Strong links between metal contamination, habitat modification and estuarine larval fish distributions.
ABSTRACT Changes to larval fish assemblages may have far reaching ecological impacts. Correlations between habitat modification, contamination and marine larval fish communities have rarely been assessed in situ. We investigated links between the large-scale distribution of stressors and larval fish assemblages in estuarine environments. Larval fish communities were sampled using a benthic sled within the inner and outer zones of three heavily modified and three relatively unmodified estuaries. Larval abundances were significantly greater in modified estuaries, and there were trends towards greater diversity in these systems. Differences in larval community composition were strongly related to sediment metal levels and reduced seagrass cover. The differences observed were driven by two abundant species, Paedogobius kimurai and Ambassis jacksoniensis, which occurred in large numbers almost exclusively in highly contaminated and pristine locations respectively. These findings suggest that contamination and habitat alteration manifest in substantial differences in the composition of estuarine larval fish assemblages.
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Article: High levels of sediment contamination have little influence on estuarine beach fish communities.
[show abstract] [hide abstract]
ABSTRACT: While contaminants are predicted to have measurable impacts on fish assemblages, studies have rarely assessed this potential in the context of natural variability in physico-chemical conditions within and between estuaries. We investigated links between the distribution of sediment contamination (metals and PAHs), physico-chemical variables (pH, salinity, temperature, turbidity) and beach fish assemblages in estuarine environments. Fish communities were sampled using a beach seine within the inner and outer zones of six estuaries that were either heavily modified or relatively unmodified by urbanization and industrial activity. All sampling was replicated over two years with two periods sampled each year. Shannon diversity, biomass and abundance were all significantly higher in the inner zone of estuaries while fish were larger on average in the outer zone. Strong differences in community composition were also detected between the inner and outer zones. Few differences were detected between fish assemblages in heavily modified versus relatively unmodified estuaries despite high concentrations of sediment contaminants in the inner zones of modified estuaries that exceeded recognized sediment quality guidelines. Trends in species distributions, community composition, abundance, Shannon diversity, and average fish weight were strongly correlated to physico-chemical variables and showed a weaker relationship to sediment metal contamination. Sediment PAH concentrations were not significantly related to the fish assemblage. These findings suggest that variation in some physico-chemical factors (salinity, temperature, pH) or variables that co-vary with these factors (e.g., wave activity or grain size) have a much greater influence on this fish assemblage than anthropogenic stressors such as contamination.PLoS ONE 01/2011; 6(10):e26353. · 4.09 Impact Factor
Page 1
Strong links between metal contamination, habitat modification
and estuarine larval fish distributions
Andrew C. McKinleya,*, Anthony Miskiewiczb, Matthew D. Taylora, Emma L. Johnstona
aEvolution & Ecology Research Centre, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, New South Wales 2052, Australia
bEnvironment and Recreation, Wollongong City Council, 41 Burelli Street, Wollongong, New South Wales 2500, Australia
a r t i c l e i n f o
Article history:
Received 4 February 2011
Accepted 14 March 2011
Keywords:
Contaminants
Pollution
Fish larvae
Habitat modification
Sediment metals
a b s t r a c t
Changes to larval fish assemblages may have far reaching ecological impacts. Correlations between
habitat modification, contamination and marine larval fish communities have rarely been assessed in
situ. We investigated links between the large-scale distribution of stressors and larval fish assemblages in
estuarine environments. Larval fish communities were sampled using a benthic sled within the inner and
outer zones of three heavily modified and three relatively unmodified estuaries. Larval abundances were
significantly greater in modified estuaries, and there were trends towards greater diversity in these
systems. Differences in larval community composition were strongly related to sediment metal levels
and reduced seagrass cover. The differences observed were driven by two abundant species, Paedogobius
kimurai and Ambassis jacksoniensis, which occurred in large numbers almost exclusively in highly
contaminated and pristine locations respectively. These findings suggest that contamination and habitat
alteration manifest in substantial differences in the composition of estuarine larval fish assemblages.
? 2011 Elsevier Ltd. All rights reserved.
1. Introduction
A variety of anthropogenic activities contribute to widespread
pollution and contamination in the marine environment, which
influences the composition and health of ecological communities
(Johnston and Roberts, 2009). Estuaries are generally believed to be
exposed to the highest levels of contamination of any marine envi-
ronment due to their proximity to human settlements and their
positiondirectly downstreamof agricultural andindustrial activities
(Kennish, 2002; Lotze et al., 2006). Similarly, habitat modification in
estuarine systems is widespread, and many estuaries around the
world have experienced losses of seagrass, mangrove, saltmarshand
other vegetated habitats (Duke et al., 2007; Lotze et al., 2006;
Waycott et al., 2009). Many of these complex estuarine habitats
provide a ‘nursery’ function for ecologically and economically
important species of fish (Beck et al., 2001; Boesch andTurner,1984;
Dorenbosch et al., 2004; Robertson and Duke, 1987; Taylor et al.,
2005). Thus, it is imperative to understand how the modification
of estuaries through contamination and loss of habitat could be
impacting the early life stages of estuarine fish. Identifying stressors
andmonitoringecologicalimpactsinthesecommunitiesiscriticalto
managing and conserving native biodiversity in these systems.
It is well documented that toxic contaminants such as metals are
found in fish at various stages of their life cycle, often at levels that
may potentially reduce growth or survivorship (Alquezar et al.,
2006; Guo et al., 2008; Isosaari et al., 2006; Kojadinovic et al.,
2007; Miskiewicz and Gibbs, 1994). Evidence also points to the
potential adverse effects of toxic substances on reproduction and
development of fishes (Arkoosh et al.,1998; Hose et al., 1989; Jones
and Reynolds, 1997; Kingsford et al., 1997; Robinet and Feunteun,
2002). The less toxic enriching contaminants (such as nutrients or
sewage) may have either a weakly negative or largely positive effect
on abundance and diversity of adult fish (McKinley and Johnston,
2010) however, the effects on the egg and larval stages have rarely
been studied in situ. There are a small number of quantitative field
studies examining these effects at the population and community
level (Bervoets et al., 2005). This includes several studies demon-
strating changes to the composition and distribution of larval fish
communities around sewage plumes (Gray, 1996, 1997; Gray et al.,
1992; Kingsford et al., 1997) and one study which found negative
effects on embryo and larval development in relation to pulp mill
effluent (Karas et al., 1991).
Modification to marine habitats represents another potential
stressor of larval fish communities. Habitat degradation is the largest
source of ecological modification globally and the greatest threat to
biodiversity (Tilman et al., 1994). Australian estuaries have experi-
encedwidespreadchangestovegetativehabitatsoverthelastcentury,
* Corresponding author.
E-mail address: andrew.mckinley@hotmail.com (A.C. McKinley).
Contents lists available at ScienceDirect
Environmental Pollution
journal homepage: www.elsevier.com/locate/envpol
0269-7491/$ e see front matter ? 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.envpol.2011.03.008
Environmental Pollution 159 (2011) 1499e1509
Page 2
with well documented losses of mangrove (Valiela et al., 2001), salt-
marsh (Saintilan and Williams, 1999), and seagrass habitats (Walker
and McComb, 1992) in south-eastern Australia. The reduced extent
of these habitats within heavily modified estuaries arises due to
a variety of anthropogenic activities including dredging, increased
siltation, nutrient enrichment, contamination, clearing for coastal
development, and alterations to natural tidal or fluvial patterns
(Saintilan and Williams, 1999; Valiela et al., 2001; Walker and
McComb, 1992). Degradation of estuarine macrophytes is likely to
lead to changes to larval fish communities, as fishes require estuarine
habitats to survive early stages of their life cycle (Beck et al., 2001;
Boesch and Turner, 1984; Dorenbosch et al., 2004; Robertson and
Duke,1987).
We explore the impacts of large-scale anthropogenic effects on
estuarine larval fish communities across heavily modified and rela-
tively unmodified estuaries in New South Wales, Australia. Specifi-
cally,weexaminehowhighlevelsofmodificationandcontamination
in the estuarine environment affect the composition, abundance,
and diversityoflarvae.Inaddition,we utilizewaterquality, sediment
metals,andhabitatcoveragedatatoestimatetherelativeimportance
of these stressors within the broader modification regime.
2. Methods
2.1. Study sites and sampling design
Larval fish were sampled in six estuaries along the south coast of New South
Wales, Australia. These included three heavily modified estuaries e Port Jackson
(33?44.2580S, 151?16.5420E), Botany Bay (33?59.3520S, 151?11.4330E), and Port Kem-
bla(34?28.1210S,150?54.4100E), aswellasthreerelatively unmodifiedestuaries e Port
Hacking (34?04.6800S,151?09.3110E), Jervis Bay (35?04.7620S,150?44.8580E), and the
Clyde River (35?44.2330S,150?14.2720E) (Fig.1). The three heavily modified estuaries
are all highly anthropogenically disturbed environments near large urban and
industrial areas and are subject to intense commercial and recreational boating
traffic, historic and ongoing contamination, greater recreational fishing activity, and
widespread urbanization of their shoreline and catchment (Birch and Taylor, 1999;
DPI, 2010; Henry and Lyle, 2003; Scanes, 2010). Compared to the modified estu-
aries, the relatively unmodified estuaries have fewer recreational fishermen, less
boating traffic, less urbanization of the coastline and catchment, and virtually no
heavy industry (Birch and Taylor, 1999; DPI, 2010; Henry and Lyle, 2003; Scanes,
2010). Both the Clyde River (within Bateman’s Bay Marine Park) and Jervis Bay
(Jervis Bay Marine Park) are within marine parks (NSW, 1999). Port Hacking is
located between the suburbs of southern Sydney and the forested slopes of Royal
National Park, which lines the southern border of the estuary. While not strictly
within a marine park, Port Hacking’s catchment is largely intact due to its proximity
tothe Royal National Park and thereis no major industrial activitywithin theestuary
(NSWDNR, 2010). Previous monitoring indicates that the heavily modified estuaries
are nutrient enriched while nutrient levels in the relatively unmodified estuaries are
less elevated (Scanes, 2010).
Each estuary was divided into an inner and outer zone which reflected predicted
physio-chemical and contamination gradients. These zones were defined based on
their physical and biological characteristics. The inner zone is further up the estuary
and represents the lower reaches of the estuarine tributary where brackish waters
occur. In this zone turbidity, temperatures, and nutrient levels are higher than in the
outer zone (Dafforn et al., in press). The outer zone sites are near the marine
entrance tothe estuaries wheresalinity, coastal flushing, wave exposure and oceanic
current systems have greater influence. In this zone sediment grain sizes are also
larger and there is greater tidal influence (Dafforn et al., in press). Within each
estuary six sites with bottom characteristics that allowed uninterrupted trawling
were selected, three in each zone. All sampling was replicated over two seasons e
the first in the Spring of 2009 and again in the late summer of 2010.
2.2. Sampling methods
Larvae were sampled using a benthic sled trawl towed along bare sediment
behind a powerboat. Trawls were conducted along relatively flat profiles at a depth
of 3e12 m. GPS was used to ensure that all trawls were 250 m in length, towed at
a speed of 1.5 knots for approximately 5 min. The trawl was rigged to a four point
bridle using an approximate 3:1 warp to depth ratio. The trawl frame consists of
a stainless steel sled measuring approximately 1.5 m across and 2 m long. Within the
sled frame two plankton nets were mounted in 50 cm diameter stainless steel rings
15 cm off the bottom. Each of these nets consisted of a 50 cm ? 300 cm (long) conical
plankton net with 250 mm mesh. A 1 L plastic sample jar was affixed to each cod end.
This yielded two sample jars for each trawl, one of which was processed for data
while the other was retained as a backup.
Because it is wellknownthat theverticaland spatial distribution of larvae canbe
influenced by light conditions and diel period, several precautions were taken to
ensure consistency in these variables (Bridger, 1956; Pittman and McAlpine, 2003).
All sampling was conducted at night following the incoming tide up the estuary
(ie. starting in the outer zone and moving inwards). In order to standardize light
conditions sampling was conducted each month within a two week window around
the new moon (one week before and one week after the new moon). All samples
were immediately preserved in a buffered 5% formalin/seawater mixture for
transportation back to the laboratory. Where possible larvae were sorted and
identified to species using the current taxonomic standard (Neira et al., 1998). For
some taxa larvae were only sorted to genus or family where current taxonomic
knowledge is insufficient for species level identification. A variety of Gobiidae sp.
Fig. 1. Location of study sites in a) Port Jackson, b) Botany Bay, c) Port Hacking, d) Port Kembla, e) Jervis Bay, and f) Clyde River estuaries. A Indicates outer zone sites C Indicates
inner zone sites.
A.C. McKinley et al. / Environmental Pollution 159 (2011) 1499e1509
1500
Page 3
were distinguished as morphologically distinct varieties and were included as
separate ‘species’ within the analysis. Due to unresolved taxonomic issues, these
unidentified goby species are presented as ‘unidentified Gobiidae sp.’. See Appendix
1 for detailed species information.
A calibrated flow meter was affixed to the trawl and readings were used to
standardize all larval abundance results to 100 m3of sea water. At each sampling
location four replicate water samples of 1 L each were taken at a depth of 1 m using
a water sampling tube. These samples were combined in a plastic container on the
vessel and basic water quality data was measured from this water at the time of
sampling using a calibrated YSI 6820 V2 sonde. In a parallel studysurficial sediments
were collected from sites in close proximity to the trawls. Samples were oven-dried
before being digested and analyzed with ICP-OES following the methods outlined by
Hill et al. (2009). Recoveries were calculated against certified reference materials
and all metals used in this study were within accepted recovery limits. Arsenic and
mercury recoveries were insufficient for further analysis (Dafforn et al., in press).
Vegetative habitat size and cover were calculated using estuarine fact sheet moni-
toring values (NSWDNR, 2010).
2.3. Statistical analysis
All multivariate and univariate analysis was conducted using mixed model
PERMANOVA in PRIMER v.6 (Anderson, 2001). Prior to analysis abundance data was
log(x þ 1) transformed. BrayeCurtis similarity matrices were calculated for multi-
variate data while Euclidean similarity matrices were used for univariate measures.
The PERMANOVA design employed in the course of this analysis consisted of the
following factors:
Moe Modification e HeavilyModified or RelativelyUnmodified (2 levels,Fixed).
Ti e Time e November or February (2 levels, Fixed).
Zo e Zone e Inner or Outer (2 levels, Fixed).
Es e Estuary(Modification) e (6 estuaries, Random).
Si e Site(Estuary(Modification) ? Zone) e (36 sites, Random).
Monte Carlo p-values were used in some places where the number of unique
permutations was less than 20. Analysis of water quality, metals, and habitat cover
covariates was conducted using the DistLM function of PERMANOVA. This program
calculates a distance-based multivariate multiple regression (e.g. dbRDA) for any
linear model on the basis of any distance measure, using permutation procedures
(McArdle and Anderson, 2001). Covariate factors were analyzed graphically using
Principal Coordinated Ordination (PCO). PCO is a computer program that performs
a principal coordinate analysis of anysymmetric distance matrix. This analysis isalso
called metric multi-dimensional scaling (Anderson, 2003).
3. Results
3.1. Estuary characteristics
Estuaries displayed similar average water quality conditions,
though differences were found in most parameters between
zones (Table 1). Highersediment metals values were recordedin the
modified estuaries, particularly in the inner zone sites where
anthropogenic contamination is greater. See Dafforn et al. (in press)
for detailed description and analysis of the sediment metals data. In
many of the modified sites sediment metals values were above
levels predicted to have biological effects according to water quality
guidelines (ANZECC, 2010; Dafforn et al., in press). On average
relatively unmodified estuaries had greater coverage of mangroves
(22.4%) and seagrass (10.5%) relative to the modified estuaries (1.8%,
2.6% respectively). These vegetated habitats are virtually absent
from Port Kembla and Port Jackson (NSWDNR, 2010). The coverage
of saltmarsh was similar between relatively unmodified (4%) and
modified (4.8%) estuaries though this was due to large saltmarsh
patches in Botany Bay (Table 2).
3.2. Larval fish assemblages
In total more than 10,200 fish larvae were collected and iden-
tified during the study. The summarized larval dataset can be found
in Appendix 1. The abundance of larval fish was significantlygreater
in the heavily modified estuaries (p ¼ 0.003). There was a non-
significant trend towards increased species richness (p ¼ 0.19) and
Table 1
Mean ? SE. Water quality and benthic sediment metals values. ‘All Metals’ represents the normalized total of values for Co, Cr, Cu, Fe, Mn, Ni, Pb and Zn from Dafforn et al. (in
press). Individual values are presented for Cu, Ni, and Pb.
Temp (?C) Sal &
pH
OuterInnerOuterInnerOuterInner
Heavily
Modified
Estuaries
Port Jackson
Botany Bay
Port Kembla
22 ? 0.2
23.5 ? 0.5
22.8 ? 0.2
21.8 ? 0.6
22.3 ? 0.4
20.1 ? 0.6
23.5 ? 0.6
24.8 ? 0.3
23.3 ? 0.2
23.6 ? 0.5
22.7 ? 0.3
23.0 ? 0.8
Cu (mg kg?1)
36.3 ? 0.3
34.7 ? 1.2
36.3 ? 0.2
35.4 ? 0.2
35.4 ? 0.4
35.5 ? 0.7
34.7 ? 0.6
29.5 ? 2.5
36.1 ? 0.2
34.9 ? 0.7
35.1 ? 0.6
30.8 ? 2.5
8.1 ? 0.0
8.2 ? 0.0
8.2 ? 0.0
8.1 ? 0.0
8.1 ? 0.0
8.1 ? 0.0
Pb (mg kg?1)
7.9 ? 8.5
8.0 ? 0.0
8.2 ? 0.0
8.0 ? 0.0
8.1 ? 0.0
7.9 ? 0.0
Relatively
Unmodified
Estuaries
Port Hacking
Jervis Bay
Clyde River
All Metals (Normalized Total)
Ni (mg kg?1)
OuterInnerOuterInnerOuterInner OuterInner
Heavily
Modified
Estuaries
Port Jackson
Botany Bay
Port Kembla
?3.9 ? 0.1
?2.7 ? 0.3
15.9 ? 1.8
?1.6 ? 0.9
?5.2 ? 0.0
?2.5 ? 0.2
6.3 ? 3.7
5.3 ? 1.0
7.5 ? 3.4
?7.4 ? 0.8
?7.9 ? 0.0
?3.7 ? 1.3
9.5 ? 3.2
15.2 ? 5.4
118.1 ? 17.4
31.6 ? 20.0
7.6 ? 2.8
1.2 ? 0.8
151.7 ? 37.7
58.6 ? 1.9
163.4 ? 64.3
0.0 ? 7.0
9.8 ? 3.2
6.9 ? 4.4
1.0 ? 0.3
1.6 ? 0.1
10.5 ? 1.9
1.8 ? 1.0
0.8 ? 0.3
2.4 ? 0.4
16.2 ? 4.1
25.0 ? 1.6
16.0 ? 2.0
0.9 ? 2.2
0.4 ? 0.1
9.8 ? 3.0
11.0 ? 0.4
13.2 ? 4.5
81.9 ? 8.6
17.3 ? 10.6
0.9 ? 0.6
2.2 ? 0.3
243.1 ? 68.7
86.0 ? 5.3
110.1 ? 37.4
5.2 ? 5.4
1.3 ? 0.6
10.0 ? 3.0
Relatively
Unmodified
Estuaries
Port Hacking
Jervis Bay
Clyde River
Table 2
Size of vegetative habitats and % of estuary with vegetative habitats (NSWDNR, 2010).
Estuary SizeHabitat Size (km2) % Habitat Cover
SeagrassMangroveSaltmarshSeagrassMangroveSaltmarsh
Heavily
Modified
Estuaries
Port Jackson
Botany Bay
Port Kembla
49.7
80
1.6
0
6.238
0
0
4.227
0
0 0.00
7.80
0.00
0.00
5.28
0.00
0.00
14.47
0.00
11.573
0
Relatively
Unmodified
Estuaries
Port Hacking
Jervis Bay
Clyde River
110.807
0.972
6.05
0.307
3.314
1.999
0.082
0.521
1.486
7.34
18.34
5.86
2.79
62.53
1.94
0.75
9.83
1.44
5.3
103.2
A.C. McKinley et al. / Environmental Pollution 159 (2011) 1499e1509
1501
Page 4
Shannon diversity (0.074) in the heavily modified estuaries (Fig. 2,
Table 3).
Multivariate analysis of the community composition found that
modifiedandunmodifiedestuaries
(p ¼ 0.028) (Fig. 3). Several of the random interaction terms were
also significantly different (e.g. Mo ? Zo ? Ti). Here and elsewhere,
the test of the main effects can still be considered, as the higher
level fixed factor effect remains relevant regardless of the outcome
of the interaction with a random factor (Quinn and Keough, 2002).
Simper analysis revealed that the top six species contributing to
this difference were Paedogobius kimurai (wide gape paedomorphic
goby), Gobiopterus semivestita (transparent goby), Arenigobius spp.
(bridled goby spp.), Hyperlophus vittatus (sandy sprat), Hyperlophus
transucidus (translucent sprat) and Ambassis jacksoniensis (Port
Jackson glassfish) (Fig. 4, Table 5). Collectively these species
accounted for 37% of the difference between the modified and
relatively unmodified estuaries.
differedsignificantly
3.3. Covariates analysis e modified vs. relatively
unmodified estuaries
Salinity, pH, temperature, all sediment metals, % seagrass, %
mangrove, and % saltmarsh cover were all found to have a signifi-
cant relationship with the larval communitycomposition according
to the DistLM analysis (Table 4b). However, DistLM is considered
a poor predictor of the relative strength of these effects and so it
was used only to identify appropriate covariates to test in the PCO
(Anderson, 2003; McArdle and Anderson, 2001). As stated earlier,
multivariate analysis of community composition found that
modified and relatively unmodified sites differed significantly
(p ¼ 0.028). PCO plots indicate that the major cluster of modified
sites correspond strongly to both increased sediment metals levels
and decreased coverage of seagrass. Salinityalso correlates strongly
but did not show a clear trend by modification (Fig. 5a). All sedi-
ment metals trended in approximatelythe same directionand were
inversely related to vegetative cover, such that the most contami-
nated sites occurred primarily in the estuaries with the lowest
seagrass cover. This suggests that there is a strong relationship
between sediment metals levels, reduced vegetative cover, and
community composition in the heavily modified estuaries. In
contrast, the major clustering of relatively unmodified sites showed
little relationship to the metals and vegetative cover covariates
(Fig. 5a, Table 4).
Fig. 5b plots the species which were highly correlated with the
major clusters of modified and relatively unmodified sites (those
with a correlation factor >0.6). In order of the power of this rela-
tionship, P. kimurai, G. semivestita, A. bifrenatus, and H. transucidus
are more abundant in the sites that are highly metal contaminated
and have lower seagrass cover (Fig. 5b). In orderof the powerof this
relationship, A. jacksoniensis, and H. vittatus are more abundant in
the relatively unmodified sties (Fig. 5b). Notably, P. kimurai and
A. jacksoniensis were the 2nd and 3rd most abundant species in this
study, and each was encountered almost exclusively in modified/
relatively unmodified sites (respectively).
4. Discussion
We documented large differences between larval fish assem-
blages living in heavily modified and relatively unmodified estu-
aries. Total abundance of fish larvae was significantly greater in the
Table 3
Univariate analysis of the impacts of modification on a) Larval abundance, b) Species richness, c) Shannon diversity. Factors: Mo ¼ Modification, Zo ¼ Zone (Inner vs. Outer),
Ti ¼ Time of Sampling, Es ¼ Estuary, Si ¼ Site. Bold values correspond to plots in Fig. 2. , Indicates Monte Carlo p value.
SourcedF a) Abundanceb) Species Richnessc) Shannon Diversity
MSF
p-valueMSF
p-valueMSF
p-value
Mo
Zo
Ti
Es(Mo)
MoxZo
MoxTi
ZoxTi
Es(Mo)xZo
Es(Mo)xTi
MoxZoxTi
Si(Es(Mo)xZo)
Es(Mo)xZoxTi
Res
1
1
1
4
1
1
1
4
4
1
19.36
11.955
8.1882
0.529
10.619
5.6766
1.238
5.4498
4.1757
3.7201
2.917
0.40023
1.2436
36.598
2.1936
1.9609
0.18135
1.9486
1.3594
3.0933
1.8683
3.3578
9.295
2.3457
0.32184
,0.003
0.189
0.254
0.958
0.243
0.29
0.143
0.131
0.033
0.042
0.024
0.855
46.722
4.5
200
20.556
12.5
80.222
10.889
32.667
36.778
18
23.167
7.7778
7.1111
2.273
0.13776
5.4381
0.88729
0.38265
2.1813
1.4
1.4101
5.1719
2.3143
3.2578
1.0937
,0.19
0.767
0.091
0.473
0.605
0.204
0.317
0.247
0.007
0.18
0.003
0.364
0.36275
0.28464
1.5799
6.36E-02
1.2568
0.58704
4.29E-03
0.51954
0.16044
0.27969
0.33933
6.51E-02
0.1669
5.7006
0.54786
9.8475
0.18753
2.419
3.659
6.59E-02
1.5311
0.96128
4.2995
2.0331
0.38977
,0.074
0.471
0.027
0.949
0.212
0.117
0.816
0.218
0.454
0.116
0.044
0.812
24
4
24
Fig. 2. Mean ? SE a) Larval abundance, b) Species richness, and c) Shannon diversity in estuaries of differing levels of modification. Dotted line is average across all samples.
A.C. McKinley et al. / Environmental Pollution 159 (2011) 1499e1509
1502
Page 5
heavily modified estuaries and trends suggest that diversity could
also be higher in these modified environments. However, certain
species were strongly negatively associated with estuary modifica-
tion.Differencesincommunitycompositionwere strongly relatedto
both sediment metal levels and reduced seagrass cover in heavily
modified estuaries. Contamination levels and seagrass cover are
inversely related and experimental work is needed to establish
causation and to parse out the relative contribution of each factor to
the observed patterns.
4.1. Positive effects of estuary modification
Increased abundances of fishes in modified environments are
unlikely to result directly from either increased levels of metal
contaminationorreducedcoverofseagrass habitat.Afarmore likely
cause of this pattern would be nutrient enrichment. Monitoring
indicates that nutrient levels in the three heavily modified estuaries
are elevated compared to the relatively unmodified estuaries
(Scanes, 2010) although data was not available at sufficient resolu-
tion to formally analyze this relationship. Trends in this study
suggest that larval fish communities mayalso be more diverse in the
modified estuaries. Several studies have demonstrated that forms of
contamination which have an enriching effect (e.g. nutrient run-off,
fish farms, sewage, hydrocarbons, etc.) increase both the abundance
and diversity of adult fish assemblages (McKinley and Johnston,
2010; McKinley et al., in review). This is the first study to observe
positive relationships between anthropogenic modification of
estuaries and the abundance of larval fish.
4.2. Impacts of metals contamination
A variety of studies indicate that adult fish are fairly resilient in
the face of anthropogenic contaminants and adult fish assemblages
do not appear to be as sensitive to contaminants as invertebrates or
fish larvae (Johnston and Roberts, 2009; McKinley and Johnston,
2010). In most field studies contaminants have been shown to
have either weakly negative or a largely positive effect (where
enriching contaminants are present) on adult fish abundance and
diversity (McKinley and Johnston, 2010). However, most of these
studies have focused primarily on adults of large bodied predatory
fishes which are highly mobile (McKinley and Johnston, 2010).
This contrasts to the larvae examined in this study, which are
primarily small bodied species that are comparatively less mobile
at maturity (e.g. Gobiidae, Clupeidae and Apogonidae spp.). Whilst
large species may accumulate contaminants to a greater degree
than larvae or invertebrates due to their high trophic position, they
Heavily Modified
Relatively Unmodified
3D Stress: 0.17
p = 0.028
Fig. 3. Three dimensional MDS plot of multivariate assemblage composition by
modification. Symbols represent centroids of the assemblage composition. Heavily
modified includes sites in Port Jackson, Botany Bay, and Port Kembla. Relatively
unmodified includes sites in Port Hacking, the Clyde River, and Jervis Bay.
Fig. 4. Mean ? SE larval abundance by estuary for top six species contributing to differences between heavily modified and relatively unmodified estuaries.
A.C. McKinley et al. / Environmental Pollution 159 (2011) 1499e1509
1503
Page 6
can be highly mobile so direct exposure times are not certain, their
diets are comparatively diverse, and they have a higher capacity for
physiological resistance and tolerance (van der Oost et al., 2003;
Wirgin and Waldman, 1998).
In contrast, significant evidence points to developmental and
reproductive susceptibility to contaminants in fish populations
(Arkoosh et al., 1998; Hose et al., 1989; Jones and Reynolds, 1997;
Kingsford et al., 1997; Robinet and Feunteun, 2002). Studies have
found reduced egg and larval abundance due to exposure to
sewage sludge (Waring et al., 1996), behavioral and metabolic
changes with heavy metal exposure (Kienle et al., 2008; Sreedevi
et al., 1992), increased incidents of larval deformity due to sewage
plumes, chemical effluent and tributylin exposure (Hu et al.,
2009; Kingsford et al., 1997; Vetemaa et al., 1997), and reduced
fish condition, survivorship and growth with exposure to metals
(Bervoets and Blust, 2003; Canli and Atli, 2003; Hutchinson et al.,
1994). While few of these effects have been verified in at the
community level in wild populations, it is not unreasonable to
expect that many of these impacts could be detected in wild
larval fish assemblages. As such, it is probable that contamination
impacts have directly contributed to differences in the larval
fish assemblage between modified and relatively unmodified
estuaries.
In this study the abundance of several species were positively
correlated with highly contaminated areas, which could imply that
these species favor these sites or are comparatively resistant to
pollution effects. Notably, P. kimurai were very strongly associated
with sediment metals levels. This species was extremely abundant
in highly contaminated sites; in such areas they accounted for
Table 4
a) Multivariate analysis of the impacts of modification on larval community
composition. Factors: Mo ¼ Modification, Zo ¼ Zone (Inner vs. Outer), Ti ¼ Time of
Sampling, Es ¼ Estuary, Si ¼ Site. b) Results of DistLM covariate analysis. Bold values
correspond to Fig. 3 plot. , Indicates Monte Carlo p value.
SourcedF a) Community Composition
MSF
p-value
Mo
Zo
Ti
Es(Mo)
MoxZo
MoxTi
ZoxTi
Es(Mo)xZo
Es(Mo)xTi
MoxZoxTi
Si(Es(Mo)xZo)
Es(Mo)xZoxTi
Res
1
1
1
4
1
1
1
4
4
1
18,770
7057.6
8514.7
6654.1
5412.3
4482.7
1968.9
4386.7
3580.9
2231.7
2154.8
1754.3
1363
2.8208
1.6089
2.3778
3.0881
1.2338
1.2519
1.1223
2.0358
2.6272
1.2721
1.5809
1.2871
,0.028
0.219
0.087
0.001
0.349
0.319
0.371
0.001
0.001
0.316
0.001
0.14
24
4
24
Variable b) DistLM Covariate Results
SSF
p-value
Temp (?C)
Sal
pH
Co 228.616
Cr 267.716
Cu 327.393
Fe 238.204
Mn 257.610
Ni 231.604
Pb 220.353
Zn 206.200
%Seagrass
%Mangrove
%Saltmarsh
Estuary Area
8.51Eþ03
7.00Eþ03
5.49Eþ03
1.82Eþ04
1.96Eþ04
1.06Eþ04
1.68Eþ04
1.42Eþ04
1.95Eþ04
1.36Eþ04
1.55Eþ04
1.10Eþ04
6.20Eþ03
9409.6
7.35Eþ03
3.1395
2.5608
1.992
7.0587
7.6637
3.9677
6.4673
5.4071
7.6265
5.1363
5.9537
4.1003
2.2589
3.4858
2.6935
0.003
0.004
0.029
0.001
0.001
0.001
0.001
0.001
0.001
0.001
0.001
0.001
0.011
0.001
0.003
Table 5
Univariate analysis of the impacts of modification on the abundance of the top six species contributing to differences between heavily modified and relatively unmodified estuaries. Factors: Mo ¼ Modification, Zo ¼ Zone (Inner
vs. Outer), Ti ¼ Time of Sampling, Es ¼ Estuary, Si ¼ Site. Bold values correspond to plots in Fig. 4. , Indicates Monte Carlo p value.
Source
dF
a) Ambassis jacksoniensis
Port Jackson Glassfish
b) Paedogobius kimurai Wide
Gape Paedomorphic Goby
c) Arenigobius spp.
Bridled Goby spp.
d) Gobiopterus semivestita
Transparent Goby
e) Hyperlophus transucidus
Translucent Sprat
f) Hyperlophus vittatus
Sandy Sprat
MS
F
p-value
MS
F
p-value
MS
F
p-value
MS
F
p-value
MS
F
p-value
MS
F
p-value
Mo
1
27.921
21.09
,0.005
106.8
5.0101
,0.092
45.827
6.2256
,0.077
47.307
3.9835
,0.107
29.698
2.9652
,0.145
0.4408
3.11E-02
,0.875
Zo
1
5.3218
1.0103
0.38
11.16
2.5078
0.178
1.1148
0.60947
0.459
41.333
5.1813
0.048
20.957
3.4281
0.079
2.25E-02
7.88E-03
0.941
Ti
1
4.9414
0.79944
0.393
3.3772
1.4373
0.301
11.025
41.378
0.003
0.81232
1.1328
0.356
1.116
1.6502
0.275
2.5402
0.22698
0.689
Es(Mo)
4
1.3239
0.58894
0.657
21.317
17.73
0.001
7.3611
4.3679
0.007
11.876
9.1728
0.001
10.016
22.901
0.001
14.19
7.4158
0.002
MoxZo
1
2.756
0.5232
0.517
12.333
2.7714
0.172
2.257
1.2339
0.298
15.455
1.9374
0.314
23.701
3.8769
0.048
0.21389
7.51E-02
0.817
MoxTi
1
2.2305
0.36086
0.583
9.1559
3.8965
0.132
5.13E-02
0.19262
0.663
0.1117
0.15577
0.693
0.58669
0.86754
0.362
3.7085
0.33138
0.601
ZoxTi
1
1.4214
10.022
0.047
1.3765
0.93777
0.409
0.61466
0.2738
0.634
0.74144
0.8802
0.409
0.47051
0.63674
0.492
2.9029
0.66492
0.457
Es(Mo)xZo
4
5.2677
2.3433
0.083
4.4502
3.7012
0.02
1.8291
1.0854
0.365
7.9772
6.1616
0.004
6.1134
13.978
0.001
2.8487
1.4887
0.24
Es(Mo)xTi
4
6.181
3.6434
0.02
2.3498
4.6984
0.008
0.26644
0.16116
0.952
0.71707
1.083
0.375
0.67627
8.6253
0.001
11.191
6.6171
0.002
MoxZoxTi
1
6.0243
42.478
0.003
0.67833
0.46214
0.515
6.9228
3.0837
0.167
8.64E-02
0.1026
0.771
0.95335
1.2902
3.13E-01
9.446
2.1637
0.204
Si(Es(Mo)xZo)
24
2.248
1.3251
0.255
1.2024
2.4041
0.021
1.6853
1.0194
0.494
1.2947
1.9554
0.052
0.43735
5.578
0.002
1.9135
1.1314
0.401
Es(Mo)xZoxTi
4
0.14182
8.36E-02
0.99
1.4678
2.9349
0.042
2.2449
1.3579
0.29
0.84235
1.2723
0.289
0.73894
9.4246
0.001
4.3658
2.5813
0.064
Res
24
1.6965
0.50012
1.6532
0.66209
7.84E-02
1.6913
A.C. McKinley et al. / Environmental Pollution 159 (2011) 1499e1509
1504
Page 7
60e95% of the larval assemblage and they were hyper-abundant
particularly in the most highly contaminated inner zone sites of
Port Jackson and Port Kembla. In contrast, this species was rarely
encountered in the relatively unmodified estuaries. P. kimurai
occurred in the highly metals contaminated sites both in estuaries
where there were virtually no vegetative habitats (Port Jackson and
Port Kembla) and directly adjacent to mangrove and seagrass
patches (Botany Bay). This implies that this species is particularly
successful in highly contaminated sites and may be unusually
resistant to contaminants. Contamination resistance in fish has
been demonstrated in some cases (Wirgin and Waldman, 2004; Xie
and Klerks, 2004). In addition, the distribution of this species is
unusually patchyand there is some speculation that it is an invasive
originating from South East Asia (eg. Thailand). However, this has
not been confirmed (Iwata et al., 2001; Neira et al.,1998). P. kimurai
is also unusual among fish as it is sexually mature at a very small
size e adults average approximately 1.5 cm in length and females
pregnant with eggs are approximately the same size as other
gobies’ larvae (Iwata et al., 2001). It has been demonstrated that
a variety of highly invasive invertebrate and fish species are rapidly
maturing and unusually contamination resistant (Alcaraz et al.,
2005; Dafforn et al., 2009; Piola and Johnston, 2008). It is
possible that this species is also a marine invader displaying these
characteristics.
4.3. Impacts of vegetative habitat alteration
Correlative studies are limited in their ability to predict the
magnitude and relative importance of covarying factors (Shipley,
2002). In this study, sites with high levels of metals in the sedi-
ment also tended to have reduced coverage of vegetative habitats;
this is likely the case because the core mechanisms of estuary
contamination exposure (e.g. run-off, urbanization of shoreline/
catchment, outflows, etc.) also tend to precipitate habitat alteration
in estuarine systems (Drinkwater and Frank, 1994; Rogers et al.,
2002). Run-off which carries metals and other contaminants is
also known to increase turbidity in many cases, hence lowering
light levels and impacting plant growth (Longstaff and Dennison,
1999). In many cases increased nutrient levels accompany other
forms of contamination (McKinley and Johnston, 2010). Increased
nutrient availability has been shown to increase the relative
dominance of epiphytic plants in seagrass beds, often to the
detriment of the seagrass community (Harlin and Thorne-Miller,
1981). For these reasons losses of some estuarine vegetative
habitats may be strongly correlated with levels of contaminant
exposure. Contaminants such as metals are also acutely toxic to
some seagrass and other plant species, and trace metal run-off is
a well documented cause of seagrass habitat loss (Macinnis-Ng and
Ralph, 2002; Prange and Dennison, 2000; Warnau et al.,1995). It is
therefore difficult to distinguish the relative effects of contamina-
tion vs. habitat loss as these stressors may be intimately related in
the estuarine system.
Many of the species which contributed strongly to the trends in
this study feed on vegetative matter, lay their eggs on plants, or use
estuarine vegetation for shelter during the larval and post settle-
ment stages of their life cycle (Miskiewicz, 1987). It is therefore
possible that changes to the larval assemblage have directly
resulted from loss of vegetative habitats in the modified estuaries.
For example, A. jacksoniensis and F. lentiginosus primarily settle in
seagrass beds during their juvenile and adult stages while juvenile
and adult Gerres subfasciatus (roach) utilize mangroves, so changes
to, or the absence of these habitats could explain decreased
abundance of these species in the modified estuaries (Gray et al.,
1996; Jelbart et al., 2007; Jenkins et al., 1997; Neira et al., 1998).
While most of the larvae sampled in this study were taken over
bare sediment and were at the pre-settlement (planktonic) stage of
their life cycle, changes to these vegetative habitats could impact
these larvae when they reach their juvenile and adult stages. It is
therefore possible that losses of vegetative habitats have reduced
the available habitat for these species, which would reduce the
population size and hence larval abundance in the long term.
4.4. Estuarine opportunists vs. truly estuarine species
It is well known that a variety of fish species utilize estuaries
during their life cycle. Many ‘estuarine opportunist’ species spawn
at sea and find their way into the estuarine environment using
oceanic currents for transport, entering the estuary at the preflex-
ion and postflexion stages (after hatching) based on a variety of
environmental cues (Neira and Potter, 1992; Norcross and Shaw,
-40-200 204060
PCO1 (17.3% of total variation)
-60
-40
-20
0
20
40
PCO2 (14.9% of total variation)
Heavily Modified
Relatively Unmodified
Salinity
Co
Cr
Cu
Fe
Mn
Ni
Pb
Zn
%Seagrass
a
-40-200 2040 60
PCO1 (17.3% of total variation)
-60
-40
-20
Gobiopterus semivestita
0
20
40
PCO2 (14.9% of total variation)
Heavily Modified
Relatively Unmodified
Ambassis jacksoniensis
Arenigobius spp.
Hyperlophus transucidus
Hyperlophus vittatus
Paedogobius kimurai
b
Fig. 5. Principal Coordinated Ordination (PCO) of correlations between covariate factors and two dimensional plots of community composition by modification. a) Metals
contamination, habitat modification, and water quality covariates. (Pearson Correlation > 0.2). b) Plots of top six species contributing to differences between heavily modified and
relatively unmodified estuaries (Pearson Correlation > 0.6).
A.C. McKinley et al. / Environmental Pollution 159 (2011) 1499e1509
1505
Page 8
1984; Potter et al., 1988). In contrast, truly estuarine species live
within the estuary for their entire life cycle, including when
spawning. Of the species which contributed most to the differences
between heavily modified and relatively unmodified estuaries four
are truly estuarine species (P. kimurai, G. semivestita, Arenigobius
spp., and H. transucidus) while the other two (A. jacksoniensis and
H. vittatus) live primarily within the estuary but spawn at sea
(Miskiewicz,1987; Neira et al.,1998). All of these species spend the
majority of their life cycle in the estuarine environment and so
changes to that environment are likely to have an impact, regard-
less of whether or not they spawn at sea or within the estuary.
However, it is possible that high levels of contamination and
habitat modification disproportionately impact species which
spawn in the estuary environment itself. Estuarine opportunist
species which spawn at sea and enter estuaries later in their life
cycle may be less affected by these stressors as they may be less
exposed to contaminants during their early (pre-hatching) growth
stages. It is therefore possible that impacts experienced during
larval stages of estuarine fishes’ could reduce their relative
competitiveness and hence increase the dominance of taxa which
spawn at sea. It is also possible that some of the estuarine oppor-
tunist species are descended from parents who lived in other
estuaries and may not have been exposed to contamination levels
reflective of the conditions of the estuary in which they were found
during the larval phase of their life cycle.
It should be noted that the temporal and spatial variability of
larval fishes has been found to be a significant issue in previous
studies (Gray,1996,1997; Gray and Miskiewicz, 2000). In this study
we sampled over a large spatial scale with a relatively high level of
spatial replication both within and between estuaries. Despite
significant differences between the random factor of sites for many
analyses, our sampling design and level of replication was suffi-
ciently robust to show clear differences by estuary and modifica-
tion. We have also sampled across two seasons, during which
a large proportion of estuarine species would have been breeding
(Neira et al., 1998). Despite a high degree of temporal variability
between these rounds of sampling, time was not sufficiently strong
to produce a significant result in most of our analyses. For these
reasons we do not believe our results to be strongly spatially or
temporally restricted.
5. Conclusion
It is clear that there are large-scale differences between the
larval fish assemblages living in heavily modified and relatively
unmodified estuaries. Differences in larval fish community
composition were strongly related to both sediment metal levels
and reduced seagrass cover in heavily modified sites. We believe
that it is likely that habitat alteration and estuarine sediment
contamination are interrelated stressors which have contributed to
the observed differencesbetween
unmodified estuaries. Ultimatelychanges to larval fish assemblages
may have far reaching ecological impacts both for the adult fish
community and other organisms. Notably, the impacts of stressors
at the larval stage of economically and culturally important fish
species are poorly studied and little understood. The absence of
studies examining anthropogenic impacts on estuarine fish larvae
represents a major gap in the environmental impact literature and
further investigation and monitoring is warranted.
modified and relatively
Acknowledgements
This research was primarily supported by the Australian
Research Council through an Australian Research Fellowship
awarded to ELJ and a Linkage Grant awarded to ELJ. The writing of
this manuscript was also supported through the Canadian National
Sciences and Engineering Research Council through an award given
to AM. We would like to thank Dr. Katherine Dafforn, Cian Foster-
Thorpe and Shinjiro Ushiama for their help and contributions of
data for the project. We would also like tothank the Bluescope Steel
Company and Marine Parks NSW for their generous support.
Appendix
Appendix 1
Averageabundance data identified tolowest taxonomic level byzone and estuary. Gobiidae sp. represent the total of all observed morphologically distinct taxawhich could not
be identified to species.
FamilyTaxon Botany BayPort Jackson Port Kembla Clyde River Jervis BayPort Hacking
Outer InnerOuterInner OuterInnerOuter Inner OuterInner Outer Inner
Ambassidae
Glassfish
Ambassis jacksoniensis
Port Jackson Glassfish
Ambassis marianus
Estuary Glassfish
Foa sp.
Cardinalfish sp.
Siphamia cephalotes
Wood’s Siphonfish
Apogonidae sp. A
Cardinalfish sp. A
Apogonidae sp. B
Cardinalfish sp. B
Apogonidae sp. C
Cardinalfish sp. C
Atherinidae sp.
Hardyhead sp.
Hempheridae sp.
Garfish sp.
26.321.125.02 0.336.623.3520.78 10.86 570.1033.34 46.69 6.66
0.00 0.00 0.340.000.00 0.000.00 0.000.00 0.000.000.00
Apogonidae
Cardinalfish
0.000.000.00 3.080.00 0.00 0.000.00 0.000.000.000.00
0.36 0.003.47 0.000.00 0.00 0.000.00 18.96 2.680.000.00
2.510.001.98 0.000.000.00 0.000.000.370.000.000.64
0.000.002.360.33 0.000.000.000.000.670.270.36 0.00
0.00 0.00 0.990.99 0.00 0.420.000.00 0.000.00 0.000.00
Atherinidae sp.
Old World Silversides
Belonidae
Needlefish
0.731.25 0.000.000.000.000.000.000.00 2.150.390.00
0.731.250.000.000.000.000.76 0.490.000.000.390.00
A.C. McKinley et al. / Environmental Pollution 159 (2011) 1499e1509
1506
Page 9
Appendix 1 (continued)
Family Taxon Botany BayPort JacksonPort Kembla Clyde River Jervis Bay Port Hacking
Outer Inner OuterInner OuterInner Outer InnerOuterInnerOuter Inner
Blenniidae
Blennies
Omobranchus anolius
Oyster Blenny
Omobranchus rotundiceps
Combtooth Blenny
Petroscirtes lupus
Brown Sabretooth Blenny
Callionymidae sp.
Dragonet sp.
Trachurus novaezelandiae
Yellowtail Scad
Cristiceps sp.
Weedfish sp.
Etrumeus teres
Maray
Herklotsichthys castelnaui
Southern Herring
Hyperlophus transucidus
Translucent Sprat
Hyperlophus vittatus
Sandy Sprat
Sardinops sagax
Pilchard
Spratelloides robustus
Blue Sprat
Creedia haswelli
Slender Sandburrower
Engraulis australis
Australian Anchovy
Gerres subfasciatus
Roach
Gobiesocidae sp.
Clingfishes sp.
Afurcagobius tamarensis
Tamar Goby
Arenigobius spp.
Half Bridled and
Bridled Goby
Favonigobius lentiginosus
Long Finned Goby
Gobiidae sp.
Unidentified Goby sp.
Gobiopterus semivestita
Transparent Goby
Paedogobius kimurai
Wide Gape Paedomorphic Goby
Pseudogobius sp.
Eastern Bluespot Goby
Redigobius macrostoma
Large Mouth Goby
Schindleriidae sp.
Schindler’s Goby
Tridentiger trigonocephalus
Trident Goby
Gonostomatidae sp.
Bristlemouth sp.
Girella tricuspidata
Luderick
Lesueurina platycephala
Common Sandfish
Lutjanidae sp.
Snapper sp.
Monacanthus chinensis
Fan Belly Leatherjacket
Monacanthidae sp.
Leatherjacket sp.
Monodactylus argenteus
Diamondfish
Schuettea scalaripinnis
Eastern Pomfret
Liza argentea
Flat Tail Mullet
Odacidae sp.
Weed Whiting sp.
5.03 3.730.50 0.00 0.35 0.000.000.60 0.00 0.00 0.000.00
1.090.00 0.005.30 0.00 0.000.380.770.000.00 0.00 0.00
0.00 0.00 0.000.34 0.00 0.00 0.000.00 0.000.00 0.00 0.00
Callionymidae
Dragonets
Carangidae
Jacks/Jack Mackerels
Clinidae
Clinids
Clupeidae
Herrings/Sprats
0.000.00 0.34 0.000.34 0.000.38 0.240.00 0.000.000.00
0.00 0.000.00 0.000.00 0.000.000.00 0.000.00 0.400.00
0.000.00 0.000.000.00 0.000.00 0.000.00 0.000.790.00
0.000.00 0.00 0.000.711.24 0.00 0.000.00 0.000.00 0.00
0.000.000.004.88 0.000.000.00 0.00 0.00 0.000.00 0.00
1.82109.62 0.0034.290.000.000.000.00 0.000.00 0.400.00
8.33 5.26 7.060.34 16.1542.9667.9258.51116.68 40.50 7.34 0.79
0.00 0.000.000.005.890.00 0.00 0.00 0.000.000.000.00
0.000.000.000.00 0.003.340.00 0.000.000.001.570.00
Creediidae
Sandburrower
Engraulidae
Anchovies
Gerreidae
Silver Biddies
Gobiesocidae
Clingfish
Gobiidae
Gobies
0.000.000.000.000.000.000.00 0.000.370.000.000.00
0.00 0.500.002.353.207.660.000.000.00 0.700.00 0.00
30.540.006.747.0212.780.8227.76 10.778.335.77 12.541.52
0.00 0.000.000.000.00 0.000.000.000.340.001.590.00
0.000.000.000.000.000.000.390.360.000.000.00 0.00
9.6748.63 10.2018.6543.8974.49 3.068.2516.501.128.092.50
2.960.00 4.840.331.130.41 0.395.063.957.1936.410.96
13.62 13.6213.62 13.6213.6213.62 13.6213.62 13.6213.6213.6213.62
5.29214.77 0.68244.131.39 1.100.001.500.007.390.000.32
0.781.5526.29 477.99 37.67164.780.350.000.340.000.794.18
Gobiidae
Gobies
0.001.2512.731.160.002.062.231.300.340.000.000.00
3.604.310.001.741.064.565.429.4513.1822.010.000.53
2.510.000.00 0.000.000.000.000.00 0.000.000.000.00
0.000.000.000.001.683.240.000.000.000.000.000.00
Gonostomatidae
Bristlemouths
Kyphosidae
Sea Chubs
Leptoscopidae
Sandfish
Lutjanidae
Snappers
Monacanthidae
Leatherjackets
0.000.000.000.000.000.000.380.000.000.000.000.00
0.000.000.000.00 0.000.000.000.00 0.00 0.630.00 0.00
0.000.000.340.000.340.000.000.000.00 0.005.09 0.00
0.00 0.000.340.00 0.000.000.000.00 0.00 0.000.000.00
0.001.680.00 1.090.00 0.000.000.000.000.000.00 0.00
0.00 0.000.340.00 0.000.000.380.000.000.000.400.00
Monodactylidae
Moonfish
0.000.000.000.000.000.000.00 0.360.000.27 1.980.00
0.000.000.000.000.000.000.760.000.00 0.000.000.00
Mugilidae
Mullets
Odacidae
Weed Whitings/Cales
0.000.000.000.000.35 0.420.00 0.000.000.000.000.00
0.000.000.000.000.000.000.000.001.380.000.000.00
(continued on next page)
A.C. McKinley et al. / Environmental Pollution 159 (2011) 1499e1509
1507
Page 10
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Appendix 1 (continued)
Family TaxonBotany Bay Port JacksonPort Kembla Clyde RiverJervis Bay Port Hacking
OuterInner OuterInner OuterInnerOuter InnerOuter InnerOuter Inner
Paralichthyidae
Large Tooth Flounders
Pempheridae
Sweepers/Bullseyes
Platycephalidae
Flatheads
Pseudorhombus jenynsii
Small Tooth Flounder
Pempheridae sp.
Bullseye sp.
Platycephalus fuscus
Dusky Flathead
Platycephalus sp.
Flathead sp.
Argyrosomus japonicus
Mulloway
Atractoscion aequidens
Teraglin
Sillago ciliata
Sand Whiting
Sillago flindersai
Eastern School Whiting
Sillago maculata
Trumpeter Whiting
Soleidae sp.
Sole sp.
Acanthopagrus australis
Yellowfin Bream
Sphyraena sp.
Barracuda sp.
Stigmatopora nigra
Wide Bodied Pipefish
Urocampus carinirostris
Hairy Pipefish
Vanacampus margaritifer
Mother of Pearl Pipefish
Synodontidae sp.
Lizardfish sp.
Pelates sexlineatus
Six Lined Trumpeter
Tetraodontidae sp.
Toadfish sp.
Centropogon australis
Fortesque
Tripterygiidae sp.
Triplefin Blenny sp.
0.00 0.000.00 0.000.000.001.830.94 0.000.270.000.47
0.42 0.000.00 0.00 0.00 0.000.00 0.00 0.370.000.000.00
0.000.000.000.00 0.000.351.14 2.20 1.600.002.290.00
0.00 0.000.87 0.000.000.000.000.000.000.000.000.00
Sciaenidae
Drums and Croakers
0.000.00 0.000.000.35 0.00 0.760.00 0.000.000.00 0.00
0.000.000.000.000.350.000.000.000.00 0.000.000.00
Silliginidae
Whitings
5.45 13.441.010.43 2.220.004.930.47 35.5010.803.61 1.46
17.991.002.820.000.00 1.201.140.00 2.270.003.900.00
1.0934.150.00 8.461.410.414.120.24 1.6812.61 1.570.32
Soleidae
True Soles
Sparidae
Sea Breams
Sphyraenidae
Barracudas
Syngnathidae
Pipefish/Seahorses
0.000.00 0.000.000.000.000.00 0.360.370.001.980.53
0.000.000.00 0.000.000.000.390.003.204.590.000.00
0.00 0.000.000.000.000.000.340.000.00 0.000.00 0.00
0.00 0.000.000.000.000.510.00 0.830.400.273.490.00
0.79 0.000.000.000.000.000.380.470.000.961.960.00
0.00 0.000.000.000.00 0.000.00 0.000.000.000.400.00
Synodontidae
Lizardfishes
Terapontidae
Grunter Perch
Tetraodontidae
Pufferfish
Tetrarogidae
Waspfish
Tripterygiidae
Triplefin Blennies
Total Abundance
0.000.000.000.00 0.000.000.000.450.000.000.000.00
0.00 0.000.000.000.000.000.000.000.000.361.57 0.47
0.000.000.00 0.00 0.000.00 0.000.001.600.000.000.00
0.003.181.01 0.000.340.00 0.39 0.451.601.26 1.590.00
28.050.001.044.581.330.000.380.002.971.841.93 0.00
169.70460.31104.91831.40153.17326.95160.77128.57816.66170.60 163.1634.96
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