Loligo Reynaudii, Chokka Squid

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Chapter II

Loligo reynaudii, Chokka Squid

Warwick H. H. Sauer1, Nicola J. Downey2,1, Marek Lipinski1, Mike J. Roberts3,1, Malcolm J. Smale4, Paul Shaw5,1, Jean Glazer6 and Yolanda Melo6 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]. 34 Warwick H. H. Sauer, Nicola J. Downey, Marek Lipinski et al.

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

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). Loligo reynaudii, Chokka Squid 37

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 38 Warwick H. H. Sauer, Nicola J. Downey, Marek Lipinski et al. 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). Loligo reynaudii, Chokka Squid 39

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

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.

Loligo reynaudii, Chokka Squid 41

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

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 Loligo reynaudii, Chokka Squid 43 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 44 Warwick H. H. Sauer, Nicola J. Downey, Marek Lipinski et al. 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 Loligo reynaudii, Chokka Squid 45

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 46 Warwick H. H. Sauer, Nicola J. Downey, Marek Lipinski et al. 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, Loligo reynaudii, Chokka Squid 47

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

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%). Loligo reynaudii, Chokka Squid 49

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

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.

Loligo reynaudii, Chokka Squid 51

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

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. Loligo reynaudii, Chokka Squid 53

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 54 Warwick H. H. Sauer, Nicola J. Downey, Marek Lipinski et al. 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). Loligo reynaudii, Chokka Squid 55

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 56 Warwick H. H. Sauer, Nicola J. Downey, Marek Lipinski et al. 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 Loligo reynaudii, Chokka Squid 57 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 58 Warwick H. H. Sauer, Nicola J. Downey, Marek Lipinski et al. 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. Loligo reynaudii, Chokka Squid 59

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

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. Loligo reynaudii, Chokka Squid 61

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 (r2=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 62 Warwick H. H. Sauer, Nicola J. Downey, Marek Lipinski et al. 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 (r2=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. Loligo reynaudii, Chokka Squid 63

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 r2=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. 64 Warwick H. H. Sauer, Nicola J. Downey, Marek Lipinski et al.

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.

Loligo reynaudii, Chokka Squid 65

References

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