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Author's personal copy

Fisheries Research 151 (2014) 148– 157

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Fisheries Research

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Life history of Argyrosomus japonicus, a large sciaenid at the southernpart of its global distribution: Implications for fisheries management

Greg J. Fergusona,∗, Tim M. Warda, Alex Iveya, Thomas Barnesb

a South Australian Research and Development Institute (Aquatic Sciences), PO Box 120, Henley Beach, South Australia 5024, Australiab School of Earth & Environmental Sciences, University of Adelaide, Adelaide, South Australia 5005, Australia

a r t i c l e i n f o

Article history:Received 26 July 2013Received in revised form 5 November 2013Accepted 7 November 2013

Keywords:SciaenidaeLife-historyAgeGrowthSize at maturityFishery biologyArgyrosomus japonicusJapanese meagreMulloway Kob

a b s t r a c t

The life-history of the sciaenid Argyrosomus japonicus in South Australia was investigated to inform areview of fisheries management. Validated, otolith-based growth coefficients for females (Linf = 1430.52,K = 0.137, t0 = −0.303, n = 209) and males (Linf = 1356.23, K = 0.159, t0 = 0.000, n = 185) suggested highasymptotic size and low growth rates, relative to other populations. A growth performance index (ω)was lower for A. japonicus in South Australia than for other populations. Sizes at 50 and 95% maturity(SAM50,95) were 850 and 1028 mm TL, respectively for females and 778 and 923 mm TL, respectively formales. Age structures from 2011 appeared truncated compared to those from 2001 and 2002 with noindividuals greater than 10 years old. The dominant year class observed in age structures from 2001and 2002 was not present in 2011. This may reflect the combined effects of historically severe droughtfrom 2002 to 2010 and fishing. This population is vulnerable to fishing as juveniles in estuarine habitatand as adults in spawning aggregations in marine habitat. Loss of protected estuarine habitat for juve-niles from flow regulation and drought may make this population particularly vulnerable to overfishing.Whilst maintenance of appropriately timed freshwater inflows to estuarine habitat is important for thispopulation their availability is uncertain. Populations of A. japonicus in South Australia would benefitfrom management measures that: (i) aim to preserve capacity for egg production; (ii) allow recruits toenter the adult population; and that (iii) rebuild and maintain long-tailed age structures. Amendmentsto the legal minimum size and the protection of juveniles in estuaries and the adult spawning/feedingaggregations are recommended.

© 2013 Elsevier B.V. All rights reserved.

1. Introduction

Body size of fishes is one of the most important factors in deter-mining vulnerability to fishing (Jennings and Kaiser, 1998; Jenningset al., 1999; Reynolds et al., 2005). Large-bodied fishes are usu-ally long-lived and their vulnerability is evident by their loss frommulti-species catches (Ferguson et al., 2013; Winemiller and Rose,1992). The life-history of such large, long-lived fishes is often basedon delayed maturity and high fecundity and has been termed ‘bethedging’ or periodic strategist (Winemiller and Rose, 1992) becausereproductive output is allocated across many years allowing popu-lations to survive periods that are unfavourable for spawning andlarval dispersal (Longhurst, 2002). For periodic strategists, recruit-ment of newly mature individuals is low relative to the number andbiomass of older adults with the exception of occasional very strongyear classes for those species with highly variable reproductivesuccess (Heppell et al., 2005).

∗ Corresponding author. Tel.: +61 8 8207 5467; fax: +61 88207 5481.E-mail address: [email protected] (G.J. Ferguson).

Many large sciaenids have “periodic strategist” life historieswith characteristic high longevity and late maturity. Additionally,many sciaenids form spawning aggregations in and near estuariesand recruitment success of several species has been linked to freshwater inflows into estuaries (Cisneros-Mata et al., 1995; Griffiths,1996; Ferguson et al., 2008; Rowell et al., 2005, 2008). The evolu-tion of late maturity in sciaenids may have been facilitated by lowjuvenile mortality in protected estuarine and surf zone habitats(Griffiths, 1996) and a possible “river-discharge” spawning rela-tionship (Ferguson et al., 2008).

The delayed maturity of some sciaenid species may make themparticularly vulnerable to overfishing (Musick, 1999; Musick et al.,2000). Recruitment overfishing resulting from the combined effectsof targeting juveniles in estuaries and adults in spawning aggrega-tions, referred to as the “one-two punch” approach (Rowell et al.,2008), has been implicated in the declines of several sciaenidspecies worldwide. Sciaenid populations in serious decline includefive species in the west Pacific (Liu and Sadovy de Mitcheson, 2008;Sadovy and Cheung, 2003), one species in Europe (Quéméner, 2002)and seven species in North America (Musick et al., 2000). For exam-ple, estuarine dependence, slow growth rates, and high age at

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G.J. Ferguson et al. / Fisheries Research 151 (2014) 148– 157 149

maturity have been identified as factors contributing to the declineof Sciaenops ocellatus and Totoaba macdonaldi in the Gulf of Mexico(Lercari and Chávez, 2007; Murphy and Crabtree, 2001) and Bahabataipingensis and Larimichthyes crocea in China (Liu and Sadovy deMitcheson, 2008; Sadovy and Cheung, 2003).

Fishery management depends on understanding the dynam-ics of the variation in population abundance and determining theimpact of fishing on the natural population processes (Hilbornand Walters, 1992). This information can be provided by val-idated, otolith-based age estimates (Campana, 2001; Campanaand Thorrold, 2001). Consideration of life-history strategies isalso important because such strategies are linked to populationdynamics and environmental forcing (King and McFarlane, 2003).Traditional stock assessment methods based on biomass maybe inappropriate for species with late age at maturity and highlongevity because of difficulties associated with estimating theinstantaneous rate of fishing mortality (Heppell et al., 2005). Conse-quently, age distribution and status of the adult stock may be criticalfor assessing population health of such species (Chale-Matsau et al.,2001).

The Japanese meagre, Argyrosomus japonicus (Temminck &Schlegel, 1843), known as mulloway in Australia, is a large, preda-tory sciaenid that is widely distributed in estuaries and nearshorecoastal waters (<100 m depth) of the Pacific and Indian Oceansincluding sub-tropical and temperate waters in Australia (Griffithsand Heemstra, 1995; Silberschneider et al., 2008). Like other sci-aenids, A. japonicus has life-history characteristics that make itvulnerable to anthropogenic impacts including estuarine asso-ciation (Ferguson et al., 2008; Griffiths, 1996), high age/size atmaturity, and high maximum age (Farmer, 2008; Griffiths, 1996;Griffiths and Hecht, 1995). Populations of A. japonicus have beenreported as overfished in South Africa and eastern Australia(Griffiths, 1997; Silberschneider et al., 2008).

For the population of A. japonicus associated with the Mur-ray River estuary in eastern South Australia, temporal trends infreshwater inflows, commercial catches, and population age struc-tures suggest estuarine dependence with a requirement for yearsof high freshwater inflow in order to establish a strong year classes(Ferguson et al., 2008). It has been suggested that poor representa-tion of older individuals in age structures from feeding/spawningaggregations in 2000 and 2001 may be due to a combination offlow regulation and fishing with potential for compromised eggproduction (Ferguson et al., 2008, 2013). From 2002 to 2010, themost severe drought on historical record combined with excessivewater abstraction, resulted in strongly reduced freshwater flowsinto the Murray River estuary (Lester and Fairweather, 2009). Addi-tionally, the population of A. japonicus in eastern South Australiaoccurs at the southernmost part of the geographic distribution ofthe species (∼35◦ S) where winter water temperatures are lower(∼14 ◦C) than the optimum temperature for growth of juveniles(25–26 ◦C, Bernatzeder and Britz, 2007). Despite such concernsthere are no robust estimates of basic life-history parameters forgrowth and reproduction available for A. japonicus in eastern SouthAustralia.

In South Australia, commercial fishers target A. japonicusthroughout their geographic range and they are considered an“icon” species by recreational fishers. Most commercial catchesare from the population located around the Murray River wheregill nets are used to target small A. japonicus in the estuaryand larger individuals from spring/summer aggregations in theadjacent nearshore marine. Catches from the estuary compriseapproximately 80% of the annual commercial catch of A. japonicusin South Australia (Ferguson et al., 2008). Recreational line fisherstarget large individuals from the austral spring–summer aggrega-tions with equivalent catches to those from the commercial sector(Jones and Doonan, 2005; Jones, 2009).

Management of this fishery assumes a single stock in SouthAustralia however regional differences in the elemental chemistryand morphology of otoliths suggest that separate populations occuralong eastern and western coasts of South Australia (Ferguson et al.,2011). Management of A. japonicus comprises (i) a legal minimumlength (LML) of 460 mm TL in the Murray River estuary and 760 mmTL for all nearshore marine waters for commercial and recreationalfishers, and (ii) bag and boat limits for recreational fishers.

This study provides validation of the ageing methodology forA. japonicus in South Australia and seeks to improve understand-ing of the life history and demography by providing estimates ofgrowth rates and age/size at maturity to inform a review of fisherymanagement. In addition, the possible impact of drought on thispopulation is examined by comparing age structures from beforeand after recent, severe drought (2002–2010). Findings are dis-cussed in the context of populations in other locations and usedto identify options for improving the management of exploitedpopulations of long-lived sciaenids.

2. Materials and methods

2.1. Samples

Biological samples from sub/adult and adult A. japonicus werecollected from commercial gill net and recreational line catchestaken from spring/summer aggregations in the nearshore marineenvironment adjacent the Murray River in eastern South Australiain 2001, 2002, and 2011 (139◦ 22′ 40.34′′ E, 35◦ 54′ 24.88′′ S).(Fig. 1, Table 1). Additional, information on size/age and reproduc-tive development of juvenile A. japonicus (460–600 mm) within theMurray River estuary was collected from commercial net catcheswithin the estuary. Information on sub-legal size fish (<460 mmTL) within the estuary were obtained from a research programmewhich used multi-panel gill (Table 1).

For all samples, each fish was measured for total and standardlengths (TL, SL, nearest mm) and where possible weighed to thenearest 100 g (to calculate GSIs). Gonads were dissected, weighed,sexed and staged according to a published method (Hunter andMacewiecz, 1985) (Table 2). Briefly, macroscopic staging of ovaries(n = 211) was to one of five developmental stages based on size,colour and visibility of oocytes and was validated by microscopicexamination of histological preparations. For these ovaries (n = 27),a segment was removed from the centre of one lobe and preservedin a fixative of formalin, acetic acid and calcium chloride (FAACC).Testes (n = 179) were classified into 3 stages (Table 2). Sagittae wereremoved via a cut through the ventral ex-occipital region of theskull and were cleaned, dried, weighed and stored in labelled plasticbags.

2.2. Age and size

2.2.1. Laboratory preparation of otolithsThe left sagitta from each pair of otoliths was embedded in

polyester casting resin, and a 500 �m thick longitudinal section wascut with a diamond blade mounted on a Gemmasta 6′′ (150 mm)bench top saw. Serial sections were cut and the section incorporat-ing the otolith centre mounted on a glass microscope slide usingcyanoacrylate glue. Mounts were ground to improve visibility ofthe opaque bands using silicon carbide polishing paper (grades1200 and 900) and were examined on a black background underreflected light using a Leica MZ-16 dissecting microscope at 5–10×magnification.

2.2.2. Validation of ageing methodBecause identification of the first annulus is difficult in many

species, the pattern of deposition in otoliths was validated both


150 G.J. Ferguson et al. / Fisheries Research 151 (2014) 148– 157

Fig. 1. Map of Australia (inset) showing South Australia (SA), New South Wales (NSW) and Western Australia (WA). Main map shows the coast of South Australia includingthe eastern coast, Murray River estuary and adjacent nearshore marine environment.

directly and indirectly. Direct validation of annuli was done frommonthly sampling of captive fish of known birth date. Indirect vali-dation was achieved by marginal increment analysis of wild caughtfish.

A. japonicus were spawned at SARDI Aquatic Sciences, Adelaidefrom 10 to 18th December 2000. The juveniles were held in a10,000 L tank with flow-through seawater pumped from the nearbySpencer Gulf and with water temperature and natural light reflect-ing the normal seasonal cycle. The fish were fed once per day oncockles (Donax deltoides, Bivalvia: Donacidae) at a rate of 5% of thetotal weight of live fish, and later on dry fish pellets at a rate of2% of total weight per day. Each month, for 12 months, 10–12 fishwere sampled, and the otoliths removed. These otoliths, as wellas all other otoliths in subsequent laboratory processing, were sec-tioned, mounted, and examined with a binocular microscope underreflected light. In addition to this, the third annulus was also val-idated directly from samples from the same spawning. These fishwere kept in sea cages at an aquaculture facility in Spencer Gulf.

Fish (n = 10 fish per sample) were sampled at 34 months (October2002), 36 months (December 2002) and 37 months (January 2002).

Indirect validation of annulus formation was done by marginalincrement analysis of monthly otolith samples from small juvenilesA. japonicus (1–2 opaque zones) caught in multi-panel researchgill nets and larger juveniles (3–4 opaque zones) from commercialgill nets. Measurements of the marginal increment of longitudi-nal sections of otoliths were made using digital imaging software(Image Pro 5.1TM, Media Cybernetics). The marginal increment ofeach otolith was defined as the distance between the outer edge ofthe single, or outermost opaque zone, and the edge of the otolith.When only one opaque zone was present this was expressed as aproportion of the distance between the primordium and the outeredge of the opaque zone. When two or more opaque zones werepresent this was a proportion of the distance between the outeredges of the two outermost opaque zones. Each measurement wasmade in the region of the cauda along an axis aligned with the pos-terior edge of the sulcus and perpendicular to the opaque zone(s)

Table 1Sample sizes for age/size structures of Argyrosomus japonicus from the Murray River estuary and adjacent nearshore marine environment in eastern South Australia.

Year Habitat Fishery Net mesh size (mm stretched) Age (n) Length (n)

2001 Estuary Research multi-panel gill net 40, 50, 70, 113, 153 151 –2001 Estuary Commercial gillnet >50 to ≤64; and >115 86 –2001 Marine Commercial gillnet >120 73 732001 Marine Recreational line Na 26 262002 Marine Commercial gillnet >150 63 782011 Marine Commercial gillnet >150 111 98



Table 2Stages of development used for macroscopic and microscopic classification of the ovaries and testes of Argyrosomus japonicus.

Ovary stage Macroscopic appearance Microscopic appearance

IImmature

Small, clear to translucent, jelly-like thread, grey to pink in colour.Close to posterior vertebral column.Oocytes invisible to naked eye

Unyolked, non atretic oocytes only

IIDeveloping

Small to medium, translucent to yellow/brown. Ovary lobe mayappear short, relative to stage III.Oocytes invisible to naked eye.

Mainly unyolked, few partially yolked oocytes

IIIDeveloped

Large, yellow to orange. Granular appearance due to visible individualoocytes. Ovary large, reaching forward into anterior gut cavity.

Dominated by advanced yolked oocytes, unyolked withpartially yolked oocytes present in low numbers.Lumen large and obvious.

IVGravid orrunning ripe

Very large orange, reaching anteriorly to/above stomach. Clearhydrated oocytes visible among opaque oocytes.

Oocytes of all stages present from unyolked to hydrated.Lumen large, obvious.

VRegressing orresting

Ovaries medium in size, brown to reddish- brown, Opaque.More flaccid than other stages.

Atretic oocytes present.Partially yolked oocytes present.Greater number of unyolked oocytes relative to yolkedthan in stage III/IV ovaries.

Testes stageIImmature

Appear as fine, white to pink threads.

IIDeveloping

Thickened thread, white/grey, no sperm or small amount of spermwhen squeezed.

IIIDeveloped

Swollen, grey, running ripe.

without knowledge of the date of capture of the fish and recordedto the nearest 0.01 mm. The values for marginal increments wereseparated into groups according to the number of opaque zones inthe otoliths. For otoliths with 1 and 2 opaque zones, samples werepooled into corresponding months from 1 January 2001 to 31stDecember 2002. Otoliths with 3 and 4 opaque zones were similarlypooled but included additional samples from 1 January 2003 to 31December 2003 to increase sample sizes.

2.2.3. Reading otolithsOtoliths were examined under reflected light and ages esti-

mated from counts of opaque zones. Opaque zones were counted inthe region of the cauda along the posterior axis of the sulcus whichhas been reported as the best area for interpreting otoliths fromA. japonicus (Farmer, 2008; Griffiths, 1996; Griffiths and Hecht,1995). The mean birth date of 1st January was estimated from themid-point of the spawning season. This, in combination with thetime at which the annulus becomes delineated on the otolith, wasused to determine the age of the individual fish on their date ofcapture.

The relative precision of age estimates between multiple read-ings by two readers was calculated using an index of the averagepercentage error (IAPE) for a subset of 360 otoliths (Beamish andFournier, 1981). All otoliths were read two times by the primaryauthor and those that did not agree on the number of annuli werere-read by a second reader. If the third reading did not agree thesample was removed from the analysis.

Separate age and length distributions were generated for recre-ational and commercial data from nearshore marine environmentin 2001 and commercial data from the nearshore marine environ-ment in 2002 and 2011.

2.3. Growth

Age structures from commercial and recreational catches in2001 were compared using the Kolmogorov–Smirnov 2-samplegoodness of fit test (SPSS 20).

Von Bertalanffy growth curves (VBGF) were fitted to the lengthsat age for male and female fish:

Lt = Linf (1 − exp−K[t−t0])

where Linf is the mean asymptotic maximum length predicted bythe equation, K is the growth coefficient and t0 is the hypotheticalage at which fish would have zero length if growth had followedthat predicted by the equation. The growth models were fitted tothe data by minimising the sums of squares using a non-linear curvefitting routine and confidence bounds for parameter estimateswere made using a bootstrap routine. Growth curves for males andfemales were compared using likelihood ratio tests (Haddon, 2001;Kimura, 1980).

For comparison, von Bertalanffy growth curves were recon-structed from published estimates of Linf, K and t0. Because Linf andK may be correlated, growth performance was compared amongpopulations using the growth index (ω) of Gallucci and Quinn(1979) where ω = K·Linf.

2.4. Reproduction

Monthly gonadosomatic indices (GSI’s, [(gonad weight)/(totalweight − gonad weight)] × 100 were prepared for sexually matureindividuals, >900 mm TL, from 2001. Size at maturity (SAM) wasestimated from males (stage III) and females (stages III, IV, andV) collected between November and March. Due to small samplesizes, samples from 2001 and 2002 were pooled and size classes of100 mm were used.

The size at which 50% and 95% of A. japonicus were maturewas estimated using a binomial generalised linear model (GLM,logistic regression) with a logit link function (R-3.02). The mod-els were fitted to the size-class mid-points with sample size asa weighting factor. Error around SAM50,95 was estimated using abootstrap procedure (percentile) with 10,000 iterations (95% con-fidence bounds). The logistic curve was plotted using the parametervalues for the logistic equation obtained from the GLM.

3. Results

3.1. Age and size

3.1.1. Validation of agesSectioned otoliths clearly showed annuli as opaque zones that

appeared lighter than the adjacent translucent zones. The first of



Fig. 2. Marginal increments and edge type of sagittal otoliths from captive spawnedArgyrosomus japonicus in first year of life. On the x-axis, black rectangles representsummer and winter months and white represents spring and autumn months.

these opaque zones were generally wider and less distinct thansubsequent zones but relatively easy to define. The IAPE value was4.9% suggesting a high level of reading precision. Opaque zonesof growth increments were formed in spring–summer in otolithsfrom captive and wild A. japonicus. Otoliths from captive spawnedfish showed that the first opaque edges appeared in July with onecomplete opaque zone and a clear edge present on all otolithsexcept one by October (Fig. 2). Additional otoliths from the samecohort (not shown in Fig. 2) revealed a complete third opaque bandin 20, 80 and 100% of otoliths, sampled at 34 (October 2003), 36(December 2003) and 37 months (January 2004) old, respectively.

Indirect validation of annuli formation from analysis ofmarginal increments in otoliths with one and two opaque zonesshowed that marginal increments increased from January toSeptember–October, then declined in November (Fig. 3). In otolithswith 3 and 4 opaque zones the marginal increment increased fromJanuary to September, then declined precipitously in October.

3.1.2. Age/size structuresFor A. japonicus from the Murray River estuary, ages from

research netting ranged from several months to 6 years whilst thosefrom commercial nets ranged from 2 to 6 years. In 2001, age dis-tributions from the nearshore marine environment adjacent to theMurray River mouth ranged from 4 to 25 years with 8 year oldsdominating the distribution (1993 year class, 35% of sample, Fig. 4).Secondary modes occurred at 11 (1990 year class, 8% of sample) and12 years (1989 year class, 4% of sample). In 2001, sizes ranged from650 to 1400 mm TL with modal sizes of 1100 and 1150 mm TL forcommercial net and recreational line catches, respectively.

For the commercial sample from 2002, ages ranged from 5 to 24years and the 1993 year class persisted as 9 year olds (41% of sample,Fig. 4) with a smaller mode of 12 year olds (1990 year class, 8% ofsample) also present. The size structure from 2002 ranged from 800to 1350 mm with a dominant mode at 1000 mm TL and a secondarymode at 900 mm TL.

For the age structure from 2011, ages ranged from 3 to 10 yearswith a dominant age class of 6 year olds. 314–319. The modal sizewas 850 mm TL with a range of 750–1380 mm TL, although only asingle individual attained this size and the next largest individualwas 1010 mm TL.

3.2. Growth

The asymptotic size (Linf) for A. japonicus was 1378 mm TL andgrowth rate (K) was 0.136 y−1 (Table 3 and Fig. 5). Growth dif-fered between females and males. For females, the asymptotic size

Fig. 3. Marginal increments (±1 SE) from sectioned sagittal otoliths of wild caughtArgyrosomus japonicus. On the x-axis, black rectangles represent summer and wintermonths and white represents spring and autumn months.

of 1430 mm TL was higher than that of 1356 mm TL for males(Kimura likelihood ratio test (KLR): Linf, p < 0.001). The growth rateof 0.137 y−1 for females was lower than the estimate of 0.159 y−1

for males (KLR: K, p < 0.001).

3.3. Reproduction

GSI’s for male and female A. japonicus increased from October toa peak in December and declined to February (Fig. 6A). Peak GSI forfemales occurred in November (n = 39) and was 1% of body weight.However, a wide range of GSI’s was observed (from <1 to 8%) withGSI’s above 7% observed in 15% of females.

Macroscopic examination of ovaries (Fig. 6B) showed that inOctober, November, and December, 23, 74 and 100% of femaleshad developed ovaries, respectively. In January 55% of ovaries wereyolked and 45% were recovering from spawning (stage V), with allovaries spent/recovering from March onwards. Months where >30%of ovaries had yolked oocytes were November to January. Maleswith running ripe (stage III) testes were present from October toMarch.

For males and females the youngest individual with developedgonads was 5 years old. Age at maturity (>50% mature) was 6 yearsfor females and 5 years for males although the age at which 100%of individuals had mature gonads was 8 and 9 years respectively.



Fig. 4. Distributions of age (panels on left) and length (panels on right) for Argyrosomus japonicus from the nearshore marine environment adjacent the mouth of the MurrayRiver. Age/size structures are for catches from recreational line fishers in 2000–2001, and from commercial net fishers in 2000–2001, 2001–2002 and 2011–2012.

Fig. 5. Von Bertalanffy growth function fitted to age-length data for female and maleArgyrosomus japonicus from eastern South Australia.

The size at 50% maturity (SAM50) was 850.3 mm TL (95% confi-dence bounds; CB: 804.8, 896.8, n = 211, p < 0.001) for females and778.2 mm TL (CB: 720.2, 824.1, n = 178, p < 0.001) for males (Fig. 7).The size at 95% maturity (SAM95) was 1027.7 for females (CB: 958.2,1075.0) and 923.2 for males (CB: 845.8, 969.5).

4. Discussion

Results from this study provide key life-history information foran exploited population of A. japonicus centred about the Mur-ray River estuary in eastern South Australia including the firstvalidated, otolith based estimates of age/growth and estimates ofsize/age at maturity. The life-history of A. japonicus is characterisedby large size/age at maturity and separate juvenile and adult phasesin estuarine and marine habitat respectively, which is similar to thatof several other sciaenids e.g. Argyrosomus regius, T. macdonaldi, andB. taipingenisis (Cisneros-Mata et al., 1995; Ferguson et al., 2008;Griffiths, 1996; Potts et al., 2010; Sadovy and Cheung, 2003).

4.1. Life-history and habitat use of A. japonicus

For the population of A. japonicus associated with the MurrayRiver estuary in eastern South Australia, early juveniles enter theestuary shortly after spawning which occurs in spring/summer inthe adjacent nearshore marine environment. Juveniles then utiliseestuarine habitat until they are 4–5 years old (Ferguson et al., 2008).

Table 3von Bertalanffy growth parameters for male (M) and female (F) and combined M, F and unknown (U) sex for Argyrosomus japonicus from South Australia. In brackets, 95%confidence bounds.

Sex Linf K t0 n

F 1430.52 (1353.53; 1507.51) 0.137 0.118; 0.156) −0.303 (−0.502 to −0.103) 209M 1356.23 (1275.42; 1437.04) 0.159 (0.143; 0.175) 0.000 (0.000; 0.000) 185M, F, U 1377.82 (1343.718; 1411.913) 0.136 (0.134; 0.157) −0.112 (−0.254; −0.031) 561



Fig. 6. For Argyrosomus japonicus from eastern South Australia: (A) monthly gonado-somatic indices for females and males and (B) monthly ovarian developmentalstages (numbers on bars are sample sizes). On the x-axis, black rectangles representsummer and winter months and white represents spring and autumn months.

The preference for estuarine habitat by juvenile A. japonicus is sup-ported by the presence of juveniles <20 mm TL in the estuary fromDecember onwards (Hall, 1986; Ye et al., 2013). Similar separa-tion of juvenile and adult habitats also occurs in populations ofA. japonicus in South Africa (Griffiths, 1996; Griffiths and Hecht,1995) but not in New South Wales where size structures from estu-arine and nearshore marine habitat are similar (Silberschneideret al., 2008). Griffiths (1996) suggested that estuaries provide pro-tection from con-specific predation which may also be the situationin the Murray River estuary because small juveniles (100–150 mmTL) have been found in the stomachs of sub-adults (Ferguson,unpublished data).

Whilst growth differed between female and maleA. japonicus in South Australia the general character of the growthcurves was similar with higher asymptotic sizes (Linf(f) = 1431 mmTL, Linf(m) = 1356 mm TL) and lower growth coefficients (females,Kf = 0.14 y−1; males, Km = 0.16 y−1) compared to those for West-ern Australia (Fig. 8). Whilst the growth curves for A. japonicusfrom Western Australia also differed between sexes, growth wascharacterised by lower asymptotic sizes (Linf(f) = 1213 mm TL,Linf(m) = 1173 mm TL) and higher growth coefficients (Kf =0.27 y−1,Km = 0.28 y−1) (Farmer, 2008). For combined sexes, the asymptoticsize for A. japonicus from South Africa (Linf(f,m) = 1483 mm TL) washigher than in South Australia (Linf(f,m) = 1377 mm TL) and thegrowth coefficient was lower (Kf,m = 0.17 y−1) (re-parameterisedgrowth curve of Griffiths and Hecht (1995) by Farmer (2003)).For A. japonicus from New South Wales the asymptotic size(Linf(f,m) = 1317 mm TL) was smaller than for South Australia andSouth Africa (Silberschneider and Gray, 2008; Farmer, 2008)

By expressing growth rate at t0, the growth performance index(ω) of Gallucci and Quinn (1979) allows for the correlation betweenthe von Bertalanffy parameters K and Linf so that growth rates maybe compared. Growth performance indices for A. japonicus in SouthAustralia (ωf = 196.05; ωf = 215.60; ωf,m = 187.27) were lower thanthose for Western Australia (ωf = 300.25; ωf = 332.36); New SouthWales (ωf,m = 259.45) and South Africa (ωf,m = 252.11).

The maximum age of A. japonicus in South Australia (41 years) issimilar to that of 42 years reported for this species in South Africa

Fig. 7. Size of maturity for (A) female and (B) male Argyrosomus japonicus fromeastern South Australia. Numbers at top of bars indicate sample size.

(Griffiths and Attwood, 2005; Griffiths and Hecht, 1995). Lowermaximum ages were recorded in New South Wales and WesternAustralia and were 24 and 32 years respectively (Farmer, 2008;Silberschneider et al., 2008). The low maximum age of A. japoni-cus in New South Wales may reflect high fishing effort althoughthis explanation is less likely in Western Australia where effortmay be lower (Farmer, 2008; Silberschneider and Gray, 2008;Silberschneider et al., 2008).

Despite the potential to reach a maximum age of 41 years inSouth Australia few individuals older than 16 years were observedin 2001 and 2002. It was hypothesised that the apparent trun-cation of age classes in 2001 and 2002 suggested that the populationmay have been depleted, presumably by a combination of habitatdegradation and over-fishing (Ferguson et al., 2008). The absence ofindividuals older than 10 years in 2011 suggests contraction of theage structure possibly due to continued fishing throughout a his-torically extreme drought from 2002 to 2010, combined with poorrecruitment during this period. It is notable that the dominant ageclasses of 8 and 9 year olds in the age structures from 2001 and2002 respectively, were absent in 2011.

Whilst selectivity of fishing gear may bias size distributions thisis less likely for the age distributions presented here because: (i) theage distributions from 2001 were consistent between samples from



Fig. 8. Comparison of Von Bertalanffy growth functions for Argyrosomus japonicus from South Australia (this study), New South Wales (Silberschneider et al., 2008), WesternAustralia (Farmer, 2008) and South Africa (Griffiths and Hecht, 1995; re-parameterised by Farmer, 2003).

recreational line and commercial net catches; (ii) age distributionsfrom commercial nets were consistent between 2001 and 2002;(iii) the age distribution from 2011 was collected at the same timeof year, using the same commercial nets, by the same fishers as in2001 and 2002; and (iv) because the size selectivity of large meshnets used in the nearshore marine environment is close to that ofasymptotic growth i.e. a wide range of ages may be sampled.

For species such as A. japonicus which have a life-history strat-egy (periodic strategists) characterised by high longevity andlate-maturity, long-tailed age structures likely evolved naturallyas protection against variable recruitment (Beamish et al., 2006;Francis et al., 2007; King and McFarlane, 2003). The population ofA. japonicus in eastern South Australia may be particularly vulnera-ble to the effects of age class truncation because of dependence onhighly variable estuarine habitat associated with the lower MurrayRiver (Ferguson et al., 2008; Longhurst, 2002).

Sexual maturity of female and male A. japonicus in SouthAustralia occurs at 6 and 5 years respectively, which is the sameas for the population in South Africa (Griffiths, 1996) and similarto that for the west coast of Western Australia (6–8 years, Farmer,2008). This contrasts with estimates of age at maturity for popu-lations on the south coast of Western Australia and New SouthWales which were 3–5, and 2–3 years, respectively although thesize ranges sampled in these studies were limited (Farmer, 2008;Silberschneider and Gray, 2008). The size at which 50% of indi-viduals were mature for female (SAM50, 850.3 mm TL) and male(778.2 mm TL) A. japonicus from eastern South Australia is smallerthan for populations in Western Australia (F, 903; M, 873 mm TL)and South Africa (F, 1070; M, 920 mm TL). Size at maturity forfemales in South Australia is 59% of Linf which is lower than forpopulations in Western Australia (77%) (Farmer, 2008) and SouthAfrica (73%) (Griffiths, 1996; Griffiths and Hecht, 1995) but higherthan in New South Wales (49%) (Silberschneider et al., 2008). Whilstmaturity occurs at a smaller size in the South Australian populationcompared to that in South Africa similarity in age of maturity sug-gests that age-specific and lifetime egg production may be lowerin South Australia. Relatively small samples (n < 10) in size classesfrom 700–900 mm TL may have resulted from (i) selectivity of thefishing gear and/or (ii) a possible movement of sub-adults at thetime of maturity. Whilst either factor may potentially affect thesizes of samples they were collected from a wide range of commer-cial net sizes and recreational line catches in both estuarine andnearshore marine habitats.

The spawning season for A. japonicus, in eastern South Australiaextends from October to January with a peak in November. Almostall individuals caught from aggregations adjacent the mouth ofMurray River during spring/summer in 2001 and 2002 were inadvanced stages of reproductive development or spent/recoveringsuggesting that these may be spawning aggregations. Previ-ous studies have also suggested that A. japonicus, aggregates in

spring–summer near the mouth of the Murray River to spawn(Ferguson et al., 2008) and similar seasonal spawning aggrega-tions in the nearshore marine environment have been reported forSouth Africa (Griffiths, 1996). Alternatively, the low mean GSI inNovember (∼1%) compared to South Africa and Western Australia(∼8%), relatively small number of samples (15%) with GSI’s of7–8%, and the absence of hydrated oocytes in any females col-lected could suggest that spawning occurs elsewhere. However,developed/regressing ovaries in females from these aggregationsand the presence of 0+ juveniles in catches from research nets inthe Coorong lagoons from December onwards in 2001 suggeststhat spawning occurs close to the Murray River Mouth duringspring–summer.

Populations of A. japonicus form spawning aggregations in SouthAfrica and South Australia (Griffiths, 1996; Ferguson et al., 2008).In eastern South Australia spawning and/or recruitment may bedependent on river flows and the formation of spawning aggrega-tions near the Murray River mouth during peak flow periods maysuggest the existence of a river-discharge spawning relationship.Such a relationship between spawning and environmental cuesmay be important in the life-history of populations of this speciesthat use protected juvenile habitat in estuaries. Release of eggs nearthe mouths of rivers may maximise the location by early juvenilesof protected habitat in estuaries. This may be critical for the pop-ulation of A. japonicus located about the Murray River estuary duethe apparent estuarine-dependence of juveniles (Ferguson et al.,2008). Low catches as well as anecdotal information from fisherssuggests that such aggregations have failed to form in recent years,apparently due to the lack of freshwater flows from 2002 to 2010when drought occurred.

4.2. Implications for management

More than 80% of the total commercial South Australian catchof A. japonicus consists of juveniles from the Murray River estu-ary where the modal size of catches (550 mm TL) is 40% of themaximum size (Linf, 1378 mm TL) and 65% of the female size atmaturity (SAM50, 850.3 mm TL). Consequently, this population islikely growth over-fished as has occurred in populations in NewSouth Wales and South Africa where the LML (450–550 mm TL) issimilar (Griffiths, 1997; Silberschneider et al., 2008).

Recruitment overfishing resulting from the combined effects oftargeting adults in spawning aggregations, targeting juveniles inestuaries, and discarding of sub-legal sized juveniles in estuarieshas been implicated in the decline of mulloway in New South Walesand South Africa (Griffiths, 1996, 1997; Silberschneider et al., 2008)as well as in populations of other sciaenid species (Rowell et al.,2008). The population of A. japonicus in eastern South Australia mayalso be vulnerable to recruitment overfishing due to the concur-rent targeting of juveniles in protected estuarine habitat and adults



in feeding/spawning aggregations in adjacent nearshore marinehabitat. While commercial catches from such aggregations are typ-ically ∼10% of the total annual commercial catch, the recreationalsector may harvest more than the commercial catch from estua-rine and marine habitat combined from these aggregations (Jones,2009; Jones and Doonan, 2005). Importantly recreational fishersmay release 71–86% of captured A. japonicus but the release mortal-ity is unknown (Jones, 2009; Jones and Doonan, 2005). The apparenttrend of increasing truncation of adult age structures and highinter-annual variability in relative abundance further suggest vul-nerability to recruitment overfishing (Ferguson et al., 2008; Hsiehet al., 2006).

The vulnerability of A. japonicus in eastern South Australia toboth growth and recruitment overfishing may be increased byhigh levels of mortality from discarding of sub-legal sized juve-niles (Ferguson, 2010), which is a common feature of estuarinefisheries (Ueno, 2001; Gray, 2002; Gray et al., 2004). High levels ofdiscarding of juveniles from trawling was implicated in the declineof the long-lived, late-maturing sciaenid T. macdonaldi (Cisneros-Mata et al., 1997). Similarly, discarding of sub-legal sized juvenilesfrom trawling in estuaries has contributed to recruitment overfish-ing of A. japonicus in New South Wales (Broadhurst and Kennelly,1994).

Results from this study indicate that legal minimum lengths forA. japonicus in South Australia should be ammended. The LML of460 mm TL for A. japonicus in the Murray River estuary is 54% ofSAM50 for females and 33.4% of Linf. The LML of 750 mm TL forA. japonicus in marine waters is set at approximately 88% of SAM50for females.

Slot limits may potentially mitigate the risk of overfishing ofjuvenile A. japonicus while reducing the loss of older, matureadults as has been used successfully for red drum S. ocellatus inthe Gulf of Mexico (Heppell et al., 2005) and has been suggestedfor the long-lived freshwater species Murray cod, Maccullochellapeelii in Australia (Hall et al., 2009; Heppell et al., 2005). Success-ful implementation of slot limits would require: (i) an improvedunderstanding of post-release mortality of A. japonicus caught fromspawning/feeding aggregations and (ii) evaluation of methods tomitigate such post-release mortality and (iii) extension of post-release mitigation methods to fishers via an education programme.

Closure to fishing of A. japonicus in the protected habitat ofthe Murray River estuary would protect juveniles, although thiscould also be achieved by increasing the size limit. Spring/summerclosures of spawning grounds adjacent the mouth of the Mur-ray River may provide protection for adult A. japonicus fromthe eastern population, particularly in years of high fresh-water outflow when feeding/spawning aggregations appear tobe greatest (Ferguson et al., 2008). Protection of spawningaggregations has been recommended for age-class truncatedpopulations of temperate reef-associated species (Berkeley et al.,2004) and has contributed to the successful recovery of thewhite seabass Atractoscion nobilis, off the Southern CaliforniaBight (Pondella and Allen, 2008; Sadovy de Mitcheson et al.,2008).

Ongoing assessment of populations of A. japonicus in SouthAustralia is important and could be achieved by interpreting agestructures within the context of life-history and stock structurewith appropriate sized samples determined from coefficient ofvariation of one or more age classes (Quinn and Deriso, 1999).Because the age structures presented in this study have beendepleted their use as baseline data for assessing population healthshould be treated with caution. Otoliths from indigenous mid-dens have the potential to provide baseline age structures thathave not been depleted by river regulation, drought and fish-ing (Disspain et al., 2011; Ferguson et al., 2008; Rowell et al.,2008).

5. Conclusion

There has been a poor management history for large sciaenidspecies and information on the life-history, demography, andreproductive biology of A. japonicus from this study is important forsustainable management (King and McFarlane, 2003; Potts et al.,2010). In eastern South Australia A. japonicus has been depletedby habitat loss associated with flow regulation and drought andestimates of growth rates and size at maturity combined withbaseline age structures will inform management of this vulnera-ble population. This population would benefit from managementmeasures that: (i) aim to preserve capacity for egg production;(ii) allow recruits to enter the adult population; and (iii) main-tain/rebuild long-tailed age structures. Results from this studyindicate that management measures associated with legal mini-mum size, protection of juveniles in estuaries, and protection ofspawning/feeding aggregations should be amended.

Acknowledgments

Funding and support for this study was provided by theDepartment of Primary Industries and Regions (Fisheries andAquaculture), South Australia, the South Australian Research andDevelopment Institute (Aquatic Sciences), and the University ofAdelaide. Commercial and recreational fishers, the Adelaide fishmarket and SARDI staff provided access to samples. Bruce Jack-son provided advice on preparation of otolith sections and ChrisIzzo kindly collated age/size data and provided a second reading ofotoliths. Paul Burch and Jonathan Carroll provided statistical advicewhich considerably improved the maturity estimate. Helpful com-ments on the manuscript were provided by Michael Steer, BronwynGillanders, and several anonymous reviewers.

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