alan cottingham bsc (hons) this thesis is presented for the degree of doctor … · 2015-11-25 ·...
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Biological characteristics of Acanthopagrus butcheri. Changes following
environmental degradation and comparisons of restocked and wild fish.
Alan Cottingham BSc (Hons)
This thesis is presented for the degree of Doctor of Philosophy
2015
Murdoch University, Western Australia
ii
Declaration
I declare that this thesis is my own account of my research and contains, as its main
content, work which has not previously been submitted for a degree at any tertiary
education institution.
Alan Cottingham
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It is not the strongest of the species that survive, nor the most intelligent, but rather
the one most adaptable to change. Clarence Darrow 1925.
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The subject of this thesis, the Black Bream Acanthopagrus butcheri.
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Abstract
The Black Bream Acanthopagrus butcheri, which is the subject of this thesis, completes its
life cycle within estuaries and has particularly plastic biological characteristics. The
overarching aims of the thesis were 1) to determine the ways in which A. butcheri has
responded to marked environmental changes in the Swan River Estuary and 2) to track the
biological performance of restocked A. butcheri in the Blackwood River Estuary in which
the stock of this species had become depleted.
Between the early 1990s and mid-2000s, the deeper waters of the upper Swan River
Estuary became increasingly hypoxic, due to a reduction in the flushing of nutrients and
organic material from the estuary as a result of declining rainfall and thus freshwater
discharge. Over that same time period, the condition, growth and length at maturity of
female and male A. butcheri declined and the age at maturity increased. Furthermore, catch
data implied that, during that period, the larger A. butcheri showed a marked tendency to
move from the deeper hypoxic waters into the shallows, occupied by smaller A. butcheri.
This habitat compression led to greatly increased densities in the shallows. It is therefore
proposed that the detrimental effects of hypoxia and high densities led to the above
retrograde changes in the biological characteristics of A. butcheri.
The development of a year-effect growth model demonstrated that the growth of
A. butcheri in the Swan River Estuary also differed substantially among years between
2007/08 and 2013/14. Annual growth of one year old A. butcheri in those seven years were
positively correlated with temperature during the main growing period, but not with
freshwater discharges in the preceding wet ‘winter’ months. That positive correlation with
temperature, which is consistent with the metabolic theory of ecology, contrasts with the
decline in growth between the early 1990s and mid-2000s, when temperatures were
increasing. This implies that the influence of temperature on growth between those two
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periods was overridden by other factors, i.e. hypoxia and increased densities, but then, in
2007-14, became the most important factor, when fish became concentrated in relatively
similar densities in nearshore waters. Although there was no evidence that the overall
abundance of A. butcheri in the Swan River Estuary had changed markedly between the
early 1990s and early 2010s, there is circumstantial evidence that the stock of this species
declined during the 1980s and 1990s in the Blackwood River Estuary, due to fishing
pressure and/or environmental changes.
Concern for the status of the stock of A. butcheri in the Blackwood River Estuary
led to a study aimed at determining the efficacy of using restocking to replenish the
population of this species in this system. The growth and maturity schedules of the 2001
and 2002 year classes of A. butcheri, which had been cultured and introduced into the
Blackwood River in south-western Australia at seven and four months old, respectively,
were determined from samples collected regularly between 2002 and 2014. Restocked A.
butcheri could always be distinguished from its wild stock because their otoliths retained
the pink coloration of the alizarin complexone with which they had been stained prior to
release. The growth and maturity schedules of restocked fish were only slightly inferior to
those of its wild stock and the mean gonad weights of these two groups did not differ
significantly in any month. As increasing numbers of restocked A. butcheri attained the
minimum legal length (MLL) of 250 mm for retention, their contribution to the
commercial fishery increased from 6% in 2005 to 74% in 2010. That contribution
subsequently declined to 39% in 2012 and 10% in 2014, due predominantly to the
introduction of the very strong 2008 year class in the commercial catches, the first
substantial recruitment into the population since 1999. As restocked fish were estimated as
contributing ~55% to the eggs produced in 2008, substantial numbers of the 2008 year
class were derived from spawning by restocked fish. The results of this and a previous
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genetic study imply that restocking is an effective and appropriate way for replenishing
stocks of an estuarine species such as A. butcheri, especially as its recruitment is highly
episodic.
Protection of riverine discharge into the estuaries of south-western Australia is
likely to be the most effective management strategy to maintain the ‘health’ of estuaries
and their fisheries. It follows that a thorough understanding of the hydrology of estuaries
will become increasingly important to managing these systems as they become subjected
further to the effects of climate change and increases in the demand for water resources by
human populations. As A. butcheri completes its life cycle within its natal estuary and has
plastic biological characteristics, it is an ideal candidate for use as an indicator of the health
of an estuary and hypothesising on the effects of climate change.
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Acknowledgements
I would first and foremost like to thank Emeritus Ian Potter for supervising my research.
His endless dedication, advice and encouragement not only facilitated the completion of
this thesis but will continue to inspire me throughout my scientific career. My gratitude is
expressed to Professor Norm Hall for his supervision, in particular, his essential advice for
the statistical and modelling component of this thesis. I would also like to acknowledge Dr
Alex Hesp for his supervision and assistance. My gratitude is also expressed to Chris
Hallett and Amanda Buckland for the many days of assistance in the field and to Gavin
Sarre, Steeg Hoeksema, Kim Smith, Michelle Gardner, Joel Williams, Eloise Ashworth
and Daniel Yeoh for providing data and to Greg Jenkins and Trevor Price who made the
studies on restocking possible. I also thank other members of the Centre for Fish and
Fisheries for their input, James Tweedley, Fiona Valesini, Thea Linke, Calais Tink, Lauren
Veale, Ben French and Elaine Lek.
Financial and other support was provided by Ian Stagles of the West Australian Fish
Foundation, Recfishwest, Murdoch University, Western Australia Department of Fisheries,
Swan River Trust and Department of Water.
Above all else, I would like to thank my mum Marion Cottingham and my gorgeous fiancé
Tek Green for their support throughout the duration of my PhD.
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Publications
Papers published from work undertaken in this thesis.
The following paper was published from Chapter 3 of this thesis.
Cottingham, A., Hesp, A, Hall, N.G., Hipsey, M. and Potter, I.C., 2014. Marked
deleterious changes in the condition, growth and maturity schedules of
Acanthopagrus butcheri (Sparidae) in an estuary reflect environmental degradation.
Estuarine, Coastal and Shelf Science 149, 109-119.
The following paper has been based on Chapter 4 of this thesis.
Cottingham, A., Hall, N.G., Potter, I.C., 2016. Factors influencing the growth of
Acanthopagrus butcheri (Sparidae) in a eutrophic estuary have changed over time.
Estuarine, Coastal and Shelf Science. 168, 1-11.
The following papers were published from Chapter 5 of this thesis, with the first of these
papers having biological and genetic components, of which I was responsible for the
former.
Gardner, M.J., Cottingham, A., Hesp, S.A., Chaplin, J.A., Jenkins, G.I., Phillips, N.M.,
Potter, I.C., 2013. Biological and genetic characteristics of restocked and wild
Acanthopagrus butcheri (Sparidae) in a south-western Australian estuary. Reviews in
Fisheries Science 21, 441-452.
Cottingham, A., Hall, N.G., Potter, I.C., 2015. Performance and contribution to
commercial catches and egg production by restocked Acanthopagrus butcheri
(Sparidae) in an estuary. Estuarine, Coastal and Shelf Science 164, 194-203.
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Reports published from work undertaken in this thesis.
Williams, J., Cottingham, A., Potter, I.C., 2014. Spatial and temporal distributions of
spawning by Black Bream (Acanthopagrus butcheri) in the Blackwood River
Estuary. Report to West Australian Fish Foundation.
Cottingham, A., Potter, I.C., 2014. Continuation of the monitoring of restocked and wild
Black Bream Acanthopagrus butcheri in commercial catches in the Blackwood River
Estuary. Report to West Australian Fish Foundation.
Cottingham, A., Buckland, A., Potter, I.C., 2013. Results and implications of monitoring
the biological characteristics of restocked and wild Black Bream, Acanthopagrus
butcheri, in the Blackwood River Estuary. Report to West Australian Fish
Foundation.
Gardner, M.J., Cottingham, A., Phillips, N.M., Hesp, S.A., Chaplin, J.A., Jenkins, G.I.,
2010. Biological performance and genetics of restocked and wild bream in the
Blackwood River Estuary. Report to the West Australian Fish Foundation.
Valesini, F.J., Hallett, C.S., Cottingham, A., Hesp, S.A., Hoeksema, S.D., Hall, N.G.,
Linke, T.E., Buckland, A.J., 2010. Development of biotic indices for establishing and
monitoring ecosystem health of the Swan-Canning Estuary. Report to the Swan
River Trust.
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Table of contents
Abstract ................................................................................................................................. 1
Acknowledgements .............................................................................................................. 4
Publications .......................................................................................................................... 5
Chapter 1 ............................................................................................................................ 10
General introduction ......................................................................................................... 10
1.1 Definition of an estuary ........................................................................................... 10
1.2 Productivity and food webs in estuaries ................................................................ 11
1.3 Classification of the ways fish use estuaries; the guild approach ........................ 12
1.4 Anthropogenic impacts on estuaries ...................................................................... 16
1.5 General characteristics of macro- and microtidal estuaries ................................ 18
1.6 Estuaries of south-western Australia ..................................................................... 19
1.7 Acanthopagrus butcheri ........................................................................................... 24
1.8 Objectives of thesis ................................................................................................... 27
Chapter 2 ............................................................................................................................ 28
General material and methods ......................................................................................... 28
2.1 Sampling methods .................................................................................................... 28
2.2 Sampling regime ...................................................................................................... 28
2.3 Laboratory procedures and measurements .......................................................... 31
2.3.1 Ageing ................................................................................................................. 31
2.3.2 Growth ................................................................................................................ 34
2.3.3 Length and age at maturity ................................................................................. 35
Chapter 3 ............................................................................................................................ 37
Marked deleterious changes in the condition, growth and maturity schedules of
Acanthopagrus butcheri in the Swan River Estuary reflect environmental degradation
............................................................................................................................................. 37
3.1 Introduction .............................................................................................................. 37
3.2 Materials and Methods ............................................................................................ 41
3.2.1 Description of the Swan River Estuary ............................................................... 41
3.2.2. Physico-chemical data and sampling regimes ................................................... 43
3.2.3 Assessment of body condition ........................................................................... 45
3.2.4 Growth and reproductive biology ....................................................................... 47
3.2.5 Measures of relative abundance .......................................................................... 47
3.3 Results ....................................................................................................................... 48
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3.3.1 Decline in freshwater discharge and relationship with hypoxia ........................ 48
3.3.2 Body condition and growth ................................................................................ 50
3.3.3. Lengths and ages at maturity ............................................................................. 54
3.3.4 Catch rates in deeper waters and densities in shallow water .............................. 58
3.4 Discussion .................................................................................................................. 59
3.4.1 Condition and growth....................................................................................... 60
3.4.2. Length and age at maturity................................................................................. 62
Chapter 4 ............................................................................................................................ 65
Factors influencing the growth of Acanthopagrus butcheri in a eutrophic estuary have
changed over time. ............................................................................................................. 65
4.1 Introduction .............................................................................................................. 65
4.2 Materials and methods ............................................................................................ 67
4.2.1 Temperature and freshwater flow ....................................................................... 67
4.2.2. Sampling regime and processing of fish ............................................................ 68
4.2.3 Year-effect growth model ................................................................................... 70
4.2.4 Relationship between growth and temperature and freshwater discharge ......... 74
4.3 RESULTS ................................................................................................................. 74
4.3.1 Temperature and freshwater discharge ............................................................... 74
4.3.2 Model parameter selection and simulation ......................................................... 75
4.3.3 Model results ....................................................................................................... 78
4.3.4 Relationship between growth and temperature and freshwater discharge .......... 83
4.4 DISCUSSION .......................................................................................................... 84
Chapter 5 ............................................................................................................................ 89
Performance and contribution to commercial catches and egg production by
restocked Acanthopagrus butcheri in the Blackwood River Estuary. ........................... 89
5.1 Introduction .............................................................................................................. 89
5.2 Materials and Methods ............................................................................................ 92
5.2.1 Collection of restocked and wild Acanthopagrus butcheri ................................. 92
5.2.2 Ageing and growth .............................................................................................. 95
5.2.3 Reproduction and fecundity ................................................................................ 96
5.3 RESULTS ................................................................................................................. 99
5.3.1 Growth .............................................................................................................. 100
5.3.2 Maturation ......................................................................................................... 102
5.3.3 Contribution of restocked fish to commercial catches ...................................... 107
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5.3.4 Egg production .................................................................................................. 110
5.4 DISCUSSION ......................................................................................................... 111
5.4.1 Survival and growth of restocked fish .............................................................. 111
5.4.2. Comparisons of the performance of restocked and wild fish .......................... 111
5.4.3 Contributions of restocked and wild fish to commercial gill net catches ......... 113
Chapter 6 .......................................................................................................................... 116
General Discussion ........................................................................................................... 116
6.1 Swan River Estuary ............................................................................................... 116
6.1.1 Influence of hypoxia ......................................................................................... 116
6.1.2 Influence of temperature ................................................................................... 118
6.1.3 Recruitment ....................................................................................................... 120
6.1.4 Management ...................................................................................................... 123
6.2 Blackwood River Estuary ..................................................................................... 123
6.3 Conclusions ............................................................................................................. 127
REFERENCES ................................................................................................................. 130
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Chapter 1
General introduction
1.1 Definition of an estuary
Estuaries are among the most productive of all aquatic ecosystems (Schelske & Odum,
1962: Kennish, 2003; Hoellein et al., 2013) and thus provide valuable nursery areas for
many commercially and recreationally important fish species (Lenanton & Potter, 1987;
Able & Fahay, 2010; Potter et al., 2013). Estuaries are also complex, with each being
influenced by a suite of biophysical processes, whose combinations differ and, as a
consequence, the environmental characteristics of these systems vary markedly (Monbet,
1992; Tagliapietra et al., 2009; Potter et al., 2010). This explains why early attempts to
produce a description of estuaries that applies to all of these systems throughout the world
were not entirely successful.
The following definition of Pritchard (1967) is widely quoted. “An estuary is a
semi-enclosed coastal body of water, which has a free connection with the open sea and
within which seawater is measurably diluted with fresh water derived from land drainage”.
This definition accommodates the macrotidal estuaries of the northern hemisphere, where
large tidal forcing and strong freshwater flow maintains “a free connection with the open
sea”. However, as Day (1980) pointed out, many estuaries in temperate regions of the
southern hemisphere, such as those in southern Africa and southern Australia, can become
periodically isolated from the ocean through the formation of a bar at their mouths, and
some estuaries in this region can become hypersaline during the warm, dry months when
evaporation rates are high. The definition of Day (1980), which took into account those
characteristics, has recently been refined by Potter et al. (2010) as follows. “An estuary is a
partially enclosed coastal body of water that is either permanently or periodically open to
the sea and which receives at least periodic discharge from a river(s), and thus, while its
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salinity is typically less than that of seawater and varies temporally and along its length, it
can become hypersaline in regions when evaporative water loss is high and freshwater and
tidal inputs are negligible”.
1.2 Productivity and food webs in estuaries
Estuaries contain large amounts of organic carbon, derived from runoff of biogenic
material, and nutrients from the surrounding land (Hopkinson et al., 2005), which fuel the
food chain in these systems (Canuel et al., 1995; McLusky & Elliott, 2004). The organic
carbon is derived from three main sources. Allochthonous sources comprise mainly plant
material that enters the estuary via runoff or from tributaries (Raymond & Bauer, 2001).
This plant material is broken down by microbial decomposers, e.g. heterotrophic bacteria,
and the organic carbon in the resultant detritus then becomes available to primary
consumers, e.g. detritivores (Cebrian, 1999; Sobczak et al., 2005). Autochthonous sources
of carbon, represented by vascular plants and macroalgae, are also routed through
decomposers, with only ~20% of the carbon ingested being consumed directly by
herbivores (Cebrian, 1999). In contrast, microalgae, e.g. phytoplankton and
microphytobenthos, are rich in nitrogen and essential fatty acids and are directly
metabolized by consumers (Furnas, 1990). While the amount of microphytobenthos can be
comparable with that of phytoplankton in some estuaries (Underwood & Kromkamp,
1999), phytoplankton is typically the dominant resource base for supporting the production
of higher trophic levels (Caddy, 2000; Breitburg et al., 2009; Gillson, 2011).
The primary consumers in estuaries, i.e. animals that feed on detritus and plant
material, include zooplankton in the water column and benthic invertebrates, such as
certain bivalve molluscs and polychaetes, and fish (Whitfield, 1989; Elliott & Hemingway,
2002). These members of the estuarine fauna are consumed by secondary consumers,
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which range from gastropod molluscs to small and large carnivorous fish and birds
(Schelske & Odum, 1962; Baird, 1999). The differences in feeding mode among fishes in
estuaries led to Elliott et al. (2007) constructing the following feeding mode functional
groups (FMFG); zooplanktivore, detritivore, herbivore, omnivore, piscivore and
zoobenthivore. It was recognised, however, that most species assigned to any one of these
groups also fed, but to a lesser extent, on the food that characterised another group. Indeed,
this was so extreme in some cases that a seventh group was constructed, i.e.
miscellaneous/opportunist, for species that fed on such a diverse range of food that they
could not readily be assigned to one of the above specialised FMFGs. The food consumed
by the Black Bream Acanthopagrus butcheri, the subject of the current study, varies
markedly among estuaries and can include large volumes of macrophytes in some systems
(Sarre & Potter, 1999; Chuwen et al., 2007) and therefore belongs to the last FMFG.
1.3 Classification of the ways fish use estuaries; the guild approach
It has long been recognised that estuaries are ‘used’ in different ways by the fish species
that are found within these systems (e.g. Cronin & Mansueti, 1971; Haedrich, 1983;
Whitfield, 1999; Elliott et al., 2007; Able & Fahay, 2010). The various schemes that have
been developed for defining that usage have recently been refined by Potter et al. (2013),
who subdivided the fishes into four categories, which, each comprised a number of guilds.
The four main overarching categories were marine for species that spawn at sea;
estuarine for populations where individuals complete their life cycle within the estuary;
diadromous for species that migrate between the sea and freshwater, and freshwater for
species that spawn in freshwater.
At the guild level, distinctions were made between those marine species that
typically enter estuaries ‘accidentally’ and usually in low numbers (marine straggler) and
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those that enter estuaries in substantial numbers, usually as juveniles (marine-estuarine
opportunist) and those that require sheltered estuarine habitats as juveniles (marine-
estuarine dependent). In the case of the estuarine category, the most important distinction
is between species that are found only in estuaries (solely estuarine) and those that are
represented by populations in both estuarine and marine waters (estuarine & marine). The
diadromous category comprises anadromous, catadromous and amphidromous species.
The freshwater category is far less represented in estuaries than the marine category (Potter
et al., 2013).
Examples of the main guilds derived from studies in different regions of the world
are given below, drawing on inter alia studies in Europe (e.g. Claridge et al., 1986; Franco
et al., 2008), North America (e.g. Able & Fahay, 2010), South America (e.g. Plavan et al.,
2010) and Africa and Australia (e.g. Whitfield, 1998; Blaber, 2000; Potter et al., 1990,
2014).
The species of marine straggler are frequently stenohaline, which are thus not
adapted to living in the low and or variable salinities often present in the main body and
distal regions of estuaries and are consequently most frequently found in the high salinity
areas near the estuary mouth (Potter et al., 2013). Many elasmobranchs, such as the Bull
Shark Carcharinas leucas are typical marine stragglers, but this guild also includes
numerous species of teleosts such as the Spanish Mackerel (Scomberomorus maculatus),
Red Porgy (Pagrus pagrus) and American Harvestfish (Peprilus paru).
The marine-estuarine opportunists, such as the European Bass (Dicentrarchus
labrax), Bluefish (Pomatomus saltatrix), Southern Kingfish (Menticirrhus americanus),
Sea Mullet (Mugil cephalus) and Atlantic Herring (Clupea harengus) are typically
euryhaline. They are thus able to penetrate the middle and upper regions of the estuary
where salinities are reduced. Several marine-estuarine opportunist species make an
14
important contribution to fisheries in coastal marine waters and sometimes also in estuaries
(Lenanton & Potter, 1987; Blaber, 1997; Costa et al., 2002; Dolbeth et al., 2008; Able &
Fahay, 2010).
Because estuaries are of recent origin and thus transitory in a geological sense,
Hedgpeth (1982) has argued that marine species are unlikely to depend on estuaries for
completing their life cycle. However, a few species, such as the Oval Moony
(Monodactylus falciformis) are regarded as dependent on estuaries in southern Africa, as
their juveniles are unable to tolerate the ‘turbulent’ conditions that occur along the coast
and thus require the more sheltered waters of estuaries for survival during early life
(Whitfield, 1999; Potter et al., 2013).
The solely estuarine category includes the Black Bream (Acanthopagrus butcheri),
Common Goby (Pomatoschistus microps) and Estuarine Round Herring (Gilchristella
aestuaria) with the last of these species also abundant in certain freshwater lakes
(Lenanton & Potter, 1987; Potter et al., 2013). The populations of some solely estuarine
species are very substantial in those estuaries when the conditions are consistently
particularly favourable for breeding and larval survival during and after the spawning
period. Species such as A. butcheri grow to a sufficient size and provide good angling and
quality of flesh to make a crucial contribution to recreational fisheries and also in some
estuaries to commercial fisheries (Lenanton & Potter, 1987; Kailola et al., 1993; Hutchins
& Thompson, 2001; Jenkins et al., 2010).
Good examples of species that can complete their life cycles in both estuaries and
marine waters are provided by the Estuary Cobbler (Cnidoglanis macrocephalus),
Longsnout Pipefish (Syngnathus temminckii), Western Gobbleguts (Ostorhinchus
rueppellii) and the Australian Anchovy Engraulis australis (Potter et al., 2013; Veale et
al., 2014). Several species in this category exhibit parental care of their eggs, larvae and/or
15
young (Blumer, 1982; Wilson et al., 2003). While the populations of C. macrocephalus in
estuaries and coastal marine waters have been shown to be genetically distinct (Ayvazian
et al., 1994), it is likely that the marine and estuarine assemblages of some species form a
continuum (Able & Fahay, 2010).
Estuaries provide a crucial route between the areas where spawning and feeding
occur. Catadromous species, such as the European Eel (Anguilla anguilla) spawn at sea
and grow in rivers (Potter et al., 2013). In contrast, anadromous species, such as many
salmonids, e.g. Pink Salmon (Oncorhynchus gorbuscha) and Atlantic Salmon (Salmo
salar) and several species of lampreys, e.g. Sea Lamprey (Petromyzon marinus) and
Pouched Lamprey (Geotria australis) and the Hilsa Shad (Tenualosa ilisha) and Allis Shad
(Alosa alosa), spawn in rivers and grow at sea (McDowall, 1988). Several anadromous
species make an important contribution to commercial fisheries (Hard et al., 2008; Al-
Dubakel, 2011). Amphidromous species, such as members of the goby subfamily
Sicydiinae, are particularly prevalent in rivers of small islands in the tropical Indo Pacific,
from which they are swept out to sea as larvae, but eventually return to rivers where they
become mature and spawn (McDowall, 1988; Tweedley et al., 2013). Such movements
enable species to be dispersed across the marine divide and into the rivers of the recently-
emerged islands of this region.
While some freshwater species (stragglers) can occur sporadically in the upper and
low salinity reaches of estuaries, few freshwater species penetrate the middle part of the
estuary in numbers and would therefore constitute the freshwater estuarine opportunist
guild (Potter et al., 2013). Good examples of freshwater estuarine opportunist species are
provided by the Mozambique Tilapia (Oreochromis mossambicus) and Three-Spined
Stickleback (Gasterosteus aculeatus).
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1.4 Anthropogenic impacts on estuaries
Estuaries have been widely exploited by human populations and sometimes to the
detriment of these systems (de Jong et al., 2002; Kennish, 2003; Lotze et al., 2006).
Estuaries have been used, for example, as important docking points for ships and for
transporting resources from other regions, thereby stimulating the development of towns
and cities along their shores. This then inevitably resulted in estuaries being used as a
repository for waste, which in cases, such as with certain heavy metals, lead to their
accumulation through the food chain, thereby posing a potential risk to the health of the
upper level components of the food chain in the estuary and to humans (Oze et al., 2005).
Runoff from the surrounding towns, agriculture and catchments has often resulted
in a greatly increased input of nutrients into the estuary and therefore the development of
severe cases of eutrophication (de Jong et al., 2002). Typical symptoms of eutrophication
include an increased frequency of macroalgal growths (Fig. 1.1) and phytoplankton
blooms, some of which are toxic, and prolonged periods of low dissolved oxygen
concentrations and fish mortalities (McComb, 1995; Whitall et al., 2007; Thronson &
Quigg, 2008; Paerl et al., 2014). The tributary rivers of many estuaries have also been
dammed to provide a source of freshwater for various purposes. This has led to a reduction
in freshwater discharge and thus to a decrease in the flushing of the estuary, which is
important for the maintenance of a well-oxygenated and ‘healthy’ system.
The degradation of temperate estuaries in recent decades as a result of, for example,
eutrophication and development of hypoxia, have led to these systems being the most
degraded of all marine environments (Jackson et al., 2001). Various studies have shown
that increases in hypoxia can have detrimental effects on the species composition of the
benthic macroinvertebrates. This results from the differential ability of, for example,
crustaceans and polychaetes, to survive such perturbations, which alter the
17
biogeochemistry of the sediment and modifies nutrient cycling between the benthos and
water column (Rakocinski et al. 1997; Gaston et al. 1998; Middleburg & Levin 2009).
Hypoxia can also lead to changes in certain biological characteristics of key species in
those estuaries. These include reductions in body condition and growth (Eby et al., 2005)
and declines in productivity in areas particularly affected by hypoxia (Diaz & Rosenberg,
2008; Breitburg et al., 2009). Furthermore, exposure to hypoxia has also been shown to
have a negative effect on maturation schedules, either through endocrine disruption (Wu et
al., 2003) or indirectly, as a result of phenotypic plasticity that depends on growth of the
individual (Morita & Morita, 2002).
Figure 1.1 Macroalgae collected in a seine net during sampling for fish in the Peel-Harvey
Estuary.
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1.5 General characteristics of macro- and microtidal estuaries
Estuaries were formed by rising sea levels during the Flandrian transgression (Perillo,
1996). In tidal-dominated regions, estuaries generally consist of a landward tapering
funnel, with the width and depth increasing exponentially at their mouths (Perillo, 1996).
While salinity declines progressively landward along the lengths of these systems, the
strong tidal amplitude in estuaries, such as the Humber and Ouse Estuary, results in the
salinity at any one point along those lengths varying markedly during each tidal cycle
(Uncles et al., 2006). The combination of large tidal amplitude, wide and deep entrance
channels and relatively consistent freshwater input ensure that these macrotidal estuaries
are well mixed (Elliott & McLusky, 2002; Savenije, 2012). The strong tidal effects also
lead to the creation of extensive and highly productive inter-tidal areas, which is very
important for wading birds (Baird et al., 1985; McLusky et al., 1992).
Many estuaries on, for example, the eastern seaboard of the United States, such as
Chesapeake Bay and the Neuse River Estuary, are microtidal. The waters in these systems
are only partially mixed, have a relatively long residence time and contain a limited inter-
tidal area (Luettich et al., 2002; Reynolds-Fleming & Luettich, 2004; Kemp et al., 2005;
Xiong & Berger, 2010).
In a large continental land mass in the southern hemisphere, such as Australia, the
estuaries in the north are located in a macrotidal region, and these possess many of the
characteristics of their counterparts in the northern hemisphere, whereas those in the south
are situated in a microtidal region (ICSM, 2014). In Australia, the microtidal estuaries
include the Swan River and Blackwood River estuaries, in which the studies for this thesis
were carried out. A combination of changes in sea level, long-shore drift and infilling by
sediments, derived from runoff from catchments, has ensured that estuaries in temperate
19
regions of the southern hemisphere typically remain relatively shallow (Hodgkin & Hesp,
1998; Cooper et al., 2008; Schumann, 2013).
1.6 Estuaries of south-western Australia
South-western Australia has a Mediterranean climate. Since the majority of precipitation in
this microtidal region thus occurs between late autumn, i.e. May, and mid spring, i.e.
October (Wright, 1997; Hoeksema & Potter, 2006; Australian Bureau of Meteorology,
2015), the volume of freshwater discharge is also highly seasonal in systems such as the
Swan River Estuary and Blackwood River Estuary, typically peaking between mid winter
and early spring (Hoeksema & Potter, 2006; Western Australia Department of Water,
2015). As a consequence of the small tidal influence and the restriction of substantial
freshwater discharge to the wet, cool period of the year, the water retention times in, for
example, the upper Swan River Estuary, can range from as short as <0.2 days in winter to
as long as a year in summer (Chan & Hamilton, 2001).
As a consequence of the long residency time in summer, the phytoplankton in these
microtidal systems exhibit high rates of photosynthesis and therefore attain far higher
concentrations than in typical macrotidal systems. This is particularly the case when the
estuary becomes nutrient enriched (McComb, 1995; Steckis et al., 1995). The estuaries of
south-western Australia are inherently susceptible to eutrophication, mainly due to
restricted tidal flushing, particularly during the protracted dry period, which results in long
residence times and the accumulation of organic material in bottom waters. Furthermore,
since the soils in this region are nutrient deficient, agriculture has relied heavily on the
addition of fertilizers for stimulating crop and pasture growth (McComb & Davis, 1993).
As the soils in south-western Australia show little ability to retain nutrients, phosphorous
in particular is readily leached and enters the estuary. Thus, for example, between 1997
20
and 2006, 251 tonnes of nitrogen and 26 tonnes of phosphorous were estimated to have
entered the Swan River Estuary each year (Swan River Trust, 2009).
Many estuaries in the low tidal amplitude regions of south-western Australia and
southern Africa become closed intermittently, seasonally or for longer periods, through the
formation of a sand bar at their mouths (Day, 1981; Potter et al., 1993; Hodgkin & Hesp,
1998; Cooper, 2001). In Western Australia, the Swan River Estuary has remained
permanently open since the removal of a rock bar at its mouth in 1886 to provide a deep
entrance for ship access (Brearley, 2005). The mouth of the natural entrance of the Peel-
Harvey Estuary, just to the south of the Swan River Estuary, is kept open by dredging the
sand that accumulates there (Brearley, 2005). While the locations of the natural entrance to
the Swan River and Peel-Harvey estuaries have remained the same, that of the Blackwood
River Estuary has varied and occasionally becomes closed and thus likewise has to be
artificially kept open (Brearley, 2013). More comprehensive descriptions of the Swan
River and Blackwood River estuaries are given in Chapter 2. The prevalence of estuaries
that become closed through the formation of a sand bar at their mouths increases in an
eastward direction along the south coast of Western Australia (Hodgkin & Hesp, 1998).
This largely reflects progressively declining rainfall that occurs from west to east along the
south coast (Hodgkin & Hesp, 1998).
South-western Australian estuaries characteristically comprise three
morphologically distinct regions, i.e. a short, narrow entrance channel, shallow and wide
central basin(s), and the relatively narrow and long saline lower reaches of the tributary
rivers (Day, 1981; Hodgkin & Hesp, 1998). In permanently-open estuaries, such as the
Swan River Estuary, salinities in the entrance channel typically remain euhaline for much
of the year, except during winter when surface waters can become fresh (Chan &
Hamilton, 2001). In the basins, salinities are typically only euhaline during
21
summer/autumn, whereas during winter, the formation of a salt wedge results in
stratification of the water column with salinities in the deeper waters remaining euhaline
whereas the surface waters can become fresh. While the basin of the Swan River Estuary is
only completely flushed during very wet winters, the upper estuary is fully flushed in most
winters (Kurup et al., 1998; Twomey & John, 2001). When freshwater discharge subsides,
the homogenous conditions found in the upper estuary during late winter and early spring
are disrupted by the tide-driven progression of the salt wedge. Although stratification is
typically evident throughout the upper estuary during the warmer months of the year
(Stephens & Imberger, 1996), as the salt wedge progresses upstream, the overlying
freshwater and seawater below gradually mix (Twomey & John, 2001). As the salt wedge
approaches its most landward position, ~60 km from the estuary mouth, salinities in the
downstream region of the upper estuary become euhaline, whereas those furthest upstream
become brackish (Swan River Trust, 2014). At the onset of winter, or following unseasonal
freshwater discharge, the salt wedge reforms and gradually retreats downstream towards
the estuary basin (Douglas et al., 1995). The consistent cyclical changes in salinity
throughout the year in the different regions of south-western Australian estuaries are a
major determinant of the compositions of the flora (e.g. Thompson, 2001; Twomey &
John, 2001) and fauna (e.g. Loneragan & Potter, 1990; Kanandjembo et al., 2001a,b;
Wildsmith et al., 2011) of these estuaries.
The different species of fishes found in south-western Australian estuaries often
exhibit pronounced spatial partitioning among the three morphologically and physico-
chemically different regions of these systems (e.g. Loneragan et al., 1987; Loneragan &
Potter, 1990; Potter & Hyndes, 1999; Potter et al., 2014). For example, among the five
most abundant species of atherinid in the Swan River Estuary, two species occupy
predominantly the lower estuary, two are mainly found in the middle estuary and one
22
largely in the upper estuary (Prince et al., 1982). Likewise, among the five most numerous
species of gobiid, one lives mainly in the lower estuary, while the other four are largely
restricted to the upper estuary (Gill & Potter, 1993). The Black Bream Acanthopagrus
butcheri, which is much larger than those atherinid and gobiid species and is the focus of
the current thesis, spends most of the year in the upper estuary, i.e. riverine reaches, but is
often swept downstream into the basin by the heavy freshwater discharge that occurs in
winter (Sarre & Potter, 2000). Thus, fishing for this iconic recreational species is largely
focused on the upper estuary (for further details see Chapters 3, 4 and 5).
Certain estuaries in south-western Australia have been subjected to extreme
eutrophication as a result of the input of nutrients from surrounding agricultural and urban
development (McComb et al., 1981; Cloern et al., 2014). In the Peel-Harvey Estuary, this
was manifested in massive growths of macroalgae and the toxic cyanobacterium Nodularia
spumiginea. The eutrophication was so extreme that a deep channel was constructed
between this large estuary and the ocean to increase greatly the flushing of nutrients out of
the system. In the Swan River Estuary, ~60 km to the north of the Peel-Harvey Estuary,
there have been periodic large blooms of microalgae, including Karlodinium micrum,
which is toxic andtherefore contributed to major mortalities of Black Bream
Acanthopagrus butcheri (Smith, 2006; Hallett et al., 2015), the main recreational fish
species in southern Australian estuaries (Lenanton & Potter, 1987; Ferguson &Ye, 2008;
Hindell et al., 2008; Williams et al., 2012). However, mortalities of this species at other
times were presumably related to the hypoxia that resulted from extreme eutrophic events.
The Swan River Estuary and also the Blackwood River Estuary have also suffered
from the effects of the decline in freshwater discharge and flushing that has occurred
during the last 20-30 years as a result of a reduction in rainfall (see Chapter 3). The marked
reduction in rainfall is a consequence of anticyclonic events that now persist over the
23
southern Indian Ocean and which cause a weakening of the north-westerly winds and a
reduction in the transport of land-bound moist air (Feng et al., 2010). These changes are
reflected in the annual rainfall at Perth Airport, close to the Swan River Estuary, declining
from 845 mm y-1
during the 1960s to 684 mm y-1
in the 2000s (Fig. 1.2). An even greater
decline in rainfall occurred at Cape Leeuwin, in the proximity of the mouth of the
Blackwood River Estuary, where rainfall declined from 1066 mm y-1
to 712 mm y-1
over
the same period (Fig. 1.2). These changes in rainfall over time have resulted in reduced
freshwater discharge, which has led to the accumulation of nutrients and other organic
material in the deeper waters and thus in exceptional circumstances led to increased levels
of hypoxia in those waters (Tweedley et al., 2014). The effects of these changes are
explored in Chapters 3 to 5.
Figure 1.2 Total annual rainfall (mm) recorded at Perth Airport (top) and Cape Leeuwin
(bottom) between 1960 and 2014. Horizontal bars represent decadal averages.
24
The compositions of the fish faunas in the different regions of south-western
Australian estuaries often differ markedly and typically undergo marked seasonal changes,
which, in the middle and upper reaches, are largely related to changes in salinity (e.g.
Potter & Hyndes, 1999; Kanandjembo et al., 2001; Hoeksema & Potter, 2006). For
example, in summer, semi-anadromous, marine-estuarine and true estuarine species are
typically most abundant in the upper reaches of the estuaries, whereas in winter, after
freshwater discharge has increased and salinities declined in the upper reaches, these
species are typically more abundant in the estuary basins, or in the case of semi-
anadromous species, migrate to sea (Kanandjembo et al., 2001).
As with other microtidal estuaries in the southern hemisphere, a number of species
complete their life cycles in south-western Australian estuaries (Potter et al., 1990; Potter
& Hyndes, 1999; Veale et al., 2014). The ability of these estuarine species to breed
successfully in these systems has been attributed to the relatively stable water conditions
that persist in the middle and upper reaches of these estuaries during the summer months,
when these species typically spawn, a stability attributed to the low tidal amplitude and
lack of freshwater flow at that time of year (Potter & Hyndes, 1999). In south-western
Australia, ‘estuarine’ species make a substantial contribution to the overall abundance of
fishes in estuaries (Potter & Hyndes, 1999; Kanandjembo et al., 2001).
1.7 Acanthopagrus butcheri
The Black Bream Acanthopagrus butcheri (Sparidae), which attains a maximum length of
533 mm and weight of 3,450 g (Hutchins & Thompson, 2001), is abundant in many
estuaries in southern Australia (Gomon et al., 2008). Although A. butcheri can swim
several kilometres in a day (Hindell et al., 2008; Sakabe & Lyle, 2010), it typically resides
for much of the year in the upper regions of estuaries, where it spawns during the spring
25
and early summer (Sarre & Potter, 2000; Nicholson et al., 2008; Williams et al., 2012).
This sparid can be swept out of the estuary during particularly high freshwater discharge
and in south-eastern Australia may occasionally enter other estuaries (Lenanton et al.,
1999; Burridge & Versace, 2006). The results of studies of the reproductive biology and
distribution of the various life stages of this species in south-western Australian estuaries
demonstrate that individuals of this sparid typically complete their life cycle within their
natal estuary in this region (Potter & Hyndes, 1999; Sarre & Potter, 2000). Such a
conclusion is consistent with the fact that the genetic compositions of A. butcheri in the
various estuaries in south-western Australia are significantly different (Chaplin et al.,
1998), as is also the case in south-eastern Australia (Burridge & Versace, 2006).
Acanthopagrus butcheri is one of the most important recreational finfish species in
the estuaries of southern Australia (Smith, 2006; Jenkins et al., 2010). In south-western
Australia, A. butcheri was also historically an important commercial species (Lenanton &
Potter, 1987; Loneragan et al., 1987; Kailola et al., 1993), although this is no longer the
case due to governmental buy-backs of existing licences, e.g. in the Swan River Estuary. In
estuaries such as Culham Inlet, the abundance of this sparid has become so reduced,
mainly through mortality associated, in particular, with the development of highly elevated
salinities brought about by reduced freshwater discharge, that it is no longer fished
commercially in those systems (Norriss et al., 2002; Hoeksema et al., 2006).
Acanthopagrus butcheri is also an important aquaculture species and has been
introduced into a large number of artificial impoundments throughout south-western
Australia (Partridge et al., 2004; Smith et al., 2009). Several illegal introductions into
natural lakes have also occurred, with a population being sustained in Lake Clifton for
many years (Smith & Norriss, 2011). In some estuaries, such as the Blackwood River
26
Estuary, restocking has been used to increase the stock following a prolonged period of
low catches (Potter et al., 2008).
Aspects of the biology of A. butcheri, such as growth, vary markedly among
estuaries (e.g. Hobday & Moran, 1983; Coutin et al., 1997; Morison et al., 1998; Sarre &
Potter, 2000; Hoeksema et al., 2006). For example, Sarre & Potter (2000) showed that A.
butcheri grew more rapidly early in life and reached a larger maximum length in the Swan
River Estuary than in each of three other estuaries they studied, i.e. Wellstead,
Nornalup/Walpole and Moore River estuaries. For example, by the age of 3 and 6 years,
female A. butcheri had attained total lengths of 266 and 368 mm, respectively, in the Swan
River Estuary compared with 146 and 232 mm, in the Moore River Estuary, which is only
~85 km further north. The early growth and maximum length in the Swan River Estuary
were, however, slightly less than in a saline coastal lake, i.e. Lake Clifton (Sarre & Potter,
2000).
Although the populations of A. butcheri in different south-western Australian
estuaries have been shown to be genetically distinct (Chaplin et al., 1998), an aquaculture
study of this species demonstrated that, when cultured under the same conditions, the
growth of the juveniles produced from broodstock from the permanently-open Swan River
and Moore River estuaries were essentially the same (Partridge et al., 2004). Thus, the
growth of this sparid in south-western Australian estuaries is influenced largely by
environmental factors rather than its genetic composition (Partridge et al., 2004). Thus, in
the Moore River Estuary, this species consumes far larger amounts of plant material, such
as Cladophora sp., than it does in the Swan River Estuary, whereas the reverse is the case
with bivalve molluscs, such as Xenostrobus securis and Fluviolanatus subtorta, which
have a greater nutritional value than plant material. Furthermore, the far greater densities
of A. butcheri in the Moore River Estuary than the Swan River Estuary were also
27
considered to contribute to A. butcheri growing less rapidly in the Moore River Estuary
(Sarre et al., 2000).
The lengths and ages at which A. butcheri in the estuaries attained maturity also
differed substantially and maturity tended to occur at a smaller size and older age in those
estuaries in which growth was less rapid (Sarre & Potter, 2000). For example, the lengths
and ages at which 50% of fish attain maturity, L50s and A50s, respectively, of females of
218 mm and 2.2 years in the Swan River Estuary differed markedly from the
corresponding values of 157 mm and 3.3 years in the Moore River Estuary.
The above examples of marked variations in several of the biological
characteristics of A. butcheri among estuaries with different environmental conditions
emphasise that these characteristics are particularly plastic in this sparid. This species is
thus likely to provide an excellent ‘model’ for exploring how changes in the environment
can influence the expression of the fundamental attributes of a species, such as condition,
growth and maturity schedules.
1.8 Objectives of thesis
The two main overarching aims of this thesis are as follows. 1) Test the hypothesis that the
detrimental changes to the environment of the Swan River Estuary have been accompanied
by a decline in the condition, growth and length at maturity of A. butcheri and an increase
in its age at maturity. 2) Compare the growth and maturity schedules of restocked and wild
A. butcheri in the Blackwood River Estuary to determine whether cultured fish perform as
well as the wild stock and estimate the contribution of the restocked fish to the commercial
fishery. These aims are developed in each of the subsequent relevant chapters.
28
Chapter 2
General material and methods
2.1 Sampling methods
The biological characteristics of Acanthopagrus butcheri have been studied in eleven
estuaries in south-western Australia and in Lake Clifton, a coastal salt lake (Sarre & Potter,
1999, 2000; Potter et al., 2008; Chuwen, 2009; Fig. 2.1a). This thesis focuses on two of
these estuaries, the Swan River Estuary (Fig. 2.1b), which contains the most extensive time
series of data, and the Blackwood River Estuary (Fig. 2.1c), in which substantial numbers
of cultured A. butcheri have been introduced.
The information provided below covers those aspects of the sampling gear and
methodology, ageing procedures, analyses of growth and determination of reproductive
characteristics that are common to the studies reported in Chapters 3 to 5. Other details of
the sampling regimes for the different studies of A. butcheri in the Swan River Estuary are
given in Chapters 3 and 4, and those for the study undertaken in the Blackwood River
Estuary are provided in Chapter 5.
2.2 Sampling regime
The Swan River and Blackwood River estuaries were sampled using 21.5 and 41.5 m long
seine nets and a 160 m long composite gill net (see Figure 2.3). The 21.5 m seine net,
which consisted of a 1.5 m wide bunt of 3 mm mesh and two 10 m long wings (each
comprising 4 m of 3 mm mesh and 6 m of 9 mm mesh), swept an area of 116 m2, while the
41.5 m seine net, which contained a 1.5 m bunt made of 9 mm mesh and two 20 m long
wings comprising 25 mm mesh, swept an area of 274 m2. The 21.5 m net was laid parallel
to the bank and then hauled onto the shore, whereas the 41.5 m net was deployed in a semi-
circle from the bank using a small boat before being hauled on to the shore.
29
Figure 2.1 a) Map showing the locations of the estuaries in south-western Australia for
which biological data have been collected for Acanthopagrus butcheri and the morphology
of the b) Swan River Estuary and c) Blackwood River Estuary, the two estuaries in which
the studies for this thesis were conducted. The box in the map of Australia in the top right
hand corner of a) shows the region where the Swan River and Blackwood River estuaries
are located in Australia.
30
Figure 2.2 Photographs of the Swan River Estuary (top left, courtesy of Kristian Maley)
and Blackwood River Estuary (bottom left, courtesy of Simon Neville) and examples of
the sites sampled by seine netting in the Swan River Estuary (top right) and the Blackwood
River Estuary (middle right) and by gill netting in the Blackwood River Estuary (bottom
right).
The composite gill net, which comprised eight 20 m long panels, each with a
different stretched mesh size, i.e. 38, 51, 63, 76, 89, 102, 115 and 127 mm, was set, just
after sunset, parallel to the shore in water depths of 2 to 6 m.
All fish were anaesthetised in an ice slurry immediately after capture.
31
Figure 2.3 Examples of the different fishing methods used to collect Acanthopagrus
butcheri, showing a gill net (top left) and 21.5 m seine netting (bottom left) and a 41.5 m
seine net being deployed (top right) and the commercial fisher boxing his catch in the
Blackwood River Estuary (bottom right).
2.3 Laboratory procedures and measurements
2.3.1 Ageing
Each A. butcheri from the Swan River and Blackwood River estuaries, apart from those
caught by the commercial fisher in the Blackwood River Estuary, were measured to the
nearest 1 mm (total length), weighed to the nearest 0.1 g and sexed by macroscopic
examination of their gonads. The A. butcheri supplied by the above commercial fisher had
been filleted (but with their gonads retained). While their lengths and sexes could be
32
recorded, it was not possible to obtain their weights. The smallest fish, which could not be
sexed, were designated randomly (and in equal numbers) as females and males.
The sagittal otoliths of each A. butcheri were removed, cleaned and stored. All
otoliths were initially examined using a dissecting microscope under reflected light. The
otoliths of cultured fish that were released into the Blackwood River Estuary were clearly
identifiable through the purple colour produced in the central region of their otoliths by the
alizarin complexone stain (Fig. 2.4; Chapter 5). Previous studies had shown that the
opaque zones in all A. butcheri otoliths could be clearly identified without sectioning when
there were up to six such zones, but this was not always the case with otoliths containing a
greater number of such zones (Sarre & Potter, 2000). Thus, when otoliths contained ≤6
opaque zones, the numbers of their zones were counted using whole otoliths, but, when
there were > 6 such zones, the numbers were counted in sectioned otoliths (see Figure 2.4).
For sectioning, otoliths were embedded in clear epoxy resin, sectioned transversely
(ca 400 µm) through their primordia and mounted on glass microscope slides using DePX
mounting adhesive. As marginal increment analysis had previously shown that the opaque
zones in the otoliths of A. butcheri are typically formed annually (Sarre & Potter, 2000),
validation of the applicability of using opaque zones in otoliths for ageing this species was
not required. To assess the level of precision of the ageing of A. butcheri, the numbers of
opaque zones in a subsample of 200 otoliths from fish covering a wide size range (and
using whole and sectioned otoliths) were counted independently by two readers, i.e., A.
Hesp and myself, and compared using the coefficient of variation (CV) (Chang, 1982;
Campana, 2001).
The equation is: {[√∑ ( )
( )⁄ ] ⁄ } , where CV j is the age
precision estimate for the jth fish, X ij is the ith age determination of the jth fish, X j is the
mean age estimate of the jth fish, and R is the number of time each fish is aged. The overall
33
CV was taken as the average of the CVs for all 200 fish. This analysis produced a value of
0.2% for the CV for A. butcheri, indicating a high degree of precision for the ageing of this
species, given that a CV value of up to 5% is considered acceptable for medium to long-
lived species (Campana, 2001).
The age of individual A. butcheri, estimated from the number of opaque zones in
their otoliths, took into account 1) that newly-formed opaque zones typically become
delineated from the otolith periphery by the beginning of November (Sarre & Potter,
2000), 2) a birth date, which corresponded to the approximate peak in the mean
standardised gonad weight and 3) the date of capture.
Figure 2.4 Comparisons of whole otoliths from 4 month old cultured Acanthopagrus
butcheri (top left) before and after the juveniles were immersed in alizarin complexone,
which left a prominent stain on their otoliths, enabling the cultured fish to be distinguished
following their release into the Blackwood River Estuary (see Chapter 6). A whole otoliths
from a 2 year wild A. butcheri (bottom left), a sectioned otolith from a 15 year old wild A.
butcheri (top right), , and a whole otolith from a cultured A. butcheri showing the retention
of the purple stain in its the primordium after 12 years (bottom right).
34
2.3.2 Growth
Using non-linear regression, the von Bertalanffy growth model (VBGM) was fitted
separately to the lengths at age of females and males of A. butcheri caught in the Swan
River and Blackwood River estuaries. The von Bertalanffy growth equation is
0exp1ˆ ttkLLt , where tL is the expected total length at age t (years), L is the
asymptotic length (mm), k is the growth coefficient (year-1
) and 0t is the hypothetical age
(years) at which fish would have zero length.
The growth curves for females and males of A. butcheri in each estuary were compared
using likelihood-ratio tests (Cerrato, 1990). For each comparison, the differences between
the negative log-likelihood (NLL) was obtained by fitting a common growth curve to the
data for both sexes and by fitting separate growth curves to each sex, and the resultant test
statistic multiplied by two. The NLL was calculated as 1ˆln)2ln(2
n
NLL ,
where n is the number of fish, ln is the natural logarithm, π is the natural constant pi, and
is determined as:
n
j
jj
n
LL
1
2ˆ
where jL and jL are the observed and expected
lengths of the j’th fish. The hypothesis that the growth of the two sexes could appropriately
be represented by a single growth curve was rejected at the α = 0.05 level of significance if
the above test statistic exceeded ( ), where q is the difference between the numbers of
parameters in the two approaches, i.e. 3 (Cerrato, 1990).
The above approach was then adopted to compare the growth of A. butcheri in
different periods in both the Swan River Estuary and between restocked and wild A.
butcheri in the Blackwood River Estuary. Precise details of the comparisons made in these
two estuaries are given in chapters 3 and 5, respectively.
35
2.3.3 Length and age at maturity
The gonads of each A. butcheri were weighed to the nearest 0.01 g and assigned to one of
the following stages on the basis of their macroscopic appearance: I/II = virgin or resting
adult, III = developing, IV = maturing, V = prespawning, VI = spawning, VII = spent and
VIII = recovering spent (Laevastu, 1965). The trends exhibited by the prevalence of the
different stages in ovarian development in sequential months, allied with those of gonad
weights, were used to determine the spawning period and the birth date of A. butcheri.,
taken as the approximate time of peak spawning.
Logistic regression analysis was used to determine the probability P that a female
or male of a given length possessed gonads at stages III-VIII during the spawning season
in the Swan River and Blackwood River estuaries. The logistic equation is
{ [ ( ) ( ) ( )]}, where L is the total length of the fish in
mm and L50 and L95 are the lengths at which 50% and 95% of fish attain maturity,
respectively. The values of L50 and L95 were estimated by minimising the negative log-
likelihood (NLL) using R (R Core Team, 2014), determined as
j
jjjj PPPMNLL 1ln1ln
where Mj is the maturity class of the j’th fish, i.e. 0
= immature and 1 = mature, and Pj is the probability of the j’th fish being mature.
Likelihood-ratio tests were used to determine whether, for each sex, the ogives relating
maturity to length were different and, if so, whether this could be attributed to a difference
in the values of L50. The analysis was repeated using OpenBUGS (Surhone et al., 2010), a
successor to WinBUGS (Lunn et al., 2000), with two chains, 1,004,000 iterations, a burn-
in of 1000 and a thinning interval of 20, to obtain estimates of the approximate 95%
credible intervals for the L50s and L95s and the expected proportion of mature fish at each
of a range of total lengths. The prior distribution for each parameter was represented by a
non-informative normal distribution. The above approach was also used to relate the
36
probability that a female or male possessed mature gonads to the age of the fish and to test
whether, for each sex, the ogives relating maturity to age were different and, if so, whether
this could be attributed to a difference in the values of A50. OpenBUGs was again
employed, but with 2,004,000 iterations of two chains, a burn-in of 4000 and thinning
interval of 40.
37
Chapter 3
Marked deleterious changes in the condition, growth and maturity schedules of
Acanthopagrus butcheri in the Swan River Estuary reflect environmental degradation
3.1 Introduction
The high productivity of estuaries (Schelske & Odum, 1962; Whittaker & Likens, 1975;
Elliott & Whitfield, 2011) helps account for the importance of these systems for many
marine fish species throughout the world and especially during juvenile life (Blaber &
Blaber, 1980; Potter et al., 1990; McLusky & Elliott, 2004; Able & Fahay, 2010). This rich
food source is also crucial for those species that complete their life cycles within estuaries,
which are particularly abundant in temperate microtidal regions of the southern
hemisphere, such as those of south-western Australia (Potter & Hyndes, 1999; Whitfield,
1999; Chuwen et al., 2011).
In view of their ecological significance, it is disturbing that temperate estuaries are
also among the most degraded of all marine ecosystems (Jackson et al., 2001), with the
prevalence of those that have become eutrophic due to anthropogenic impacts increasing
markedly during recent decades (Kennish & Townsend, 2007; Vaquer-Sunyer & Duarte,
2008). Furthermore, eutrophication in estuaries that have strong vertical stratification leads
to the accumulation of organic matter in their deeper waters and thus ultimately to hypoxia
(Diaz, 2000; Eby et al., 2005; Breitburg et al., 2009). Hypoxic conditions can be lethal to
fish (Kramer, 1987; Eby et al., 2005; Breitburg et al., 2009) or lead to reductions in their
body condition, growth rates and metabolism (Pichavant et al., 2000, 2001; Wu, 2002; Eby
et al., 2005) and have detrimental effects on their early development (Wannamaker &
Rice, 2000; Thronson & Quigg, 2008; Hassell et al., 2008a, b) . While fish sometimes have
the opportunity to move from hypoxic to better oxygenated habitats (Pihl et al., 1992;
38
Howell & Simpson, 1994; Thiel et al., 1995), such as from deeper to nearshore, shallow
waters in estuaries, this can lead to density-dependent effects on growth (Eby & Crowder,
2002; Campbell & Rice, 2014) and/or to exposure to suboptimal temperatures and
salinities (Kramer, 1987; Craig et al., 2001; Eby et al., 2005).
Most studies of the ways in which reductions in growth are reflected in changes in
the maturity schedules of fish populations have been undertaken on populations subjected
to substantial fishing pressure (e.g. Morita & Fukuwaka, 2007; Stahl & Kruse, 2008). In
many cases, such reductions in growth were accompanied by a decline in the length at
maturity (Morita & Morita, 2002; Morita & Fukuwaka, 2007) and an increase in the age at
maturity, which is consistent with, for example, the model of Stearns (1992) in which such
trends represent a balance between reducing fecundity and increasing mortality. Certain
studies support this model (Helle & Hoffman, 1998; Morita & Morita, 2002; Grover, 2005;
Morita & Fukuwaka, 2007), but none has demonstrated quantitatively, and in a composite
manner, that the body condition and growth decline and maturation schedules of a species
in an estuary change when that system becomes degraded.
During the last 20 years, the Swan River Estuary has become increasingly
eutrophic (Stephens & Imberger, 1996; Hamilton & Turner, 2001; Thomson et al., 2001;
Robson & Hamilton, 2003; Hallegraeff et al., 2010; Kristiana et al., 2012). Thus, while
phytoplankton blooms were rarely observed in the 1980s (Zammit et al., 2005), they
occurred intermittently in the 1990s (Viney & Sivapalan, 2001) and in most years in the
2000s (Robson & Hamilton, 2003; Hallegraeff et al., 2010; Kristiana et al., 2012). Indeed,
this system was one of the two most hypertrophic of the 131 estuarine coastal ecosystems
worldwide for which data were recently collated by Cloern et al. (2014). The upper reaches
of the Swan River Estuary often experience strong stratification during the warm summer
months, when freshwater discharge is typically limited and the salt wedge penetrates
39
rapidly upstream along the bottom of the estuary. As the deeper waters are poorly flushed,
they have a long residence time (Chan & Hamilton, 2001),substantial amounts of organic
material are thus retained in those waters, resulting in high biological oxygen demand and
therefore reductions in oxygen concentrations (Norlem et al., 2014; Tweedley et al., 2014).
This problem has become exacerbated over the last three decades by a decline in
freshwater discharge (Western Australian Department of Water, 2015), due to a reduction
in rainfall (Australian Bureau of Meteorology, 2014), and a greater penetration of the salt
wedge upstream. This has led to elevated nutrient concentrations (Robson et al., 2008) and
a greater prevalence of prolific algal and cyanobacterial blooms (Twomey & John, 2001),
some of which are toxic (Orr et al., 2004; Mooney et al. 2009) and have resulted in an
increased prevalence of fish kills (Smith, 2006; Kristiana et al., 2012).
Acanthopagrus butcheri is abundant in the upper reaches of estuaries throughout
southern Australia (Sarre & Potter, 2000; Nicholson et al., 2008; Williams et al., 2012). As
with other sparids, certain biological characteristics of A. butcheri are plastic, varying
markedly among estuaries with different environmental characteristics. Thus, for example,
among four south-western Australian estuaries, the total lengths reached after three years
ranged widely from 146 to 266 mm (Sarre & Potter, 2000) and the L50s and A50s for
maturity for females ranged markedly from 157 to 218 mm and 1.9 to 4.3 years,
respectively. It is also evident that maturity tends to occur at a smaller size and older age in
those estuaries in which growth is less rapid (Sarre & Potter, 1999, 2000), which is
consistent with the model of Stearns (1992).
The present study has determined certain biological characteristics of A. butcheri in
the Swan River Estuary in 2007-11 and compared these with those derived from data for
that estuary in 1993-95 (Sarre & Potter, 1999, 2000). These comparisons were used to test
the hypothesis that increased environmental degradation in this estuary during recent years
40
has been accompanied by a decline in the body condition, growth and length at maturity of
A. butcheri and an increase in its age at maturity. The trends exhibited by the catch data
derived from fishery-independent sampling over time were compared to determine whether
there was evidence that an increase in the extent of hypoxia in deeper waters had been
accompanied by a reduction in the relative abundance of A. butcheri in those waters and a
resultant increase in nearshore, shallow waters.
41
3.2 Materials and Methods
3.2.1 Description of the Swan River Estuary
The Swan River Estuary, which is located on the lower west coast of Australia ( o31 57’ S
and o116 04’ E), flows through Perth, the capital city. This permanently-open estuary
enters the Indian Ocean at the port city of Fremantle and, with an area of 55 km2, is the
second largest estuary in south-western Australia (Brearley, 2005). The Swan River
Estuary has two main tributaries, the Swan and Canning rivers (Fig. 3.1).
Figure 3.1 Map showing the location of the sites sampled in the upper region of the Swan
River Estuary.
As with many other south-western Australian estuaries, the Swan River Estuary
comprises three morphologically distinct regions (Fig. 2.1). The lower estuary comprises a
long (~7.5 km) and narrow (~200 m) entrance channel, while the middle estuary consists
42
of two basins, i.e. Melville Water and Perth Water. Melville Water is 12 km long and 2 km
wide and has a maximum depth of 21 m. Perth Water is 2.5 km long, 1.5 km wide, and
typically ~1 m deep (Hodgkin, 1987; Thomson et al., 2001). The upper estuary, which
includes the 38 km long saline and tidally-influenced lower reaches of the Swan River, and
of the corresponding 6 km region in the Canning River (Stephens & Imberger, 1996).
The Swan River Estuary and its catchments (141,000 km2) have been extensively
modified since European settlement in 1829 (Smith, 2006). Prior to settlement, tidal
exchange was restricted, due to the shallowness of the entrance channel of this estuary, i.e.
maximum depth was 2 m, which acted as a partial barrier between the estuary and the
ocean. Since the 1890s, the entrance channel has been deepened (ca 13 m) and widened on
several occasions, thereby increasing tidal exchange (Brearley, 2005). As a result, the
salinities in the two basins and upper estuary now remain elevated for several months of
the year (Thomson et al., 2001). The damming of several tributary rivers, e.g. the Helena
River by the Mundaring Weir and the Canning River by the Canning Dam, has resulted in
a marked reduction in freshwater flow and thus of discharge into the estuary. The extent of
such reductions was augmented by the marked reduction that has occurred during recent
years in the amount of freshwater entering the catchment of this estuary annually, with
these declining to about half of the level recorded in the years prior to 1975 (Smith, 2006).
The Swan-Avon River Catchment, which contributes ca 85% of the total freshwater
input to the estuary, has also been ~70% cleared (Kurup & Hamilton, 2002; Brearley,
2005). To manage flash flooding in the 1950-60s (largely resulting from the clearing of
land), a 187 km stretch of the Swan-Avon River was straightened and deepened, and
riparian vegetation and snags removed (Brearley, 2005). It is estimated that the above
modifications led to a five-fold increase in stream flow, a forty-fold increase in
sedimentation and a sixteen-fold increase in nutrient input (Viney & Sivapalan, 2001).
43
3.2.2. Physico-chemical data and sampling regimes
Measurements of freshwater discharge, entering the Swan River Estuary at gauging station
616011 upstream of the study area, were provided by the Western Australian Department
of Water. That department also provided weekly vertical profiles of oxygen concentration,
temperature and salinity, recorded since 1995 using a YSI sonde (model 6600V2) or
equivalent, at five of its sampling stations (KIN, MAY, RON, STJ, SUC) within the study
area. The average oxygen concentration in the bottom 1 m of the water column at each
station was calculated for each weekly sample from 1995 up to and including those in
2010, the last year for which data have thus far been collated (data collection and
calculations by M. Hipsey, University of Western Australia). Linear interpolation between
stations was then used to determine the average weekly oxygen concentrations along the
central channel of the upper estuary for each year. Oxygen concentrations <4 mg L-1
are
regarded as hypoxic. The percentages of the total distance along the channel that was
hypoxic in each week were then determined and used to calculate each annual mean.
During the fieldwork for this thesis, Acanthopagrus butcheri was sampled at nine
sites in the upper Swan River Estuary (Fig. 3.1). Nearshore, shallow waters were sampled
using the 21.5 and 41.5 m long seine nets in each season between winter 2007 and autumn
2011, and thus seasonally in four consecutive 12 month intervals (Table 3.1). Gill netting
was undertaken in waters adjacent to each seine net site at the same time (season) as seine
netting between winter 2007 and autumn 2009 (i.e. seasonally over two consecutive 12
month intervals), after which it was discontinued as it was catching few fish. The data on
condition and growth of A. butcheri caught by the above seine and gill netting are
subsequently regarded as representing the 2007-11 period.
44
Table 3.1 Regime for sampling Acanthopagrus butcheri in the upper Swan River Estuary
using seine and gill nets between 1993 and 2011.
Sampling seasons Period Net type Number of sites
Spring 1993-Autumn 1995 1993-95 41.5 m seine 6 (lower sites)
Spring 1993- Summer 1995 Gill 9
Summer 2000-Spring 2000 2000 Gill (catch rate only) 9
Spring 2003-Winter 2004 2003-04 21.5 m seine 6 ( lower sites)
41.5 m seine 6 (lower sites)
Gill 9
Winter 2007-Autumn 2009 2007-11 21.5 m seine 9
41.5 m seine 9
Gill 9
Winter 2009-Autumn 2011
2007-11
21.5 m seine
9
41.5 m seine 9
The data derived from samples collected seasonally from nine sites in 2007-11 (see
above) were collated with those obtained monthly between winter 1993 and autumn 1995
for the six lower sites using a 41.5 m long seine net and for those obtained monthly
between spring 1993 and summer 1995 for all nine sites using the same 160 m gill net
(Sarre & Potter, 2000; Table 3.1). This earlier period is subsequently referred to as the
1993-95 period when making comparisons with the condition and growth of A. butcheri in
2007-11. Comparisons were also made with the data from a subsample of A. butcheri
collected in each season between spring 2003 and winter 2004 using both seine nets
(21.5 m and 41.5 m) at the same six lower sites and the gill net at the same nine sites as in
1993-95 (S. Hoeksema, unpublished data; Table 3.1). Each net had the same dimensions
and mesh sizes as in the other studies. This 12 month interval is subsequently referred to as
the 2003/04 period.
45
Catches of A. butcheri during the summer and spring of 2000, obtained as part of
another study that involved gill netting at the same nine sites as in 1993-95 and 2007-11
(S. Hoeksema, unpublished data), were used to provide catch per unit effort data for 2000
to complement those for other years.
3.2.3 Assessment of body condition
Following the approach of Froese (2006), the length-weight relationships of each sex of A.
butcheri in 2007-11 and 1993-95 were calculated from data for ten randomly-selected fish
from each of three length categories, i.e. <160, 180-220, >240 mm, in each calendar
season, except for winter in which ten fish were not always available for each of these
length categories due to the pronounced tendency for A. butcheri to be flushed downstream
in that season when freshwater discharge is far greater than in other seasons (Sarre &
Potter, 1999). The parameters period and period of the length-weight relationships,
period period were estimated by fitting linear equations of the form:
( ) ( period) period ( ) period , to the masses (g) and total lengths (mm) for
the 90 females and 90 males in the 2007-11 and 1993-95 periods. In this equation, ln refers
to the natural logarithm, and are the observed mass and length, respectively, of the
j’th fish, and the deviations of the logarithms of the observed masses from the values
predicted by the regression equations were assumed to be normally distributed with means
of zero and variances that differed between the two periods, i.e. period ( period ). In
the case of both sexes, the linear equations were fitted simultaneously to the data for the
two periods using R (R Core Team, 2013). Likelihood-ratio tests were employed to
compare, for each sex, the model that assumed a common length-weight relationship for
the two periods against the best fitting (i.e. smaller negative log-likelihood, NLL) of the
46
two three-parameter models, which assumed that either the slope or the intercept (but not
both) remained constant, and that latter model against the model that assumed that both the
intercept and slope of the regression equation differed between the two periods.
Approximate 95% confidence intervals for period and period were estimated as the 2.5 and
97.5 percentiles of the distributions of 1000 parameter estimates obtained by drawing (with
replacement) a sample from the data for each sex and period (with the same sample size as
the original sample) and refitting the linear regression equation to that sample. When
calculating the expected masses of fish from their total lengths, the correction factor
exp( period ) was employed (Beauchamp & Olson, 1973) to account for the bias
associated with back-transformation of the predicted values from the values of their natural
logarithms. Thus, for each period and sex, the back-transformed allometric equation
became [ period exp( )] period , where period
is the estimated variance of the
residuals from the fitted linear equation.
The allometric condition factor, , for fish j of mass and total length for
each period and sex was calculated as ⁄ using the value of period that was
estimated for the length-weight relationship for that period (Tesch, 1968). A t-test was
used to compare, for each sex, the mean value of the resulting estimates of CF for 2007-11
with that for 1993-95. As period period
exp( ), where ( period ), the expected
value of for the period and sex was calculated as period period exp( period ⁄ ).
Approximate 95% confidence intervals for period were calculated for each period and sex
from the 1000 bootstrapped samples that were drawn to estimate the confidence intervals
for the parameters period and period of the weight-length relationships.
47
3.2.4 Growth and reproductive biology
Likelihood-ratio tests demonstrated that the growth of females and males in the Swan
River Estuary in both 2007-11 and in 2003/04 were significantly different (P<0.01), and
the same had previously been shown to apply in 1993-95 (Sarre & Potter, 2000). Thus,
comparisons between the growth curves in these three periods were undertaken separately
for each sex. As the tests demonstrated that the growth curves differed between these
periods (see Results), likelihood-ratio tests were also used to determine which of the
growth parameters for each sex in those three periods likewise differed.
As described in Chapter 2, logistic regression analysis was used to determine the
probability P that a female or male of a given length possessed gonads at stages III-VIII in
November, i.e. just after the mid-point of the spawning period in October, when no
immature fish would be expected to become mature during the current spawning season
and would have included all fish that had spawned or were destined to spawn in a given
spawning season. This procedure used data derived from samples collected in the
Novembers of 1993 and 1994 collectively, and the Novembers in each year between 2007
and 2010, collectively.
3.2.5 Measures of relative abundance
The numbers of A. butcheri caught on each sampling occasion in each season except
winter (see above for rationale), using the 41.5 m seine net at six sites in nearshore,
shallow waters of the upper estuary in different years (Table 3.1), were converted to a
density (fish 100 m-2
). The numbers of fish caught using the multi-mesh gill net at nine
sites in offshore, deeper waters of the upper estuary on each sampling occasion were
expressed as number of fish gill net-1
. Although A. butcheri typically occupies the lower
and saline regions of the tributary rivers, which constitute the upper estuary, many
48
individuals are flushed downstream during winter when freshwater discharge increases
sharply (Sarre & Potter, 1999). The limited data for this season were thus not included in
analyses of the densities and catch rates. Note also that, except in 2000, the mean densities
and catch rates and 95% confidence interval for a ‘year’ were calculated using consecutive
seasonal data for the spring in one year and summer and autumn of the following year and
thus encompass seasons in two consecutive calendar years.
Prior to subjecting the densities and catch rates for the different ‘years’ to Analysis
of Variance (ANOVA), examination of these data demonstrated that both required ln(x+1)
transformations to meet the test assumption of homogeneous dispersions among a priori
groups (see Clarke & Warwick, 2001). If ANOVA detected a significant difference
between the densities and/or catch rates among years (P<0.05), Scheffé’s test was used to
identify where the variable differed significantly between each pair of years.
3.3 Results
3.3.1 Decline in freshwater discharge and relationship with hypoxia
The annual discharge of freshwater entering the upper estuary declined markedly during
the 20 years between 1992 and 2011 (Fig. 3.1, r2=0.35, P<0.01). The influence of this
discharge on oxygen concentrations is reflected in the close relationship between the
annual values for the average extent of hypoxia and discharge (Fig. 3.2, r2=0.50, P<0.005),
reflecting the tight coupling between the persistence of the salt-wedge and freshwater
discharge.
49
Figure 3.1. Freshwater discharge into the Swan River Estuary in the 20 years between
1992 and 2011. Data provided by the Western Australian Department of Water.
Figure 3.2. Relationship between the annual average extent of hypoxia (%) in the upper
Swan Estuary and freshwater discharge between 1995 and 2010. The extent of hypoxia in
each year was estimated by interpolating available oxygen profile data for each sampling
cruise within the study domain for each weekly profile and then averaging the values for
each year.
50
3.3.2 Body condition and growth
The three-parameter model, representing the relationship between the natural logarithms of
body mass and length for females of A. butcheri in the Swan River Estuary in 1993-95 and
2007-11, when using linear equations with a common slope and different intercepts
(NLL=-234.2), provided a better fit than the alternative three-parameter model, which
assumed a common intercept and different slopes (NLL=-234.0). It also provided a
significantly better fit (P<0.001) than the two-parameter model that assumed a common
linear relationship between body mass and length in the two periods (NLL=-217.0). A
further increase in model complexity, by allowing both the intercepts and slopes to differ
(NLL=-234.6), failed to significantly improve the fit (P>0.05). The results for males were
similar to those for females, with the model assuming a common slope and different
intercepts (NLL=-229.6) producing a slightly better fit to the data than that assuming a
common intercept and different slopes (NLL=-229.3) and improving the fit significantly
(P<0.001) over that provided by the model with a common slope and common intercept
(NLL=-216.4). Again, extension of the model to allow both the intercepts and slopes to
differ (NLL=-229.9) failed to significantly improve the fit (P>0.05). Thus, the linear
relationships between the natural logarithms of body mass and total length for each sex in
1993-95 and 2007-10 were best represented by equations with different intercepts and a
common slope (Table 3.2).
The mean values of the allometric condition factors for each sex in 1993-95
differed significantly (both P<0.001) from those in 2007-11 (Table 3.2). As the power
terms of the length-weight relationships for neither sex differed significantly between
1993-95 and 2007-11, the allometric condition factors for fish from the two periods were
directly comparable as a common power term could be employed to calculate their values.
51
Thus, between 1993-95 and 2007-11, the expected values of the allometric condition factor
for females and males declined by 6 and 5%, respectively.
Table 3.2. Estimated values of parameters of relationships ( period period) between
body mass (g) and total length (mm) for Acanthopagrus butcheri collected from the Swan
River Estuary in 1993-95 and 2007-11, with estimates of expected values of the allometric
condition factors for these periods, period, and with bootstrap estimates of 95%
confidence intervals.
Females Males
1993-95 2007-11 1993-95 2007-11
period Estimate 9.370 10-6
8.883 10-6
1.147 10-5
1.086 10-6
Lower 7.603 10-6
7.153 10-6
9.389 10-6
8.921 10-6
Upper 1.152 10-5
1.091 10-5
1.423 10-5
1.350 10-5
period Estimate 3.116 3.116 3.080 3.080
Lower 3.076 3.076 3.040 3.040
Upper 3.155 3.155 3.116 3.116
period Estimate 9.391 10-6
8.851 10-6
1.149 10-5
1.089 10-6
Lower 7.622 10-6
7.170 10-6
9.408 10-6
8.942 10-6
Upper 1.155 10-5
1.093 10-5
1.426 10-5
1.353 10-5
The von Bertalanffy growth curves provided a good fit to the lengths at ages of
females and males of A. butcheri in 1993-95 and 2007-11 (Table 3.3; Fig. 3.4). The curve
for the females in 1993-95 lay above and differed significantly (P<0.001) from that of this
sex in 2007-11 and the same was true for those of males in these two periods (Fig. 3.5).
Furthermore, the growth parameters k and L∞ for each sex differed significantly between
periods (all P<0.001) and were less in 2007-11 than in 1993-95. The values for the t0 of
both sexes were slightly more negative in 2007-11 than in 1993-95 (both P<0.001).
Based on the von Bertalanffy growth parameters, the TLs of female A. butcheri at
ages two and six years were 142 and 248 mm, respectively, in 2007-11 and thus far less
than the corresponding TLs of 203 and 366 mm in 1993-95. Likewise, the estimated TLs
of males of 144 and 235 mm, respectively, at those same ages in 2007-11 were far less
than the corresponding values of 199 and 354 mm in 1993-95.
52
Table 3.3. von Bertalanffy growth curve parameters and their 95% confidence limits for
females and males of Acanthopagrus butcheri caught in the upper Swan River Estuary in
the 1993-95, 2003-04 and 2007-11 periods. L∞, asymptotic total length (mm); k, growth
coefficient (years-1
); t0, hypothetical age (years) at which fish would have zero length; r2,
coefficient of determination. n is the number of fish.
Period L∞ k t0 r2 n
1993-95 Females
Estimate 441 0.29 -0.12 0.94 680
Lower 427 0.27 -0.19
Upper 454 0.31 -0.06
Males
Estimate 424 0.29 -0.19 0.99 754
Lower 413 0.27 -0.26
Upper 436 0.31 -0.13
2003/04 Females
Estimate 322 0.35 -0.13 0.96 111
Lower 284 0.26 -0.21
Upper 371 0.44 -0.06
Males
Estimate 351 0.28 -0.13 0.99 88
Lower 279 0.19 -0.42
Upper 300 0.42 -0.13
2007-11 Females
Estimate 341 0.19 -0.84 0.89 3438
Lower 321 0.17 -0.92
Upper 362 0.22 -0.76
Males
Estimate 288 0.25 -0.76 0.90 3248
Lower 274 0.22 -0.85
Upper 306 0.28 -0.68
The growth curves for the more limited samples for females and males in 2003-04
lay between and differed significantly from those for the corresponding sex in 1993-95 and
2007-11 (Fig. 3.5, all P<0.001). In the case of each sex, the value for k in 2003-04 differed
significantly from that in 2007-11 (both P<0.001), and the same was true for females for
2003-04 vs 1993-95 (P<0.05). The L∞ for females and males in 2003-04 each differed
significantly from that of the corresponding sex in 1993-95 and 2007-11 (all P<0.001),
except with females in 2003-04 vs 2007-11 (P>0.05). The values for t0 in 2003-04 were
significantly different from those for females (P<0.001) and males (P<0.05) in 2007-11.
53
Figure 3.4. von Bertalanffy growth curves for female and male Acanthopagrus butcheri
caught in the Swan River Estuary in 1993-95, 2003-04 and 2007-11.
54
Figure 3.5. Comparisons of von Bertalanffy growth curves for female and male
Acanthopagrus butcheri in the Swan River Estuary in 1993-95, 2003/04 and 2007-11.
3.3.3. Lengths and ages at maturity
The smallest TL of the mature female and male A. butcheri during the spawning period
were 170 and 151 mm, respectively, in 1993-94, and 144 and 143 mm, respectively, in
2007-10. As the prevalence of mature females and males increased with length, the
percentage of mature individuals in each corresponding length class was less in 1993-94
than in 2007-10 (Fig. 3.6). Although the ogive describing the relationship between the
proportion of mature females and total length in 1993-94 was not significantly different
from that for 2007-10 (NLL=75.5 vs 78.7 for a common curve, P<0.05), and the same was
true for males (NLL=56.3 vs 57.9, P>0.05), the L50s at maturity for females and males in
1993-94 (174 and 172 mm) were substantially greater than the 155 and 156 mm for the
corresponding sex in 2007-10 (Table 3.4, Fig. 3.6).
55
Table 3.4 Estimates of the total lengths (mm) and ages (years), and associated 95%
credible intervals, at which 50% (L50 and A50) and 95% (L95 and A95) of female and male
Acanthopagrus butcheri were mature in the Swan River Estuary in 1993-95 and in 2007-
10. ML = Maximum likelihood. Lower and upper credible limits were determined using
OpenBUGS. n is the number of fish.
Period Sex Statistic nlength nage
1993-95 Females ML estimate 174 210 1.9 2.2 156 103
Lower 159 194 1.6 2.0
Upper 187 234 2.0 2.6
Males ML estimate 172 189 2.0 2.1 196 136
Lower 152 175 1.4 1.8
Upper 181 206 2.0 2.2
2007-10 Females ML estimate 155 189 2.5 4.7 422 422
Lower 151 181 2.4 4.4
Upper 161 198 2.7 4.1
Males ML estimate 156 183 2.5 4.5 329 329
Lower 150 176 2.3 4.2
Upper 160 192 2.7 4.9
Only one fish had reached maturity by the end of its first year of life in 2007-10
(Fig. 3.7). However, while most females and males had become mature at the end of their
second year of life in 1993-94, only 56% of females and 35% of males had attained
maturity at this age in 2007-10 (Fig. 3.7). The ogives describing the relationships between
the proportion of mature females and age in 1993-94 and 2007-10 were significantly
different (NLL=82.9 vs 99.7, P<0.001) and the same was true for males (NLL= 55.2 vs
94.8, P<0.001). The A50 of 1.9 years for females at maturity in 1993-94 was less than and
significantly different to the 2.5 years for females at maturity in 2007-10 (P<0.001) and the
same significant trend (P<0.001) was exhibited by the corresponding values of 2.0 and 2.5
years for males at maturity in those periods (Table 3.4, Fig. 3.7).
56
Figure 3.6. Percentage frequency of occurrence of Acanthopagrus butcheri with immature
(white bars) and mature gonads (grey bars) in sequential 20 mm total length classes during
the spawning seasons of this species in the Swan River Estuary in different years. Females
in (a) 1993 and 1994 collectively and (b) 2007-10 and males in (c) 1993 and 1994
collectively and (d) 2007-10. Logistic curves (solid lines) and their 95% credible intervals
(dotted lines) for the probability that a fish at a given length is mature were estimated using
OpenBUGS. Sample size for each length class is shown. Comparisons of logistic curves
for females and males in 1993 and 1994 (solid line) and 2007-10 (dashed line) are shown
in e and f.
57
Figure 3.7. Percentage frequency of occurrence of Acanthopagrus butcheri with immature
(white bars) and mature gonads (grey bars) in sequential ages during the spawning seasons
of this species in the Swan River Estuary in different years. Females in (a) 1993 and 1994
collectively and (b) 2007-10 and males in (c) 1993 and 1994 collectively and (d) 2007-10.
Logistic curves (solid lines) and their 95% credible intervals (dotted lines) for the
probability that a fish at a given age is mature were estimated using OpenBUGS. Sample
size for each length class is shown. Comparisons of logistic curves for females and males
in 1993 and 1994 (solid line) and 2007-10 (dashed line) are shown in e and f.
58
3.3.4 Catch rates in deeper waters and densities in shallow water
ANOVA demonstrated that the mean annual catch rates of A. butcheri, derived from
samples obtained using gill nets at nine sites in offshore, deeper waters, differed
significantly among years (F (5, 186)=4.4, P<0.01). Mean catch rates ranged downwards
from a maximum of 3.7 fish net-1
in 1993-94 to a minimum of 0.3 fish net-1
in 2007-08
(Fig.3.8), with Scheffé’s test showing that the mean catch rates in 1993-94 and in 2007-08
were significantly different (P<0.01).
Figure 3.8. Back-transformed mean and associated 95% confidence intervals for a) catch
rates derived from gill net samples in offshore, deeper waters and b) densities derived from
seine net samples in nearshore, shallow waters of Acanthopagrus butcheri in the Swan
River Estuary in the various years of sampling. Number of samples for each year is shown.
59
The mean densities of A. butcheri, derived from samples obtained using a 41.5 m
seine net at six sites in nearshore waters, differed significantly among years (F(6,
17)=14.2, P<0.001). The mean densities in 1993-94 and 1994-95 were ≤1.0 fish 100 m-2
and thus far less than in 2003-04 and 2007-08 to 2010-11, which ranged from 3.6 to 8.4
fish 100 m-2
(Fig. 3.8). The mean density of fish in 1993-94 and 1994-95 differed
significantly from those in 2003-04, 2007-08, 2008/09, 2009-10 and 2010-11 (P<0.001).
3.4 Discussion
The present study provides the first demonstration that the condition factor, growth and
maturity indices of a fish species, whose entire life cycle is confined to estuaries, have all
changed in association with marked detrimental modifications to the environment.
Furthermore, each change was shown to occur in the direction hypothesised from the
results of other relevant studies (see below) and the model of Stearns (1992). When
considering the implications of the inter-period comparisons of particularly the growth of
A. butcheri, it is important to recognise that the growth curves for 1993-95 and for 2007-11
represent the cumulative effects of the growth of the individuals during those periods and,
in the case of older fish, that which occurred prior to the commencement of those two
periods. The possibility that changes in the biological characteristics of A. butcheri were
induced by an increase in intensity of fishing, as described for a number of other species
(e.g. Sharpe & Hendry, 2009; Devine et al., 2012; Diaz & Heino, 2014), can be rejected
for the following reasons. The small seasonal commercial fishery for A. butcheri in the
Swan River Estuary has been negligible since 2007, due to a government buy-back of
commercial fishing licences (Smith et al., 2014), and the recreational catch per unit effort
data indicate that the abundance of A. butcheri has remained relatively stable since the
early 1990s (Smith, 2006; Smith et al., 2014).
60
3.4.1 Condition and growth
As body condition is a reliable indicator of the health of a fish (Peig & Green, 2009), it is
highly relevant that the allometric condition factor for female and male A. butcheri in the
upper Swan River Estuary declined significantly between 1993-95 and 2007-11.
Furthermore, this decline in condition was accompanied by a marked reduction in the
growth of both sexes, with the growth curve for the intervening 2003-04 period occupying
an approximately intermediate position between the earlier and later periods. Indeed, on
the basis of von Bertalanffy growth parameters, the predicted lengths at two and six years
in age declined between 1993-95 and 2007-11 by as much as 32 and 34%, respectively,
with females, and by 67 and 73%, respectively, with males.
The significant decline in the condition factor and growth of A. butcheri in the Swan
River Estuary between 1993-95 and 2007-11 parallels the observation by Eby et al. (2005)
that the condition and growth of the Atlantic Croaker Micropogonias undulatus in the
Neuse River Estuary was least in years when the extent of hypoxia was greatest. The
results of controlled laboratory experiments, in which M. undulatus was exposed to four
and ten weeks of hypoxia subsequently supported the conclusion that the condition and
growth of this species can be adversely affected by reduced oxygen concentrations (Mohan
et al., 2014). A number of laboratory studies on other fish species have produced similar
results, particularly with growth (e.g. Kramer, 1987; Pichavant et al., 2001; Roberts et al.,
2011). Declines in the condition and growth of fishes exposed to hypoxia have been
attributed, inter alia, to a reduction in metabolism and changes in the quantity and quality
of potential food (Pichavant et al., 2001; Wu, 2002; Eby et al., 2005; Powers et al., 2005).
In the context of food, the volumetric contributions made to the diets of A. butcheri in the
Swan River Estuary by low-calorie food, such as algae, macrophytes and detritus,
increased from 15 to 30% between 1993-95 and 2007-11, whereas high-calorie prey, such
61
as bivalve molluscs, declined from 64 to 19% (cf Sarre et al., 2000; Linke, 2011). These
trends parallel those recorded during studies of M. undulatus in the Neuse River Estuary,
which showed that, following exposure to hypoxia, the density of food and particularly of
bivalves (Macoma spp.) declined and was thus considered to be one of the factors that led
to reductions in the growth (Eby et al., 2005). Unfortunately, there are no quantitative data
to facilitate comparisons between the quantity and quality of the benthic
macroinvertebrates and macroalgae of A. butcheri in offshore and nearshore waters in the
two periods and which are known to constitute the diet of this species (Sarre et al., 2000;
Chuwen et al., 2007).
In the context of factors that could also have attributed to the decline in the
condition and growth of A. butcheri between 1993-95 and 2007-11, it is pertinent that data,
derived from gill and seine net catches, provided strong circumstantial evidence that the
abundance of A. butcheri in offshore, deeper waters has declined, whereas that in
nearshore, shallow waters has increased markedly. This therefore constitutes habitat
compression of the type induced by hypoxia among demersal fish in the Neuse River
Estuary on the east coast of North America (Eby et al., 2005), pelagic fish in tropical
waters in the eastern Pacific (Prince & Goodyear, 2006) and certain species in other
environments (e.g. Pihl et al., 1991; Tyler & Targett, 2007; Craig, 2012). A tendency,
during the past 10 to 20 years, for A. butcheri to have moved from deeper to shallow
waters, and the demonstration that its density in the shallow waters has become far greater,
raises the strong possibility that density-dependent effects may also have played an
important role in leading to a decline in the growth of this species over time. It is thus
noteworthy that density dependent factors were also considered responsible for the decline
in growth of M. undalatus in the Neuse River Estuary (Eby et al., 2005). In addition, the
use of fishery-independent data demonstrated that the growth of the 0+ and 1+ age classes
62
of the Red Drum Sciaenops ocellatus were negatively related to the density of their own
age classes (Bacheler et al., 2012). Furthermore, analysis of long-term records of size at
age and biomass data for 16 fish populations revealed that the growth of individuals in nine
of those populations was inversely related to density (Lorenzen & Enberg, 2002).
3.4.2. Length and age at maturity
As the ogives relating maturity to length in females and to age in both sexes of A. butcheri
differed significantly between 1993-94 and 2007-10, the maturity characteristics of this
species have changed between the two periods. It was particularly striking that, between
1993-94 and 2007-10, the L50 of females and males at maturity both declined by 10%,
respectively, whereas, in contrast, the A50 of females and males at maturity increased by
the equivalent of 32 and 25%, respectively. The direction of the changes between the two
periods is consistent with the model of Stearns (1992), which predicted that reductions in
growth will lead to maturity occurring at a smaller size and older age (see also Chen &
Mello, 1999; Morgan & Colbourne, 1999). This finding is also consistent with the results
of a three year tag-recapture study, which demonstrated that the slower-growing residents
of the White Spotted Charr Salvelinus leucomaenis reached maturity at a smaller size but
older age than faster-growing individuals, a feature considered to reflect adaptive
phenotypic plasticity (Morita & Morita, 2002). For A. butcheri, the changes in both the
length and age at maturity were pronounced and developed within a relatively short period,
highlighting the plasticity of the biological characteristics of this species and thus its ability
to respond to the effects of environmental change.
The dynamic nature of estuaries means that few species are able to complete their
life cycle within these systems. Most of the exceptions are small and short-lived species
and thus mature at a young age and often at the end of the first year of life. The investment
63
of energy to reproduction at an early age is a particularly useful strategy for species that
reside in unpredictable environments and therefore subjected to high natural adult
mortality. This strategy thus enables sufficient offspring to be produced and thereby ensure
the production of future generations. This type of strategy contrast with that of many fish
that reside in stable environments, which are long-lived and mature at an old age. Based on
the relationship between maximum age and age at maturity, derived by Froese and
Binohlan (2000) from 432 populations, a fish with a maximum age of 30 years would, on
average, attain maturity at ~ 9 years of age.
Species, such as A. butcheri, have adopted an intermediate strategy, in
which they mature at an early age but have a relatively long life span (up to ~30 years).
The flexibility of species, such as A. butcheri, to allocate energy into growth and/or
reproduction also allows them to delay maturity, in favour of allocation of energy to
somatic growth, when resources become limited (Grover, 2005). Although delayed
maturation and the resultant increase in generation time can lead to reduced population
growth rates, such a phenomenon is far more pronounced in short-lived than long-lived
species (Bjørkvoll et al., 2012). Thus, as A. butcheri matures at a young age, has a
relatively long life span, and a single large female can produce seven million eggs in a
single spawning season, a delay in maturation would not be likely to have a conspicuous
deleterious effect on population growth. This has helped account for A. butcheri remaining
abundant in the upper Swan River Estuary, even though conditions there have deteriorated
over the past 20 years. In summary, the results of this study demonstrate that the
deleterious changes that have occurred in the environmental conditions of the permanently-
open microtidal Swan River Estuary since the 1990s have been accompanied by significant
changes in certain biological characteristics of A. butcheri. The marked decline in the
condition and growth of A. butcheri is consistent with the established effects of hypoxia,
64
which are known to result in inter alia reductions in metabolism and changes in the
quantity and/or quality of food. The declines in condition and growth between the two
periods are, however, also considered to reflect density-dependent effects as fish have
increasingly tended to aggregate inshore. The reduction in growth would also account for
A. butcheri attaining maturity at a smaller size and older age. The results of this study thus
contribute to our understanding of how, and the extent to which environmental degradation
can influence the biological characteristics of a demersal fish species and will therefore be
of value to fisheries and environmental managers when considering the changes that could
occur with other species exposed to the impacts of a decline in water quality.
65
Chapter 4
Factors influencing the growth of Acanthopagrus butcheri in a eutrophic estuary
have changed over time.
4.1 Introduction
An understanding of the growth of individuals in a fish stock is crucial for determining the
status of that stock and thus for assessing its resilience to fishing pressure (Beverton &
Holt, 1957; Hilborn & Walters, 1992; Quinn & Deriso, 1999; Haddon, 2011). The growth
of fish in a population is traditionally described by fitting a von Bertalanffy growth model
to the lengths at age of individuals in that population, using data collected over several
years (Fabens, 1965; Ricker, 1979; Quinn & Deriso, 1999; Jennings et al., 2009). This
enables the expected lengths at age of fish to be estimated for the period for which lengths
and ages were recorded, irrespective of the extent to which growth varies among years.
The overall von Bertalanffy growth curves of the females and males of the
estuarine species Acanthopagrus butcheri in the Swan River Estuary in south-western
Australia in 1993-95 were compared with those in 2007-11 (Chapter 3). This showed that
growth was less in the latter period, when environmental conditions had declined due to
detrimental effects produced by reductions in freshwater discharge, as a result of declining
rainfall. These detrimental effects included a pronounced increase in the extent of hypoxia
in deeper water, which, on the basis of other studies, would have inhibited the growth of
fish that remained within those waters (Pichavant et al., 2000, 2001; Eby et al., 2005). The
increases in hypoxia also led, however, to the larger A. butcheri tending to move from
deeper waters into the shallow and better oxygenated waters, where, as a consequence,
densities increased markedly, but subsequently remained relatively constant through 2007-
11. It was thus proposed that density-dependent effects made a major contribution to the
66
reduction in the growth of A. butcheri between those two periods. As this reduction
occurred when water temperatures were increasing (Western Australia Department of
Water, 2015), and growth would thus have been expected to increase (Brown et al., 2004),
it was assumed to have been due to factor(s) other than temperature.
Few studies have explored the extent to which the growth of individuals of an
estuarine species, i.e. whose life cycle is completed within the estuary (Potter et al., 2013),
vary either between or within periods in a given system. However, a detailed modelling
study, based on samples collected in 1993-98 and 2003-08, demonstrated that, in south-
eastern Australia, the growth of otoliths of the Estuary Perch Percalates colonorum was
related more closely to temperature than to any of the other variables examined
(Morrongiello et al., 2014). Although the growth of P. colonorum was also related to
freshwater discharge, this effect was not as pronounced as with certain other estuarine
species, such as the Barramundi Lates calcarifer in a tropical estuary, where growth was
greatest under high flow (Robins et al., 2006). In contrast, there were indications that the
growth of the Spotted Seatrout Cynoscion nebulosus in San Carlos Bay, Florida, was
negatively related to freshwater discharge (Bortone et al., 2006). The use of a common
curve to describe the growth of individuals in a particular population, based on data
collected over a period, assumes that, within each year of life, all year classes experienced
the same environmental conditions, density-dependent effects and other factors that
influence growth (Szalai et al., 2003). To take into account possible inter-annual variation
in such conditions, Szalai et al. (2003) employed a von Bertalanffy growth curve with
time-varying parameters to predict the growth increments for each age class in each
successive year. They described annual changes in L∞ as a random walk on the log scale
and assumed that the relationship between L∞ and k was linear, thereby enabling the
parameters of that relationship to be estimated. That model was subsequently modified by
67
He & Bence (2007) to allow each year-specific von Bertalanffy growth parameter to vary
over time and then developed a further model to incorporate a cohort effect as well as a
year effect. When fitting these models, they employed a hierarchical Bayesian approach,
which permitted statistical inferences to be drawn as to the direction and magnitude of any
potential correlations among those parameters.
The first aim of this study was to determine the extents to which the growth of
female and male A. butcheri in the Swan River Estuary varied among years within 1993-95
and 2007-11, the periods for which overall growth had previously been determined
(Chapter 3), but extending the latter period to incorporate data subsequently acquired for
2012-14. A year-effect growth model was thus developed, based on the ‘Fabens year-
effect’ model of He & Bence (2007), but fitted using a simpler maximum likelihood
approach. The resultant data, and those for some intermediate years, were employed to
elucidate how the growth of this sparid changed during more than two decades. The
hypothesis was then tested that, in 2007-14, annual growth in the shallows, where the
majority of fish were now located, was positively related to temperature during the
warmest and main growth phase (late spring to early autumn). The data were also used to
explore whether annual growth in 2007-14 was related to freshwater discharge in the
immediately preceding mid-winter to early spring, when the vast majority of freshwater
discharge occurs.
4.2 Materials and methods
4.2.1 Temperature and freshwater flow
Mean annual values of the maximum daily air temperatures, recorded between 1990 and
2014 at Perth Airport in the vicinity of the Swan River Estuary, were taken from the
68
website of the Australian Bureau of Meteorology (2015). A linear equation was used to
describe the relationship between these temperatures and years. A one-tailed t-test was
then employed to determine whether the Pearson’s correlation coefficient relating
temperature to year was statistically significant and thus confirm that air temperature
increased over that period. The annual freshwater discharges entering the Swan River
Estuary at gauging station 616011, upstream of the study area, in each year between 1990
and 2014 were taken from the website of the Western Australia Department of Water
(2015). A log-linear equation was used to describe the curvilinear relationship between
freshwater discharge and year. Back-transformed predicted values for freshwater discharge
were corrected to account for the bias associated with the log transformation (Beauchamp
& Olson, 1973). A one-tailed t-test was employed to determine whether Pearson’s
correlation coefficient between the log-transformed values of freshwater discharge and
year was statistically significant and thereby confirm that, as previously shown for 1992 to
2011 (Chapter 3), annual freshwater discharge declined between 1990 and 2014.
4.2.2. Sampling regime and processing of fish
Acanthopagrus butcheri was sampled at nine sites in the upper Swan River Estuary (Fig.
3.1 in Chapter 3). Nearshore, shallow waters were sampled using 21.5 and 41.5 m long
seine nets in each season between spring 2007 and winter 2011. Offshore waters were
sampled by gill netting in waters adjacent to each seine net site. Gill netting was
undertaken at the same time (season) as seine netting between spring 2007 and winter
2009, after which it was discontinued as it was catching few fish. Acanthopagrus butcheri
was also caught at intervals between the spring and following winter in 2011 to 2014 using
seine and gill nets in the same region of the upper Swan River Estuary as the above nine
sampling sites.
69
Acanthopagrus butcheri had previously been caught in the upper Swan River
Estuary between spring 1993 and winter 1995 by using the 41.5 m long seine net at six of
the above nine sites in nearshore, shallow waters, and by employing a gill net (comprising
panels of the same dimensions and mesh sizes as described above) at all nine sites in
offshore waters (Sarre & Potter, 2000). Full details of the sampling regime and net
dimensions are given in Chapter 2.2. Additional samples of A. butcheri were collected
irregularly during other studies from the upper Swan River Estuary between spring 2003
and winter 2007.
Throughout the subsequent text, the data for each of the 12 months between the
spring of one year and the winter of the next year (which thus commences when
A. butcheri spawns) is subsequently referred to as a ‘year’, e.g. spring 2008 to winter 2009
is referred to as 2008/09. Note that there were continuous data for the spring to winter
seasons in the seven ‘years’ from 2007/08 to 2013/14, which formed the focus of many of
the comparisons.
Following their capture, A. butcheri were euthanised in an ice slurry and
transported to the laboratory where they were sexed and their total length measured to the
nearest 1 mm. The otoliths of each fish were removed and the growth zones in whole
otoliths counted, when their number was ≤6, and in sectioned otoliths when that number
was >6. The number of growth zones in the otoliths of each fish, together with the birth
date (peak time of spawning) and knowledge of when the new opaque zone becomes
delineated, were used to age that fish. Full details for the rationale for this procedure are
given in Chapter 2.3.
70
4.2.3 Year-effect growth model
The growth model developed in this study, subsequently termed the ‘year-effect model’,
has essentially the same structure as that of He & Bence (2007), but differed as follows. (1)
Deviations from the growth curve are assumed to be normally-distributed, and thus the
predicted lengths at age represent the mean rather than median length at age. (2)
Parameters include the lengths at age of each year-class (except that of the 0+ age class) at
the start of the sampling period during which fish were collected, rather than parameters
for the lengths of fish at a specific age, i.e. 3 years old. (3) The lengths at age zero for fish
that entered the population in the first and subsequent years of sampling were calculated
using the von Bertalanffy growth equation and the growth parameters for that year. (4) The
model was fitted by maximising the log-likelihood rather than employing a hierarchical
Bayesian approach.
The modified year-effect model was used to calculate, separately for each sex,
year-specific growth parameters and expected lengths at different ages in each year. As a
single growth model could not be fitted to the entire series, due to gaps in the data, the
year-effect model was fitted first to the lengths at age of fish collected during 1993/94 and
1994/95 and then to those for each year between 2007/08 and 2013/14.
For the year-effect growth model, t1 and tn denote the first and last year of
sampling, respectively, and A represents the maximum age at the beginning of year t1 for
the year classes of fish present in that year. Note that these fish would be A + n – 1 years
old at the beginning of the last sampling period, i.e. the beginning of year tn. The model
assumes that, within each year t (t1 ≤ t ≤ tn), fish grow in accordance with a von Bertalanffy
growth curve with year-specific growth parameters, L∞t and kt, which represent the
asymptotic length and a coefficient that determines the rate at which fish of a given length
approach that asymptotic length, and t0, the age at which, in theory, the fish would have
71
zero length, and is assumed to be constant for all year classes. The model also assumes that
fish do not undergo negative growth, and that the length at age 0 years of fish within each
year class y, which was recruited to the population during the sampling period, may be
calculated using the von Bertalanffy growth curve and the growth parameters for that year,
i.e. for t = y, and the common value of t0. The initial lengths at the beginning of year t1 of
the fish of year classes already recruited to the population before the first year of the
sampling period, i.e. fish of ages 1 to A years, vary and are represented as the parameters
to .
Let represent the expected length of a fish from year class y at the start of year
t, where and where the age of the fish at that time is years. From the
above assumptions, it follows that if , otherwise
( )[ exp( )]. It also follows that, when captured at
decimal age years, the length of the j’th fish, which was of year class , may be
estimated as ⌊ ⌋ if ⌊ ⌋ ⌊ ⌋, otherwise
⌊ ⌋ ( ⌊ ⌋ ⌊ ⌋ ) { exp [ ⌊ ⌋( ⌊ ⌋)]}, where the
year in which the fish is caught is calculated as ⌊ ⌋, and where ⌊ ⌋ represents the
‘floor’ function of x, i.e. the greatest integer less than or equal to x. The above equation
represents the expected length following a period of growth of ⌊ ⌋ years from
an initial length ⌊ ⌋ at the start of year t, where growth is in accordance with a von
Bertalanffy growth model with the growth parameters for the year of capture, i.e. ⌊ ⌋
and ⌊ ⌋. For year classes to , { exp[ ]} where is
common. Finally, for year classes ,
When fitting the above model, the log-likelihood (LL) was calculated assuming that
the observed length at age of each fish at its date of capture was normally distributed, with
72
common variance, about the estimated length at age at that date. The parameters estimated
when fitting the model comprised the year-specific values of and (where
), a common value of , and the initial lengths for .
For each set of lengths at age for each sex in 1993-95 and 2007-14, a traditional
von Bertalanffy growth curve, with parameters , k and , was first fitted by maximizing
LL. The year-effect model was then fitted, using common values for and k for each year
and a common , to obtain estimates of the parameters for the initial lengths for
. ‘All subsets regression’ (Berk, 1978) was then used to identify the model with
year-specific values of and which, as parameters were successively added (while
retaining common values for and k for the remaining years), provided the best
representation of the lengths at age at each successive level of increasing complexity, i.e.
with A + 4, A + 5, …, A + 2n +1 parameters. With the addition of each parameter, the
Akaike Information Criterion (AIC) of the best fitting model at each level of complexity
was compared with that of the best fitting model at the previous level of complexity. The
model with the smaller AIC value was accepted as the better of the two models. AIC was
calculated as AIC = 2np - 2LL, where np is the number of parameters.
The observed lengths at age of each year class within each yearly sample were
resampled (with replacement) to produce samples of the same size as in the original data
for that year class. The resampled data for the different year classes were then combined
and the model fitted (as described above) to the resultant data set. This bootstrapping
process was repeated 1000 times. The approximate 95% confidence limits for the
parameters and estimated length of fish within each year class at each age were taken as
the 2.5 and 97.5 percentiles of the estimates produced by the resampling procedure. The
means of the predicted lengths were plotted against the means of the observed lengths at
age of the 2+, 3+ and 4+ age classes, which had each passed through two or more summers
73
of growth and were represented by substantial numbers, to demonstrate that the model
provided a good representation of the data.
A simulation study was used to confirm that, for each sex in 1993-95 and 2007-14,
a model of the form described above was capable of producing reliable parameter
estimates when applied to the type of data recorded for A. butcheri in the Swan River
Estuary. Thus, the model was fitted to simulated lengths at age to test whether it could
recover the specified ‘true’ values of the model parameters used to generate the simulated
data. Simulated lengths at age were generated for each of the observed ages at capture of
the fish within each year class in each annual sample, assuming that these lengths were
normally distributed about the mean lengths at age calculated using the different values of
L∞ and k for each year and a common standard deviation. The values of these parameters
and the standard deviation of ‘observed lengths at age’ about the predicted lengths at age
were those that had been determined when first fitting the year-effect model to each sex
within each period. The same sample sizes for each year class within each annual sample,
as in the original data set, were used when generating each simulated data set. The process
was repeated for 1000 simulated data sets and the resultant parameters compared with the
parameters employed to generate the data. Overall percentage bias was estimated
separately for L∞, k and the parameters representing the initial lengths for each sex and
each period as [∑ ( ( ) )
] ⁄ , where is the specified value
for parameter i and is the mean of that parameter estimated for the n = 1000 simulated
data sets. Percentage Root Mean Square Error (%RMSE) of that estimate was calculated as
∑ √
∑ (( ) ⁄ )
.
74
4.2.4 Relationship between growth and temperature and freshwater discharge
The year specific growth parameters were used to calculate annual length increments for
females and males of A. butcheri in each year in 2007/08 to 2013/14. The length (growth)
increments were calculated for fish with a TL of 115 mm, the approximate TL attained at
the end of the first year of life. Mean annual growth increments were plotted against the
mean annual values of the maximum daily air temperatures in the months between
November and March, i.e. warmest part of the year and when growth mainly occurs, and
against mean freshwater discharge in the immediately preceding months of June to
September, i.e. when the vast majority of rainfall occurs. A one-tailed t-test of the Pearson
correlation coefficient was used to test whether annual growth increments between
2007/08 and 2013/14 were positively related to temperature as hypothesised and a two-
tailed t-test employed to test whether those increments were related to freshwater
discharge, for which there was no clear hypothesis.
4.3 RESULTS
4.3.1 Temperature and freshwater discharge
Mean annual values of the maximum daily air temperatures increased progressively and in
an essentially linear manner between 1990 and 2014, with the least value of 23.5°C
recorded in 1990 and the greatest of 26.1°C in 2010 (Fig. 4.1, r = 0.73, P<0.001). The
linear equation relating temperature (T) to year (Y) was T = 0.07Y – 109.5 and thus mean
annual values of the maximum daily air temperatures increased on average by 0.07°C y-1
over that period. Conversely, the mean annual freshwater discharge decreased in an
exponential fashion with year (Fig. 4.1), as described by the log-linear equation relating
freshwater discharge (D) and year, i.e. ln(D) = -0.08Y + 159 (r = -0.63, P<0.001). Mean
annual freshwater discharge ranged from 5.6 to 21.9 m3s
-1 between 1990 and 1999, from
75
2.6 to 9.4 m3s
-1 between 2000 and 2009 and never exceeded 4.8 m
3s
-1 between 2010 and
2014.
Figure 4.1 Mean annual values of the maximum daily air temperatures, recorded at Perth
Airport in the vicinity of the Swan River Estuary (Australian Bureau of Meteorology,
2015), and mean annual freshwater discharge, recorded at gauging station 616011
upstream of the study area (Western Australian Department of Water, 2015) in each year
between 1990 and 2014. The fitted lines are also displayed.
4.3.2 Model parameter selection and simulation
The inclusion of parameters representing the initial lengths of the females and males of
A. butcheri with ages ≥ 1 year at the start of 2007-14 resulted in better fits of the model to
the lengths at age for both sexes than when using traditional von Bertalanffy growth
models for that period. Thus, the inclusion of the initial length parameters led to the AIC
decreasing from 37384 to 36961 for females and from 35836 to 35489 for males. The AICs
for females in 2007-14 continued to decline with the addition of nine of the twelve year-
specific growth parameters (L∞s and ks) for those years (AIC = 36203, Tables 4.1, 4.2) and
the same trend was true for males with the addition of ten of the twelve year-specific
growth parameters (AIC = 34710).
76
Table 4.1 Year-specific von Bertalanffy growth parameter estimates, derived by fitting a
year-effect growth model to the lengths at age of females and males of Acanthopagrus
butcheri caught in the Swan River Estuary in 2007-14 and 1993-95. Approximate lower
and upper 95% confidence limits were derived by bootstrapping. Italics are used to
designate parameters that remained common among years.
Females
von Bertalanffy parameters
Males
von Bertalanffy parameters
Year k (y-1
) L∞ (mm) t0 (y) k (y-1
) L∞ (mm) t0 (y)
2007/08 Average 0.32 318 -0.43 0.34 301 -0.44
Lower 0.29 271 -0.39 0.25 273 -0.52
Upper 0.37 340 -0.47 0.36 332 -0.42
2008/09 Average 0.52 192 -0.43 0.51 193 -0.44
Lower 0.36 187 -0.39 0.38 187 -0.52
Upper 0.55 243 -0.47 0.54 236 -0.42
2009/10 Average 0.14 582 -0.43 0.20 417 -0.44
Lower 0.11 413 -0.39 0.16 338 -0.52
Upper 0.21 717 -0.47 0.26 509 -0.42
2010/11 Average 0.43 282 -0.43 0.34 340 -0.44
Lower 0.29 252 -0.39 0.25 324 -0.52
Upper 0.51 379 -0.47 0.36 423 -0.42
2011/12 Average 0.32 318 -0.43 0.57 236 -0.44
Lower 0.29 271 -0.39 0.45 192 -0.52
Upper 0.37 340 -0.47 0.98 258 -0.42
2012/13 Average 1.03 161 -0.43 0.98 165 -0.44
Lower 0.75 117 -0.39 0.77 122 -0.52
Upper 3.68 187 -0.47 2.47 179 -0.42
2013/14 Average 0.32 280 -0.43 0.34 269 -0.44
Lower 0.29 249 -0.39 0.25 258 -0.52
Upper 0.37 308 -0.47 0.36 329 -0.42
1993/94 Average 0.42 373 -0.14 0.20 451 -0.54
Lower 0.35 352 -0.24 0.14 399 -0.78
Upper 0.49 403 -0.06 0.26 546 -0.36
1994/95 Average 0.42 373 -0.14 0.32 451 -0.54
Lower 0.35 352 -0.24 0.20 399 -0.78
Upper 0.49 403 -0.06 0.42 546 -0.36
77
Table 4.2 Parameters representing the initial lengths ( ) of the females and males of
Acanthopagrus butcheri with ages ≥ 1 year at the start of 2007-14 and 1993-95. Gaps
denote no fish of that age class.
2007-14 1993-95
Age (years) Females (mm) Males (mm) Females (mm) Males (mm)
1 106 105 110 138
2 135 132 208 212
3 165 163 268 257
4 205 190 329 310
5 246 214 316
6 274 235 364
7 311 288 387
8 375
9 377
10 397
As with 2007-14, the inclusion of parameters representing the initial lengths of the
females and males of A. butcheri with ages ≥ 1 year at the start of 1993-95 improved the
model fits for both sexes beyond those produced by traditional von Bertalanffy growth
models (AIC = 5491 vs 5543 for females and 6059 vs 6074 for males). In contrast to 2007-
14, however, the inclusion of separate year-specific L∞s and ks for females in the model did
not further improve the fit in 1993-95. The inclusion of separate year-specific ks, but not
L∞s (Table 4.2), did improve slightly, however, the fit of the model for males in 1993-95
(AIC = 6054 vs 6059).
As demonstrated by the overall absolute percentage biases and %RMSEs, the year-
effect model estimated accurately the year-specific parameters and the initial length
parameters for both sexes and periods (Table 4.3).
78
Table 4.3 Overall percentage bias and percentage root mean squared error (%RMSE) in
model estimates of the year-effect growth parameters L∞, k and initial length parameters
( ) at the start of each sampling period for female and males of Acanthopagrus butcheri ≥
1 year in the Swan River Estuary in 1993-95 and 2007-14.
Females Males
Parameter %Bias %RMSE %Bias %RMSE
L∞2007-14 (mm) -1.58 3.41 1.21 3.03
k2007-14 (y-1
) 2.91 5.64
-3.39 7.14
L∞1993-95 (mm) -0.30
0.42 -1.15
1.62
k1993-95 (y-1
) -0.13 0.19 0.01 0.14
Length parameters2007-14 (mm) 0.14 0.23 -0.03 0.04
Length parameters1993-95 (mm) 0.12 0.20 0.01 0.04
4.3.3 Model results
The lengths at age predicted by the year-effect model for females and males of A. butcheri
in the two years in 1993-95 and seven years in 2007-14 did not exhibit any conspicuous
systematic deviations from the observed lengths at age (Fig. 4.2). There were, however,
discontinuities between the curves describing the lengths at age of successive age classes
in each year (i.e. 12 month interval). These discontinuities reflect the fact that the growth
of fish of a particular age varies among years and thus fish of the same age attain different
lengths in the different years. For example, for females at 4.0 years of age, the predicted
mean length of 217 mm in 2010/11 was greater than the 192 mm in 2009/10 (Fig. 4.2). The
inter-annual variations in lengths at age are reflected in differences in both of the year-
specific von Bertalanffy growth parameters (k and L∞) for each sex in 2007-14 (Table 4.1).
Thus, for example with females, the mean values for k ranged from 0.14 to 1.03 y-1
and
those for L∞ ranged from 161 to 582 mm.
79
Figure 4.2 Lengths at age of females and males of Acanthopagrus butcheri caught in the
Swan River Estuary in the two years in 1993-95 and four years in 2007-11 and the lengths
at age predicted by the fitted year-effects growth model.
80
The means of the lengths at age of capture of females and males of A. butcheri of
the 2+, 3+ and 4+ age classes in each year, predicted by the year-effect growth models in
the 1993-95 period, were greater than in each of the seven years in 2007-14 (Fig. 4.3).
Thus, for example, the means of the predicted lengths for 2 year old females in 1993/94,
i.e. 241 mm, and 1994/95, i.e. 214 mm, were greater than in each of the seven years in
2007-14, which ranged from 145 to 202 mm. Moreover, the differences between the means
of the predicted lengths for 1993-95 and 2007-14 increased with age. For example, in the
case of females, the means of the predicted lengths for 1993/94 and 2007/08 differed by 70
mm for 2 year old fish and by 127 mm for 4 year old fish (Fig. 4.3).
The means of the predicted lengths at age of capture for females and males of
A. butcheri of the 2+, 3+ and 4+ age classes in each year in the 1993-95 and 2007-14
periods were very similar to the corresponding means of the observed lengths at capture
(Fig. 4.3). The means of the observed lengths of each age class of fish in the intervening
years between 1993-95 and 2007-14 (for which the data were obtained using a slightly
different sampling regime and thus not included in the year-effect model) declined in a
manner consistent with the trends exhibited by the means of the predicted and observed
lengths of those age classes in the preceding and subsequent years (Fig. 4.3). The mean
observed lengths for each age class followed a smooth trend over the 21 years of sampling.
Thus, the means of the observed lengths of both sexes declined progressively from 1993-
95 to ~2007/08 and then rose until ~2011/12, before declining again in 2013/14. For
example, with 4 year old females, the means of the observed lengths decreased from >300
mm in the 1990s to 192 mm in 2007/08 and then rose to 233 mm in 2012/13 before falling
to 215 mm in 2013/14 (Fig. 4.3).
81
Figure 4.3 Mean lengths at age of female and male Acanthopagrus butcheri (and 95%
confidence intervals) for sequential age classes caught in each year in the 1993-95 and
2007-14 periods, as predicted by the year-effect growth models (closed circles) and for the
observed lengths at age at capture (open circles). Mean observed lengths at age (and 95%
confidence intervals) for the smaller samples of fish collected in 2003/04, 2004/05,
2005/06 and 2006/07 are also shown.
82
On the basis of the growth parameters of the year-specific growth model and an
initial length of 115 mm (the average predicted length at the completion of the first year of
life), female A. butcheri increased in length by 88 mm in both 1993/94 and 1994/95 (Fig.
4.4). These annual increments were greater than those estimated for females in each of the
seven years in 2007-14, which ranged from 29 to 63 mm. The trends exhibited by the
annual length increments by males followed a very similar pattern, with the annual
increment of 63 mm in 1993/94 and 82 mm in 1994/95 being greater than in each year
between 2007-14, apart from 2010/11 in which the maximum value of 64 mm was
virtually the same as in 1994/94 (Fig. 4.4).
Figure 4.4 Mean values (and 95% confidence intervals) for predicted annual increases in
the lengths of one year old females and males of Acanthopagrus butcheri during each year
in the 1993-95 and 2007-14 periods, using a common starting length of 115 mm, the
average length of fish when they commence their second year of life.
83
4.3.4 Relationship between growth and temperature and freshwater discharge
The predicted annual growth increments for A. butcheri in the years between 2007/08 and
2013/14, based on a length of 115 mm at the commencement of each year, were positively
correlated with mean annual values of the maximum daily air temperatures in each month
between November to March with both females (Fig. 4.5, r =0.68, P<0.05) and males (Fig.
4.5, r = 0.77, P<0.05). The same growth increments were not significantly correlated with
freshwater discharge in the preceding months of June to September, i.e. when the vast
majority of rainfall occurs, in the case of either the females (Fig. 4.5, r = 0.26, P>0.05) or
the males (Fig. 4.5, r = - 0.01, P>0.05).
Figure 4.5 Relationship between annual growth increments for females and males of
A. butcheri between 1 October and 30 September in each year of 2007/08 to 2013/14 and
(a, b) mean annual values of the maximum daily air temperatures in each month between
November and March and (c, d) mean of the daily freshwater discharge between June and
September. Linear equations relating growth increments to temperature are shown.
84
4.4 DISCUSSION
The year-effect model, developed for this study, provided a better description of the
growth of female and male Acanthopagrus butcheri in the Swan River Estuary in the two
years in 1993-95 and seven years in 2007-14 than that produced by the traditional von
Bertalanffy growth model. It thus enabled an exploration of whether the growth in different
years was significantly related to environmental variables that had been selected because
they were known to influence growth in other species. Such an approach allowed factors
that influence growth to be identified, without specifying the precise functional
relationships required to include these factors as covariates in a growth model (Szalai et
al., 2003; He & Bence, 2007).
The year-effect model demonstrated that the growth of both sexes of A. butcheri in
this estuary varied markedly among years in 2007-14, the period for which there were data
for a number of sequential years. These inter-annual differences are emphasised by the
discontinuities in the growth trajectories derived for sequential age classes in each year
from the year effect model. The differences in growth reflect the plasticity of certain
biological characteristics of A. butcheri and its ability to respond to changes in
environmental conditions. This type of plasticity in this species and other sparids is also
reflected in the marked differences between the biological characteristics of such species in
different water bodies in the southern hemisphere (e.g. Sarre & Potter, 2000; Griffiths et
al., 2002; Partridge et al., 2004; Chuwen et al., 2007; Sim-Smith et al., 2012; Wakefield et
al., 2015).
As A. butcheri was not sampled in eight of the years between 1994/95 and 2007/08
and sampling for the other four years in that period was opportunistic, the year-effect
model was not applied to the lengths at age for fish in this period. It is highly relevant,
however, that the mean lengths predicted for an age class in 1993/94 and 1994/95 and in
85
each year between 2007/08 and 2013/14 were very similar to the means of the observed
lengths for those age classes in each of those years. Thus, the means of the observed
lengths for the years in the intervening period in which sampling was conducted are
considered broadly representative of those that would have been derived from the year-
effect model, if sufficient data had been available to construct a reliable model.
Consequently, the decline in the means of the observed lengths at age for the 2+, 3+ and 4+
age classes, from their maxima in 1993/94 to their minima in 2007-10, followed by a slight
rise and then decline to 2013/14, reflect a genuine smooth pattern of change in the growth
of A. butcheri over more than two decades.
The smoothness of the changes may be due to growth being continuous over years
rather than changing abruptly at intervals, with the means of the observed lengths of each
age class of A. butcheri representing the cumulative effect of the present and past growth
of the individuals constituting each age class. In contrast, the mean annual growth
increments, predicted by the year-effect model for a fish with a TL of 115 mm at the
beginning of each year, represent the amount of growth of a fish during the ensuing year.
The greater annual growth increments recorded for females and almost invariably males in
1993/94 and 1994/95 than in any year between 2007/08 and 2013/14 are consistent with
the trends exhibited by the means of the observed lengths over more than two decades.
The above trends emphasise that the growth of A. butcheri in the Swan River
Estuary declined between the early 1990s and more recent years and are thus entirely
consistent with the differences recorded previously for overall growth, based on the lengths
at age data for 1993-95 and 2007-11 (Chapter 3). As temperature increased markedly
between 1993-95 and 2007-14, the decline in growth runs counter to the relationship
recorded with temperature for many species and is inconsistent with the metabolic theory
86
of ecology (Brown et al., 2004; Angilletta et al., 2004; Weber et al., 2015). Temperature is
thus not considered responsible for the decline in growth between periods.
The years between 1993-95 and 2007-11 were accompanied by a decline, not only
in growth, but also in body condition and length at maturity and by an increase in age at
maturity (Chapter 3). These changes were consistent with those which, on the basis of
studies of other species, would be expected if the environment had undergone deleterious
changes (Stearns, 1992; Eby et al., 2005; Morita & Fukuwaka, 2007). It was thus highly
relevant that the deeper waters of the upper Swan River Estuary became increasingly
hypoxic between 1993-95 and 2007-11 (Chapter 3), which would presumably have led to a
decline in the metabolic rate of A. butcheri and thus account, in part, for the decline in
growth and changes in maturity schedules. As the abundance of large A. butcheri in deeper
waters, the typical habitat of these individuals, declined markedly between these two
periods, whereas that in nearshore, shallow waters increased sharply, hypoxia is also
assumed to have led to large fish moving from deep waters to the better oxygenated
nearshore shallow waters. It was thus proposed that the marked increase in density in
nearshore waters resulted in a density-dependent inhibitory effect on growth and changes
in the other biological characteristics listed above.
In contrast to the marked increase in the densities of A. butcheri in the shallow
waters of the estuary between 1993-95 and 2007-11, the mean densities in those nearshore
waters remained similar throughout the four years in the latter period and that trend
continued through to the end of the present study in 2014 (A. Cottingham unpublished
data). The marked inter-annual variations in growth in 2007-14 were thus presumably
attributable to factor(s) other than density. It is therefore relevant that, in 2007-14, the
annual growth increments of both the females and males of A. butcheri, during their second
year of life, were significantly correlated with temperature, which is consistent with the
87
trends exhibited by many fish species and predictions based on the metabolic theory of
ecology regarding growth rates of younger fish (Brown et al., 2004; Angilletta et al., 2010;
Neuheimer et al., 2011). It also parallels the results of a study by Morrongiello et al.
(2014), which demonstrated that the growth of the Estuary Perch Percalates colonorum in
south-eastern Australia was related more closely to temperature than to any of the other
variables examined.
Freshwater inflow into an estuary has often been regarded as important in
influencing the biological characteristics of a fish species in estuaries (Gillanders &
Kingsford, 2002; Robins et al., 2006; Bortone et al., 2006; Glover et al., 2013). For
example, it supplies nutrients which promote primary and thus secondary productivity,
thereby enhancing the growth of fish in these systems (Darnaude, 2005). It is therefore
relevant that the growth, and also condition, of A. butcheri in the Swan River Estuary, were
greater in 1993-95 than in 2007-11 and thus when freshwater discharge was significantly
greater (Chapter 3). In this case, however, the beneficial effects arise from greater flushing
in 1993-95 and thus the removal of excessive amounts of nutrients and a reduction in the
levels and extent of hypoxia in this eutrophic estuary. The present study demonstrated that,
in the shallows of this estuary in 2007-14, when flow remained relatively low and the
densities of A. butcheri were relatively constant, the annual growth increments of one year
old fish were not significantly correlated with freshwater discharge in June to September,
when the vast majority of discharge occurs. Although Morrongiello et al. (2014) found that
the growth of P. colonorum was related to freshwater discharge, this relationship was far
less influential than temperature.
In summary, the year-effect model demonstrated that the growth of both female and
male A. butcheri varied among successive years within a seven year period (2007-14). The
results also demonstrated that, over those seven years, the growth of both sexes of
88
A. butcheri was related to temperature, but not to freshwater discharge. The overall growth
and other biological characteristics of A. butcheri have previously been shown to decline
between 1993-95 and 2007-11, during which there was a marked deterioration in
environmental conditions and particularly in deeper waters, which became increasingly
hypoxic. It was proposed that the resultant increased aggregation of A. butcheri in the
better oxygenated nearshore shallow waters led to a density dependent effect on the growth
and associated characteristics of this species. This decline in growth was unlikely to be
related to temperature as this variable increased between those two periods. Thus, the
factors proposed as influencing growth between 1993-95 and 2007-11, i.e. hypoxia and
density-dependent effects, differed from the major factor, i.e. temperature, that influenced
the growth of A. butcheri over the seven years between 2007 and 2014.
As A. butcheri is confined to its natal estuary for the whole of its life cycle, the
individuals of this species are exposed, throughout life, to any ongoing deleterious changes
in the environmental quality within the estuary. This feature, allied with its plastic
biological characteristics, makes A. butcheri an ideal candidate for exploring the ways and
extent to which certain key biological characteristics of a fish species respond to
detrimental and other changes in its environment. This species thereby serves as a valuable
indicator of the health of an estuary and for hypothesising on the effects of climate change.
89
Chapter 5
Performance and contribution to commercial catches and egg production
by restocked Acanthopagrus butcheri in the Blackwood River Estuary.
5.1 Introduction
Restocking is increasingly being used to restore fish stocks that have become depleted
through over-exploitation and to meet the global demand for seafood (e.g. Bell et al., 2006;
Gomez & Mingoa-Licuanan, 2006; Strøttup et al., 2008; Loneragan et al., 2013).
Furthermore, certain fish stocks have been enhanced through the introduction of cultured
fish. For example, the several million Japanese Flounder Paralichthys olivaceus and Red
Sea Bream Pagrus major, which had been hatchery-reared and released into Kagoshima
Bay, Japan, contributed 26 and 36% to the commercial catches of those two species in that
bay (Kitada & Kishino, 2006). In Australia, the ~350,000 Sand Whiting Sillago ciliata and
86,000 Dusky Flathead Platycephalus fuscus, which were hatchery-reared and released as
juveniles into the Maroochy Estuary, Queensland, subsequently contributed as much as 52
and 28%, respectively, to the commercial catches of those two species in that system
(Butcher et al., 2000).
The use of restocking overcomes the need to impose politically and socially less
acceptable options for the recovery of a depleted stock, such as reducing size limits and
total allowable catch and closing areas to fishing (Travis et al., 1998; Bell et al., 2006).
Many culture and release programmes have failed, however, to demonstrate that they
increased the yield or abundance of the stock (Blankenship & Leber, 1995; Hilborn, 1998;
Bell et al., 2008). The introduction of the cultured fish of a species can have, however, a
negative effect on the wild population of that species through, for example, increasing
90
inbreeding, introducing diseases and leading to a decrease in the abundance of wild fish
(Einum & Fleming, 2001; Lorenzen et al., 2012; Camp et al., 2014).
Restocking is a particularly useful method of replenishing a depleted stock of those
species that complete their life cycle within estuaries or inland waters and whose stocks
cannot thus be augmented naturally by recruitment from outside that system (Lenanton et
al., 1999; Taylor et al., 2005; Ward, 2006). Furthermore, if restocking does have a
deleterious impact on the genetic composition of a species in such water bodies, it is
restricted to the population within the system into which the individuals were introduced
(Potter et al., 2008).
The Black Bream Acanthopagrus butcheri is a very important recreational fish
species in the estuaries of southern Australia and is fished commercially in some of these
systems (e.g. Lenanton & Potter, 1987; Jenkins et al., 2010; Chapter 3). This sparid, which
can live for ~30 years (Morison et al., 1998; Potter et al., 2008), completes its life cycle
within its natal estuary and typically spends most of the year within its upper reaches,
where it spawns during spring and early summer (Potter & Hyndes, 1999; Sarre & Potter,
1999; Williams et al., 2013; Chapter 3).
Several stocks of A. butcheri in south-western Australia were reported by Lenanton
et al. (1999) to have become depleted. It is not clear, however, whether increased fishing
pressure and/or environmental changes were responsible for the decline in the abundance
of this species in the Blackwood River Estuary, which supports a recreational fishery and a
small commercial gill net fishery (Prior & Beckley, 2007; Potter et al., 2008). As the
recruitment of A. butcheri into a population can be highly episodic, the recreational and
commercial fisheries in some systems rely almost entirely on a few year classes (Morison
et al., 1998). Concern for the status of the stock of A. butcheri in the Blackwood River
Estuary led to a study aimed at determining the efficacy of using restocking to replenish
91
the population of this species in this system (Potter et al., 2008). Brood stock from this
estuary were thus used in 2001 and 2002 to culture juveniles, whose otoliths were stained
with alizarin complexone to allow these fish to be distinguished from the wild stock in
samples collected in years following their release (Potter et al., 2008). This marking
method has been successfully employed with other species, such as the Chum Salmon
Oncorhynchus keta and the Pink Salmon Oncorhynchus gorbusha (Sato et al., 2011) and
the Black Rockfish Sebastes schlegeli (Nakagawa et al., 2007).
The results of sampling A. butcheri in the Blackwood River Estuary in the period
up to November 2005 indicated that, in comparison with wild fish, the cultured fish had
not grown quite as rapidly. Furthermore, in contrast to the wild stock, approximately 33%
of restocked fish at four years old had not reached maturity (Potter et al., 2008). It was
suggested that these small disparities may have been related to the effects of hatchery-
rearing. The data did show, however, that, by 2005, a few cultured fish had reached the
minimum legal length (MLL) of 250 mm for the retention of this sparid by commercial and
recreational fishers.
Examination of individuals in fishery-independent samples and in commercial gill
net catches of A. butcheri in the Blackwood River Estuary, during the nine years that
followed the completion of the earlier study in 2005, demonstrated that the alizarin
complexone stain remained prominent in the otoliths of restocked fish throughout that
period and that cultured fish were contributing to the commercial fishery. Biological data
from the earlier study and recent periods were thus collated to compare statistically the
biological performance of cultured and wild A. butcheri, which had coexisted for more
than a decade, and to estimate the relative contribution of cultured and wild stock
A. butcheri to commercial catches. The combined data were used to determine whether,
when comparisons were made using data collected over more than a decade, (1) the
92
restocked fish grew less rapidly than wild stock fish, and the extent and significance of any
differences; (2) all surviving restocked fish eventually became mature and, if so, determine
whether the length and age at maturity of restocked fish differed from those of the wild
stock; (3) restocked fish made a substantial contribution to successive annual commercial
catches of A. butcheri and the extent of any such contributions, and (4) restocked fish
eventually made a major contribution to egg production and if there was strong
circumstantial evidence that the progeny of the restocked fish could have contributed to
commercial catches.
5.2 Materials and Methods
5.2.1 Collection of restocked and wild Acanthopagrus butcheri
Fifty-six female and 50 male A. butcheri were collected from the Blackwood River Estuary
and taken to the Australian Centre for Applied Aquaculture Research, Challenger Institute
of Technology, where they were maintained under light/dark and temperature conditions
that paralleled those in the estuary. When these fish became mature in the springs of 2001
and 2002, i.e. at the same time as A. butcheri spawns in the estuary, they were used as
brood stock for culturing A. butcheri (Potter et al., 2008). Fertilised eggs were produced by
simultaneously stripping all females and males and subsequently by the natural spawning
of these individuals on the following day.
The larvae and juveniles were reared as reported in Partridge et al. (2004) and the
otoliths of all juveniles were stained with alizarin complexone as described in Potter et al.
(2008). The 70,000 juveniles cultured in 2001 were released into the Blackwood River
Estuary at ~ seven months old in winter 2002, while the 150,000 reared in 2002 were
released at ~ four months old in autumn 2003 (Potter et al., 2008). During subsequent
93
sampling, these cultured individuals were clearly identifiable through the purple colour
produced in the central region of their otoliths by the alizarin complexone stain.
In the earlier study, the results of which were reported in Potter et al. (2008),
restocked and wild stock A. butcheri were obtained from the upper Blackwood River
Estuary (Fig. 5.1) by fishery-independent gill netting at regular intervals between 2000 and
2005 (Table 5.1). The composite sunken gill net used by Potter et al. (2008), which
comprised six 20 m long and 2 m high panels, each containing a different mesh size, i.e.
38, 51, 63, 76, 89 and 114 mm, was set at dusk and retrieved at first light on the following
morning. Fishery-independent samples were also obtained in 2006, using gill nets with the
same dimensions as described above, and in 2013 and 2014, but with two additional panels
being added with mesh sizes of 102 and 127 mm (see Chapter 2.2 for details of gill net).
Samples were also collected using a 41.5 m seine net in 2000-05, 2012 and 2014 and by
rod and line fishing in 2000-05 and 2012-14 (Table 5.1). The dimension of the 41.5 m
seine net is given in detail in Chapter 2.2.
Random subsamples of the catches of A. butcheri taken by the commercial gill net
fisher in the Blackwood River Estuary were obtained annually between 2005 and 2014,
except for 2008 and 2011. The commercial (sunken) gill net was 20 m long and 2 m high
and made of 105 mm stretched mesh, which was chosen by the fisher so that it essentially
caught only fish with total lengths ≥ 250 mm, the MLL. While fishery-independent
sampling was undertaken at different times of the year (Table 5.1), the commercial fisher
set his gill net in winter and spring to catch A. butcheri as they are flushed downstream by
the heavy freshwater discharge that occurs at that time of the year (Potter et al., 2008). The
commercial subsamples were provided as frames (i.e. with fillets removed), together with
their intact gonads.
94
Figure 5.1 Map showing the six sites at which Acanthopagrus butcheri was sampled in
the Blackwood River Estuary by fishery-independent methods (open circles) and the
stretch of the estuary in which the commercial gill net fisher operated. Arrow in insert map
location of the Blackwood River Estuary in Western Australia.
The sampling and collection of data on restocked and wild A. butcheri in the
Blackwood River Estuary between 2009 and 2014 were undertaken as part of the work for
this thesis, as were all analyses of data collected during the full duration of this project. As
mentioned previously, the results of sampling prior to 2005 were reported in Potter et al.
(2008), while the previously unanalysed data for 2005 to 2009 were obtained as an
extension of that earlier study.
95
Table 5.1 Numbers of Acanthopagrus butcheri caught by fishery-independent sampling
and in subsamples obtained by commercial gill netting in the Blackwood River Estuary
between 2000 and 2014. Unless otherwise stated, the fishery-independent gill net
comprised eight 20 m long panels, each with a different mesh size, i.e. 38, 51, 63, 76, 89,
102, 114 and 127 mm. Data for 2000-05 were reported in Potter et al. (2008). n is number
of fish.
Year Season Method n
2000-05 All Fishery independent gill net (38-89 & 114 mm),
seine net and rod & line
1451
2005 Winter Commercial gill net 271
2006 Winter
Winter
Commercial gill net
Independent gill net (38-89 &114 mm)
103
102
2007 Winter/spring Commercial gill net 344
2009 Winter/spring Commercial gill net 383
2010 Winter Commercial gill net 290
2012 Autumn-spring
Summer
Commercial gill net
Independent seine net & rod & line
220
56
2013 Winter/spring
Spring/summer
Commercial gill net
Independent gill net & rod & line
320
147
2014 Winter
Summer/winter
Commercial gill net
Independent gill & seine net & rod & line
216
192
5.2.2 Ageing and growth
Each A. butcheri caught by fishery-independent sampling and by the commercial fisher
was measured to the nearest 1 mm (total length) and sexed through macroscopic
examination of its gonads. The methods used for ageing fish and describing growth are
given in detail in Chapter 2.3. The ageing of each fish took into account the date of capture
and a birth date of 1 November, the mid-point in the spawning period (see Results). In
brief, the otoliths of each fish were removed and those of restocked fish identified through
96
the presence of the purple alizarin complexone stain. von Bertalanffy growth curves were
fitted to the lengths at age of the restocked and wild stock fish, which for both groups
comprised the 2001 and 2002 year classes collectively. Note, however, that while all fish
caught by fishery-independent methods were used, the commercially-caught fish were
restricted to those >5 years old, i.e. the minimum age by which the total length of all fish
would be expected to have reached 250 mm (see Results), the MLL for retention of A.
butcheri.
Although preliminary analyses, using likelihood-ratio tests, demonstrated that the
von Bertalanffy growth curves of the females and males of both the restocked and wild
stock of A. butcheri differed significantly (P<0.001 and 0.01, respectively), the differences
between the lengths at age of the two sexes at all ages in both the restocked and wild stock
fish were always less than 5%. As such differences are unlikely to be of major biological
significance, the lengths at age for both sexes of the restocked fish and of the wild stock
fish have been pooled for comparing the growth of these two groups of fish, an approach
adopted in a number of studies on other species (e.g. White et al., 2002; Hesp et al., 2004).
Likelihood-ratio tests were then used to determine whether the von Bertalanffy growth
curves of the restocked and wild stock fish differed and, if so, the extent of any differences
in lengths at age across the ages sampled. If the latter differences exceeded 5%, likelihood-
ratio tests were then used to ascertain whether the growth coefficients, k, and/or the
asymptotic lengths, L∞, of the restocked and wild stock fish were significantly different.
5.2.3 Reproduction and fecundity
The gonads of each restocked and wild A. butcheri were examined macroscopically and
allocated to one of the following maturity stages described by Sarre & Potter (1999), i.e.
I/II = virgin/resting adult, III = developing, IV = maturing, V = prespawning, VI =
97
spawning, VII = spent and VIII = recovering spent. Previous histological studies of ovaries
had demonstrated that assignment of gonads to these stages on the basis of macroscopic
appearance was appropriate (Sarre & Potter, 1999; Chuwen, 2009).
For determining the length and age at maturity, A. butcheri with gonads at stages
I/II during the spawning period were considered immature, whereas those with gonads at
stages III to VIII were considered mature, i.e. destined to spawn or had spawned during
that period. This procedure was adopted after careful recent examination of the pattern of
sequential change in gonadal stages in the months immediately prior to and during the
spawning period in the Swan River Estuary (see Chapter 3). The designation of fish with
gonad stages III and IV as mature leads to lower estimates of the L50 and A50 than when
they are classified as immature, as in earlier studies of A. butcheri in the Blackwood River
Estuary (Potter et al., 2008) and other estuaries (Sarre & Potter, 1999). Note also that the
reproductive schedules were restricted to data derived from samples collected by fishery
independent methods and did not include commercial samples as the exact month of
collection was not always recorded.
The trends exhibited in sequential months by the prevalence of the different stages
in ovarian development and mean gonad weights were used to determine the spawning
period of A. butcheri in the Blackwood River Estuary. The gonad weights and lengths of
restocked and wild stock females ≥ the corresponding L50s at maturity (see Results) were
standardised for length (231 mm) using ANCOVA. Prior to analyses, the total length and
gonad weight for each individual was ln(x + 1) transformed, where ‘ln’ is the natural
logarithm. To account for bias introduced with the logarithmic transformation, when ln( )
is back-transformed, the correction factor exp( ) was employed (Beauchamp & Olson,
1973).
98
Logistic regression analysis was used to determine, for both the restocked and wild
stock, the probability P that a female or male of a given length and age possessed gonads at
stages III-VIII during the spawning season in the Blackwood River Estuary, i.e. October,
November and December. Likelihood-ratio tests were employed to determine whether the
ogive relating maturity to length for both the females and males of restocked fish differed
from that for the corresponding sex of wild stock fish and, if so, whether this was
accompanied by differences in the values of the L50 and/or L95, the lengths at which 50 and
95%, respectively, of fish were expected to be mature. The same approach was used to
determine whether the ogives relating maturity to age of the restocked females and males
differed from that of the corresponding sex of wild stock fish and, if so, whether this was
accompanied by differences in the values of the A50 and/or A95, the ages at which 50 and
95%, respectively, of fish were expected to be mature. The reader is referred to Chapter 2.3
for details of the maximum likelihood method used to determine the relationship between
the length and age at maturity and the Bayesian approach employed to determine the 95%
credible limits.
Comparisons of the relationships between the lengths and the ages at maturity of
the females and males of restocked fish (2001 and 2002 year classes collectively) with
those of the wild stock employed data collected during the spawning period, with the data
for wild stock fish of the 1999 and 2000 year classes being added to those of the wild stock
of the 2001 and 2002 year classes. This increased the number of fish in length and age
classes of the 2001 and 2002 year classes of the wild stock that were poorly represented in,
or absent from, samples collected during the spawning season.
The relative contributions of each year class of the wild stock and restocked
A. butcheri to egg production in the Blackwood River Estuary in 2007 and 2009 were
estimated using the lengths of individual fish in each year class in the commercial catches
99
and the equation of Sarre & Potter (1999), which described the relationship between batch
fecundity and the lengths of females in the Swan River Estuary. These two years were
chosen for analysis because they straddled 2008, for which no commercial samples were
available (see Results), and because the 2008 year class was very well represented in
commercial samples from 2012-14, i.e. when they exceeded the MLL for A. butcheri of 250
mm. The total number of eggs produced (F) in 2007 and 2009 by each year class of the
wild stock and restocked fish was thus calculated as ∑ [ - ]
,
where is the total length of the j’th fish, with the summation covering all fish
within each year class, yc, separately for both the restocked fish and wild stock in each
year, y. This enabled the relative percentage contribution to total egg production by each
year class of wild stock and restocked A. butcheri in 2007 and 2009 to be estimated . As the
GSIs of females during the spawning period in the Swan River Estuary were similar to
those in the other two estuaries that were sampled during the main part of that period (Sarre
& Potter, 1999), the relationship between batch fecundity and length is considered unlikely
to differ markedly among systems.
5.3 RESULTS
During the 12 years of sampling since cultured fish were first introduced into the
Blackwood River Estuary, i.e. 2002 to 2014, a total of 1584 restocked fish were obtained
from fishery-independent sampling and subsamples of the commercial gill net catches.
These restocked fish comprised 193 individuals of the 2001 cohort and 1391 of the 2002
cohort.
100
5.3.1 Growth
The von Bertalanffy growth curve provided a good fit to the lengths at ages of the wild
stock and of the restocked fish of the same two year classes collectively, i.e. 2001 and
2002 (Fig. 5.2a-c, Table 5.2). The growth curves for the restocked fish lay below and
differed significantly from that of wild stock fish (P<0.001). The differences between the
lengths at age across all ages from 1 to 12 years were between 7 and 11%. While the
growth coefficient (k) of 0.29 y-1
for restocked fish was less than and did not differ
significantly (P>0.05) from the 0.31 y-1
of wild stock fish, the L∞ of 323 mm for restocked
fish was less than and differed significantly (P<0.01) from the 350 mm of wild stock fish
(Fig. 5.2c). The growth curve for the limited age range of the 2008 year class lay between
the curves for the restocked and wild stock fish.
Table 5.2 von Bertalanffy growth parameters and their 95% confidence intervals for wild
stock and restocked Acanthopagrus butcheri in the Blackwood River Estuary. L∞,
asymptotic length (mm); k, growth coefficient (year-1
); t0, hypothetical age at which fish
would have zero length (years). r2, coefficient of determination; n, number of fish in
sample.
L∞ (mm) k (year-1
) t0 (years) r2
n
Wild stock fish Estimate 350 0.31 -0.70 0.88 163
Lower 336 0.26 -1.01
Upper 364 0.36 -0.40
Restocked fish
Estimate 323 0.29 -0.79 0.90 1321
Lower 318 0.26 -0.93
Upper 328 0.30 -0.64
Based on the von Bertalanffy growth equation, the TLs of female restocked A. butcheri
at two and six years of age were 179 and 278 mm, respectively, and thus less than the
corresponding TLs of 198 and 306 mm for the wild stock.
101
Figure 5.2. von Bertalanffy growth curves fitted to the lengths at age of (a) wild stock and
(b) restocked Acanthopagrus butcheri of the same year classes, i.e. 2001 and 2002,
collectively, and (c) comparison of the growth curves shown in a and b for wild stock fish
(long dashed line), restocked fish (continuous line) and the 2008 year class (short dashed
line).
102
5.3.2 Maturation
The mean monthly gonad weights of the females of both the restocked and wild stock fish
rose to a sharp peak in October and then declined progressively in the following months
(Fig. 5.3). The mean gonad weights of restocked and wild stock fish did not differ
significantly (P>0.05) in any month.
Figure 5.3 Mean gonad weights and 95% confidence intervals in sequential months for
wild stock (closed circles) and restocked (open circles) females of Acanthopagrus butcheri
with lengths ≥ L50 at maturity and which were caught by fishery-independent sampling in
the Blackwood River Estuary between 2000 and 2014. Gonad weights have been
standardised for fish of a common length (230 mm) using ANCOVA. Black bars, summer
and winter; white bars, autumn and spring. Sample size for each month is shown.
103
All wild stock females <179 mm and all restocked females <155 mm were
immature (Fig. 5.4a,b). The wild stock females in the 180-199 mm and subsequent length
classes were mature (Fig. 5.4a). The prevalence of mature restocked females increased
from 25% in the 140-159 mm length class to 76% in the 180-199 mm length class, and all
restocked females ≥240 mm were mature (Fig. 5.4b).
The ogive describing the relationship between the proportion of mature restocked
females and total length differed significantly from the corresponding ogive for wild stock
females (P<0.01, Fig. 5.4a-c, Table 5.3). The L50s at maturity of 174 mm for restocked
females was greater than the 165 mm of wild stock, but the difference was not significant
(P>0.05). The L95 of 224 mm for restocked females was greater than the 168 mm for wild
stock females and the difference was significant (P<0.001, Fig. 5.4c).
Table 5.3 Estimates of total lengths (mm) and ages (years) and associated 95% credible
limits at which 50% (L50 and A50, respectively) and 95% (L95 and A95, respectively) of the
females and males of the wild stock and restocked Acanthopagrus butcheri were mature.
ML = Maximum Likelihood. n is the number of fish.
L50
(mm)
L95
(mm)
A50
(years)
A95 (years) n
Wild stock fish
Females
ML Estimate 165 168 1.7 2.0 87
Lower 150 153 1.4 1.8
Upper 179 196 1.9 2.2
Males
ML Estimate 149 159 1.2 1.6 133
Lower 141 138 1.1 1.4
Upper 153 203 1.3 2.0
Restocked fish
Females
ML Estimate 174 224 2.1 3.2 139
Lower 166 210 1.8 2.8
Upper 184 245 2.2 3.9
Males
ML Estimate 154 177 1.8 2.3 176
Lower 146 168 1.6 2.2
Upper 160 194 1.9 2.8
104
Figure 5.4. Percentage frequency of occurrence, in sequential 20 mm length classes, of
females and males of wild stock and restocked Acanthopagrus butcheri with immature
(white bars) and mature gonads (grey bars), derived from samples collected during the
spawning season of A. butcheri. Logistic curves (solid lines) and their 95% credible
intervals (dotted lines) for the probability that a fish at a given length is mature are
superimposed on a, b, d and e. Sample size for each length class is provided. Comparisons
105
of logistic curves for wild stock (dashed line) and restocked (continuous line) females and
males are shown in c and f.
All wild stock males <147 mm and all restocked males <146 mm were immature
(Fig. 5.4d,e). While all wild stock males in the 160-179 mm and subsequent length classes
were mature, about 25% of the restocked males in the 160-179 mm length class were
immature (Fig. 5.4d,e).
The ogive describing the relationship between the proportion of mature restocked
males and total length did not differ significantly from the corresponding ogive for wild
stock males (P>0.05, Fig. 5.4d-f, Table 5.3). Although the L50 of 154 mm and L95 of 177
mm at maturity for restocked males were both greater than the corresponding values of 149
and 159 mm, respectively for wild stock males, the differences were likewise not
significant (P>0.05, Fig. 5.4f).
No wild stock or restocked females reached maturity by the end of its first year of
life (Fig. 5.5a,b). While virtually all wild stock females had become mature by two years
of age, only 54% of restocked females had become mature by that age and some restocked
females had not become mature by 3 and 4 years of age.
The ogive describing the relationship between the proportions of mature restocked
females and age was significantly different (P<0.001) from the corresponding ogive for
wild stock fish (Fig. 5.5a-c, Table 5.3). The A50 for maturity of 2.1 years of restocked
females was greater than the corresponding value of 1.7 years for wild stock females, but
this difference was not significant (P>0.05). The A95 for restocked females of 3.2 years was
appreciably greater (P<0.001) than the 2.0 years for wild stock females (Fig. 5.5c).
Some wild stock males attained maturity at the end of their first year of life and all
became mature at the end of their second year of life, whereas no restocked males became
mature at the end of their first year of life and nearly 20% were still immature at the end of
their second year of life (Fig. 5.5d,e).
106
Figure 5.5. Percentage frequency of occurrence, in sequential ages, of females and males
of wild stock and restocked Acanthopagrus butcheri with immature (white bars) and
mature gonads (grey bars), derived from samples collected during the spawning season of
A. butcheri. Logistic curves (solid lines) and their 95% credible intervals (dotted lines) for
the probability that a fish at a given age is mature are superimposed on a, b, d, e. Sample
size for each length class is provided. Comparisons of logistic curves for wild stock
(dashed line) and restocked (continuous line) females and males are shown in c and f.
107
The ogive describing the relationship between the proportions of mature restocked
males and age differed significantly (P<0.001) from the corresponding ogive for wild stock
fish (Fig. 5.5d-f , Table 5.3). The A50 of 1.8 years and A95 of 2.3 years for restocked males
were both greater than and differed significantly (P<0.001) from the corresponding values
of 1.2 and 1.6 years, respectively, for the wild stock males (Fig. 5.5f).
5.3.3 Contribution of restocked fish to commercial catches
In any description of the length compositions of A. butcheri in commercial catches from
the Blackwood River Estuary, it must be borne in mind that the stretched mesh size of the
commercial gill net (105 mm) was chosen by the commercial fisher so that it essentially
caught only A. butcheri with lengths ≥250 mm, the MLL for retention of this species. The
commercial catches of A. butcheri in 2005 comprised almost exclusively wild stock fish,
with their lengths ranging from 257 to 412 mm and producing a modal length class of 280-
299 mm (Fig. 5.6a). The samples in 2005 did contain, however, two restocked fish of the
2002 year class and 14 restocked fish of the 2001 year class, whose lengths collectively
ranged from 255 to 295 mm. In 2006, the overall modal length class decreased to 260-279
mm, which was due to the recruitment into the fishery of appreciable numbers of restocked
fish of the 2002 year class, whose lengths ranged from 253 to 325 mm. The modal length
class of restocked fish, produced predominantly by the 2002 year class, increased from
260-279 mm in both 2006 and 2007 to 280-299 mm in 2009 and 2010. During this period,
the lower end of the overall distribution of lengths was dominated by cultured fish, whose
lengths were almost invariably <340 mm, whereas the upper end contained several wild
fish with lengths extending up to 426 mm (Fig. 5.6a).
108
Figure 5.6 a) Length and b) age-frequency distributions for samples of commercial gill net
catches of Acanthopagrus butcheri in the Blackwood River Estuary between 2005 and
2014. White and black bars represent the 2001 and 2002 year classes of restocked fish,
respectively, and the grey bars the wild fish, i.e. those whose otoliths did not contain the
purple colouration of the alizarin stain that characterises those of cultured fish. Arrows
track the 1999 year class of the wild stock and the 2002 year class of restocked fish, which
were the dominant year classes between 2006 and 2010.
109
In contrast to 2010, when virtually all fish with lengths <320 mm were restocked
fish, the majority of A. butcheri <320 mm caught in 2012, and even more particularly in
2013 and 2014, were fish whose otoliths were not stained with alizarin complexone, and
were thus spawned naturally in the wild (Fig. 5.6a).
The ages of A. butcheri in commercial catches in 2005, which comprised almost
exclusively wild stock fish, ranged from 2 to 10 years old, with one fish 15 years old and
another 18 years old (Fig. 5.6b). The samples in that year were dominated by the 5+ and to
a lesser extent the 4+ age class, i.e. fish spawned in 1999 and 2000, respectively. The 1999
year class remained the most abundant year class of wild stock fish in the years up to 2010,
being represented, for example, by substantial numbers of the 7+ age class in 2007 and of
the 10+ age class in 2010. However, restocked fish, mainly of the 2002 year class,
increasingly dominated the catches in this period, with their contributions to commercial
catches increasing progressively from 32% in 2006 to 74% in 2010 (Fig. 5.6b).
Although there had been little or no recruitment of year classes of wild stock fish
into the fishery in 2006 to 2010, this situation changed dramatically in 2012, when a strong
new cohort, representing the 2008 year class, appeared in samples, at which time they were
3 years old (Fig. 5.6b). This strong recruitment was reflected in the marked increase in the
prevalence of smaller fish in 2012 to 2014 (Fig. 5.6a). The 2008 year class became so strong
in 2013 and 2014, when its individuals were 4 and 5 years old, respectively, that it
dominated the age-frequency distributions for those years (Fig. 5.6b). The dominance of
this year class in 2013 and 2014 accounts, in part, for the decline in the relative contribution
of restocked fish from 74% in 2010 to 19% in 2013 and 10% in 2014 (Fig. 5.6b).
110
5.3.4 Egg production
On the basis of the relationship between fecundity and total length (Sarre & Potter, 1999)
and the lengths and numbers of fish in each year class, the contribution to egg production by
the 1999 year class of wild stock females was 25% in 2007 and 18% in 2009, in which years
these fish were 8 and 10 years old, respectively (Fig. 5.7). These were the greatest
contributions by any year class of wild stock females in both years and particularly in 2007.
The contribution to total egg production by females of restocked fish was 54% in 2007 and
55% in 2009, due predominantly to that made by the 2002 year class. Thus, the restocked
fish made a greater contribution than wild stock fish to total egg production in 2007 and
2009 (Fig. 5.7).
Figure 5.7 Percentage contributions made to egg production by the different year classes
of wild stock and restocked Acanthopagrus butcheri in 2007 and 2009 and by the wild
stock and restocked fish overall in those two years. Data were derived from the lengths of
individuals of each age class in commercial gill net samples and employed the fecundity-
length relationship for A. butcheri in Sarre & Potter (1999).
111
5.4 DISCUSSION
5.4.1 Survival and growth of restocked fish
Although the number of A. butcheri cultured in 2001 and released into the estuary in 2002
was nearly half that cultured in 2002 and released in 2003, i.e. 70,000 vs 150,000, only 6%
of the restocked A. butcheri taken by commercial gill netting between 2005 and 2014
belonged to the 2001 cohort. The far lower survival of the 2001 than 2002 cohort of
cultured fish may have been related to differences in environmental conditions at the time
of their release. Thus, whereas the 2001 cohort was released in winter, when freshwater
discharge was increasing and water temperatures were at their minimum, the 2002 cohort
was released during autumn, when freshwater discharge was limited and water
temperatures were still relatively high. The more ‘benign’ water conditions in autumn than
winter would have afforded the individuals of the 2002 cohort a better opportunity to
‘adjust’ to their new environment before facing the rigours of heavy freshwater discharge
in winter. The longer time spent in the hatchery by the 2001 cohort (7 vs 4 months) may
also have had a negative impact on their ability to adjust to their environment.
5.4.2. Comparisons of the performance of restocked and wild fish
This study demonstrated that, in terms of growth and maturity schedules, restocked
A. butcheri did not perform as well as its wild stock in the Blackwood River Estuary.
However, any consideration of the efficacy of using restocking as a tool for replenishing
the depleted stock of this species in this system should take into account the extent of the
differences and how the performance of cultured fish compares with that of this species in
other estuaries. Thus, while the L∞s of restocked and wild stock fish differed significantly,
the difference was only 8% and the rates, k, at which the total lengths at age of restocked
112
and wild stock fish approached their respective asymptotic lengths, were not significantly
different. The fact that the growth curve, fitted to the lengths at age of the 2008 year class
lay between that for the restocked and wild stock, suggests that the growth of this year
class is intermediate, recognising, however, that the difference between the growth of the
restocked and wild fish was relatively small.
On the basis of the von Bertalanffy growth equation, restocked fish took 4.3 years
to reach the MLL of 250 mm for A. butcheri and thus longer than the 3.4 years taken by
wild fish. However, the MLL was reached at an earlier age by restocked fish in the
Blackwood River Estuary than recorded by Sarre & Potter (2000) for this species in 1993-
95 in two other south-western Australian estuaries (~6.7 and 7 years) and at a similar age
in another estuary in that period (4.4 years). While restocked A. butcheri took longer to
reach the MLL in the Blackwood River Estuary than required in a fourth system, the Swan
River Estuary, in that earlier period, i.e. ~2.8 years, they attain the MLL far more rapidly
than in that same system in recent years, i.e. ~7 years, when it had become severely
degraded (Chapter 3).
Some restocked fish, and particularly their females, were still immature in the
length and age classes at which all wild stock fish had become mature. This accounts for
the L50 and A50 at maturity, and, to an even greater extent, the L95 and A95, all being greater
for restocked females than wild stock females, recognising that the differences were
statistically significant only in the case of the L95s and A95s. Although restocked males
matured at a greater length and age than wild stock males, the differences were statistically
significant only for the A50s and A95s at maturity. Furthermore, restocked females attained
maturity at an age very similar to the 1.9 years for A. butcheri in 1993-95 in the Swan
River Estuary, ~300 km further north, and at a slightly younger age than the 2.5 years
estimated for that system in 2007-11 (Chapter 3).
113
Although the differences in growth and maturity schedules of restocked and wild
A. butcheri in the Blackwood River Estuary were relatively small, they parallel the trend in
other studies for the long-term performance of the cultured fish of a species to be inferior
to that of its wild stock (Jonsson & Jonsson, 2006; Lorenzen et al., 2012).
5.4.3 Contributions of restocked and wild fish to commercial gill net catches
The progressive rise, in the relative contributions of restocked fish to the annual
commercial catches of A. butcheri, from negligible levels in 2005 to about three-quarters in
2010 is attributable to two factors. First, through growth, the number of restocked fish that
attained the MLL of 250 mm increased progressively each year. Second, the recruitment
into the commercial fishery of all year classes of the wild stock of A. butcheri, except for
the 1999 year class, was relatively low between 2005 and 2010, probably representing poor
spawning success in earlier years. It is thus evident that restocked fish made a major
contribution to the commercial catches for a number of years and thus, implicitly, also to
those of recreational fishers.
The decline in the contribution of restocked fish to commercial catches in 2012 was
largely due to an increase in the contribution of the 2008 year class. The subsequent
increase in the proportion of the 2008 year class in 2013 and 2014 reflected an increase in
the numbers of that year class that would have reached the MLL and a decline in the
abundances of both the 2002 cohort of restocked fish and the 1999 cohort of wild stock
fish as a result of natural and fishing mortality.
The question now arises as to whether the progeny of cultured fish could
potentially have contributed to the substantial number of individuals that comprised the
2008 year class. On the basis of the A50 at maturity of ~2 years, the restocked A. butcheri
of the 2002 year class would, on average, have matured in 2004 and thus could potentially
114
have spawned in that and subsequent years. However, as mentioned above, the age
compositions in commercial catches imply that spawning success was very limited
between 2000 and 2007. Thus, as the vast majority of wild stock fish in 2007 and 2009,
and thus implicitly in 2008, were ≥8 years in age, the relatively strong spawning success in
2008 was presumably due to spawning by cultured fish (particularly of the 2002 year class)
and/or wild stock fish or to interbreeding between these two groups.
Although commercial catch samples were not available in 2008, it is relevant that
restocked fish were estimated to contribute 54 to 55% to the total egg production by legal-
sized A. butcheri in the Blackwood River Estuary in 2007 and 2009. Restocked fish would
thus presumably have made a similar contribution in 2008, the year in which recruitment
into the population, and thus implicitly spawning success, was particularly strong.
The spawning success of the restocked individuals of some species has been shown
to be inferior in certain respects from that of the wild stock of that species, due, for
example, to differences in the timing of breeding and/or selection of suitable nest sites
(Fleming & Petersson, 2001, McGinnity et al., 2003; Weir et al., 2004). However, as the
monthly trends in ovarian weights and locations of capture were the same in restocked fish
as wild stock fish, the two groups spawn at the same time and in the same region of the
estuary. Furthermore, as discussed earlier, the differences in the reproductive schedules of
the restocked and wild stock fish were relatively small. It is also relevant that the results of
a thorough genetic study strongly indicated that the prevalence of inbreeding was not
demonstrably greater among the restocked than wild stock A. butcheri (Gardner et al.,
2013).
In summary, this study has shown that the growth of restocked A. butcheri in the
Blackwood River Estuary was only slightly less than that of wild fish likewise hatched in
2001 and 2002 and therefore exposed to the same environmental conditions for the twelve
115
to thirteen years since those cultured fish were introduced into this system. It also
demonstrated that an appreciable number of restocked fish were still present in the estuary,
eleven years after their introduction to this system, and that all restocked fish, which
survived to five years of age, reached maturity and therefore potentially could spawn and
contribute to future generations of A. butcheri in this estuary. In addition, the restocked
fish were shown to make a very substantial contribution to the commercial gill net fishery
for this sparid in the Blackwood River Estuary in 2007-10. There is also strong
circumstantial evidence that the cultured fish had contributed progeny that were caught by
the commercial fisher for A. butcheri in the Blackwood River Estuary. The results of this
study provide a rare example of a continuing investigation into the consequences of a fish
restocking programme in an estuary and demonstrate that it is a worthwhile proposition to
consider the use of restocking with appropriately cultured fish to replenish a stock of a
species such as A. butcheri, whose individuals are confined to their natal estuary.
Acanthopagrus butcheri is also a very good candidate for restocking in the Blackwood and
some other estuaries as natural recruitment is so episodic in these systems (Morison et al.,
1998) and density dependent interactions between wild and restocked fish would be likely
to be low.
116
Chapter 6
General Discussion
6.1 Swan River Estuary
6.1.1 Influence of hypoxia
As discussed in the General Introduction, the opportunities provided by estuaries for
agriculture, industry and urban development have been widely exploited, resulting in the
input into these systems of organic material, other nutrients and toxic materials, thereby
leading inter alia to eutrophication, hypoxia and mortality among their faunas (de Jong et
al., 2002; Kennish, 2002; Breitburg et al., 2009). This has led to estuaries in temperate
regions becoming the most degraded of all marine environments (Jackson et al., 2001).
Such degradation has become so pronounced in the Swan River Estuary that it was rated
one of the two most hypertrophic of the 131 estuarine and coastal ecosystems worldwide
for which Cloern et al. (2014) collated data.
Because the estuaries in south-western Australia are poorly flushed, they are
particularly prone to accumulating nutrients and thus to eutrophication (Tweedley et al.,
2013, 2014). This poor flushing is the result of the small tidal water movements in the
estuaries of this microtidal region and to the restriction of most freshwater discharge to the
wet ‘winter’ months. As freshwater discharge is very restricted during summer, flushing is
limited at the time when water temperatures are greatest and biological oxygen demand
(BOD) is therefore also greatest. Furthermore, the problem of removing organic material
and other nutrients from the Swan River Estuary through flushing has been exacerbated
during recent years by a marked decline in the volume of freshwater discharge entering the
estuary in winter and early spring as a consequence of a reduction in rainfall (Chapter 3).
117
The results reported in Chapter 3 demonstrated that the decline in freshwater
discharge in the Swan River Estuary between the early 1990s and late 2000s led to
progressive increases in hypoxia in its upper region. These marked deleterious changes in
environmental conditions were shown to be accompanied by reductions in the body
condition, growth and length at maturity of Acanthopagrus butcheri and by an increase in
age at maturity (Fig. 6.1, Chapter 3). The direction of each of these changes is consistent
with the stress that would be expected on the individuals of a species exposed to
detrimental conditions (Kramer, 1987; Pichavant et al., 2001; Stearns, 1992; Eby et al.,
2005; Roberts et al., 2011). It was concluded that the changes in biological characteristics
were attributable to the effects of hypoxia directly and to a density-dependent effect. The
latter was produced by the increase in density that occurred through larger A. butcheri
moving from the deeper hypoxic waters into the better oxygenated shallow waters where
the smaller fish are found. Such habitat compression parallels that observed with certain
pelagic fish species in the eastern tropical Pacific and Atlantic oceans, where, as a response
to hypoxia, they became concentrated in the better oxygenated surface waters (Prince &
Goodyear, 2006; Stramma et al., 2012), which, in one study, were shown to extend
downwards to the thermocline at 25 m, below which lies the cold hypoxic water (Prince &
Goodyear, 2006).
Although the development of severe hypoxia in the deeper waters led to habitat
compression and an overall decline in the biological performance of A. butcheri in the
Swan River Estuary between the early 1990s and the early to mid-2000s, the limited CPUE
data indicated that this did not result in a marked overall decline in the abundance of this
species in the upper region of this estuary between these years (Chapter 3).
118
Figure 6.1 Graphical representation of the changes in that occurred in the environment of
the Swan River Estuary between 1994/95 and 2007/08 and the accompanying changes in
certain biological characteristics of Acanthopagrus butcheri. Symbols courtesy of the
Integration and Application Network (ian.umces.edu/symbols/)
6.1.2 Influence of temperature
On the basis of the metabolic theory of ecology (Angilletta et al., 2004; Brown et al., 2004;
Weber et al., 2015), the growth rate of A. butcheri in the Swan River Estuary would be
expected to increase with increasing temperature. However, although the annual mean
value of the maximum daily air temperatures for the months between November and
March, when growth mainly occurs, increased by ~1.0 °C between the end of the first
sampling period (1994/95) and the beginning of the final sampling period (2007/08), the
overall growth of A. butcheri decreased between these periods. Thus, any potential
influence of temperature on the changes in growth between the earlier and later periods
was over-ridden by other factors, i.e. hypoxia and increased densities. However, between
2007 and 2014, when A. butcheri resided predominantly in shallow waters and densities
remained high and freshwater discharge consistently low, growth was positively correlated
119
with temperature. As temperature also influences the frequency and amount of food
ingested, as well as the rate of digestion and absorption (Brander, 2009), the increased
temperatures were also presumably accompanied by an increased availability to utilize
prey. The optimum temperature for growth has also been shown to be higher for younger
fish (Árnason et al, 2009; Brander, 2009). Thus, although increasing temperatures may
result in faster growth of small fish, larger fish may fall outside their optimal temperature
range and growth becomes depressed (Árnason et al, 2009; Brander, 2009).
Although the growth of A. butcheri in the Swan River Estuary during recent years
was related to temperature (Chapter 4), comparisons of the growth of this sparid in four
estuaries in 1993-95 (Sarre & Potter, 2000) suggested that there is no consistent
relationship between growth and temperature when considered across estuaries. Thus, the
growth rates of juveniles were lowest in the Moore River Estuary, the most northern and
therefore warmest of these systems, and were far less than those in the Wellstead Estuary,
which is much further south and therefore cooler.
An example of the extent to which the growth of A. butcheri can be influenced by
different environmental conditions is provided by the results of a study in which A.
butcheri were cultured separately from brood stock from the Moore River and Swan River
estuaries and the growth of the resultant juveniles recorded for ~270 days (Partridge et al.,
2004). Despite the growth of A. butcheri being far slower in the Moore River Estuary than
the Swan River Estuary, the cultured juveniles grew at the same rate when maintained
under identical conditions in the laboratory. This clearly implies that, in some way,
conditions in the Moore River Estuary were far less favourable for growth than those in the
Swan River Estuary. It therefore appears relevant that the densities of the juveniles of A.
butcheri in the Moore River Estuary were greater than in the other three estuaries studied
by Sarre & Potter (2000) and that the diet of this species in that estuary comprised a far
120
higher component of macrophytes than those in the other three estuaries (Sarre et al.,
2000). Thus, density-dependent effects and/or quality of available food could account for
the differences in the growth of A. butcheri in those systems. In addition, the results of the
above culture experiment demonstrate that, although the populations in the two estuaries
are genetically distinct (Chaplin et al., 1998), the differences in the growth of A. butcheri
in the two systems are not genetically based.
6.1.3 Recruitment
The studies reported in this thesis for the Swan River Estuary were aimed at comparing the
condition, growth and reproductive schedules of A. butcheri in two periods between which
this estuary has undergone very pronounced anthropogenic changes. The sampling regime
was thus not designed to explore rigorously the extent of any inter-annual differences in
recruitment and the factors that influence any such variations. However, the data compiled
for the Swan River Estuary does allow some tentative conclusions to be made regarding
recruitment, taking into account the results of extensive studies on the recruitment of
A. butcheri in estuaries in eastern Australia (Nicholson et al., 2008; Jenkins et al., 2010,
2015; Williams et al., 2012, 2013).
The age compositions of A. butcheri in the Swan River Estuary in the years
between 2007 and 2014 showed that recruitment varied to some degree among years, with,
for example, the 2005 year class well represented and the 2006 year class poorly
represented (Fig. 6.2). A more extreme situation was recorded for A. butcheri in the
Gippsland Lakes in south-eastern Australia where, on the basis of the age composition in
samples collected between 1993 and 1996, recruitment was highly episodic and thus the
commercial and recreational fishers relied very heavily on just two age classes (Morison et
121
al., 1998). Recruitment of A. butcheri in this estuary was shown also to be episodic in
subsequent years (Jenkins et al., 2010).
Studies in south-eastern Australian estuaries demonstrated that the recruitment of
A. butcheri was negatively correlated with freshwater discharge during the spawning
season and positively correlated with the level of stratification in that period (Jenkins et al.,
2015). However, on average, freshwater discharge peaks earlier and much more sharply in
the Swan River Estuary than in the Mitchell River, which flows into the Gippsland Lakes
(Fig. 6.3). Furthermore by November, i.e. just after peak spawning, it has declined to
relatively far lower levels in the Swan River Estuary than in the Mitchell River. In at least
relative terms, the trend exhibited by freshwater discharge in the Swan River Estuary
differed from that in the Mitchell River. An examination of the vertical salinity profiles in
the Swan River Estuary in November provided no clear evidence that a year of good
recruitment is related to the presence of a well-defined halocline. It would thus appear that
the factors influencing recruitment in the Swan River Estuary and south-eastern Australian
estuaries differ and that inter-annual variations in recruitment are not as pronounced in the
Swan River Estuary.
It would be worthwhile to establish standardised sampling regimes for A. butcheri
in south-western Australia, along the lines of that in Victoria (Jenkins et al., 2010;
Williams et al., 2012, 2013), aimed at collecting larvae in the period immediately
following peak spawning and representative samples of 0+ fish just after the spawning
period. This would enable the relationship between recruitment and freshwater discharge
and thus salinity stratification to be explored in detail.
122
Figure 6.2 Age-frequency distributions of Acanthopagrus butcheri caught in the Swan
River Estuary between 2007 and 2014. Solid and dashed lines track the 2005 and 2006
year classes, respectively.
Figure 6.3 Mean monthly freshwater discharges into the Mitchell River (gauging station
224203) and Swan River (gauging station 616011) recorded between 1990 and 2015 as
percentages of annual totals. Data were provided by Victorian Water Measurement
Information System (http://data.water.vic.gov.au/ monitoring.htm) and the Western
Australian Department of Water (2015), respectively.
123
6.1.4 Management
It has to be borne in mind that the CPUEs for A. butcheri during the last 25 years were
derived from the catches of a limited number of recreational fishers and that the
commercial fishery declined markedly during that period as a result of a government buy-
back of licences (Chapter 3; Smith, 2006; Smith et al., 2014). Thus, caution must be
exercised when drawing conclusions from those CPUEs. It would be useful if reliable
recreational catch and effort data for A. butcheri in the Swan River Estuary (and other
estuaries) could be collected on a regular basis as such data would facilitate exploration
more fully of the trends in abundance of this species and the factors influencing that
abundance.
6.2 Blackwood River Estuary
The results of the study in the Blackwood River Estuary demonstrate that, in terms of
growth and maturity schedules, the A. butcheri that had been cultured from brood stock
from this estuary performed almost as well as the resident wild stock (Chapter 5). They
also showed that, once the cultured fish had reached the MLL of 250 mm, they made a
very substantial contribution to the commercial catches for A. butcheri in this estuary (Fig.
6.4). The results also provide strong circumstantial evidence that the restocked fish made a
significant contribution to the successful spawning of A. butcheri in the Blackwood River
Estuary in 2008. The importance of the restocked fish to the population and fishery for
A. butcheri in the Blackwood River Estuary cannot thus be overestimated.
Although restocking can overcome the need for imposing stringent size and bag
limits and fishing closures, prior to any restocking, a review of alternative management
options require evaluation. Furthermore, any restocking would need to be undertaken in a
manner that maintains the biological integrity of the wild stock and does not have a
significant effect on other species or the environment.
124
Figure 6.4 Graphical representation showing the introduction of cultured fish (pink) in
2002/03 and their growth and contribution to the commercial fishery between 2005 and
2014. Symbols courtesy of the Integration and Application Network
(ian.umces.edu/symbols/).
The above results for the Blackwood River Estuary can now be considered in the
context of those for the Swan River Estuary to develop concepts as to the why the stock of
A. butcheri in the Blackwood River Estuary declined in the past (Lenanton et al., 1999).
The age-frequency distributions of the wild stock of A. butcheri in commercial catches
from 2005 to 2014 emphasise that, in contrast to the Swan River Estuary, natural
recruitment of this species in the Blackwood River Estuary was very poor in most years.
The basis for this poor recruitment probably represents a continuation of the unidentified
problem that led to a decline in the fishery in earlier years. It is thus relevant to revisit how
A. butcheri in the Swan River Estuary responded, in its behaviour, to the detrimental
environmental changes that occurred in that system.
The data presented in Chapter 3 provide strong evidence that, as freshwater
discharge declined, the deeper waters of the upper Swan River Estuary became
increasingly hypoxic. During the same period, the mean annual freshwater discharge in the
Blackwood River Estuary declined significantly (Fig. 6.5, P<0.05, r = -0.35). It is thus
125
relevant that oxygen concentrations at the bottom of the water column in the deeper waters
of the Blackwood River Estuary were frequently <2 mgL-1
between 2001 and 2010, and
particularly so since 2006 (Brearley, 2013). In contrast, oxygen concentrations were
usually >2mgL-1
in 1999 to 2001 and fragmentary records indicate that oxygen
concentrations were higher in earlier years (Brearley, 2013). There is thus very strong
circumstantial evidence that, as in the upper Swan River Estuary, the decline in freshwater
discharge in the Blackwood River Estuary was accompanied by an increase in the extent of
hypoxia in the deeper waters of this system.
Figure 6.5 Mean freshwater discharge in the Blackwood River Estuary in each year
between 1990 and 2015.
The question now arises as to why the abundance of A. butcheri apparently
declined in the Blackwood River Estuary and yet, from the restricted CPUE data, did not
change markedly in the Swan River Estuary. The problem posed by hypoxia to large A.
butcheri in the deeper waters of the Swan River Estuary was overcome by their tending to
move into the wide and better oxygenated shallow margins of this estuary (Chapter 3). The
corresponding margins of the Blackwood River Estuary are, however, far narrower (Fig.
6.6). It is thus proposed that there was insufficient nearshore habitat to accommodate many
126
large, as well as numerous small A. butcheri, and thus the overall abundance of this species
in the Blackwood River Estuary declined. At the same time, some large A. butcheri are
present in nearshore, shallow waters and, from the results of our early, preliminary studies
using gill nets, are in greater abundance in the shallows than in deeper waters. The view
that the distribution of fish changes in response to decreasing flow and increasing hypoxia
in deeper waters would explain why, in the past, commercial fishers for A. butcheri
changed from setting their gill nets in deeper waters to shallow, nearshore waters, a
practice still adopted by the sole commercial fisher for A. butcheri in the Blackwood River
Estuary (T. Price, pers. comm.).
Figure 6.6 Graphical illustration of a cross section of the upper region of a) the Swan
River Estuary and b) Blackwood River Estuary showing the differences in their
morphology. Symbols courtesy of the Integration and Application Network
(ian.umces.edu/symbols/).
The decline in freshwater discharge and increasing hypoxia in the Blackwood River
Estuary may also have had a detrimental effect on the larvae of A. butcheri in this system.
Work in south-eastern Australia demonstrated that the larvae of this species aggregate in
the vicinity of the halocline and thus in the same region of the water column as its
zooplankton prey (Williams et al., 2012, 2013). However, preliminary studies by Joel
Williams (pers. comm.) indicate that, in contrast, the larvae of A. butcheri are distributed
below the halocline and in much deeper water in the Blackwood River Estuary. Williams
127
suggests that this represents a mechanism for avoiding predation in the region around the
halocline, which, through the presence of greater visibility due to much lower turbidity,
would make the larvae more susceptible to being consumed by visual predators. However,
migration of the larvae into the deeper waters of the Blackwood River Estuary would take
the larvae into areas where the oxygen concentrations and abundance of prey are greatly
reduced. The proposal that low oxygen concentrations could lead to substantial mortality
of the early life cycle stages of A. butcheri is consistent with the results of Hassell et al.
(2008a,b).
From the above, it follows that the success of the cultured fish for restocking A.
butcheri could be due to the bypassing of the sensitive larvae phase. If this proves to be the
case, restocking may be the best way of replenishing depleted stocks of this species in
other estuaries.
6.3 Conclusions
The conclusion that marked declines in rainfall and thus freshwater discharge in the Swan
River and Blackwood River estuaries has led to hypoxia and other related detrimental
effects for A. butcheri raise the question of how widespread such effects are in south-
western Australian estuaries. It is thus relevant that the volume of freshwater discharge
entering other estuaries in south-western Australia has also declined (Fig 6.7). Further
studies are thus clearly required to determine whether this has also led to similar
detrimental effects on A. butcheri. If this proves to be the case, there is clearly a need to
ensure that discharge levels in those estuaries are not impeded any further through, for
example water abstraction and farm dams and, better still, are improved. Indeed, protecting
natural flow regimes is likely to be the most effective management strategy to maintain the
128
‘health’ of estuaries and their fisheries (see also Gillson, 2011). It follows that a thorough
understanding of the hydrology of estuaries will become increasingly important to
managing these systems as they become subjected further to the effects of climate change
and increases in the demand for water resources by human populations.
In view of anticipated climatic and other anthropogenic changes, it would be very
useful to have a long time series of data for a well-studied species whose biological
characteristics can be used to monitor the biological effects of those changes.
Acanthopagrus butcheri possesses many of the required characteristics to act as an
indicator species. It is widely distributed and relatively abundant in many estuaries in
southern Australia and is relatively long-lived for an estuarine species. It is also confined
to its natal estuary and thus subjected to essentially the same environment throughout the
whole of their life (Bortone, 2003). As A. butcheri is an important recreational and
commercial fish species, there is a solid database on its biological characteristics (e.g.
Morison et al., 1998; Sarre & Potter, 1999, 2000; Jenkins et al., 2010, 2015; Williams et
al., 2013). Furthermore, the plasticity of certain biological characteristics and the durability
of A. butcheri means that this species will respond to environmental differences (Partridge
et al., 2004) and is capable of surviving relatively severe environmental changes.
129
Figure 6.7 Freshwater discharge into five estuaries in south-western Australia in the years
between 1990 and 2015. Data provided by the Western Australia Department of Water.
130
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