ICES Journal of
Marine Science
ICES Journal of Marine Science (2015), 72(8), 2341– 2349. doi:10.1093/icesjms/fsv108
Original Article
Marked variations in reproductive characteristics of snapper
(Chrysophrys auratus, Sparidae) and their relationship
with temperature over a wide latitudinal range
Corey B. Wakefield 1 *, Ian C. Potter 2, Norman G. Hall 1,2, Rodney C. J. Lenanton 1, and Sybrand A. Hesp 1,2
1
Western Australian Fisheries and Marine Research Laboratories, Department of Fisheries, Government of Western Australia, PO Box 20, North Beach,
WA 6920, Australia
2
Centre for Fish and Fisheries Research, School of Veterinary and Life Sciences, Murdoch University, 90 South Street, Perth, WA 6150, Australia
*Corresponding author: tel: + 61 08 9203 0111; fax: + 61 08 9203 0199; e-mail: corey.wakefield@fish.wa.gov.au
Wakefield, C. B., Potter, I. C., Hall, N. G., Lenanton, R. C. J., and Hesp, S. A. Marked variations in reproductive characteristics of
snapper (Chrysophrys auratus, Sparidae) and their relationship with temperature over a wide latitudinal range. – ICES Journal
of Marine Science, 72: 2341 – 2349.
Received 13 January 2015; revised 14 May 2015; accepted 22 May 2015; advance access publication 16 June 2015.
The timing and duration of spawning and maturation schedules of Chrysophrys auratus were determined for populations in one subtropical
(258S on the upper west coast) and two temperate regions (328S on the lower west and 358S on the south coasts) over .2000 km of coastline along the west coast of Australia. This study thus encompassed the wide latitudinal range of this recreationally and commercially important
sparid in this region. The results were used, in conjunction with previously published data, to explore traditional paradigms regarding the relationships between the reproductive characteristics and variations in water temperature. Spawning at each latitude occurred mainly at 19– 218C, but
following a decline in temperature in the subtropical region and after a rise in temperature in the two temperate regions. Spawning on the upper
west coast thus occurred between mid-autumn and early spring (7 months) as opposed to late winter to early summer on the lower west coast
(6 months). Spawning on the south coast was mainly restricted to mid-spring to early summer (2 – 3 months) in 2003 and 2004 and did not
occur in 2005 when temperatures in this period were the coldest on record. Thus, marked interannual differences in the prevalence of mature fish on
the south coast probably reflect the “marginality” of the population. The length (L50) and age (A50) at which C. auratus matured increased markedly
from 25 to 328S. Studies such as this allow for latitudinal variations in reproductive characteristics to be incorporated into population models to
optimize fisheries sustainable yield, and contribute towards appropriate spatial scales for sustainable management strategies (e.g. minimum legal
lengths consistent with latitudinal variation in length-based maturity schedules). The narrow temperature range over which this species spawns
accounts for its current latitudinal distribution and enables predictions of how this distribution might alter with climate change. This study provides
relevant information for management and climate change implications for similar subtropical and temperate marine teleosts.
Keywords: fisheries management, global climate change, maturity, Pagrus, reproductive period, spawning omission, water temperature.
Introduction
In his classic review of reproduction in fish, Lam (1983) concluded
that, in temperate and subtropical species, gametogenesis is typically
stimulated by long or increasing photoperiod and/or high or rising
temperatures with those species that spawn in spring and summer,
whereas the reverse trend applies to species that spawn in autumn or
winter (de Vlaming, 1972; Bye, 1984; Lowerre-Barbieri et al., 2011).
Lam (1983) considered temperature to be more important in
# International
initiating spawning, which often requires a minimum temperature
and a pronounced change (de Vlaming, 1975; Lowerre-Barbieri
et al., 2011). The spawning of a species typically persists for longer
at lower latitudes, reflecting the presence of a more protracted
period over which temperatures are optimal for the spawning
of that species (Lam, 1983; Bye, 1990; Kokita, 2004; LowerreBarbieri et al., 2011). Furthermore, the length and age at maturity
of a species both tend to increase with latitude, recognizing that
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2342
these two reproductive variables are generally related to growth,
which, in turn, is typically related to temperature (Stearns and
Crandall, 1984; Abookire and Macewicz, 2003; Lek et al., 2012). In
an extension of the Metabolic Theory of Ecology (MTE, Brown
et al., 2004), Zuo et al. (2011) advise that, while an increase in the
age at maturity is expected with decreasing water temperatures,
the size at maturity will increase if the rate of reproductive development is more sensitive to temperature than the somatic growth rate,
otherwise the converse will occur.
The Sparidae is a diverse family occupying marine and estuarine
waters in tropical and temperate regions throughout the Atlantic,
Indian, and Pacific Oceans (Carpenter and Johnson, 2001;
Nelson, 2006). Sparids are noted for the plasticity of their biological
characteristics, which is reflected in their ability to adapt to a range
of environmental conditions (Atz, 1964; Buxton and Garratt, 1990;
Buxton, 1993; Sarre and Potter, 1999; Partridge et al., 2004). For
example, although the growth rates of the wild fish of Acanthopagrus
butcheri in two estuaries differed markedly, those of the juveniles
cultured from broodstocks from those estuaries and raised under
the same conditions, were essentially the same (Sarre and Potter,
2000; Partridge et al., 2004).
The snapper Chrysophrys auratus (Forster 1801), which can
attain total lengths (TLs) of 1300 mm, weights of 20 kg, and
live for up to 40 years (Gomon et al., 2008; Norriss and Crisafulli,
2010), is an iconic commercial and recreational fish species in
Australia and New Zealand. This sparid is typically a rudimentary
hermaphrodite (functional gonochorist) sensu Buxton and
Garratt (1990), whereby juveniles possessing gonads with both
ovarian and testicular tissue develop permanently into either
females or males before maturation (Francis and Pankhurst,
1988). Batch spawning occurs in aggregations, can occur on
consecutive days, and is strongly correlated with environmental
cycles (Scott et al., 1993; Wakefield, 2010). The results from published studies on the reproductive biology of different populations
of this species across its geographical range suggest that C. auratus
generally spawns at water temperatures ranging from 15 to 228C
(Crossland, 1977; Scott and Pankhurst, 1992; Jackson et al., 2010;
Wakefield, 2010), and exhibits marked variations in the timing
and duration of spawning between locations, i.e. autumn to spring
in northwestern Australia compared with spring and summer in
South Australia and New Zealand (Scott and Pankhurst, 1992;
Jackson et al., 2010; Saunders et al., 2012). However, the specific relationship between the annual timing and duration of spawning with
water temperatures over the wide latitudinal range of this species
has not been investigated. Furthermore, data on the lengths and
ages at which C. auratus reaches maturity at different locations
throughout its geographic range are limited and/or published in
reports (e.g. Crossland, 1981; Sumpton, 2002; Coutin et al., 2003;
Jackson, 2007; Stewart et al., 2010), and their correlation with
latitude and thus water temperature is poorly understood.
As C. auratus spawns along the extensive and continuous coastline of western Australia, from as far north as 23830′ S on the west
coast to 35800′ S on the south coast, it provides an excellent model
for exploring the extent to which paradigms, such as those of Lam
(1983) and extensions to the MTE (Brown et al., 2004; Zuo et al.,
2011), apply to the relationships between the reproductive characteristics of a species and latitude, and thus temperature. Data on
the reproductive characteristics of C. auratus have thus been collected from three widely separated regions along this coastline,
which represent both subtropical and temperate waters, to test the
following hypotheses regarding this sparid on the west coast of
C. B. Wakefield et al.
Australia. (i) Spawning in each region occurs over a similar
restricted range of water temperatures. (ii) As such temperatures
occur in late autumn to mid-spring in subtropical regions and in
spring and summer in temperate regions, spawning takes place
during these markedly different periods in these regions. (iii)
Consequently, gametogenesis occurs during declining photoperiod
and temperature in the subtropics and during rising photoperiod
and temperature in temperate waters. (iv) The persistence of
temperatures of 15 –228C for a greater duration in lower than
higher latitudes is reflected in a longer spawning period. The questions of whether the length and/or age at maturity of C. auartus are
related to latitude and thus temperature are also addressed. The data
obtained for the reproductive characteristics of C. auratus during
the present study have been collated with those for this sparid elsewhere to elucidate the extent to which they follow similar trends
across the geographical range of this species.
Methods
Sampling regime and environmental variables
Chrysophrys auratus was collected between 2002 and 2006 from the
upper west (23830′ –26830′ S), lower west (31800′ –33800′ S), and
south coast (34800′ – 35830′ S and 115830′ –125800′ E) regions on
the west coast of Australia (Figure 1). Most C. auratus were caught
using hook and line (93.6%), with a few smaller individuals
Figure 1. Map showing the locations of the three study regions in
Western Australia, i.e. upper west (excluding Shark Bay, black shade,
inset a), lower west and south coasts, and the main nearshore areas
sampled in each region (insets a, b, and c). Black crosses in insets a, b, and
c denote the location where water temperature was measured.
2343
Marked variations in reproductive characteristics of snapper
(juveniles) obtained by trawling in the upper and lower west coast
regions and traps in the lower west and south coast regions.
Mean monthly water temperatures in the upper west region
between 1998 and 2005 were derived from data recorded using a
data logger (Onset StowAway Tidbitw, Model No. TBI32-05+37)
suspended just above the substratum (depth of 12 m) of the
Uraine Bank on the eastern side of Dorre Island at 25816.84′ S and
113813.09′ E (Figure 1a). This logger was located close to two areas
where C. auratus is known to spawn. Water temperatures in the
lower west coast region were recorded monthly from 2001 to 2005
in Cockburn Sound at 32811.75′ S and 115843.35′ E, the main spawning location for C. auratus in that region (Figure 1b, Wakefield,
2010), using a conductivity meter with a built-in temperature
probe (WTW 315i conductivity meter with a WTW tetraconw325
conductivity cell). Water temperatures in the south coast region
were recorded using the same meter at approximately monthly
intervals from 1997 to 2002 in King George Sound at 35801.25′ S
and 117856.33′ E (Figure 1c), where C. auratus forms spawning
aggregations. The water temperatures for the corresponding calendar months in each region were pooled.
The TL and fork length (FL) of each fish were measured to the
nearest 1 mm. As TL is the length measurement used for management regulations in Western Australia and FL has often been used
elsewhere, the relationship between TL and FL was determined to
enable the results of different studies to be compared. When possible, the wet weight (WM) of each C. auratus from the lower west
and south coast regions was recorded to the nearest 0.1 g. An allometric relationship between FL and WM was derived by fitting a
linear function using least-squares to the log-transformed data for
the two more southerly regions. This equation, in combination
with the length –weight relationship, WM ¼ 0.0000741(FL2.788),
which had been estimated by Moran and Burton (1990) for
C. auratus from the upper west coast region, was used to estimate
the weights of C. auratus donated by fishers as frames (skeletons)
in these regions. The back-transformed estimates of body mass
were adjusted for the bias associated with the log transformation
(Quinn and Deriso, 1999). The relationships between weight (g)
and length (mm) of C. auratus did not differ significantly between
females and males in either the lower west or south coast regions,
or between the pooled data for both sexes in those regions (likelihood ratio test: all p . 0.05, n ¼ 966). The combined equation for
the weight–length relationship for both sexes in these two regions
was WM ¼ 0.00006439(FL2.8076). The ages of the C. auratus used in
this study were determined during a previous study (Wakefield,
2006).
The gonads of each fish were weighed (GW) to the nearest 0.01 g,
identified as either ovaries or testes and macroscopically allocated to
one of the following stages using the criteria in Wakefield et al.
(2011), i.e. stage I (immature/resting), stage II (developing), stage
III (developed), stage IV (ripe), and stage V (spent). Freshly dissected gonads were preserved in pH neutral 10% buffered formalin
for investigating histological characteristics for a subsample of specimens. Medial transverse sections of the preserved gonads were embedded in paraffin wax, sectioned at 5 mm, mounted on slides, and
stained with Mayer’s haematoxylin and eosin. The lengths, weights,
and ages of smaller juveniles in each region (n ¼ 122 upper west, 62
lower west, and 20 south coasts), whose sex could not be determined
macroscopically from their gonad morphology, were randomly
assigned, in equal numbers, to the female and male datasets. The
data for gonadal stages and gonadosomatic indices (GSI) of fish in
each corresponding calendar month in each of the three
geographical regions were pooled. The GSI of each fish ≥the L50
at maturity in each region was determined using the equation,
GSI ¼ (GW × 100)/(WM 2 GW), where GW and WM are wet
weight of the gonad and whole fish in g, respectively.
Maturity
The spawning period of C. auratus for each region was defined as
those months during which both females and males were found
with developed (stage III) and/or spawning (stage IV) gonads.
The lengths at which 50% of the females and males of C. auratus
attain sexual maturity (L50) during the spawning period in each
region were estimated using logistic regression analysis to determine
the relationships with length of the probability that a female or male
during the spawning period possesses gonads at stages II –V. During
the spawning period, fish with gonads of these stages would have
had the potential to spawn, were spawning, or had recently
spawned and were thus regarded as mature (see Results), whereas
fish with gonads at stage I were considered immature. The relationship used, i.e. PL = {1 + exp[−loge (19)(L − L50 )/(L95 − L50 )]}−1 ,
was a re-parameterized form of the logistic equation (e.g. Punt
and Kennedy, 1997; Hesp et al., 2004; Wakefield et al., 2007,
2010), where PL is the proportion of mature C. auratus at a particular length L, and the L50 and L95 are the estimated lengths at
which 50 and 95% of C. auratus attained sexual maturity, respectively. The L50s and L95s for the females and males in each region,
and their 95% confidence intervals, were determined by bootstrapping, where 2000 sets of estimates of the parameters of the
logistic equation were obtained from the analysis of data produced by random resampling, with replacement. The point estimates and 95% confidence limits of the proportions of mature
fish in each length class were calculated as the median, 2.5 and
97.5 percentiles, respectively, of the 2000 bootstrap estimates.
Estimates of the age at sexual maturity were calculated using the
same equation and approach, but with the ages at which 50 and
95% of individuals were mature, i.e. A50 and A95, substituted
for L50 and L95, respectively.
Results
On the upper west coast, stage II (developing) ovaries of C. auratus
were first recorded in February, stage III (developed) and IV (ripe) in
April, and stage V (spent) in May, with this last stage increasing
in prevalence until October and then not found in the following
6 months (Figure 2). Note that females with stage IV ovaries, characterized by containing hydrated oocytes, were present from April to
October. In contrast, on the lower west coast, female C. auratus with
stages II ovaries did not appear until July. Furthermore, the ovaries
of fish caught between October and January were predominately at
stages III and IV, and stage V (spent) ovaries were recorded only
from November to February. A few female C. auratus on the south
coast contained stage II ovaries between June and August and
those with stage III and IV ovaries were found between September
and December, and those with stage V ovaries were present from
November to March (Figure 2).
As females with stage III ovaries were found only in those months
when those with stage IV ovaries were present, the transition from
stage III to IV, and thus to the production of hydrated oocytes,
occurs within a month (Figure 2). Furthermore, depending on the
time of day and lunar phase, stage III ovaries sometimes contained
migratory nucleus oocytes and/or post-ovulatory follicles, implying that spawning was about to occur or had just taken place
2344
C. B. Wakefield et al.
Figure 3. Mean monthly GSIs +1 SE and percentage of females (left)
and males (right) of Chrysophrys auratus with developed (stage III,
white bars) or ripe (stage IV, grey bars) gonads for fish ≥L50 at maturity
in the upper west, lower west, and south coast regions. On the x-axis, the
closed rectangles represent winter and summer months and the open
rectangles autumn and spring months.
Figure 2. Percentage frequency of occurrence of the different stages of
ovarian development in samples of Chrysophrys auratus from the (a)
upper west, (b) lower west, and (c) south coasts of Western Australia.
Data are derived from fish ≥L50 at maturity in their respective regions.
Black bars represent ovaries containing hydrated oocytes (stage IV).
(Wakefield, 2010). Thus, the prevalence of females with stage III or
IV ovaries was used to estimate the spawning period.
On the upper west coast, the spawning period of C. auratus
extends from April to October, but with little spawning in the first
and last of these months. The mean monthly GSIs for females
increased sharply from 0.4 in April to 2.7 in June and then declined
to 0.5 in September, a trend paralleled by the GSIs of males (Figure 3).
The percentage of C. auratus with gonad stages III or IVexceeded 20%
in each month from May to September (Figure 3). In contrast, the
mean monthly GSIs of females and males on the lower west coast
did not start increasing until August and reached a broad peak in
October to December before declining precipitously in January
(Figure 3). The prevalence of female C. auratus with ovaries at
stage III or IV collectively exceeded 20% in each month from August
to January (Figure 3).
Although the mean monthly GSIs and percentages of females
and males with gonads at stage III or IV on the south coast peaked
at a similar time as on the lower west region, the maxima were far
less than those for either the upper west or lower west coasts
(Figure 3). Furthermore, females and males with either stage III or
IV gonads were found only in 4 months on the south coast, compared with 6 –8 months in the upper west and lower west coasts
(Figure 3). The extent to which the individuals of C. auratus on
the south coast became sexually mature varied markedly among
years (Figure 4). Thus, in both 2003 and 2004, females and males
with stage III or IV gonads were present in 3 or 4 months and comprised ≥60% of fish in at least 1 month, whereas the few such fish in
2005 were all caught in December (Figure 4).
Mean monthly water temperatures on the upper west coast
declined from 258C in April to 218C in June to October and
then rose sharply to 258C in February and March (Figure 5).
Although monthly water temperatures on the lower west and
south coasts followed similar trends, they were almost invariably
far lower than in the upper west coast. This difference was particularly pronounced during winter when, for example, in August, the
mean water temperatures of 168C on the lower west coast and
of 14.58C on the south coast were 5 and 6.58C, respectively, less
than on the upper west coast (Figure 5). Furthermore, maximum
mean monthly water temperatures of 248C on the lower west
coast and 228C on the south coast were 1 and 38C, respectively,
less than on the upper west coast (Figure 5). The ranges in mean
monthly water temperatures of 88C on the lower west coast and
7.58C on the south coast were far greater than the corresponding
range of 48C on the upper west coast.
2345
Marked variations in reproductive characteristics of snapper
Figure 4. Mean monthly GSIs +1 SE and percentage of females
(above) and males (below) of Chrysophrys auratus with developed
(stage III, white bars) or ripe (stage IV, grey bars) gonads for fish ≥L50 at
maturity in the south coast region between July 2003 and February
2006. On the x-axis, closed rectangles represent winter and summer
months and the open rectangles spring and autumn months.
Figure 5. Mean monthly water temperatures and percentage
(represented by the graduation of circles) of female Chrysophrys
auratus with developed and ripe (stages III and IV) gonads in the (i)
upper west (light grey circles), (ii) lower west (dark grey circles), and (iii)
south coast regions (2003 and 2004 only, black circles). Horizontal
dashed lines denote water temperatures of 19 and 218C. On the x-axis,
open rectangles represent autumn and spring months and closed
rectangles winter and summer months.
On the upper west coast, the prevalence of females with stage III
or IV ovaries increased markedly from only 6% in April to 58% in
May and 90% in June as mean monthly water temperatures declined
from 25 to 23 then 218C (Figure 5). The prevalence of females with
stage III or IV ovaries remained high in the next 3 months, when
mean monthly water temperatures remained at 218C, but then
declined to 4% in October, although water temperature was still
218C, and no females with stage III or IV ovaries were found in
the subsequent 5 months as temperatures rose.
In marked contrast to the situation in the upper west region, the
prevalence of fish with stage III or IVovaries in the other two regions
increased as water temperature rose. Thus, on the lower west coast,
such females first appeared in August, following a precipitous
decline in mean water temperature to their minima of 168C in
July and then rose progressively from 30% in August to 68% in
October and 95% in November as water temperatures increased
from 16 to 17.5 then 19.58C (Figure 5). The prevalence of females
with stage III or IV ovaries was still very high in December (93%)
when water temperature was 218C. Although sample sizes were
low in subsequent months as fish had undergone their typical seasonal emigration from their spawning grounds in Cockburn
Sound where sampling on the lower west coast was concentrated
(Wakefield et al., 2011), a mature female was caught in both
January and March. Females with stage III or IV ovaries were first
found on the south coast in September, when the mean water temperature was 15.68C and had thus started to rise from its winter
minimum of 14.68C. The prevalence of such females increased
from 7% in September to 21% at 16.58C in October and 48% at
198C in November and then declined to 8% at 218C in
December, after which no females with stage III or IV ovaries were
found during the following 8 months (Figure 5).
The mean monthly water temperatures when spawning activity
peaked, as reflected in a high prevalence of females with stage III
or IV ovaries, were similar in all three regions (Figure 5). Thus,
spawning in the upper west region peaked in June and July, when
mean monthly water temperature was 218C, and far later on the
lower west coast, i.e. in November and December, when mean
monthly water temperatures had risen to 20 –218C. Spawning on
the south coast peaked in November when the mean monthly water
temperature was 198C (Figure 5). Thus, the mean monthly water
temperatures during peak spawning activity in all three regions
along the large coast of Western Australia ranged only from 19 to
218C (Figure 5). However, considerable spawning activity did
occur in the upper west coast in the month before when these mean
monthly water temperatures were recorded, and in three months
prior and 1 month later on the lower west coast.
The minimum TL at which females reached maturity was far
lower on the upper west coast (270 mm) than lower west coast
(375 mm) and even more particularly the south coast (466 mm).
This regional trend was paralleled by the L50s, for which the corresponding values were 378, 585, and 600 mm, and by the A50s, for
which the corresponding values were 4.0, 5.7, and 7.0 years
(Table 1). The trends exhibited by the length and age at maturity
for the males in the three regions mirrored those for females, with
the L50 of 353 mm and A50 of 3.9 years for the upper west coast,
being substantially less than the values of 566 mm and 5.6 years
for the lower west coast and the 586 mm and 6.5 years for the
south coast (Table 1). It should be noted that small sample sizes of
C. auratus between 300 and 500 mm TL (Figure 6) and ages 4
for males and 5 for females from the south coast (Figure 7) may
be influencing the precision of estimates of the L50 and A50,
respectively.
Discussion
Studies investigating latitudinal variations in life history characteristics of demersal teleosts rarely encompass the broad latitudinal
range covered in this study. The plasticity expressed in reproductive
characteristics of demersal teleosts over such wide spatial scales
are likely to be species-specific and related to environmental variables, with greater variations exhibited in more highly variable
environments such as the temperate rather than tropical regions
(Choat et al., 2003; Caselle et al., 2011; Hamilton et al., 2011).
Understanding the extent of the plasticity exhibited in life history
characteristics of exploited teleosts across the extent of their latitudinal distribution, particularly those at higher latitudes, is an important consideration for population models, stock assessments,
2346
C. B. Wakefield et al.
Table 1. Total lengths (mm, TL) and ages (years, y) at which 50 and
95% (L50, L95, A50, and A95, respectively) of female and male
Chrysophrys auratus reach sexual maturity on the upper west, lower
west, and south coast regions, together with the minimum TL and
age of mature fish (Lmin and Amin) on those coasts.
Upper west
Female
Estimate
Upper
Lower
Male
Estimate
Upper
Lower
Lower west
Female
Estimate
Upper
Lower
Male
Estimate
Upper
Lower
South
Female
Estimate
Upper
Lower
Male
Estimate
Upper
Lower
L50
L95
Lmin
n
A50
A95
Amin
n
378
388
367
482
499
467
270
1010
4.0
4.2
3.7
6.0
6.5
5.5
3.2
406
353
366
340
484
504
465
257
938
3.9
4.1
3.6
6.2
6.9
5.6
3.1
418
585
602
567
752
784
720
375
708
5.7
5.9
5.5
8.0
8.6
7.5
2.8
588
566
583
546
730
756
691
407
661
5.6
5.8
5.3
8.5
9.1
8.0
2.9
561
600
635
562
899
987
809
466
168
7.0
8.1
5.9
15.5
26.6
11.8
3.8
172
586
618
550
839
909
780
369
6.5
7.2
5.8
11.5
13.4
10.0
3.1
172
175
and sustainable management strategies. Incorporating demographic variation into regional management regulations within the latitudinal distribution of a population can lead to better optimisation of
fisheries sustainable yield (e.g. Hamilton et al., 2011).
Spawning periodicity and relationship with water
temperature
On the west coast of Australia, the timing of recrudescence and duration of the spawning period for Chrysophrys auratus varied markedly between the subtropical and temperate regions. As a few females
of C. auratus with developing (stage II) ovaries appeared in February
and March in the upper west coast and were subsequently relatively
abundant until May, gonadal recrudescence in this region occurred
mainly when temperature and daylight hours were declining. These
trends are thus consistent with the generalities proposed by Lam
(1983) regarding the environmental factors that “trigger” gonadal
recrudescence for temperate species in subtropical waters.
In marked contrast to the situation in the subtropical waters,
C. auratus with gonads at stage II (developing) were first found in
the lower west in small numbers in July and then in greater
numbers in August. Thus, at this higher latitude, gonadal recrudescence commences when daylength and temperature are starting to
increase from their minima (i.e. 168C), which is also consistent
with the trends proposed by Lam (1983) for fish species in temperate
regions. Although data for the south coast are less comprehensive,
and there is evidence that C. auratus does not spawn every year on
this coast, the prevalence of fish with stage II gonads remains low
in this region until September.
Figure 6. Percentage frequency of female (left) and male (right)
Chrysophrys auratus with immature gonads (stage I, white bars) and
mature gonads (stages II– V, grey bars) in sequential 50 mm TL classes
from the upper west, lower west, and south coasts of Western Australia.
Logistic curves and their 95% confidence limits (dashed lines) were
derived from the probability that a fish of a given TL is mature. Samples
sizes for each TL class are shown above bars.
As females of C. auratus with developed (stage III) or ripe (stage
IV) ovaries were caught on the upper west coast between April and
October, this species spawns in this region during the 7 months
between mid-autumn and mid-spring. The prevalence of such
females was, however, very low in April and October and thus
spawning occurs mainly over 5 months on the upper west coast.
Spawning peaked in June and July and continued until October
during which period the mean monthly water temperature was
close to 218C, the minimum such value recorded for this region.
The trends exhibited by the mean monthly GSIs and abundance
of larvae around Moreton Island in Queensland demonstrate that
this sparid spawns at a comparable time of the year at a similar latitude on the east coast of Australia (Sumpton, 2002).
The presence of C. auratus with developed or ripe ovaries on the
lower west coast between August and March, and in relatively large
numbers in October to December, provides strong evidence that,
while spawning occurs between late winter and early autumn, it
peaked in mid-spring to early summer when water temperatures
were between 18 and 218C. Thus, these water temperatures
during peak spawning are close to the corresponding temperatures
when spawning peaked on the upper west coast. However, appreciable spawning also occurred on the lower west coast when the
mean monthly water temperatures had risen to 248C in January.
This timing, which is consistent with the trends exhibited by the
GSIs of both sexes, is similar to that of C. auratus in Spencer Gulf
in South Australia, at a slightly higher latitude (Saunders et al.,
2012).
2347
Marked variations in reproductive characteristics of snapper
temperate waters, parallels the differences between the spawning
periods of the populations sampled in Queensland at 278S and at
far higher latitudes in South Australia and Victoria (Sumpton,
2002; Coutin et al., 2003; Saunders et al., 2012). These trends also
parallel those for many other fish species elsewhere in the world
(e.g. Conover, 1992; Abookire and Macewicz, 2003; Kokita, 2004).
The concentration of the spawning of C. auratus, in three widely
separated regions, to months when mean monthly water temperatures ranged from 19 to 218C, and thus within only 28C, supports
the hypothesis that, irrespective of region, the spawning of this
species on the west coast of Australia is closely related to a relatively
narrow range in water temperature. This conclusion is broadly consistent with those drawn from studies on this species elsewhere
(Crossland, 1980; Foscarini, 1988; Pankhurst et al., 1991; Battaglene
and Talbot, 1992; McGlennon, 2004). However, substantial spawning
does occur at higher temperatures in the month before spawning
peaks on the upper west coast and in the months preceding and the
month after spawning peaks on the lower west coast.
Lengths and ages at maturity
Figure 7. Percentage frequency of female (left) and male (right)
Chrysophrys auratus with immature gonads (stage I, white bars) and
mature gonads (stages II – V, grey bars) in each age class from the upper
west, lower west, and south coasts of Western Australia. Logistic curves
and their 95% confidence limits (dashed lines) were derived from the
probability that a fish of a given age is mature. Samples sizes for each age
class are shown above bars.
The trends exhibited by the monthly values for the mean GSIs for
both sexes and prevalence of developed or ripe females on the south
coast of Western Australia demonstrated that, while spawning can
occur between September and December, it takes place mainly in
October and November. However, spawning can be very restricted,
or not occur, in some years, such as in 2005. The spawning period of
C. auratus on the south coast at 358S is slightly earlier than at the
higher latitude of 378S in New Zealand (Scott and Pankhurst,
1992) and of 388S in Victoria (Coutin et al., 2003). The mean
water temperature in the south coast region in November, the
only month in 2003 and 2004 in which the prevalence of developed
and ripe ovaries collectively exceeded 50%, was just over 198C
(Figure 5). Furthermore, temperatures during spring and summer
of 2005, when spawning on this coast may not even have occurred,
were the lowest for over 40 years (Bureau of Meteorology, 2005,
2006). In this context, it is thus also relevant that the durations of
the spawning periods of C. auratus in New Zealand and South
Australia were shortest in years when water temperatures were
lowest (Scott and Pankhurst, 1992; Fowler and Jennings, 2003).
The above comparisons for the data for the three populations
along the extensive west coast of Australia demonstrate that the
spawning period of C. auratus is most protracted at the lowest latitude (i.e. upper west, 7 months), and least protracted, or spawning
did not occur, at the highest latitude (i.e. south coast, 0 – 3 months),
with that at the intermediate latitude falling within this range (i.e.
lower west coast, 6 months). The decline in the duration of the
spawning period with increasing latitude, i.e. from subtropical to
The data produced during this study strongly support the hypothesis that the L50s and A50s of females and males of C. auratus at maturity increased markedly between the upper and lower west coast
regions and, to a lesser extent, also between the lower west and
south coast regions. Such latitudinal trends are not, however, universal for C. auratus throughout their geographical range. For
example, the L50 at maturity for females in Queensland (278S)
towards the northern end of the distribution of C. auratus is
274 mm TL (Sumpton, 2002) and thus similar to the corresponding
L50 of 290 mm TL in New South Wales (328S) and 250 mm
TL in New Zealand (378S), towards the middle and southernmost
part of its latitudinal distribution (Crossland, 1981; Stewart et al.,
2010). The increase in length at maturity with increasing latitude
by C. auratus on the west coast of Australia parallels the trend
recorded by Abookire and Macewicz (2003) for females of the
Dover sole Microstomus pacificus in the north Pacific over a
similar latitudinal range.
As expected, given the decrease in water temperatures with increasing latitude between the different regions, the age at maturity
of C. auratus increased with latitude (Zuo et al., 2011). The fact
that the length at maturity also increased with increasing latitude
suggests that, for this species, both the rate of reproductive development and the rate of somatic growth are sensitive to differences in
temperature (Zuo et al., 2011).
Management and climate change implications
The susceptibility of a species to overexploitation from fishing is
greatly increased when that species forms spawning aggregations
at a few predictable locations. Such is the case with stocks of
C. auratus throughout Australia and New Zealand. In Western
Australia, the fact that such aggregations were increasingly being targeted and estimates of fishing mortality appeared excessive led managers to conclude that action to reduce the level of exploitation was
necessary (see Wakefield, 2010). The data on reproduction of
C. auratus collected in this study proved invaluable to managers
in determining aspects of the regulations that subsequently were
introduced. For example, information on the seasonality and duration of spawning of this species and their relationship with water
temperature and latitude were considered when determining an appropriate period within the year for a fishing closure to protect
spawning aggregations of C. auratus in the nearshore marine
2348
embayments of Cockburn and Warnbro Sounds on the lower west
coast of Australia (see Wakefield, 2010). In addition, the data on the
lengths at which C. auratus mature obtained during this study led
to an increase in the minimum legal length from 410 to 500 mm TL
in the lower west coast region since 2008 (Department of Fisheries,
2010).
Given the strong correlations between spawning and water temperature, the distribution of mature C. auratus is constrained at both
higher and lower latitudes to waters where 19 –218C is regularly
experienced at some time during the year. Considering the spawning
of C. auratus peaks within a narrow water temperature range, it is
feasible that even minor increases in water temperature due to
global climate change, despite possibly being within the range of
temperatures tolerated by adults, may impose limits on spawning
and recruitment. Evidence of limitations on the annual spawning
of this species has been demonstrated in this study, where spawning
essentially did not occur in 2005 on the south coast of Western
Australia during the coolest spring–summer in over 40 years.
Furthermore, water temperatures along the lower west coast of
Western Australia have been increasing since the 1950s, particularly
during the austral autumn –winter (Pearce and Feng, 2007; Caputi
et al., 2009). It is therefore anticipated that, if water temperature
continues to increase along the west coast of Australia to the point
where winter temperatures exceed 19 –218C in the upper west
region, the latitudinal distribution of mature C. auratus in the
lower, subtropical latitudes could shift south. Predictions of potential range shifts in the distribution of mature C. auratus from climate
change, however, may also need to consider the habitat requirements associated with spawning and nursery (0+ aged juveniles)
areas (Nahas et al., 2003; Wakefield, 2010; Wakefield et al., 2011,
2013; Breheny et al., 2012). The detailed information provided in
this study on the relationships between marked variations in reproductive characteristics of a demersal teleost and temperature over a
wide latitudinal range provides a useful case for management and
climate change implications of similar species, across Australia
and subtropical and temperate oceans elsewhere.
Acknowledgements
Our thanks are extended to the commercial and recreational fishers,
fish processors, staff, and students from Murdoch University
and staff of the Department of Fisheries, Western Australia for
help with collecting Chrysophrys auratus. We also thank Martin
Holtz for constructive comments on an early version of this paper.
Financial support was provided by Murdoch University, Australian
Fisheries Research and Development Corporation (FRDC), and
Department of Fisheries, Government of Western Australia.
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