Although the number of

individuals investigated (six) was small, he found a number of species ingested, including

Calanus agulhensis, euphausiids and polychaetes. Subsequently C. agulhensis has been

recognized as the most important paralarval prey (Roberts 2005).

Lipinski (1987, 1990) was the first to publish an account of feeding behavior based both

on aquarium observations and field studies. In aquarium experiments (temperature constant at

16°C), live mullets (Liza richardsoni) were provided as food, their numbers far exceeding

squid requirements. In a limited space (circular tank of 5 m diameter and 0.8 m deep) squid

easily caught their prey, but were not successful with mullets larger than half the size of their

mantle length. At times they captured 2-3 fish in quick succession. Where prey was abundant,

the squid discarded the fish heads. Feeding usually started from the dorsal side just past the

head. Ingestion of food was completed within 10 minutes. The weights of stomachs

immediately after ingestion varied from 2 to 6.3% of the predator’s body weight

(mean 4.1%).


The change in the consistency of food in the stomachs over time is shown in Figure

2.14a. During the first 2.3 hours after ingestion, the food was almost unchanged, but over the

next 2 hours most was digested. A mean evacuation time was 7.5 hours and stomachs were

empty after 10 h. The change in the colour of fluid (emulsion) in the caecum is shown in

Figure 2.14b and drop in pH in Figures 2.15 and 2.16. In squid, this drop in pH happens as

digestion progresses, so fasting squid have the lowest pH both in their stomach and caecum.

Although a surprise finding, it may be that squid acidity plays a limited role (Bidder,1950,

1966; Boucher-Rodoni et al., 1987) and rather a medley of powerful enzymes is kept

constantly in the stomach and caecum. Introduction of prey fluids increases pH, as most of

these fluids are neutral (pH = 7), compensated only to a limited degree by the release of squid

digestive fluids from the digestive gland and/or appendages. This form of digestion (“up-front

readiness for quick action”) is in contrast with the digestion mode of vertebrates.

Figure 2.14. (a) Food, and (b) caecum colour change with time in chokka. Numbers represent hours

after ingestion of food. (Lipinski, 1987).


Figure 2.15. Decrease of pH with time in chokka stomach (a) and caecum (b) in an aquarium

experiment. (Lipinski, 1987).

Lipinski (1992) provided some data to assess the impact of predation by L. reynaudi on

commercial species of fish, concluding that additional research was required to improve the

confidence limits associated with analysis of available data. Nevertheless preliminary results

demonstrate that there may be considerable impact on anchovy (Engraulis capensis) in the

range of 100 000 t per year, and on hake (Merluccius capensis) some 70 000 t per year.


Figure 2.16. The means and standard deviations of pH measurements in the caeca of chokka (both sexes

combined). Values on top of standard deviation axes represent frequency of occurrence of squid with

food in stomachs. (Lipinski, 1990).

3.3.2. Reproduction

It is possible to identify squid spawning concentrations using conventional echosounders

(Sauer et al., 1992), a necessary precursor to being able to dive (depths less than 50 m) and

observe spawning squid, as the spawning area is limited and unless marked with a marker

buoy most dives will be unsuccessful. The pattern observed appears as a dark complex

pattern, generally shaped like a mushroom (Figure 2.17; Lipinski et al. 1998; Sauer et al.,

1992). Inshore spawning sites are located both in relatively protected bays and open, exposed

parts of the coast, where the egg strands are found below the zones of high wave energy,

usually below 15 m (Augustyn,1989, 1990; Sauer et al., 1992).

Egg beds comprise either a few egg strands or numerous strands which form beds up to 4

m in diameter (Sauer et al., 1992). The mean number of eggs per strand is 148 ± 37 (Sauer et

al., 1993). As fishing activity concentrates on spawning animals the intensity of fishing effort

may be used to infer spawning activity.

Fishing activity is concentrated in depths of less than 60 m, suggesting that the major

spawning grounds are found in fairly shallow water. Nevertheless, catches of adult animals in

deeper water (> 60m) off the south and eastern Cape, hydroacoustic traces showing potential

spawning animals, (Roberts et al., 2002) and eggs recovered from research trawls (Roberts

and Sauer, 1994, Roberts et al., 2012) reveal that the inshore spawning area may extend to

deeper waters, but the significance of these sites and intensity of spawning there is unclear

(Roberts et al., 2002).


Figure 2.17. A mushroom-shaped spawning squid concentration, based on hydroacoustic observations.

(Lipinski et al., 1998).

A total of 238 temporary inshore spawning sites have been identified along the South-

Eastern Cape (Sauer, 1995). Squid are present for weeks or months at a time, a portion of the

sites being used during consecutive years (Sauer et al., 1992). The number of spawning sites

used per year varies considerably (Figure 2.18; Sauer, 1995).

Clear peaks in adult abundance in winter and summer recorded from trawl and jig data

support the theory of at least two major spawning peaks in some years, although much inter

annual variability exists (Olyott et al., 2006). Olyott et al. (2006) found a lack of spatial

variability in the number of mature squid from research trawl data, suggesting, as mentioned

earlier, that squid from across the Agulhas Bank have at least equal reproductive potential,

and that some spawning may take place across the entire bank, at least in some years.

Figure 2.18. Known chokka squid spawning sites on the south east coast of South Africa.


Hanlon et al. (2002) used hand held video recordings (on SCUBA), to establish that the

operational sex ratio on the spawning grounds may often be skewed towards males, indicating

a ratio in the order of ca 1.4M:1F. This is further confirmed by monthly data collected from

the jig fishery; in 1988 males outnumbered females in 11 of the 15 months investigated

(Olyott et al., 2006).

In situ observations of spawning are difficult for this species as sea conditions are often

unfavorable, and spawning takes place from 22 m to more than 35 m which restricts diving

time on SCUBA. Although ROV’s have been used, they have provided limited information

on behaviour, as it is difficult to follow individual animals over any extended period.

The most comprehensive overview of spawning and mating behaviour is given in Hanlon

et al. (2002) and depicts the general 3-dimensional layout and zones of activity on a typical

spawning arena (Figure 2.19).

Figure 2.19. General scheme of behavioral zones in a typical mating arena of the squid Loligo reynaudi

off South Africa; (a) Upon arriving on the spawning grounds, most females already have stored sperm

in the seminal receptacle, indicating ‘head-head’ mating, which was not seen in the mating arenas. (b)

Temporary pairings of large consort males result in ‘male-parallel’ matings. (c) Small lone ‘sneaker’

males occasionally succeed in obtaining extra-pair copulations in a slightly different position. As pairs

move to/from the egg mops, they are intercepted by lone large male ‘intruders’ that engage the paired

consorts in agonistic contests that often result in successful takeovers. Females are rarely susceptible to

predation by benthic sharks when they oviposit. (Hanlon et al., 2002).

The following description is taken directly from this work; “Immediately around the egg

mop is the ‘egg-laying zone’ in which there are concentrated groups of male/female pairs that

descend to deposit individual egg capsules in the mop. Integrated with this is the ‘agonistic

zone’ in which lone large males intercept pairs and engage consort males in agonistic

contests. Beyond this is the ‘mating/sneaker zone’ in which squid density is low by


comparison, and in which large males are accompanying and mating females, and also in

which sneaker males are cruising the area seeking opportunities for extra-pair copulations

(EPC). Finally there is a ‘transitory zone’ in which there is immigration and emigration to the

mating arena. Movement among these zones is variable but after egg laying the pair usually

jets vigorously out of the egg-laying zone through the agonistic zone and then the pair moves

gradually into the mating zone where they may circle like airplanes awaiting their turn to land

at a busy airport. During this time the large consort male mates the female. Lone large males

compete for paired females on the spawning grounds; thus the most common interaction was

to see a large lone male ‘intruding’ on the pair and engaging the paired consort male in an

agonistic contest.”

There is some evidence from telemetry studies (Sauer et al., 1997) that pairing may occur

at first light as squids aggregate each day after a night of dispersed feeding. It is clear from

diving observations that pairs are temporary because they change frequently during the day

(Hanlon et al., 2002). Preliminary ROV footage from 1990 indicated that pair formation

broke down at about dark; mostly females were present just before all squids dispersed.

Females arriving on the spawning grounds often have sperm present in a storage organ

below the buccal mass. In addition, females commonly mate with multiple males over short

time periods (hours), during which males deposit discrete packages of sperm

(spermatophores) in the vicinity of the oviduct (Sauer and Smale, 1993). These behavioural

dynamics indicate that females have access to sperm from different males and that multiple

paternity within the offspring of individual females may be common. Genetic studies have

confirmed this; of 4 broods typed, 2 were sired by a single male, whereas 2 were sired by 4 or

5 different males (Figure 2.20; Shaw and Sauer, 2004).

Figure 2.20. Distribution of embryos sired by different males within egg strands (embryo positions

marked with areas are arbitrary: P = proximal, D = distal, M = middle. (Shaw and Sauer, 2004).


Visual signaling is important, noted by Augustyn and Roel (1998) and Sauer et al.

(1992). A detailed study of body patterning was subsequently undertaken by Hanlon et al.

(1994) and provides a useful catalogue of body patterns recorded in spawning concentrations.

Observations of nocturnal spawning behaviour suggest that egg strand deposition may be

performed by solitary females, not associated with attendant males.

No guarding or defense of the egg beds has been recorded at any time by either paired or

individual squid of either sex (Sauer and Smale, 1993).

The re-use of spawning sites suggests specific environmental requirements for spawning

(Augustyn et al., 1994) and both scientists and fishermen believe that the environment plays a

role in the formation of spawning aggregations (Roberts, 1998). Studies suggest the initial

formation of spawning aggregations is triggered by upwelling (Downey et al., 2010; Roberts,

1998; Sauer et al., 1991; Schön, 2000) and a positive relationship has been shown between

wind-induced upwelling and squid catches (Schön, 2000). As it is believed that vision is

essential to communication during the mating process (Hanlon et al., 1994; Hanlon et al.,

2002; Sauer et al., 1992), large-scale turbidity events are thought to disrupt spawning

(Dorfler, 2002; Roberts, 1998; Schön, 2000) due to reduced visibility.

Distribution of egg mops within a spawning site appears to be unrelated to fishing

pressure, but rather influenced by substratum type and possibly the presence of natural

predators in the area (Lipinski and Soule, 2007; Sauer, 1995; Smale et al., 1995; Smale et al.,

2001). Observations show that low-profile reef areas tend to have only small egg mops

present over a wide area (Sauer, 1995), and the absence of a large central egg bed may not,

therefore, be indicative of disruption of spawning.

Fishing on spawning animals, particularly females will almost certainly influence

spawning to some extent. Sauer (1995) used seven criteria to depict natural behaviour and

found that these were present on all occasions where sampling was undertaken by SCUBA

below intensive fishing activity.

Observations revealed that, when the squid were least cautious, there were

correspondingly good catches, and these were always associated with spawning behaviour.

Catches may, however, influence a recently formed spawning concentration where only a few

egg strands have been deposited.

The number of eggs damaged by anchors and anchor chains was less than one would

expect intuitively (Sauer, 1995). However sudden wind change, which may result in anchor

chains being dragged along the bottom as the vessel realigns itself relative to the wind

direction, may inflict substantial damage to the eggs (Sauer, 1995). The recent introduction of

double anchors has raised concerns that the damage by anchor gears might now be

considerable and merits investigation.

Little research has been done on the possible disruptive effects of light-fishing on the

stocks. Squid near the vessel appeared to be feeding on the shoals of small fish attracted there.

The squid remained in the dark areas before jetting into the lighted area to catch prey (Sauer,

personal observation). Sauer and Smale (1993) noted that on two night dives below actively

fishing vessels that spawning continued in the presence of lights and fishing activity.

No dead or moribund squid have been observed (Sauer et al., 1992). As they have been

confirmed to be serial spawners (Melo and Sauer, 2007; Sauer and Lipinski, 1990), only a

few may die at any one time and mortality might be sporadic over a prolonged period. A

combination of serial spawning and any weak and dying individuals being highly susceptible


to cannibalism and predation may account for the absence of moribund or dead squid in the

area (Sauer and Smale, 1993).

3.4. Predators

Chokka squid are the dominant cephalopod prey of numerous coastal predators. These

include seabirds such as penguins (Rand, 1960; Randall et al., 1981) and gannets (Batchelor

and Ross, 1984; Klages et al., 1992), marine mammals including fur seals (Lipinski and

David, 1990; Stewardson, 2001) and dolphins (Ross, 1984; Sekiguchi et al., 1992). Numerous

fish species feed on chokka squid, including both pelagic fishes such as yellowtail (Smale,

1986) and demersal teleosts including kob (Argyrosomus spp.) (Griffiths, 1997; Smale and

Bruton, 1985), hake (Lipinski et al., 1992) and sharks (Smale, 1991; Smale and Compagno,

1997; Smale and Goosen, 1999).

These predators generally charge at the prey and attack successfully because of their

larger size and greater speed. Behavioural interactions and feeding have been described at

spawning aggregations between predators and their squid prey by Sauer and Smale (1991)

and Smale et al. (2001).

In contrast, ambush predation by both sharks and rays, allows slow-moving taxa, such as

catsharks (Poroderma spp.) and benthic rays such as the diamond ray (Gymnura natalensis)

to lie immobile either in the egg beds or in sand abutting the egg bed waiting to attack egg

laying females when they attach the egg strands.

Other species such as short-tail stingray (Dasyatis brevicaudata) swim actively over the

egg beds and trap squids close to the substrate (Smale et al., 2001). In the water column,

smaller teleosts may attack mating individuals and feed on the ejecta from mating squids

escaping the attack (Smale et al., 2001).

Prey variation according to locality and time in seals and fishes is a reflection of their

distribution patterns, abundance and behaviour. Inshore predators show strong switching to

highly abundant prey during the spawning aggregations (Augustyn et al., 1992; Lipinski and

David, 1990; Sauer and Smale, 1991; Stewardson, 2001). Predators may feed on squids when

more nutritionally valuable prey is absent (Randall et al., 1981).

Direct observations of predator behaviour have been described, revealing the focus of a

variety of predatory species around the spawning aggregation and the vulnerability of mating

pairs during egg laying. Judging by the behavioural responses of the squids to a suite of

predators, Smale et al. (2001) suggested that the rapid dispersal of aggregated spawning squid

with the arrival of both seals and dolphins infers that these homeotherms pose a particularly

high threat to mating squid.

Although eggs are highly abundant potential prey, few, if any predators feed on them

(Smale et al., 2001). Furthermore, little is known about the fate of paralarvae, but they are

likely to be preyed on by both vertebrate and invertebrate pelagic planktivores.

3.5. Parasites

Parasites of L. reynaudi have not been studied in any detail. Nematodes from the family

Anisakidae (probably Anisakis sp.) have been observed frequently in the mantle tissue and


inside of the stomach wall (more frequently on the outer side) (Lipinski, personal

observation). Among the Cestoda, larvae of Phyllobothrium and Dinobothrium have also

been frequently observed (Lipinski, personal observation).

4. Fisheries

4.1. Fishing Methods

Chokka squid are targeted by a commercial handline jig fishery operating primarily off

the Eastern Cape of South Africa. Jigs are small grapnels with one or two rings of barbless

hooks, attached to the hand-held lines (Sauer, 1995). Most crew members work two lines at a

time, each line with two jigs, a lead jig and a plastic "floater" a metre or so above it (Sauer,

1995). The vessels used in the South African squid fishery comprise large decked vessels

equipped with freezing facilities (Sauer, 1995). Fishing takes place throughout the day and

night, with strong lights (1-2kW) being used at night to attract squid to the vessel

(Sauer, 1995).

4.1.1. Industrial Methods

Squid are caught as a bycatch in the commercial inshore demersal trawl fishery where the

main target species are hake (Merluccius spp.) and sole (Austroglossus pectoralis), which has

been in operation since the turn of the 19th century (Rademeyer, 2003). Catches of L.

reynaudi in the trawl fishery were initially very high, peaking at just over 5 000 t in 1979 as a

result of being exploited by both foreign and local trawlers. The introduction of an Exclusive

Economic Zone (EEZ) in the early 1980s saw the removal of foreign vessels from South

African waters and a subsequent drastic reduction in catches. Furthermore, squid targeted

trawling is not possible due to a ban on trawling in inshore bayed environments since 1987

(Augustyn and Roel, 1998). In recent years the South African trawl fleet has caught between

200 and 500 tons annually. Although, as research has shown, purse-seining is a viable method

of catching chokka (Lipinski, 1994), it is considered too destructive on the spawning habitat

and will also have a negative impact on employment. It has therefore been banned outright

(Augustyn and Roel, 1998).

4.2. Landings and CPUE

Annual catches taken by the jig and trawl fisheries respectively are shown in Figure 2.21.

Catches in the jig fishery have in the past varied quite considerably from year to year, with

the highest catch recorded in 2004 of just over 12 000 tons. In recent years jig catches have

remained relatively stable at around 9 000 tons.

The jig fishery is an effort controlled fishery, while the inshore trawl fishery is TAC-

controlled, with no catch limits applied to the catches of by-catch squid. Effort in the jig

fishery was initially uncapped, but between 1986 and 1988 a licensing system was introduced

where licenses were awarded based on historical performance (Roel, 1998). This led to an

almost halving of the number of vessels active in the fishery. In 1988 an annual closed season


of 5 weeks over October/November was introduced to protect spawning squid and in 2008-

2010 two additional closed seasons, each of 3 weeks duration, were introduced in order to

reduce fishing effort.

Prior to 2006 catch and effort data from the jig fishery were recorded together with

catches of linefish and were captured on the National Marine Linefish System (NMLS). In

2006 a separate database was created for the sole purpose of capturing more detailed catch

and effort information from the jig fishery than was catered for in the linefish system. New

logbooks were developed and the information collected from these suggests that the previous

data (from the linefish system) may not have been as reliable as originally assumed.

Verification of this is work in progress, and until it has been concluded management of this

resource has followed the precautionary approach in terms of effort control.

Figure 2.21. Annual chokka squid jig catches.

Figure 2.22. Nominal CPUE.


The nominal CPUE indices for the jig fishery are shown in Figure 2.22. These indices

have been derived from a sub-set of vessels whose information is considered to be fairly

accurate. The accuracy of information was based on a reconciliation of catch and effort

information as reported in the NMLS compared with that which operators declared in their

applications for long-term rights in 2008.

4.4. Recruitment and Environmental Variability

4.4.1. ENSO and Recruitment

The chokka squid fishery has the highest variability in both biomass and catches of all the

South African commercial fisheries (Figure 2.23) with annual catches varying from 2 000 to

13 000 tons (Figure 2.23b). This variability has largely been attributed to changes in the

environment.

Figure 2.23. (a) Estimated chokka squid biomass determined from demersal research surveys on the

Agulhas Bank since 1985. Missing data indicate no survey (b) total annual landings for the commercial

jig fishery (c) monthly landings of jig catches.


Roberts (2005) produced a synthesis of basic ecosystem components for the domain in

which chokka squid live. CTD and dissolved oxygen (DO) data from 86 demersal surveys

were used to produce maps depicting the minima, means and maxima of bottom temperature

and DO. These highlighted the stark difference in bottom DO between the west coast and

eastern Agulhas Bank (see Figure 2.2a for Agulhas Bank divisions), with the inner central and

western Bank forming a transition zone of high variability. Bottom DO on the west coast was

found to be ~1 ml.l-1

less than on the Agulhas Bank (3.39 vs. 4.24 ml.l-1

).

Roberts and Sauer (1994) demonstrated that adult chokka squid are not found inshore on

the west coast where bottom DO is low, suggesting a lower threshold of 3 ml.l-1

. Roberts

(2005) concluded that both bottom DO and bottom temperature on the eastern Agulhas Bank

and the inner central Agulhas Bank, to be optimal for chokka squid spawning. It therefore

appears that chokka squid have found, or evolved to use, an environmental niche on the

eastern Agulhas Bank that optimizes spawning and their early life stages (Roberts, 2005).

Nowhere else on the shelf are both bottom temperature and bottom dissolved oxygen

simultaneously at optimal levels for egg development (Roberts, 2005).

In the summer of 1988-89, some 10 000 tons were landed by the jig fishery (Figure

2.23b). Roberts and Sauer (1994) noted that this period of high catches corresponded to

exceptional coastal upwelling on the Agulhas Bank, and moreover, a well developed La Niña

in the Pacific Ocean (Figure 2.24a). It was also pointed out that poor catches in 1987 and

1991-2 (shaded in Figure 2.23) corresponded with El Niño phases. They suggested that the El

Niño and La Niña phases of the Southern Oscillation enhance winter and summer climatic

conditions on the Agulhas Bank, respectively. In the case of winter, this implied severe

westerly winds which produce large swells and elevate near-seabed turbidity levels. This was

thought to negatively influence spawning behaviour of chokka inshore and consequently, the

catch. In summer, an increased frequency and severity of easterly winds will increase coastal

upwelling frequency and intensity along the coast which appeared to improve catches.

Several years later the El Niño of 1997-8, the largest on record this century (Figure

2.24a), sparked renewed interest in the ENSO phenomenon and its impact on the chokka

fishery. In a detailed analysis Roberts (1998) demonstrated a good correlation between the

summer easterly wind and coastal upwelling (i.e. low water temperatures) on the Agulhas

Bank, and that El Niño events (1977-78, 1982-83, 1987, 1991-3; Figure 2.24a) were

associated with subdued summer easterly winds and anomalous higher water temperatures

along the coastal region. This resulted in warmer benthic temperatures on the inshore

spawning grounds (measured at 24 m) which he suggested could impact egg development and

hence deter spawning squid from laying their eggs inshore. The intensive El Niño in 1997-98

changed this trend. Easterly winds were prominent, especially in February and March during

the summer of 1997-98, with strong evidence of upwelling in the Tsitsikamma SST data (see

depressed monthly SST peak in Figure 2.24b). The intensity of upwelling was reported to be

so severe (i.e. a drop from 22ºC to 10ºC in 4 hours) that it caused fish-kills on the

Knysna‒ Tsitsikamma coast (see Figure 2.2a for location). The mechanisms responsible for

the overall breakdown of the (apparent) El Niño‒ southern Africa climatic tele-connection

was investigated by Jury (1998) who suggested that a warm SST anomaly observed in the

South Atlantic was responsible for disrupting El Niño-induced upper westerly winds over the

Atlantic. The warm SST seemingly caused upper easterlies to oppose the El Niño-induced

westerlies, shielding southeast Africa from the adverse effects of the strong Pacific El Niño.


Figure 2.24. (a) Southern Oscillation Index (SOI) between January 1985 and March 2011 (b) monthly

averaged SST measured at Knysna (blue) and Tsitsikamma (red; start July 1991). Low values of the

summer SST peak indicate the extent of coastal upwelling. The shaded bands highlight ENSO events.

As seen in Figure 2.25, some correlation also seems to exist between annual catch and the

autumn estimated biomass (calculated from demersal research surveys), particularly for the

years 1990, 1992 and 1997. Roberts (2005) showed this correlation (r2=0.45) to be linear for

the years 1988-1997. However, updating this analysis with data for the period 1988 to 2008

now shows a deterioration of this correlation (r2=0.28). The correlation improves (r

2=0.44) if

the data for 2004 is removed on the grounds of it being an outlier. Interestingly though, 2004

in terms of the SST and SOI (Figure 2.24) is a very ordinary year suggesting other parameters

are at play during spawning and fishing which at times can clearly boost catch

(see Roberts, 1998).

Roberts (2005) postulated that the cold ridge ─ a highly productive upwelling filament

commonly found on the central Agulhas Bank during the summer months ─ plays an

important role in the survival and hence recruitment of paralarvae (Figure 2.1b). He

postulated that for optimal recruitment, paralarvae need to be advected westward to the cold

ridge region ─ a scenario he coined the westward transport hypothesis (WTH). Since then,

Martins (2010), using a coupled ocean model (ROMS-Regional Oceanic Modeling System)

and IBM (Individual-based Model) ─ has added credence to the WTH by demonstrating that

the main direction of transport on the eastern Agulhas Bank is indeed westward and that


recruitment of paralarvae spawned in the Tsitsikamma-St Francis Bay region is optimal in the

cold ridge region. However, satellite SST imagery indicates that the cold ridge (which has a

surface signature) is not always present during summer or can be weak. This is also supported

by the in situ SST measured at the base of the cold ridge (i.e. Knysna/Tsitsikamma; Figure

2.24) which showed that the strength and stability of coastal upwelling, which leads to the

formation of the cold ridge, is variable and dependant on the seasonal duration of the easterly

wind. Using the peak (highest) monthly averaged summer SST (usually December or

January) measured at Knysna for the period 1988‒ 1997, Roberts (2005) found a good

correlation with the following year’s annual biomass (r2=0.94) and catch (r

2=0.69), which he

argued supported the “coastal upwelling‒ well developed cold ridge‒ high levels of food

good recruitment” relationship. He noted that this relationship also held promise for

prediction.

Figure 2.25. (a) Correlation between annual autumn biomass of chokka squid (determined from

demersal trawl surveys) and annual commercial jig catches for the period 1992-2008 (b) correlation

between the highest (peak) monthly averaged SST measured at Tsitsikamma and the annual autumn

biomass.


Updating the cold ridge‒ biomass correlation with data for the period 1992‒ 2008 yields

a deterioration in the fit with an r2=0.24 (Figure 2.25a). The correlation improves to r

2=0.32 if

the SST measured at Tsitsikamma rather than Knysna is used (Figure 2.25b). This is justified

as Tsitsikamma is situated on the coast in the center of the main upwelling area whereas the

Knysna SST site is situated in the mouth of the lagoon and is subject to diurnal heating and

warmer lagoon water on an ebb tide (see temperature differences in Figure 2.24b).

Surprisingly, an average of SSTs (Tsitsikamma) for the summer months November,

December and January (thought to be a better index of coastal upwelling) yields an even

poorer correlation with an r2=0.21.

As for catches, the SST trend with ENSO events also seems to hold for the “coastal

upwelling well developed cold ridge-high levels of food-good recruitment” relationship,

suggesting that variability in the biomass is influenced by changes in weather patterns.

4.5. Management and Stock Assessment

The current primary management objective for this fishery is to cap effort at a level

which secures the greatest catch, on average, in the long term without exposing the resource

to the threat of reductions to levels at which recruitment success is compromised or catch

rates become economically unviable (Anon, 2010). Currently (2010) effort is capped at 136

vessels and a maximum of 2 422 crew.

Although this fishery has been in operation since 1985, the first formal stock assessment

was only conducted in 1998. It was based on an observation error estimator (Roel, 1998; Roel

and Butterworth, 2000) and comprised a biomass dynamic model which incorporated jig and

trawl catch and effort data, as well as biomass indices obtained from demersal trawl research

surveys.

The model assumed a hockey-stick stock recruitment function and required an

assumption that disturbance of spawning by jigging negatively impacted recruitment in order

to fit the abundance indices available (Roel, 1998). Results from this model indicated that the

resource was at a high risk (~90%) of collapsing at the then level of effort of around 3.6

million man-hours, where risk was defined as the probability of the spawner biomass

dropping below 20% of carrying capacity at least once within a 10 year projection period

under a fixed level of effort.

A 33% reduction in effort was required in order to bring the risk down to a more

acceptable level (~20%), but as a result of social (employment) reasons and concerns

regarding industry stability, a 10% reduction in effort was implemented, with an associated

risk of 72% (Roel, 1998). It is not clear whether this reduction in effort was indeed realized,

yet the industry continued to fish at an effort level of around 3 million man-hours for another

6 years without any obvious signs of increasing stress to the resource or the fishery (Glazer

and Butterworth, 2006).

The model of Roel (1998) was refined by Glazer and Butterworth (2006) by

incorporating process error into the model and replacing the hockey-stick stock recruitment

function with a Beverton-Holt stock recruitment function. Furthermore, Glazer and

Butterworth (2006) took full account of estimation uncertainty through a Bayesian estimation

approach.


The most recent update of this model, incorporating data to 2008, indicates that the squid

resource is in a healthier condition than previously thought, largely due to several successive

years of above-average recruitment. Despite this, there is concern that latent effort exists in

the fishery in that several vessels are fishing fewer days than they are capable of. Verification

of this is currently underway, and until some resolution has been obtained, and an updated

and more reliable assessment can be conducted, the TAE has been maintained at a constant

level for the past four years (Anon, 2010).

4.6. Fisheries and the Wider Ecosystem

Marine communities have changed enormously over recent decades, largely as a result of

human impact through fisheries reducing the abundance of apex predatory fishes and

mammals (Jackson et al., 2001; Pauley et al., 1998). These changes have had direct and

indirect effects on numerous marine communities, perhaps best illustrated by the kelp - sea

urchin- sea otter and killer whale interactions initiated by humans hunting for the fur trade

(Estes, 2005). Some attempts have been made to model these interactions to understand them

better (Stevens et al., 2000). Declines have similarly been recorded in stocks of most

predatory fishes exploited off South Africa (Attwood and Farquhar, 1999; Griffiths, 1997).

These declines would have had similar impacts on food webs here and they may partly

explain the abundance of inshore squids off South Africa’s south coast in the 1970’s and

1980’s when the chokka fishery rapidly expanded. It has been speculated that this increase in

fishing catch and effort was possible because of predator decrease (Smale et al., 2001).

Understanding predator-prey interactions in the marine environment that is largely driven by

environmental effects is a challenge because these interactions are highly dynamic. Predicting

the consequences of changes in predators and their prey in marine food webs is a challenge

because of the need to include both direct and indirect effects in models. Heithaus et al.

(2008) suggest that marine predators should be managed for demographic persistence as well

as the maintenance of density and risk driven processes.

In addition to fishery impact on edible fishes, people also have a direct and negative

impact on seals and dolphins by shooting “competitors” that take the catch or damage fishing

gear during operational conflicts, as well as potentially out competing seals as “super-

predators” (Wickens et al., 1992; Stewardson, 2001; Sauer and Smale unpublished data). In

the case of the squid fishery, fishers argue that they need to shoot “problem” animals because

of their major disruptions to squid spawning, which was also documented by Smale et al.

(2001).

As mentioned above, both seals and dolphins caused much greater disruption of

spawning aggregations than fishes, causing squids to desert the egg beds over which fishing

boats anchor to catch squid in shallow water, probably as they are perceived by the squids as

more of a threat than fish predators (Smale et al., 2001). The spawning aggregations may be

disrupted for at least tens of minutes, reducing the catch and often causing fishermen to

respond by shooting the mammals although this practice is illegal.

Managing these conflicts will remain a challenge given the declining resource base and

the expanding demand for marine products by expanding human populations.


References

Anon. 2010. Status of the South African Marine Fishery Resources 2010. Compiled by the

Chief Directorate: Fisheries Research, Fisheries Branch, Department of Agriculture,

Forestry and Fisheries.

Arkhipkin, A.I., Roa-Ureta, R., 2005. Identification of ontogenetic growth models for squid.

Mar Freshwater Res. 56, 371-386.

Arnold, J.M., 1965. Normal embryonic stages of the squid, Loligo pealii (Lesueur). Biol Bull.

128, 24-32.

Attwood, C.A., Farquhar, M., 1999. Collapse of linefish stocks between Cape Hangklip and

Walker Bay, South Africa. S. Afr. J. Mar. Sci. 21, 415-432.

Augustyn, C.J., 1989. Systematics, life cycle and resource potential of the chokker squid

Loligo vulgaris reynaudii. PhD Thesis, University of Port Elizabeth. 378 pp.

Augustyn, C.J., 1990. Biological studies on the chokker squid Loligo vulgaris reynaudii

(Cephalopoda: Myopsida) on spawning grounds off the south-east coast of South Africa.

S. Afr. J. mar. Sci. 9, 11-26.

Augustyn, C.J., 1991. The biomass and ecology of chokka squid Loligo vulgaris reynaudii off

the west coast of South Africa. S. Afr. J. Zool. 26(4), 164-181.

Augustyn, C.J., Lipinski, M.R., Sauer, W.H.H. 1992. Can the Loligo squid fishery be

managed effectively? A synthesis of research on Loligo vulgaris reynaudii. S. Afr. J. mar.

Sci. 12, 903-918.

Augustyn, C.J., Lipinski, M.R., Sauer, W.H.H., Roberts, M.J., Mitchell-Innes, B.A., 1994.

Chokka squid on the Agulhas Bank: life history and ecology. S. Afr. J. Sci. 90, 143-154.

Augustyn, C.J., Roel, B.A., 1998. Fisheries biology, stock assessment, and management of

the chokka squid (Loligo vulgaris reynaudii) in South African water: an overview.

CCOFI Rep. 39, 71-80.

Augustyn, C.J., Roel, B.A., Chochrane, K.L., 1993. Stock assessment in the chokka squid

Loligo vulgaris reynaudii fishery off the coast of South Africa, in: Okutani, T., O'Dor,

R.K., Kubodera, T. (Eds.), Recent advances in fisheries biology. Tokai University Press,

Tokyo, pp. 3-14.

Badenhorst, J.H., 1974. The morphology and histology of the male genital system of the

squid Loligo reynaudii (d’Orbigny). Ann. Univ. Stellenbosch (Ser A). 49(1), 1-36.

Batchelor, A.L., Ross, G.J.B., 1984. The diets and implications of dietary change of Cape

gannets on Bird Island, Algoa Bay. Ostrich. 55(2), 45-63.

Bidder, A.M., 1950. The digestive mechanism of the European squid Loligo vulgaris, Loligo

forbesii, Allotheuthis media, and Alloteuthis subulata. Q Jl microscopil Sci. 91(1), 1-43.

Bidder, A.M., 1966. Feeding and digestion in cephalopods, in: Wilbur, K.M., Yonge, C.M.

(Eds.), Physiology of Mollusca 2. London, Academic Press, pp. 97-124.

Blackburn, S., Sauer, W.H.H., Lipinski, M.R., 1998. The embryonic development of the

chokka squid Loligo vulgaris reynaudii d' Orbigny, 1845. The Veliger. 41(3): 249-258.

Boucher-Rodoni, R., Bocaud-Camou, E., Mangold, K., 1987. Feeding and digestion, in:

Boyle, P.R. (Ed), Cephalopod life-cycles 2. London, Academic Press, pp. 85-108.

Boyd, A.J., Shillington, F., 1994. Physical forcing and circulation patterns on the Agulhas

Bank. S. Afr. J. Sci. 90. 114-122.


Chapman, P., Shannon, L.V., 1987. Seasonality in the oxygen minimum layers at the

extremities of the Benguela system. S. Afr. J. Mar. Sci. 5, 85-94.

Crawford, R.J.M., 1982. Demersal trawling in the nearshore region between Cape Seal and

Klippen Point, Republic of South Africa, 1977-1979. Koedoe. 25, 33-42.

Dorfler, K., 2002. The dynamics of turbidity on the spawning grounds of the chokka squid

Loligo vulgaris reynaudii and links to squid catches. MSc Thesis, University of Port

Elizabeth. 157 pp.

Downey, N.J., Roberts, M.J., Baird, D., 2010. An investigation of the spawning behaviour of

the chokka squid Loligo reynaudii and the potential effects of temperature using acoustic

telemetry. ICES J. Mar. Sci. 67, 231-243.

Duncombe-Rae, C.M., 1991. Agulhas retroflection rings in the South Atlantic Ocean; an

overview. S. Afr. J. mar. Sci. 11, 327-344.

Durholtz, M.D., Lipinski, M.R., Field, J.G., 2002. Laboratory validation of periodicity of

incrementation in statoliths of the South African squid Loligo vulgaris reynaudii

(d'Orbigny, 1845): a reevaluation. J. Exp. Mar. Biol. Ecol. 279, 41-59.

Estes, J. A., 2005. Carnivory and trophic connectivity in kelp forests, in: Ray, J.C., Redford,

K.H., Steneck, R.S., Berger, J. (Eds), Large carnivores and the conservation of

biodiversity. Island Press, Washington, D.C., USA, pp. 61–81.

Glazer, J.P., Butterworth, D.S., 2006. Some refinements of the assessment of the South

African squid resource, Loligo vulgaris reynaudii. Fish. Res. 78, 14-25.

Griffiths, M.H., 1997. Feeding ecology of South African Argyrosomus japonicus (Pisces:

Sciaenidae), with emphasis on the Eastern Cape surf zone. S. Afr. J. mar. Sci. 18, 249-

264.

Hanlon, R.T., Smale, M.J., Sauer, W.H.H., 1994. An ethogram of body patterning behaviour

in the squid Loligo vulgaris reynaudii on spawning grounds in South Africa. Biol. Bull.

187, 363-372.

Hanlon, R.T., Smale, M.J., Sauer, W.H.H., 2002. The mating system of the squid Loligo

vulgaris reynaudii (Cephalopoda, Mollusca) off South Africa: Fighting, guarding,

sneaking, mating and egg laying behaviour. Bull. Mar. Sci. 71(1), 331-345.

Heithaus M.R., Frid, A., Wursig, A.J., Worm, B., 2008. Predicting ecological consequences

of marine top predator declines. Trends Ecol. Evol. 23(4), 202-210.

Hoving, H.J.T., Venter, J.D., Wortst, D.E., Lipinski, M.R., 2005. Adaptation of an

immunodot assay for multiple prey identification of squid paralarvae in field trials. J.

Mar. Biol. Assoc. U.K. 85, 1499-1501.

Hunter, J.R., Macewicz, B.J., 1980. Sexual maturity, batch fecundity, spawning frequency

and temporal patterns of spawning for the northern anchovy, Engraulis mordax, during

the 1979 spawning season. CCOFI Rep. 21, 139-149.

Jackson, J.B.C., Kirby, M.X., Berger, W.H., Bjorndal, K.A., Botsford, L.W., Bourque, B.J.,

Bradbury, R.H., Cooke, R., Erlandson, J., Estes, J.A., Hughes, T.P., Kidwell, S., Lange,

C.B., Lenihan, H.S., Pandolfi, J.M., Peterson, C.H., Steneck, R.S., Tegner, M.J., Warner,

R.R., 2001. Historical overfishing and the recent collapse of coastal ecosystems. Science.

293, 629–638.

Jackson, G.D., O’Dor, R.K., 2001. Time, space and ecophysiology of squid growth, life in the

fast lane. Vie Milieu. 51, 205-215.

Jury, M.R., 1998. Global significance of climatic variability in the tropical South Atlantic:

modulation of the ENSO circulation. Presented at the International Symposium on


Environmental Variability in the- Southeast Atlantic, Swakopmund, Nambia, March 30

to April 4 1098.

Klages, N.T.W., Willis, A.B., Ross, G.J.B., 1992. Variability in the diet of Cape gannet at

Bird Island, Algoa Bay, South Africa. S. Afr. J. mar. Sci. 12, 761-771.

Largier, J.L., Swart, V.P., 1987. East-west variation in thermocline breakdown on the

Agulhas Bank. S. Afr. J. mar. Sci. 5, 263-272.

Lipinski, M.R., 1978. The age of squids, Illex illecebrosus (Lesueur, 1821), from their

statoliths. International Commission for the Northwest Atlantic Fisheries, Research

Document No. 15, Serial No. 5167, 4 pp.

Lipinski, M.R., 1987. Food and feeding of Loligo vulgaris reynaudii from St Francis Bay,

South Africa. S. Afr. J. mar. Sci. 5, 557-564.

Lipinski, M.R., 1990. Changes in the pH caecum of Loligo vulgaris reynaudii during

digestion. S. Afr. J. mar. Sci. 9, 43-51.

Lipinski, M.R., 1992. Cephalopods and the Benguela ecosystem: Trophic relationships and

impact. S. Afr. J. mar. Sci. 12, 791-802.

Lipinski, M.R., 1994. Differences among basic biological parameters in a population of

chokka squid Loligo vulgaris reynaudii (Cephalopoda: Loliginidae) sampled by three

methods. S. Afr. J. mar. Sci. 24, 281-286.

Lipinski, M.R., 1998. Cephalopod life cycles: Patterns and Exceptions. S. Afr. J. mar. Sci. 20,

439-447.

Lipinski, M.R., 2002. Growth of cephalopods: conceptual model. Gabhanlungen der

Geologischen Bundesanstalt 57: 133-138.

Lipinski, M.R., David, J.H.M., 1990. Cephalopods in the diet of the South African fur seal

(Arctocephalus pusillus pusillus). J. Zool. 221, 359-374.

Lipinski, M.R., Durholtz, M.D., 1994. Problems associated with ageing squid from their

statoliths: towards a more structured approach. Antarct. Sci. 6(2), 215-222.

Lipinski, M.R., Durhotlz, M.D., Underhill, L.G., 1998. Field validation of age readings from

the statoliths of chokka squid (Loligo vulgaris reynaudii d'Orbigny, 1845) and an

assessment of associated errors. ICES J. Mar. Sci. 55, 240-257.

Lipinski, M.R., Hampton, I., Sauer, W.H.H., Augustyn, C.J., 1998. Daily net emigration from

a spawning concentration of chokka squid (Loligo vulgaris reynaudii d'Orbigny, 1845) in

Kromme Bay South Africa. ICES J. Mar. Sci. 55, 258-270.

Lipinski, M.R., Payne, A.I.L., Rose, B., 1992. The importance of cephalopods as prey for

hake and other groundfish in South African waters. S.Afr.J. Mar. Sci. 12, 651-662.

Lipinski, M.R., Soule, M.A., 2007. A new direct method of stock assessment of the loliginid

squid. Rev. Fish Biol. Fish. 17, 437–453.

Lipinski, M.R., Underhill, L.G., 1995. Sexual maturation in squid: Quantum or continuum. S.

Afr. J. mar. Sci. 15, 207-223.

Lipinski, M.R., unpublished. The age of squids, Illex illecebrosus (Lesueur, 1821) from their

statoliths. ICNAF Res. Doc. 15 (5167): 4 pp.

Lutjeharms, J.R.E., 2001. Agulhas Current, in: Steele, J.H., Thorpe, S.A., Turekian, K.K.

(Eds), Encyclopedia of Ocean Science, Academic Press, San Diego, pp. 104-113.

Lutjeharms, J.R.E., Cooper, J., 1996. Interbasin leakage through Agulhas Current filaments.

Deep-Sea Res. (1 Oceanogr. Res. Pap.). 43, 213-238.

Lutjeharms, J.R.E., Cooper, J., Roberts, M.J., 1999. Upwelling at the inshore edge of the

Agulhas Current. Cont. Shelf Res. 20, 737-761.


Lutjeharms, J.R.E., Monteiro, P.M.S., Tyson, P.D., Obura, D., 2001. The oceans around

southern Africa and regional effects of global change. S. Afr. J. mar. Sci. 97, 119-130.

Martins, R.S., 2010. Some factors influencing the transport of chokka squid (Loligo reynaudii

D'Orbigny, 1839) paralarvae off the Eastern Cape, South Africa. PhD Thesis, Univeristy

of Cape Town. 131 pp.

Martins, R.S., Roberts, M.J., Vidal, E.A.G., Moloney, C.L., 2010. Effects of temperature on

yolk utilization in chokka squid (Loligo reynaudii d'Orbigny, 1839) paralarvae. J. Exp.

Mar. Biol. Ecol. 386 (1-2), 19-26.

Melo, Y.C., 1994., Spawning frequency of the anchovy Engraulis capensis. S. Afr. J. mar.

Sci, 14, 321-331.

Melo, Y.C., Armstrong, M.J., 1991. Batch spawning behaviour in light fish Maurolicus

muelleri. S. Afr. J. mar. Sci. 10, 125-130.

Melo, Y.C., Sauer, W.H.H., 1999. Confirmation of serial spawning in the chokka squid

Loligo vulgaris reynaudii off the coast of South Africa. Mar. Biol. 135 (2), 307-313.

Melo, Y.C., Sauer, W.H.H., 2007. Determining the daily spawning cycle of the chokka squid

Loligo vulgaris reynaudii off the South African Coast. Rev. Fish Biol. Fish. 17(2-3), 247-

257.

Naef, A., 1928. Die Cephalopoden. Fauna und Flora des Golfes von Neapel. 35(II), 357.

Olyott, L.J.H., Sauer, W.H.H., Booth, A.J., 2006. Spatio-temporal patterns in maturation of

the chokka squid (Loligo vulgaris reynaudii) off the coast of South Africa. ICES J. Mar.

Sci. 63, 1649-1664.

Olyott, L.J.H., Sauer, W.H.H., Booth, A.J., 2007. Spatial patterns in the biology of the chokka

squid, Loligo vulgaris reynaudii on the Agulhas Bank, South Africa. Rev. Fish Biol. Fish.

17(2-3), 159-172.

Oosthuizen, A. 1999. The effects of temperature on embryonic development and hatching

success of squid (Loligo vulgaris reynaudii) eggs. MSc Dissertation, University of Port

Elizabeth. 118p

Oosthuizen, A., Roberts, M. J., 2009. Bottom temperature and in situ development of chokka

squid eggs (Loligo vulgaris reynaudii) on the deep spawning grounds, South Africa.

ICES J. Mar. Sci. 66, 1967-1971.

Oosthuizen, A., Roberts, M. J., Sauer, W. H. H., 2002. Early post-cleavage stages and

abnormalities identified in the embryonic development of chokka squid eggs Loligo

vulgaris reynaudii. S. Afr. J. mar. Sci. 24, 379-382.

Pauly, D., 1998. Why squid, though not fish, might be better understood by pretending they

are. S. Afr. J. mar. Sci. 20, 47-58.

Pauly, D, Christensen, V, Dalsgaard, J, Froese, R, Torres, F Jr., 1998. Fishing down marine

food webs. Science. 279, 860-863.

Prabhu, M.S., 1956. Maturation of intra-ovarian eggs and spawning periodicities in some

fishes. Indian J. Fish. 3(1), 59-90.

Rademeyer, R.A., 2003. Assessment and management procedures for the hake stocks off

Southern Africa. MSc Thesis, University of Cape Town. 209 pp.

Rand, R.W., 1960. The biology of guano producing sea-birds. The distribution, abundance

and feeding habits of the Cape penguin, Spheniscus demersus, off the south-western coast

of the Cape Province. Investl. Rep. Div. Fish. S. Afr. 41, 1-28.

Randall, R.M., Randall, B.M., 1981. Species diversity and size ranges of cephalopods in the

diet of Jackass penguins from Algoa Bay, South Africa. S. Afr. J. Zool. 16(3), 163-166.


Roberts, M.J., 1998. The influence of the environment on chokka squid Loligo vulgaris

reynaudii spawning aggregations: Steps towards a quantified model. S. Afr. J. mar. Sci.

20, 267-284.

Roberts, M.J., 2005. Chokka squid (Loligo vulgaris reynaudii) abundance linked to changes

in South Africa's Agulhas Bank ecosystem during spawning and the early life cycle.

ICES J. Mar. Sci. 62(1), 33-55.

Roberts, M.J., Barange, M., Lipinski, M. R., Prowse, M. R., 2002. Direct hydroacoustic

observations of chokka squid Loligo vulgaris reynaudii spawning activity in deep water.

S. Afr. J. mar. Sci. 24, 387-393.

Roberts, M.J., Downey, N.J., Sauer, W.H.H., 2012. The relative importance of shallow and

deep shelf spawning habitats for the South African chokka squid (Loligo reynaudi). ICES

J. Mar. Sci. In press.

Roberts, M.J., Mullon, C., 2010. First Lagrangian ROMS-IBM simulations indicate large

losses of chokka squid Loligo reynaudii paralarvae from South Africa's Agulhas bank.

Afr. J. Marine Sci. 32(1), 71-84.

Roberts, M.J., Sauer, W.H.H., 1994. Environment: the key to understanding the South

African chokka squid (Loligo vulgaris reynaudii) life cycle and fishery? Antarct. Sci.

6(2), 249-258.

Roel, B., 1998. Stock assessment of the chokka squid Loligo vulgaris reynaudii. Ph.D. thesis,

University of Cape Town. 217 pp.

Roel, B., Butterworth, D.S., 2000. Assessment of the South African chokka squid Loligo

vulgaris reynaudii. Is disturbance of aggregations by the recent jig fishery having a

negative impact on recruitment. Fish. Res. 48, 213-228.

Ross, G.J.B., 1984. The smaller cetaceans of the south east coast of southern Africa. Ann.

Cape Prov. Mus. (nat. Hist.) 15(2), 173-410.

Sauer, W.H.H., 1995. The impact of fishing on chokka squid Loligo vulgaris reynaudii

concentrations on inshore spawning grounds in the South-Eastern Cape, South Africa. S.

Afr. J. mar. Sci. 16, 185-193.

Sauer, W.H.H., Goschen, W.S., Koorts, A.S., 1991. A preliminary investigation of the effect

of sea temperature fluctuations and wind direction on catches of chokka squid Loligo

vulgaris reynaudii off the Eastern Cape, South Africa. S. Afr. J. Mar. Sci. 11, 467-473.

Sauer, W.H.H., Lipinski, M.R, 1990. Histological validation of morphological stages of

sexual maturation in chokker squid Loligo vulgaris reynaudii D’Orb (Cephalopoda:

Loliginidae). S. Afr. J. mar. Sci. 9,189-200.

Sauer, W.H.H., Lipinski, M.R., 1991. Food of squid Loligo vulgaris reynaudii (Cephalopoda:

Loliginidae) on their spawning grounds off the Eastern Cape, South Africa. S. Afr. J. mar.

Sci. 10, 193-201.

Sauer, W.H.H., Lipinski, M. R., Augustyn, C. J., 2000. Tag recapture studies of the chokka

squid Loligo vulgaris reynaudii d’Orbigny, 1845 on inshore spawning grounds on the

south-east coast of South Africa. Fish. Res. 45, 283-289.

Sauer, W.H.H., McCarthy, C., Smale, M. J., Koorts, A. S., 1993. An investigation of the egg

distribution of the chokka squid, Loligo vulgaris reynaudii, in Krom Bay, South Africa.

Bull. Mar. Sci. 53(3), 1066-1077.

Sauer, W.H.H., Melo, Y.C., De Wet ,W., 1999. Fecundity of the chokka squid Loligo vulgaris

reynaudii on the south-eastern coast of South Africa. Mar. Biol. 135 (2), 315-319.


Sauer, W.H.H., Roberts, M.J., Lipinski, M. R., Smale, M.J., Hanlon, R.T., Webber, D.M.,

O’Dor, R.K., 1997. Choreography of the squid’s “nuptial dance”. Biol. Bull. 192(2), 203-

207.

Sauer, W.H.H., Smale, M.J., 1991. Predation patterns on the inshore spawning grounds of the

squid Loligo vulgaris reynaudii (Cepahlopoda: Loliginidae) off the south-eastern cape,

South Africa. S. Afr. J. mar. Sci. 11, 513-523.

Sauer, W.H.H., Smale, M. J., 1993. Spawning behaviour of Loligo vulgaris reynaudii in

shallow coastal waters of the south-Eastern Cape, South Africa, in: Okutani, T., O'Dor,

R.K., Kubodera, T. (Eds), Recent Advances in Fisheries Biology. Tokai University Press,

Tokyo, pp. 489-498.

Sauer, W.H.H., Smale, M.J., Lipinski, M.R., 1992. The location of the spawning grounds,

spawning and schooling behaviour of the squid Loligo vulgaris reynaudii (Cephalopoda:

Myopsida) off the eastern Cape coast, South Africa. Mar. Biol. 114, 97-107.

Schön, P., 2000. An investigation into the influence of the environment on spawning

aggregations and jig catches of chokka squid Loligo vulgaris reynaudii off the coast of

South Africa. PhD Thesis, University of Port Elizabeth. 130 pp.

Schumann, E.H., Perrins, L.A., Hunter, I.T., 1982. Upwelling along the south of the Cape

Province, South Africa. S. Afr. J. Sci. 78, 238-242.

Sekiguchi, K., Klages, N.T.W., Best, P.B., 1992. Comparative analysis of the diets of smaller

odontocetes cetaceans along the coast of southern Africa. S. Afr. J. mar. Sci. 12, 843-861.

Shannon, L.V., Nelson, G., 1996. The Benguela: large scale features and processes and

system variability, in: Wefer, G., Berger, W.H., Siedler, G., Webb, D., (Eds). The South

Atlantic: Present and Past Circulation. Springer, Berlin, pp. 163-210.

Shaw, P.W., Hendrickson, L., McKeown, N.J., Stonier, T., Naud, M.-J., Sauer, W.H.H.,

2010. Discrete spawning aggregations of loliginid squid do not represent genetically

distinct populations. Mar. Ecol. Prog. Ser. 408, 117-127.

Shaw, P.W., Sauer, W.H.H., 2004. Multiple paternity and complex fertilisation dynamics in

the squid Loligo vulgaris reynaudii. Mar. Ecol. Prog. Ser. 270, 173-179.

Smale, M.J. 1986. The feeding biology of four predatory reef fishes off the south-eastern

Cape coast, South Africa. S. Afr. J. Zool. 21(1), 111-130.

Smale, M.J. 1991. Occurrence and feeding of three shark speices, Carcharhinus brachyurus,

C. obscurus and Sphyrna zygaena on the Eastern Cape coast of South Africa. S. Afr. J.

mar Sci. 11, 31-42.

Smale, M.J., M.N. Bruton, 1985. Predation and prey selectivity by Argyrosomus

hololepidotus (Osteiechthyes: Sciaenidae) in the south-eastern Cape waters of South

Africa. S. Afr. J. Zool. 20(3), 97-108.

Smale, M.J. Compagno L.J.V., 1997. Life history and diet of two southern African

smoothhound sharks, Mustelus mustelus (Linnaeus, 1758) and Mustelus palumbes Smith,

1957 (Pisces Triakidae) S. Afr. J. mar. Sci. 18, 229-248.

Smale, M.J., A.J.J. Goosen, 1999. Reproduction and feeding of spotted gully shark, Triakis

megalopterus, off the Eastern Cape. S. Afr. Fish. Bull. 97, 987-998.

Smale, M.J., Sauer, W.H.H., Hanlon, R.T., 1995. Short Communications: Attempted ambush

predation on spawning squids Loligo vulgaris reynaudii by benthic pyjama sharks,

Poroderma africanum, off South Africa. J. Mar. Biol. Assoc. U.K. 75, 739-742.


Smale, M.J., Sauer, W.H.H., M.J. Roberts, 2001. Behavioural interactions of predators and

spawning chokka squid off South Africa: towards quantification. Mar. Biol. 139, 1095-

1105.

Soule, M.A., Hampton, I., Lipinski, M.R., 2010. Estimating the target strength of live, free-

swimming chokka squid Loligo reynaudii at 38 and 120 kHz. ICES J. Mar. Sci. 67, 1381-

1391.

Spratt, J.D. 1978. Age and growth of the market squid, Loligo opalescens Berry, in Monterey

Bay. Calif Dep. Fish. Game Fish Bull. 169, 35-44.

Stevens, J.D., Bonfil, R., Dulvy, N.K., Walker, P.A., 2000. The effects of fishing on sharks,

rays, and chimaeras (chondrichthyans), and the implications for marine ecosystems. ICES

J. Mar. Sci. 57, 476-494.

Stewardson, C.L., 2001. Biology and conservation of the Cape (South African) fur seal

Arctocephalus pusillus pusillus (Pinnipedia:Otariidae) from the Eastern Cape Coast of

South Africa. PhD thesis, The Australian National University. 172 pp.

Tyson, P.D., Preston-White, R.A., 2000. The Weather and Climate of Southern Africa.

Oxford University Press, Cape Town. 408 pp.

Vecchione, M., Lipinski, M.R., 1995. Descriptions of the paralarvae of two loliginid squids in

Southern African waters. S. Afr. J. Mar. Sci. 15, 1-7.

Venter, J.D., Wyngaardt, S. van, Lipinski, M.R., Verheye, H.M., Verschoor, J.A., 1999.

Detection of zooplankton prey in squid paralarvae with immunoassay. Journal of

Immunoassay 20, 127-149.

Wickens, P.A., Japp, D.W., Shelton, P.A., Kriel, F., Goosen, P.C., Rose, B., Augustyn, C.J.,

Bross, C.A.R., Penney, A.J., Krohn, R.G., 1992. Seals and fisheries in South Africa -

competition and conflict. S. Afr. J. Mar. Sci. 12, 773-789.

loligo reynaudii, chokka squid - nova science publishers...loligo reynaudi) are found on the west...

Documents