Life History of Argyrosomus Japonicus, a Large Sciaenid at the Southern Part

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Fisheries Research 151 (2014) 148–157

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Life history of Argyrosomus japonicus, a large sciaenid at the southern

part of its global distribution: Implications for ﬁsheries management

a,∗ a a b

Greg J. Ferguson , Tim M. Ward , Alex Ivey , Thomas Barnes

South Australian Research and Development Institute (Aquatic Sciences), PO Box 120, Henley Beach, South Australia 5024, Australia

School of Earth & Environmental Sciences, University of Adelaide, Adelaide, South Australia 5005, Australia

r t a b

i s

c l e i n f o t r a c t

Article history: The life-history of the sciaenid Argyrosomus japonicus in South Australia was investigated to inform a

Received 26 July 2013

review of ﬁsheries management. Validated, otolith-based growth coefﬁcients for females (Linf = 1430.52,

Received in revised form 5 November 2013

K = 0.137, t0 = −0.303, n = 209) and males (Linf = 1356.23, K = 0.159, t0 = 0.000, n = 185) suggested high

Accepted 7 November 2013

asymptotic 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

Keywords:

(SAM50,95) were 850 and 1028 mm TL, respectively for females and 778 and 923 mm TL, respectively for

Sciaenidae

males. Age structures from 2011 appeared truncated compared to those from 2001 and 2002 with no

Life-history

Age individuals greater than 10 years old. The dominant year class observed in age structures from 2001

Growth and 2002 was not present in 2011. This may reﬂect the combined effects of historically severe drought

Size at maturity from 2002 to 2010 and ﬁshing. This population is vulnerable to ﬁshing as juveniles in estuarine habitat

Fishery biology and as adults in spawning aggregations in marine habitat. Loss of protected estuarine habitat for juve-

Argyrosomus japonicus niles from ﬂow regulation and drought may make this population particularly vulnerable to overﬁshing.

Japanese meagre

Whilst maintenance of appropriately timed freshwater inﬂows to estuarine habitat is important for this

Mulloway Kob

population their availability is uncertain. Populations of A. japonicus in South Australia would beneﬁt

from management measures that: (i) aim to preserve capacity for egg production; (ii) allow recruits to

enter the adult population; and that (iii) rebuild and maintain long-tailed age structures. Amendments

to the legal minimum size and the protection of juveniles in estuaries and the adult spawning/feeding

aggregations are recommended.

1. Introduction Many large sciaenids have “periodic strategist” life histories

with characteristic high longevity and late maturity. Additionally,

Body size of ﬁshes is one of the most important factors in deter- many sciaenids form spawning aggregations in and near estuaries

mining vulnerability to ﬁshing (Jennings and Kaiser, 1998; Jennings and recruitment success of several species has been linked to fresh

et al., 1999; Reynolds et al., 2005). Large-bodied fishes are usu- water inflows into estuaries (Cisneros-Mata et al., 1995; Griffiths,

ally long-lived and their vulnerability is evident by their loss from 1996; Ferguson et al., 2008; Rowell et al., 2005, 2008). The evolu-

multi-species catches (Ferguson et al., 2013; Winemiller and Rose, tion of late maturity in sciaenids may have been facilitated by low

1992). The life-history of such large, long-lived ﬁshes is often based juvenile mortality in protected estuarine and surf zone habitats

on delayed maturity and high fecundity and has been termed ‘bet (Grifﬁths, 1996) and a possible “river-discharge” spawning rela-

hedging’ or periodic strategist (Winemiller and Rose, 1992) because tionship (Ferguson et al., 2008).

reproductive output is allocated across many years allowing popu- The delayed maturity of some sciaenid species may make them

lations to survive periods that are unfavourable for spawning and particularly vulnerable to overﬁshing (Musick, 1999; Musick et al.,

larval dispersal (Longhurst, 2002). For periodic strategists, recruit- 2000). Recruitment overﬁshing resulting from the combined effects

ment of newly mature individuals is low relative to the number and of targeting juveniles in estuaries and adults in spawning aggrega-

biomass of older adults with the exception of occasional very strong tions, referred to as the “one-two punch” approach (Rowell et al.,

year classes for those species with highly variable reproductive 2008), has been implicated in the declines of several sciaenid

success (Heppell et al., 2005). species worldwide. Sciaenid populations in serious decline include

ﬁve 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-

Corresponding author. Tel.: +61 8 8207 5467; fax: +61 88207 5481.

E-mail address: [email protected] (G.J. Ferguson). 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 decline Management of this ﬁshery assumes a single stock in South

of Sciaenops ocellatus and Totoaba macdonaldi in the Gulf of Mexico Australia however regional differences in the elemental chemistry

(Lercari and Chávez, 2007; Murphy and Crabtree, 2001) and Bahaba and morphology of otoliths suggest that separate populations occur

taipingensis and Larimichthyes crocea in China (Liu and Sadovy de along eastern and western coasts of South Australia (Ferguson et al.,

Mitcheson, 2008; Sadovy and Cheung, 2003). 2011). Management of A. japonicus comprises (i) a legal minimum

Fishery management depends on understanding the dynam- length (LML) of 460 mm TL in the Murray River estuary and 760 mm

ics of the variation in population abundance and determining the TL for all nearshore marine waters for commercial and recreational

impact of fishing on the natural population processes (Hilborn fishers, and (ii) bag and boat limits for recreational fishers.

and Walters, 1992). This information can be provided by val- This study provides validation of the ageing methodology for

idated, otolith-based age estimates (Campana, 2001; Campana A. japonicus in South Australia and seeks to improve understand-

and Thorrold, 2001). Consideration of life-history strategies is ing of the life history and demography by providing estimates of

also important because such strategies are linked to population growth rates and age/size at maturity to inform a review of ﬁshery

dynamics and environmental forcing (King and McFarlane, 2003). management. In addition, the possible impact of drought on this

Traditional stock assessment methods based on biomass may population is examined by comparing age structures from before

be inappropriate for species with late age at maturity and high and after recent, severe drought (2002–2010). Findings are dis-

longevity because of difﬁculties associated with estimating the cussed in the context of populations in other locations and used

instantaneous rate of ﬁshing mortality (Heppell et al., 2005). Conse- to identify options for improving the management of exploited

quently, age distribution and status of the adult stock may be critical populations of long-lived sciaenids.

for assessing population health of such species (Chale-Matsau et al.,

2001). 2. Materials and methods

The Japanese meagre, Argyrosomus japonicus (Temminck &

Schlegel, 1843), known as mulloway in Australia, is a large, preda- 2.1. Samples

tory sciaenid that is widely distributed in estuaries and nearshore

coastal waters (<100 m depth) of the Paciﬁc and Indian Oceans Biological samples from sub/adult and adult A. japonicus were

including sub-tropical and temperate waters in Australia (Grifﬁths collected from commercial gill net and recreational line catches

and Heemstra, 1995; Silberschneider et al., 2008). Like other sci- taken from spring/summer aggregations in the nearshore marine

aenids, A. japonicus has life-history characteristics that make it environment adjacent the Murray River in eastern South Australia

◦ ◦

vulnerable to anthropogenic impacts including estuarine asso- in 2001, 2002, and 2011 (139 22 40.34 E, 35 54 24.88 S).

ciation (Ferguson et al., 2008; Grifﬁths, 1996), high age/size at (Fig. 1, Table 1). Additional, information on size/age and reproduc-

maturity, and high maximum age (Farmer, 2008; Grifﬁths, 1996; tive development of juvenile A. japonicus (460–600 mm) within the

Grifﬁths and Hecht, 1995). Populations of A. japonicus have been Murray River estuary was collected from commercial net catches

reported as overﬁshed in South Africa and eastern Australia within the estuary. Information on sub-legal size ﬁsh (<460 mm

(Grifﬁths, 1997; Silberschneider et al., 2008). TL) within the estuary were obtained from a research programme

For the population of A. japonicus associated with the Mur- which used multi-panel gill (Table 1).

ray River estuary in eastern South Australia, temporal trends in For all samples, each ﬁsh was measured for total and standard

freshwater inﬂows, commercial catches, and population age struc- lengths (TL, SL, nearest mm) and where possible weighed to the

tures suggest estuarine dependence with a requirement for years nearest 100 g (to calculate GSIs). Gonads were dissected, weighed,

of high freshwater inﬂow in order to establish a strong year classes sexed and staged according to a published method (Hunter and

(Ferguson et al., 2008). It has been suggested that poor representa- Macewiecz, 1985) (Table 2). Brieﬂy, macroscopic staging of ovaries

tion of older individuals in age structures from feeding/spawning (n = 211) was to one of ﬁve developmental stages based on size,

aggregations in 2000 and 2001 may be due to a combination of colour and visibility of oocytes and was validated by microscopic

ﬂow regulation and ﬁshing with potential for compromised egg examination of histological preparations. For these ovaries (n = 27),

production (Ferguson et al., 2008, 2013). From 2002 to 2010, the a segment was removed from the centre of one lobe and preserved

most severe drought on historical record combined with excessive in a ﬁxative of formalin, acetic acid and calcium chloride (FAACC).

water abstraction, resulted in strongly reduced freshwater ﬂows Testes (n = 179) were classiﬁed into 3 stages (Table 2). Sagittae were

into the Murray River estuary (Lester and Fairweather, 2009). Addi- removed via a cut through the ventral ex-occipital region of the

tionally, the population of A. japonicus in eastern South Australia skull and were cleaned, dried, weighed and stored in labelled plastic

occurs at the southernmost part of the geographic distribution of bags.

◦

the species (∼35 S) where winter water temperatures are lower

◦

∼

( 14 C) than the optimum temperature for growth of juveniles 2.2. Age and size

◦

(25–26 C, Bernatzeder and Britz, 2007). Despite such concerns

there are no robust estimates of basic life-history parameters for 2.2.1. Laboratory preparation of otoliths

growth and reproduction available for A. japonicus in eastern South The left sagitta from each pair of otoliths was embedded in

Australia. polyester casting resin, and a 500 ␮m thick longitudinal section was

In South Australia, commercial ﬁshers target A. japonicus cut with a diamond blade mounted on a Gemmasta 6 (150 mm)

throughout their geographic range and they are considered an bench top saw. Serial sections were cut and the section incorporat-

“icon” species by recreational ﬁshers. Most commercial catches ing the otolith centre mounted on a glass microscope slide using

are from the population located around the Murray River where cyanoacrylate glue. Mounts were ground to improve visibility of

gill nets are used to target small A. japonicus in the estuary the opaque bands using silicon carbide polishing paper (grades

and larger individuals from spring/summer aggregations in the 1200 and 900) and were examined on a black background under

adjacent nearshore marine. Catches from the estuary comprise reﬂected light using a Leica MZ-16 dissecting microscope at 5–10×

approximately 80% of the annual commercial catch of A. japonicus magniﬁcation.

in South Australia (Ferguson et al., 2008). Recreational line ﬁshers

target large individuals from the austral spring–summer aggrega- 2.2.2. Validation of ageing method

tions with equivalent catches to those from the commercial sector Because identification of the first annulus is difficult in many

(Jones and Doonan, 2005; Jones, 2009). species, the pattern of deposition in otoliths was validated both

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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 including

the eastern coast, Murray River estuary and adjacent nearshore marine environment.

directly and indirectly. Direct validation of annuli was done from Fish (n = 10 ﬁsh per sample) were sampled at 34 months (October

monthly sampling of captive ﬁsh of known birth date. Indirect vali- 2002), 36 months (December 2002) and 37 months (January 2002).

dation was achieved by marginal increment analysis of wild caught Indirect validation of annulus formation was done by marginal

ﬁsh. increment analysis of monthly otolith samples from small juveniles

A. japonicus were spawned at SARDI Aquatic Sciences, Adelaide A. japonicus (1–2 opaque zones) caught in multi-panel research

from 10 to 18th December 2000. The juveniles were held in a gill nets and larger juveniles (3–4 opaque zones) from commercial

10,000 L tank with ﬂow-through seawater pumped from the nearby gill nets. Measurements of the marginal increment of longitudi-

Spencer Gulf and with water temperature and natural light reﬂect- nal sections of otoliths were made using digital imaging software

ing the normal seasonal cycle. The ﬁsh were fed once per day on (Image Pro 5.1 , Media Cybernetics). The marginal increment of

cockles (Donax deltoides, Bivalvia: Donacidae) at a rate of 5% of the each otolith was deﬁned as the distance between the outer edge of

total weight of live ﬁsh, and later on dry ﬁsh pellets at a rate of the single, or outermost opaque zone, and the edge of the otolith.

2% of total weight per day. Each month, for 12 months, 10–12 ﬁsh When only one opaque zone was present this was expressed as a

were sampled, and the otoliths removed. These otoliths, as well proportion of the distance between the primordium and the outer

as all other otoliths in subsequent laboratory processing, were sec- edge of the opaque zone. When two or more opaque zones were

tioned, mounted, and examined with a binocular microscope under present this was a proportion of the distance between the outer

reﬂected light. In addition to this, the third annulus was also val- edges of the two outermost opaque zones. Each measurement was

idated directly from samples from the same spawning. These ﬁsh made in the region of the cauda along an axis aligned with the pos-

were kept in sea cages at an aquaculture facility in Spencer Gulf. terior edge of the sulcus and perpendicular to the opaque zone(s)

Table 1

Sample 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 73

2001 Marine Recreational line Na 26 26

2002 Marine Commercial gillnet >150 63 78

2011 Marine Commercial gillnet >150 111 98

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

Table 2

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

Ovary stage Macroscopic appearance Microscopic appearance

I Small, clear to translucent, jelly-like thread, grey to pink in colour. Unyolked, non atretic oocytes only

Immature Close to posterior vertebral column.

Oocytes invisible to naked eye

II Small to medium, translucent to yellow/brown. Ovary lobe may Mainly unyolked, few partially yolked oocytes

Developing appear short, relative to stage III.

Oocytes invisible to naked eye.

III Large, yellow to orange. Granular appearance due to visible individual Dominated by advanced yolked oocytes, unyolked with

Developed oocytes. Ovary large, reaching forward into anterior gut cavity. partially yolked oocytes present in low numbers.

Lumen large and obvious.

IV Very large orange, reaching anteriorly to/above stomach. Clear Oocytes of all stages present from unyolked to hydrated.

Gravid or hydrated oocytes visible among opaque oocytes. Lumen large, obvious.

running ripe

V Ovaries medium in size, brown to reddish- brown, Opaque. Atretic oocytes present.

Regressing or More ﬂaccid than other stages. Partially yolked oocytes present.

resting Greater number of unyolked oocytes relative to yolked

than in stage III/IV ovaries.

Testes stage

I Appear as ﬁne, white to pink threads.

Immature

II Thickened thread, white/grey, no sperm or small amount of sperm

Developing when squeezed.

III Swollen, grey, running ripe.

Developed

without knowledge of the date of capture of the ﬁsh and recorded

where Linf is the mean asymptotic maximum length predicted by

to the nearest 0.01 mm. The values for marginal increments were

the equation, K is the growth coefﬁcient and t0 is the hypothetical

separated into groups according to the number of opaque zones in

age at which ﬁsh would have zero length if growth had followed

the otoliths. For otoliths with 1 and 2 opaque zones, samples were

that predicted by the equation. The growth models were ﬁtted to

pooled into corresponding months from 1 January 2001 to 31st

the data by minimising the sums of squares using a non-linear curve

December 2002. Otoliths with 3 and 4 opaque zones were similarly

ﬁtting routine and conﬁdence bounds for parameter estimates

pooled but included additional samples from 1 January 2003 to 31

were made using a bootstrap routine. Growth curves for males and

December 2003 to increase sample sizes.

females were compared using likelihood ratio tests (Haddon, 2001;

Kimura, 1980).

2.2.3. Reading otoliths For comparison, von Bertalanffy growth curves were recon-

Otoliths were examined under reﬂected light and ages esti- structed from published estimates of Linf, K and t0. Because Linf and

mated from counts of opaque zones. Opaque zones were counted in K may be correlated, growth performance was compared among

the region of the cauda along the posterior axis of the sulcus which populations using the growth index (ω) of Gallucci and Quinn

ω ·

has been reported as the best area for interpreting otoliths from (1979) where = K Linf.

A. japonicus (Farmer, 2008; Grifﬁths, 1996; Grifﬁths and Hecht,

1995). The mean birth date of 1st January was estimated from the

2.4. Reproduction

mid-point of the spawning season. This, in combination with the

time at which the annulus becomes delineated on the otolith, was

Monthly gonadosomatic indices (GSI’s, [(gonad weight)/(total

used to determine the age of the individual ﬁsh on their date of

weight − gonad weight)] × 100 were prepared for sexually mature

capture.

individuals, >900 mm TL, from 2001. Size at maturity (SAM) was

The relative precision of age estimates between multiple read-

estimated from males (stage III) and females (stages III, IV, and

ings by two readers was calculated using an index of the average

V) collected between November and March. Due to small sample

percentage error (IAPE) for a subset of 360 otoliths (Beamish and

sizes, samples from 2001 and 2002 were pooled and size classes of

Fournier, 1981). All otoliths were read two times by the primary

100 mm were used.

author and those that did not agree on the number of annuli were

The size at which 50% and 95% of A. japonicus were mature

re-read by a second reader. If the third reading did not agree the

was estimated using a binomial generalised linear model (GLM,

sample was removed from the analysis.

logistic regression) with a logit link function (R-3.02). The mod-

Separate age and length distributions were generated for recre-

els were ﬁtted to the size-class mid-points with sample size as

ational and commercial data from nearshore marine environment

a weighting factor. Error around SAM50,95 was estimated using a

in 2001 and commercial data from the nearshore marine environ-

bootstrap procedure (percentile) with 10,000 iterations (95% con-

ment in 2002 and 2011.

ﬁdence bounds). The logistic curve was plotted using the parameter

values for the logistic equation obtained from the GLM.

2.3. Growth

3. Results

Age structures from commercial and recreational catches in

2001 were compared using the Kolmogorov–Smirnov 2-sample

3.1. Age and size

goodness of ﬁt test (SPSS 20).

Von Bertalanffy growth curves (VBGF) were ﬁtted to the lengths

3.1.1. Validation of ages

at age for male and female ﬁsh:

Sectioned otoliths clearly showed annuli as opaque zones that −K t−t

[ 0]

Lt = L (1 − exp )

inf appeared lighter than the adjacent translucent zones. The ﬁrst of

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

Fig. 2. Marginal increments and edge type of sagittal otoliths from captive spawned

Argyrosomus japonicus in ﬁrst year of life. On the x-axis, black rectangles represent

summer and winter months and white represents spring and autumn months.

these opaque zones were generally wider and less distinct than

subsequent zones but relatively easy to deﬁne. The IAPE value was

4.9% suggesting a high level of reading precision. Opaque zones

of growth increments were formed in spring–summer in otoliths

from captive and wild A. japonicus. Otoliths from captive spawned

ﬁsh showed that the ﬁrst opaque edges appeared in July with one

complete opaque zone and a clear edge present on all otoliths

except one by October (Fig. 2). Additional otoliths from the same

cohort (not shown in Fig. 2) revealed a complete third opaque band

in 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 of

marginal increments in otoliths with one and two opaque zones

showed that marginal increments increased from January to

September–October, then declined in November (Fig. 3). In otoliths

with 3 and 4 opaque zones the marginal increment increased from

January to September, then declined precipitously in October.

Fig. 3. Marginal increments (±1 SE) from sectioned sagittal otoliths of wild caught

3.1.2. Age/size structures

Argyrosomus japonicus. On the x-axis, black rectangles represent summer and winter

For A. japonicus from the Murray River estuary, ages from

months and white represents spring and autumn months.

research netting ranged from several months to 6 years whilst those

from commercial nets ranged from 2 to 6 years. In 2001, age dis-

tributions from the nearshore marine environment adjacent to the of 1430 mm TL was higher than that of 1356 mm TL for males

Murray River mouth ranged from 4 to 25 years with 8 year olds (Kimura likelihood ratio test (KLR): Linf, p < 0.001). The growth rate

−1 −1

dominating the distribution (1993 year class, 35% of sample, Fig. 4). of 0.137 y for females was lower than the estimate of 0.159 y

Secondary modes occurred at 11 (1990 year class, 8% of sample) and for males (KLR: K, p < 0.001).

12 years (1989 year class, 4% of sample). In 2001, sizes ranged from

650 to 1400 mm TL with modal sizes of 1100 and 1150 mm TL for

3.3. Reproduction

commercial net and recreational line catches, respectively.

For the commercial sample from 2002, ages ranged from 5 to 24

GSI’s for male and female A. japonicus increased from October to

years and the 1993 year class persisted as 9 year olds (41% of sample,

a peak in December and declined to February (Fig. 6A). Peak GSI for

Fig. 4) with a smaller mode of 12 year olds (1990 year class, 8% of

females occurred in November (n = 39) and was 1% of body weight.

sample) also present. The size structure from 2002 ranged from 800

However, a wide range of GSI’s was observed (from <1 to 8%) with

to 1350 mm with a dominant mode at 1000 mm TL and a secondary

GSI’s above 7% observed in 15% of females.

mode at 900 mm TL.

Macroscopic examination of ovaries (Fig. 6B) showed that in

For the age structure from 2011, ages ranged from 3 to 10 years

October, November, and December, 23, 74 and 100% of females

with a dominant age class of 6 year olds. 314–319. The modal size

had developed ovaries, respectively. In January 55% of ovaries were

was 850 mm TL with a range of 750–1380 mm TL, although only a

yolked and 45% were recovering from spawning (stage V), with all

single individual attained this size and the next largest individual

ovaries spent/recovering from March onwards. Months where >30%

was 1010 mm TL.

of ovaries had yolked oocytes were November to January. Males

with running ripe (stage III) testes were present from October to

3.2. Growth March.

For males and females the youngest individual with developed

The asymptotic size (Linf) for A. japonicus was 1378 mm TL and gonads was 5 years old. Age at maturity (>50% mature) was 6 years

−1

growth rate (K) was 0.136 y (Table 3 and Fig. 5). Growth dif- for females and 5 years for males although the age at which 100%

fered between females and males. For females, the asymptotic size of individuals had mature gonads was 8 and 9 years respectively.

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G.J. Ferguson et al. / Fisheries Research 151 (2014) 148–157 153

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 Murray

River. 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.

4. Discussion

Results from this study provide key life-history information for

an exploited population of A. japonicus centred about the Mur-

ray River estuary in eastern South Australia including the ﬁrst

validated, otolith based estimates of age/growth and estimates of

size/age at maturity. The life-history of A. japonicus is characterised

by large size/age at maturity and separate juvenile and adult phases

in estuarine and marine habitat respectively, which is similar to that

of several other sciaenids e.g. Argyrosomus regius, T. macdonaldi, and

B. taipingenisis (Cisneros-Mata et al., 1995; Ferguson et al., 2008;

Grifﬁths, 1996; Potts et al., 2010; Sadovy and Cheung, 2003).

Fig. 5. Von Bertalanffy growth function ﬁtted to age-length data for female and male

Argyrosomus japonicus from eastern South Australia.

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

The size at 50% maturity (SAM50) was 850.3 mm TL (95% conﬁ- For the population of A. japonicus associated with the Murray

dence bounds; CB: 804.8, 896.8, n = 211, p < 0.001) for females and River estuary in eastern South Australia, early juveniles enter the

778.2 mm TL (CB: 720.2, 824.1, n = 178, p < 0.001) for males (Fig. 7). estuary shortly after spawning which occurs in spring/summer in

The size at 95% maturity (SAM95) was 1027.7 for females (CB: 958.2, the adjacent nearshore marine environment. Juveniles then utilise

1075.0) and 923.2 for males (CB: 845.8, 969.5). estuarine habitat until they are 4–5 years old (Ferguson et al., 2008).

Table 3

von 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) 209

M 1356.23 (1275.42; 1437.04) 0.159 (0.143; 0.175) 0.000 (0.000; 0.000) 185

M, F, U 1377.82 (1343.718; 1411.913) 0.136 (0.134; 0.157) −0.112 (−0.254; −0.031) 561

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

Fig. 6. For Argyrosomus japonicus from eastern South Australia: (A) monthly gonado-

somatic indices for females and males and (B) monthly ovarian developmental

stages (numbers on bars are sample sizes). On the x-axis, black rectangles represent

summer 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 from

December onwards (Hall, 1986; Ye et al., 2013). Similar separa-

tion of juvenile and adult habitats also occurs in populations of

A. 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 (Silberschneider

et al., 2008). Grifﬁths (1996) suggested that estuaries provide pro-

tection from con-speciﬁc predation which may also be the situation

in the Murray River estuary because small juveniles (100–150 mm

TL) have been found in the stomachs of sub-adults (Ferguson,

unpublished data).

Fig. 7. Size of maturity for (A) female and (B) male Argyrosomus japonicus from

Whilst growth differed between female and male eastern South Australia. Numbers at top of bars indicate sample size.

A. japonicus in South Australia the general character of the growth

curves was similar with higher asymptotic sizes (Linf(f) = 1431 mm

TL, Linf(m) = 1356 mm TL) and lower growth coefficients (females, (Griffiths and Attwood, 2005; Griffiths and Hecht, 1995). Lower

−1 −1

Kf = 0.14 y ; males, Km = 0.16 y ) compared to those for West- maximum ages were recorded in New South Wales and Western

ern Australia (Fig. 8). Whilst the growth curves for A. japonicus Australia and were 24 and 32 years respectively (Farmer, 2008;

from Western Australia also differed between sexes, growth was Silberschneider et al., 2008). The low maximum age of A. japoni-

characterised by lower asymptotic sizes (Linf(f) = 1213 mm TL, cus in New South Wales may reﬂect high ﬁshing effort although

−1

Linf(m) = 1173 mm TL) and higher growth coefﬁcients (Kf =0.27 y , this explanation is less likely in Western Australia where effort

−1

Km = 0.28 y ) (Farmer, 2008). For combined sexes, the asymptotic may be lower (Farmer, 2008; Silberschneider and Gray, 2008;

size for A. japonicus from South Africa (Linf(f,m) = 1483 mm TL) was Silberschneider et al., 2008).

higher than in South Australia (Linf(f,m) = 1377 mm TL) and the Despite the potential to reach a maximum age of 41 years in

−1

growth coefﬁcient was lower (Kf,m = 0.17 y ) (re-parameterised South Australia few individuals older than 16 years were observed

growth curve of Grifﬁths and Hecht (1995) by Farmer (2003)). in 2001 and 2002. It was hypothesised that the apparent trun-

For A. japonicus from New South Wales the asymptotic size cation of age classes in 2001 and 2002 suggested that the population

(Linf(f,m) = 1317 mm TL) was smaller than for South Australia and may have been depleted, presumably by a combination of habitat

South Africa (Silberschneider and Gray, 2008; Farmer, 2008) degradation and over-ﬁshing (Ferguson et al., 2008). The absence of

By expressing growth rate at t0, the growth performance index individuals older than 10 years in 2011 suggests contraction of the

( ) of Gallucci and Quinn (1979) allows for the correlation between age structure possibly due to continued ﬁshing throughout a his-

the von Bertalanffy parameters K and Linf so that growth rates may torically extreme drought from 2002 to 2010, combined with poor

be compared. Growth performance indices for A. japonicus in South recruitment during this period. It is notable that the dominant age

ω ω ω

Australia ( f = 196.05; f = 215.60; f,m = 187.27) were lower than classes of 8 and 9 year olds in the age structures from 2001 and

ω ω

those for Western Australia ( f = 300.25; f = 332.36); New South 2002 respectively, were absent in 2011.

ω ω

Wales ( f,m = 259.45) and South Africa ( f,m = 252.11). Whilst selectivity of ﬁshing gear may bias size distributions this

The maximum age of A. japonicus in South Australia (41 years) is is less likely for the age distributions presented here because: (i) the

similar to that of 42 years reported for this species in South Africa age distributions from 2001 were consistent between samples from

Author's personal copy

G.J. Ferguson et al. / Fisheries Research 151 (2014) 148–157 155

Fig. 8. Comparison of Von Bertalanffy growth functions for Argyrosomus japonicus from South Australia (this study), New South Wales (Silberschneider et al., 2008), Western

Australia (Farmer, 2008) and South Africa (Grifﬁths and Hecht, 1995; re-parameterised by Farmer, 2003).

recreational line and commercial net catches; (ii) age distributions spring–summer near the mouth of the Murray River to spawn

from commercial nets were consistent between 2001 and 2002; (Ferguson et al., 2008) and similar seasonal spawning aggrega-

(iii) the age distribution from 2011 was collected at the same time tions in the nearshore marine environment have been reported for

of year, using the same commercial nets, by the same ﬁshers as in South Africa (Grifﬁths, 1996). Alternatively, the low mean GSI in

2001 and 2002; and (iv) because the size selectivity of large mesh November (∼1%) compared to South Africa and Western Australia

∼

nets used in the nearshore marine environment is close to that of ( 8%), relatively small number of samples (15%) with GSI’s of

asymptotic growth i.e. a wide range of ages may be sampled. 7–8%, and the absence of hydrated oocytes in any females col-

For species such as A. japonicus which have a life-history strat- lected could suggest that spawning occurs elsewhere. However,

egy (periodic strategists) characterised by high longevity and developed/regressing ovaries in females from these aggregations

late-maturity, long-tailed age structures likely evolved naturally and the presence of 0+ juveniles in catches from research nets in

as protection against variable recruitment (Beamish et al., 2006; the Coorong lagoons from December onwards in 2001 suggests

Francis et al., 2007; King and McFarlane, 2003). The population of that spawning occurs close to the Murray River Mouth during

A. japonicus in eastern South Australia may be particularly vulnera- spring–summer.

ble to the effects of age class truncation because of dependence on Populations of A. japonicus form spawning aggregations in South

highly variable estuarine habitat associated with the lower Murray Africa and South Australia (Grifﬁths, 1996; Ferguson et al., 2008).

River (Ferguson et al., 2008; Longhurst, 2002). In eastern South Australia spawning and/or recruitment may be

Sexual maturity of female and male A. japonicus in South dependent on river ﬂows and the formation of spawning aggrega-

Australia occurs at 6 and 5 years respectively, which is the same tions near the Murray River mouth during peak ﬂow periods may

as for the population in South Africa (Grifﬁths, 1996) and similar suggest the existence of a river-discharge spawning relationship.

to that for the west coast of Western Australia (6–8 years, Farmer, Such a relationship between spawning and environmental cues

2008). This contrasts with estimates of age at maturity for popu- may be important in the life-history of populations of this species

lations on the south coast of Western Australia and New South that use protected juvenile habitat in estuaries. Release of eggs near

Wales which were 3–5, and 2–3 years, respectively although the the mouths of rivers may maximise the location by early juveniles

size ranges sampled in these studies were limited (Farmer, 2008; of protected habitat in estuaries. This may be critical for the pop-

Silberschneider and Gray, 2008). The size at which 50% of indi- ulation of A. japonicus located about the Murray River estuary due

viduals were mature for female (SAM50, 850.3 mm TL) and male the apparent estuarine-dependence of juveniles (Ferguson et al.,

(778.2 mm TL) A. japonicus from eastern South Australia is smaller 2008). Low catches as well as anecdotal information from ﬁshers

than for populations in Western Australia (F, 903; M, 873 mm TL) suggests that such aggregations have failed to form in recent years,

and South Africa (F, 1070; M, 920 mm TL). Size at maturity for apparently due to the lack of freshwater ﬂows from 2002 to 2010

females in South Australia is 59% of Linf which is lower than for when drought occurred.

populations in Western Australia (77%) (Farmer, 2008) and South

Africa (73%) (Grifﬁths, 1996; Grifﬁths and Hecht, 1995) but higher

4.2. Implications for management

than in New South Wales (49%) (Silberschneider et al., 2008). Whilst

maturity occurs at a smaller size in the South Australian population

More than 80% of the total commercial South Australian catch

compared to that in South Africa similarity in age of maturity sug-

of A. japonicus consists of juveniles from the Murray River estu-

gests that age-speciﬁc and lifetime egg production may be lower

ary where the modal size of catches (550 mm TL) is 40% of the

in South Australia. Relatively small samples (n < 10) in size classes

maximum size (Linf, 1378 mm TL) and 65% of the female size at

from 700–900 mm TL may have resulted from (i) selectivity of the

maturity (SAM50, 850.3 mm TL). Consequently, this population is

ﬁshing gear and/or (ii) a possible movement of sub-adults at the

likely growth over-ﬁshed as has occurred in populations in New

time of maturity. Whilst either factor may potentially affect the

South Wales and South Africa where the LML (450–550 mm TL) is

sizes of samples they were collected from a wide range of commer-

similar (Grifﬁths, 1997; Silberschneider et al., 2008).

cial net sizes and recreational line catches in both estuarine and

Recruitment overﬁshing resulting from the combined effects of

nearshore marine habitats.

targeting adults in spawning aggregations, targeting juveniles in

The spawning season for A. japonicus, in eastern South Australia

estuaries, and discarding of sub-legal sized juveniles in estuaries

extends from October to January with a peak in November. Almost

has been implicated in the decline of mulloway in New South Wales

all individuals caught from aggregations adjacent the mouth of

and South Africa (Grifﬁths, 1996, 1997; Silberschneider et al., 2008)

Murray River during spring/summer in 2001 and 2002 were in

as well as in populations of other sciaenid species (Rowell et al.,

advanced stages of reproductive development or spent/recovering

2008). The population of A. japonicus in eastern South Australia may

suggesting that these may be spawning aggregations. Previ-

also be vulnerable to recruitment overﬁshing due to the concur-

ous studies have also suggested that A. japonicus, aggregates in

rent targeting of juveniles in protected estuarine habitat and adults

Author's personal copy

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

in feeding/spawning aggregations in adjacent nearshore marine 5. Conclusion

habitat. While commercial catches from such aggregations are typ-

ically ∼10% of the total annual commercial catch, the recreational There has been a poor management history for large sciaenid

sector may harvest more than the commercial catch from estua- species and information on the life-history, demography, and

rine and marine habitat combined from these aggregations (Jones, reproductive biology of A. japonicus from this study is important for

2009; Jones and Doonan, 2005). Importantly recreational ﬁshers sustainable management (King and McFarlane, 2003; Potts et al.,

may release 71–86% of captured A. japonicus but the release mortal- 2010). In eastern South Australia A. japonicus has been depleted

ity is unknown (Jones, 2009; Jones and Doonan, 2005). The apparent by habitat loss associated with ﬂow regulation and drought and

trend of increasing truncation of adult age structures and high estimates of growth rates and size at maturity combined with

inter-annual variability in relative abundance further suggest vul- baseline age structures will inform management of this vulnera-

nerability to recruitment overﬁshing (Ferguson et al., 2008; Hsieh ble population. This population would beneﬁt from management

et al., 2006). measures that: (i) aim to preserve capacity for egg production;

The vulnerability of A. japonicus in eastern South Australia to (ii) allow recruits to enter the adult population; and (iii) main-

both growth and recruitment overﬁshing may be increased by tain/rebuild long-tailed age structures. Results from this study

high levels of mortality from discarding of sub-legal sized juve- indicate that management measures associated with legal mini-

niles (Ferguson, 2010), which is a common feature of estuarine mum size, protection of juveniles in estuaries, and protection of

ﬁsheries (Ueno, 2001; Gray, 2002; Gray et al., 2004). High levels of spawning/feeding aggregations should be amended.

discarding of juveniles from trawling was implicated in the decline

of the long-lived, late-maturing sciaenid T. macdonaldi (Cisneros-

Acknowledgments

Mata et al., 1997). Similarly, discarding of sub-legal sized juveniles

from trawling in estuaries has contributed to recruitment overﬁsh-

Funding and support for this study was provided by the

ing of A. japonicus in New South Wales (Broadhurst and Kennelly,

1994). Department of Primary Industries and Regions (Fisheries and

Aquaculture), South Australia, the South Australian Research and

Results from this study indicate that legal minimum lengths for

Development Institute (Aquatic Sciences), and the University of

A. japonicus in South Australia should be ammended. The LML of

Adelaide. Commercial and recreational ﬁshers, the Adelaide ﬁsh

460 mm TL for A. japonicus in the Murray River estuary is 54% of

market and SARDI staff provided access to samples. Bruce Jack-

SAM50 for females and 33.4% of Linf. The LML of 750 mm TL for

son provided advice on preparation of otolith sections and Chris

A. japonicus in marine waters is set at approximately 88% of SAM50

Izzo kindly collated age/size data and provided a second reading of

for females.

otoliths. Paul Burch and Jonathan Carroll provided statistical advice

Slot limits may potentially mitigate the risk of overﬁshing of

which considerably improved the maturity estimate. Helpful com-

juvenile A. japonicus while reducing the loss of older, mature

ments on the manuscript were provided by Michael Steer, Bronwyn

adults as has been used successfully for red drum S. ocellatus in

Gillanders, and several anonymous reviewers.

the Gulf of Mexico (Heppell et al., 2005) and has been suggested

for the long-lived freshwater species Murray cod, Maccullochella

peelii in Australia (Hall et al., 2009; Heppell et al., 2005). Success- References

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