127
Hydrobiologia 362: 127–143, 1998.
c 1998 Kluwer Academic Publishers. Printed in Belgium.
Mangrove zooplankton of North Queensland, Australia
I. Plankton community structure and environment
A. D. McKinnon & D. W. Klumpp
Australian Institute of Marine Science, P.M.B. No. 3, Townsville M.C., Queensland 4810, Australia
E-mail:d.mckinnon@aims.gov.au
Received 15 April 1997; in revised form 5 November 1997; accepted 18 November 1997
Key words: Mangrove, zooplankton, community, particulates, mixing
Abstract
Measurements of plankton community structure and trophic resources potentially available to planktonic copepods
were made in the mangrove estuaries of six rivers in Northeastern Australia. The Pascoe, Claudie, Lockhart,
McIvor and Daintree Rivers represent wet tropical systems on Cape York, whereas the Haughton River estuary
has restricted freshwater inflow because of a drier climate and freshwater diversion for agriculture. The Haughton
River was sampled approximately monthly between October 1992 and May 1994, and had a mean abundance
of zooplankton > 37 m of 200 l 1 (range 60–500 l 1 ). The Cape York rivers were sampled infrequently, and
zooplankton abundances ranged between 0.4 and 1400 l 1 . The zooplankton of all rivers was dominated by
copepods, particularly representatives of the genus Oithona which were characteristic of a distinct mangrove
fauna. Physical forcing influenced the zooplankton of mangrove estuaries much more than the measured biological
variables. The water column was characterised by high concentrations of particulate matter, up to 3.3 mg l 1 C and
1.1 mg l 1 N, of low food quality (as indicated by the C:N ratio). Phytoplankton biomass (as chlorophyll a) in all
six rivers was on average four-fold greater than in neighbouring coastal waters (1.1–12.6 g l 1 ), and 25% of this
chlorophyll a was derived from cells > 10 m, and thus potentially available to copepods. The degree of mixing,
determined by the combination of tidal state and the extent of freshwater input, appears to drive both the quantity
and quality of particulate material available to higher consumers and the distribution of zooplankton communities
within mangrove estuaries.
Introduction
Mangrove forests are important coastal habitats in tropical and sub-tropical regions of the world, and represent
a special case of estuarine environment characterised
by a close association between macrophyte production
and marine littoral communities (Por & Dor, 1984).
Mangrove forests have rates of leaf fall as high as
any other forest system (Pool et al., 1975), and nearly
all the organic detritus is derived from tree components (Alongi et al., 1992). Consequently, the majority
of above-ground production ultimately reaches marine
detrital food webs (Por, 1984). However, the importance of mangrove-based detrital food webs in sustaining nearshore pelagic secondary production is still
unclear, and it is possible that phytoplankton production plays a more important role than has previously been acknowledged (Robertson & Blaber, 1992).
The role of zooplankton in mangrove ecosystems is
virtually unknown (Robertson et al., 1992), despite
their pivotal role as intermediaries between these alternative carbon sources and higher consumers such as
fish. Zooplankton abundance within mangrove riverways is higher than in adjacent coastal waters, often by
more than order of magnitude (Robertson et al., 1988;
Robertson & Blaber, 1992). Furthermore, the few cases in which chlorophyll a concentration and primary
production have been measured indicate that mangrove
estuaries, at least in tropical Australia, are very productive areas when compared to neighbouring coastal
Pipsnr. 159406; Ordernr.: 7011559 BIO2KAP
hydr3992.tex; 8/06/1998; 20:36; v.5; p.1
Figure 1. (a) Location of the mangrove estuaries sampled, in North Queensland, Australia; (b) location of Haughton River sampling stations.
128
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129
waters (Robertson & Blaber, 1992). A large proportion of the juvenile fish found in mangrove systems
are zooplanktivorous (Robertson & Blaber, 1992), and
yet little is known about the trophic links supporting
these fish (Robertson et al., 1992). The limited zooplankton literature simply describes community structure and abundance, and there are no data available on
the growth rates or secondary production of mangrove
zooplankton.
By comparison, the physics of water and sediment transport in mangrove forests is relatively well
understood (Wolanski et al., 1992; Wolanksi, 1992,
1995). Tidal circulation in mangrove systems is the
dominant cause of water movement, and tidal currents
often exceed 1 m s 1 . Moreover, these currents are
strongly asymmetrical, with peak ebb currents up to
50% greater than peak flood currents. This phenomenon maintains the physiognomy of mangrove creeks
by exporting sediments, yet maintaining a deep tidal
channel which usually discharges into expansive areas
of inter-tidal mudflats (Wolanski et al., 1992). In addition to this physical barrier, lateral trapping of water
originating from mangrove estuaries within the coastal
boundary layer leads to the retention of water within
these systems (Wolanski et al., 1980). The waters of
mangrove estuaries are characterised by high turbidity,
high turbulence, and strong tidal currents, resulting in
an environment to which planktonic organisms must
have specific adaptations. This, together with limited
exchange with coastal waters, results in the development of a distinct mangrove pelagic community.
Our goal is to better understand the contribution of
zooplankton to energy flow in mangrove ecosystems.
In this paper we identify the components of zooplankton communities in a number of North Queensland
mangrove estuaries and the major trophic resources
available to pelagic consumers within them. Productivity of the main components of these systems is estimated elsewhere (McKinnon & Klumpp, 1998).
Methods
Study sites
The mangrove estuaries of Queensland are mostly
riverine forests (sensu Lugo & Snedaker, 1974), which
are periodically inundated by high tides and episodically flooded during the wet season. We consider
here five rivers on the Cape York Peninsular of North
Queensland, Australia, and one south of Townsville
(Figure 1a). The foreshore and major waterways of the
estuaries of these rivers are dominated by four species
of Rhizophora, with Ceriops (3 spp.) and Avicennia
marina behind them (Danaher, 1995). River systems
with substantial fresh water input, such as the Pascoe, Claudie and Lockhart Rivers, also support mangroves such as Bruguiera (5 spp.) and Heritiera littoralis, and the mangrove palm Nypa fruticans (Danaher, 1995). The Pascoe, Claudie, Lockart and McIvor
Rivers are in essentially pristine condition, whereas
appreciable areas in the Daintree and Haughton River catchments have been cleared for agriculture, and
consequent runoff may threaten the water quality of
these rivers (Bucher & Saenger, 1989). In addition,
two weirs on the Haughton River impound water for
agricultural use and prevent continuous freshwater flow
downstream except in periods of flood.
Field collection
Haughton River plankton was sampled at Cromarty
Landing on 18 occasions between 24 October 1992
and 25 May 1994. Transects comprising an additional
three stations from the mouth of the Haughton River
to Cromarty Landing (Figure 1b) were sampled with
triplicate midwater Niskin casts on three occasions to
establish the extent of upstream transport of coastal
plankton (= the null point, sensu Miller, 1983). We
endeavoured to sample during the day on or about the
high spring tide, although on 2 occasions (February
and April 1993) we sampled on the flood tide, and on
2 occasions (October 1993 and January 1994) we sampled on the ebb tide. At each station water temperature
and salinity was measured at 1 m depth intervals with
a portable salinometer, and secchi depth was recorded.
At Station C triplicate water samples were taken near
the bottom and surface with a Niskin bottle, and 5 l
volumes from each cast were filtered through a 37 m
nitex screen and the > 37 m fraction preserved. A
second set of Niskin casts collected water samples for
chlorophyll a, particulate carbon, particulate nitrogen,
and bacteria.
The Pascoe, Claudie, McIvor and Daintree rivers
were sampled in the dry season in May 1993 and June
1995 using the same techniques. Each river was sampled along a three-station transect from river mouth to
as close as practicable to fresh water. A reduced set
of samples lacking collections for bacteria and seston
C and N, was collected in the wet season from the
Lockhart and McIvor rivers in December 1995, and
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130
determination of > 37 m particulate carbon and nitrogen (hereafter referred to as ‘seston’). Two 100 ml
subsamples of the filtrate were filtered on 25 mm GF/F
filters for the analysis of chlorophyll a and of particulate carbon and nitrogen. An additional 250 ml subsample of the < 37 m filtrate was taken for analysis of
> 10 m chlorophyll a on a nitex screen. Filters were
frozen and stored until subsequent extraction in 90%
acetone and analysis of chlorophyll a by fluorometry
(Strickland & Parsons, 1972). Nitrogen content of filters was measured with an ANTEK chemi-luminescent
nitrogen analyser, with a Beckman 880 NDIR analyser
mounted in series for carbon analysis. A preliminary
set of samples measured for both inorganic and organic
carbon contained no measurable inorganic carbon, and
subsequently all particulate carbon was assumed to be
organic.
Zooplankton community composition and abundance
Figure 2. Station C (Cromarty Landing), Haughton River (a) Temperature profiles at; (b) salinity; (c) flow, measured at the Clare
gauging station 21 kilometres upstream of Station C. Flow data are
courtesy of Queensland Water Resources Commission.
the Pascoe, Lockhart and McIvor rivers in February
1996.
Determination of Chlorophyll a, particulate carbon
and nitrogen
From each Niskin sample, 1 l of water was filtered
through a 37 m nitex screen, which was then backwashed on to a pre-combusted Whatman GF/F filter for
A single 20 ml water sample from each Niskin sample
was fixed with 800 l of formaldehyde for the later enumeration of bacterial abundance using the direct count
method and the fluorochrome DAPI (4’6-diamidino-2phenylindole) to stain bacterial cells (Porter & Feig,
1980). Our zooplankton sampling targeted the small
copepod species typical of mangrove systems. These
taxa are under-sampled by conventional plankton nets,
but are usually abundant enough to be sampled with
a Niskin bottle. By sampling a discrete volume of
water, we have great confidence in the densities we
have measured, and the sampling procedure was gentle enough for most egg sacs to remain attached to
female copepods, allowing us to easily calculate the
egg-ratio (McKinnon & Klumpp, 1998). However, this
method is less adequate for the larger zooplankton,
since the variance in the estimated densities increases
with inverse abundance and with body size. Zooplankton abundance in the water column was calculated by
counting either the entire 5-l water samples or appropriate subsamples taken with either a Stempel pipette
or a Folsom Plankton Splitter. We identified adult copepods and cladocerans to species, and juveniles where
practicable. The two species of Oithona which dominate the zooplankton of this study are new to science
and are designated as Oithona sp. 1 and Oithona sp.
2. Juveniles of copepods were assigned to oithonid,
pseudodiaptomid/centropagid, paracalanid, acartiid or
‘other’ types. Other taxa were counted to convenient
higher groupings.
hydr3992.tex; 8/06/1998; 20:36; v.5; p.4
131
Figure 3. Station C, Haughton River. Total and > 10 m chlorophyll. Data are mean
SE.
Multivariate analysis
Results
Plankton data were related to the environmental variables (temperature, salinity, tide height, secchi depth,
total chlorophyll, > 10 m chlorophyll, particulate C,
particulate N, seston C, seston N and bacterial abundance) in a canonical correspondence analysis (CCA)
with the program CANOCO (ter Braak, 1987–1992).
Briefly, CCA is a form of multivariate gradient analysis, or canonical ordination, which escapes the assumption of linearity and is able to detect unimodal relationships between species and external variables. For the
multivariate analysis we separated naupliar, juvenile
and adult stages of the common copepod species and
included all other taxa present, resulting in a total of
62 taxa. The plankton count data was log(n + 1) transformed, and analysed in conjunction with 11 environmental variables. Group means were inserted for missing data in the environmental data set (see Tabachnik
& Fidell, 1989), and entire groups which were missing
were omitted from the analysis.
Haughton River temporal sampling
Secchi depth at Station C (Cromarty Landing) varied between 0.35 m and 1.3 m. Temperature ranged
between 21.9 (June 1993) and 30.3 (December 1992)
with little stratification (Figure 2a). Station C was generally hypersaline (Figure 2b), with salinities up to 40.8
occurring towards the end of the dry season. Low salinity periods in 1994 corresponded with increased river
flow, and dropped as low as 7.8. Weekly flow through
the Haughton River system, as measured at the Clare
gauging station 21 km upstream from Cromarty Landing, was less than 3000 megalitres d 1 throughout the
study period, except for periods of flood in January
and February of 1993 and 1994 (Figure 2c). The 1994
flood greatly exceeded that of 1993, with flow rates of
up to 21 664 megalitres d 1 . Hyposaline conditions in
March-June of 1993 cannot be fully explained by river
flow and may have resulted from sheet runoff in the
lower catchment. Stratification with respect to salinity
only occurred in the April and June sampling periods
of 1993.
Chlorophyll a concentration was distributed equally throughout the water column, and was lowest in the
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132
Figure 4. Station C, Haughton River. Particulate carbon and nitrogen (a) < 37 m carbon; (b) < 37 m Nitrogen; (c ) > 37 m carbon; (d)
> 37 m nitrogen. Data are mean SE.
Figure 5. Station C, Haughton River. Bacteria abundance. Data are mean
dry season (April-August). Highest chlorophyll concentration occurred following periods of high river flow
(Figure 3). Cells > 10 m averaged 25% of the total
chlorophyll (Figure 3). Total chlorophyll: phaeopig-
SE.
ment ratios averaged 1.32 for deep samples, and 1.71
for shallow samples. Particulate carbon and nitrogen
(< 37 m) showed a similar pattern to that of chlorophyll (Figure 4), except that the high concentrations
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133
Table 1. Percentage frequency of occurrence and mean
density of taxa which occurred in 10% or more of samples from Cromarty Landing.
Taxon
Frequency Density
%
no. m 3
Oithona juveniles
100
Paracalanid juveniles
100
Acartia juveniles
95
Oithona sp. 1
95
Oithona aruensis
92
Appendicularia
90
Bestiolina similis
87
Pseudodiaptomus spp.
85
Polychaete larvae
79
Gastropod larvae
78
Unidentified Harpacticoida
77
Parvocalanus crassirostris
77
Barnacle naups
74
Bivalve larvae
73
Isopod microniscus larvae
53
Euterpina acutifrons
52
Brachyuran zoea
51
Unidentified ‘cyclopoids’
49
Acartia sinjiensis
34
Unidentified copepod juveniles 33
Acartia pacifica
26
Chaetognatha
21
Ostracoda
20
Acarina
13
Decapod larvae
12
Oithona simplex
12
Medusae
10
102,720
29,785
18,841
5,641
5,117
6,287
7,036
5,130
4,936
2,664
2,940
4,516
2,198
1,714
632
3,486
1,404
732
1,470
7,056
493
357
400
400
400
338
400
after the flood of Jan 1994 were found only in the
deeper water. C:N ratios were between 7 and 20 (mean
of 12), though an extreme value of 27 occurred in the
deep sample of Feb 94. The highest measured concentration of seston carbon (> 37 m) occurred in the
summer of 1992–93 (Figure 4), but some in the summer
of 1993–94 exceeded the range of our carbon detector.
Seston nitrogen (> 37 m) was highest in the summer of 1993–94, with a temporal pattern similar to
that of the < 37 m particulate nitrogen. Seston C:N
ratios ranged between 3.6–14.1 (mean of 6.6.). Bacterioplankton ranged between 0.5 and 3.5 106 cells
ml 1 in abundance, and showed little overall temporal
pattern (Figure 5). No consistent pattern of aggregation
of bacterial cells on particulate material was observed.
Overall, copepods comprised 92% of the zooplankton at Station C. The copepod families Oithonidae,
Figure 6. Station C, Haughton River. > 37 m zooplankton abundance. Error bars are SE of mean total abundance.
Paracalanidae, Acartiidae and Pseudodiaptomidae
were dominant. Juvenile stages of each of these families were not discriminated. Oithonidae, represented by three species, Oithona sp. 1, O. aruensis and
O. simplex, were by far the most abundant copepods
(Table 1). Paracalanidae were the next most important, and were represented by two taxa, Bestiolina
similis and Parvocalanus crassirostris, though there
were rare occurrences of coastal species of Paracalanus and Acrocalanus. Acartiidae were represented
by the estuarine A. sinjiensis, and the neritic A. pacifica. Pseudodiaptomidae occurred mostly as nauplii and
early copepodites, since the strongly demersal habit of
adult pseudodiaptomids resulted in few adults being
taken. Three species occurred, Pseudodiaptomus australiensis, P. baylyi and P. inflexus. Harpacticoid copepods were also common, especially the cosmopolitan,
planktonic Euterpina acutifrons, but most were a mixture of benthic or littoral taxa which were not identified
further.
Zooplankton abundances ranged between 35 and
880 organisms l 1 (mean of 200 organisms l 1 ),
and were lowest during the dry season and highest
some time after periods of increased river flow (Figure 6). The highest abundance was recorded in April
1993 when nauplii occurred at densities in excess
of 600 l 1 in sub-surface water. Naupliar stages of
Oithona, Paracalanidae and Acartia were all significantly more abundant in surface samples than in nearbottom samples (ANOVA, p < 0.0001), whereas copepodite stages of Paracalanidae and Acartia were significantly more abundant in the near bottom samples
(ANOVA, p < 0.0001). Copepodite stages of Oithona
were similar in abundance in the surface and nearbottom samples. Oithona sp. 1, O. aruensis, Bestiolina
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134
Figure 7. Station C, Haughton River. Time courses of abundance of (a) Oithona sp. 1; (b) O. aruensis; (c) Bestiolina similis; (d) Parvocalanus
crassirostris. Data are mean SE.
similis and Parvocalanus crassirostris were the most
abundant adult copepods (Table 1). Oithona sp. 1 was
very much more abundant near the bottom than at the
surface (ANOVA, p < 0.0001; Figure 7), and was abundant throughout the sampling period, though peaks of
abundance occurred in April 1993 and February 1994.
In contrast, O. aruensis was distributed throughout
the water column (Figure 7) and was uncommon in
samples collected between February and June 1993,
but abundances were high in those months in 1994. B.
similis was the most abundant calanoid and was characterised by highly variable abundances with no apparent
seasonal pattern (Figure 7). P. crassirostris had peaks
in abundance in September 1992 and August 1993, but
was most abundant in May 1994 (Figure 7). However,
P. crassirostris did not occur at all in June 1993, and
was often rare. Acartia sinjiensis had a highly sporadic
pattern of abundance, only occurring in densities over
2 l 1 in February, April, and June 1993 and in February
1994.
CCA analysis of 102 samples from Station C (the
Sept. 1992 set was eliminated because of missing data)
resulted in most taxa and sites being oriented along
Axis 2 (Figure 8). Environmental variables were more
important than taxa in determining the distribution of
the main site group, since taxa with extreme scores on
Axis 2 only occurred rarely. For instance, Temora and
Centropages only occurred in one sample, Labidocera
in 2, Calanopia in 3, and pluteus larvae in 5 samples. Sites from January 1994 co-occurred as a group
with high scores on Axis 2 and were characterised
by bloom conditions: high temperature, turbidity and
seston. Sites from other dates were not cohesive and
formed the rest of the main cluster. Taxa occurring
in these stations were tightly grouped around the origin of the two axes indicating an estuarine plankton
community which was homogeneous over time and
relatively independent of the environmental variables.
On the other hand, the 6 sites from February 1994,
when the river was in flood, were characterised by
a community distinct from the estuarine assemblage
because of the occurrence of freshwater taxa such as
the cladoceran Moina sp., Cyclopidae, and the calanoid
copepod genus Boeckella. The main environmental
effects driving the differentiation of this community
were total chlorophyll, > 10 m chlorophyll, C:N ratio
and low salinity (Figure 8). The maximum predicted
tidal height for the day of sampling, which we have
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135
Figure 8. Station C, Haughton River. Canonical Correspondence Analysis ordination diagram of planktonic taxa, samples and environmental
data. Only species with high scores are labelled (the postscript ‘j’ refers to juvenile stages); sample dates which grouped together are indicated
by ellipses.
used as a proxy for tidal current speed, was correlated
with all variables except salinity. Secchi depth has a
strong negative correlation with tide height, and the
highest values of most particulate variables occurred
when the water was most turbid as a result of tidal
mixing.
Haughton River transects
There was a general trend of decreasing secchi depth
(i.e. increasing turbidity), increasing salinity, and
increasing chlorophyll along each of the transects from
the river mouth upstream undertaken in December
1992, August 1993, and January 1994 (Table 2). Particulate carbon and nitrogen and seston carbon and nitrogen tended to be lower at M than at the other stations.
Total zooplankton abundance showed differing patterns on each sampling occasion (Figure 9). In December 1992 and January 1994 abundances were higher
upstream than at the mouth, but were lower at Station
C than at Stations A and B. In contrast, in August 1993
there was a pattern of diminishing zooplankton abundance from the mouth to Cromarty Landing. On each
occasion there was a distinct estuarine community,
characterised by the increased contribution of Oithona
species and the decreased contribution of paracalanid
copepods. Paracalanid copepods within the Haughton
River system comprised two main species, Bestiolina
similis and Parvocalanus crassirostris. Comparison of
abundances of adults of these two species suggests
that P. crassirostris abundances diminish inside the
river system, whereas B. similis abundances increase
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136
Figure 9. Zooplankton community composition along 3 transects in the Haughton River estuary. For Oithona sp. 1, Parvocalanus crassirostris
and Bestiolina similis, abundances are of adult copepods only.
(Figure 9). In December 1992 the ratio of oithonids:
paracalanids increased from 1.5 at M to over 8 inside
the estuary but decreased again at C because of the high
abundance of B. similis at C. This subsequent decrease
in the oithonid: paracalanid ratio was not apparent in
August 1993 and January 1994, when the estuarine
community comprised only stations C and B (Figure 9).
The location of the null point therefore appears to lie
somewhere between stations A and B.
Cape York Rivers
Freshwater input into the Cape York rivers was sufficient to lower salinities to near zero at upstream sampling sites on most occasions (Table 3). However, low
rainfall at the end of 1994 resulted in high salinities in
the December 1995 sampling, especially in the Lockhart and McIvor systems where salinities in excess of
40 occurred inside the river mouth. Chlorophyll values were lower in the Pascoe River than in the other
rivers (Table 3), reflecting the higher current speeds
in this river. Chlorophyll tended to increase closer to
the mouth of the Claudie River and Lockhart Rivers
rivers, though the reverse was the case in June 1995.
The McIvor River had the highest chlorophyll concentrations on all trips except that of June 1995, when
the Daintree River exceeded it. The highest recorded
chlorophyll concentration measured in this study was
15.7 g l 1 (McIvor River, February 1996). The high
end of the range of particulate and seston C and N values in the Cape York rivers corresponded to the low end
of the range in the Haughton River (Figure 4, Table 3).
For instance, the PC range in the Cape York Rivers was
243–2306 g l 1 compared to 528–33088 g l 1 in the
Haughton, and the PN range 26–159 g l 1 compared
to 77–1142 g l 1 in the Haughton. There was a general pattern of higher values of PC and PN in the Cape
York rivers in the wet season than in the dry season.
Bacteria numbers ranged between 0.91 and 3.77 106
cells ml 1 , and showed no consistent pattern within or
between rivers, but were similar in magnitude to those
in the Haughton (Figure 5, Table 3).
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137
Table 2. Physico-chemical variables on Haughton River transects. Data for chlorophyll and carbon and nitrogen are means of
duplicate measurements for stations M, A and B. Values for Station C are the means of top and bottom samples.
Station Depth Secchi Temp. Salinity Total chl. > 10 m chl. PC
m
m
˚C
g l 1 g l 1
g l
15-Dec-92
M
A
B
C
19-Aug-93
M
2.5
A
3.2
B
1.2
C
6.5
27-Jan-94
M
4.3
A
4.6
B
1.8
C
7
1
PN
g l
1
Seston C Seston N
g l 1 g l 1
1.90
1.70
0.90
0.80
29.40
29.10
29.80
30.05
37.80
38.90
39.20
37.92
2.54
1.16
1682.00 124.86 504.94
0.70
0.60
0.40
0.60
21.10
19.90
21.40
22.15
37.20
37.90
38.20
37.45
0.97
1.94
2.51
1.54
0.16
1.53
0.96
0.75
2220.45
3591.20
4477.10
3512.87
130.75
230.00
280.10
217.47
1.00
0.90
0.90
0.40
28.40
27.90
26.50
29.25
37.70
38.50
39.30
40.05
1.07
1.43
3.40
4.91
0.21
0.37
1.27
1.98
658.85
777.90
2506.40
3404.67
103.80
138.55
298.20
423.47
Bacteria
cells ml
1
72.99
2.09E + 06
376.81
551.65
691.16
517.09
51.34
95.24
103.57
79.59
1.25E + 06
9.71E + 05
1.32E + 06
1.50E + 06
331.24
344.32
116.82
196.07
37.16
1.51E + 06
59.92
1.61E + 06
1.83E + 06
2.05E + 06
Figure 10. Zooplankton community composition in the Cape York rivers. The Claudie River was not sampled in December 1995 and February
1996; instead data from the nearby Lockhart River are presented. Bars are placed according to salinity at each of 3 transect stations; in the
Pascoe River in February 1996 two stations were fresh water.
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138
Table 3. Environmental variables for the Cape York Rivers. Data are mean and standard error, of 3 samples (1993 and June 1995) or 4 samples
(Dec. 1995 and Feb. 1996). In June 1993 separate subsurface (S) and near-bottom (D) collections were made.
Stn
Sal. Temp. Depth Secchi Chlorophyll
˚C
m
m
g l 1
Pascoe River
27-May-93
1
0.3
2
9.6
3
17.8
15-Jun-95
1
1
2
17.6
3
35.5
6-Feb-96
1
0
2
0
3
31.5
Claudie River
28-May-93
1
4.9
2
15.7
3
20.4
16-Jun-95
1
2.4
2
20.2
3
32.3
Lockhart River
15-Dec-95
1
34.4
2
39.3
3
42.7
5-Feb-96
1
0
2
17
3
23.8
McIvor River
31-May-93
1
5.7
2
12.6
3
21.8
17-Jun-95
1
10
2
20.7
3
31
19-Dec-95
1
26.2
2
39.2
3
40.6
PC
g l
PN
g l
1
Sest C
g l 1
1
24.9
24.9
25
1.5
1.7
2
>1.5
>1.7
1.85
0.24
0.50
0.53
0.02
0.02
0.01
640.47
688.93
926.90
98.14
44.91
58.89
46.67
72.30
76.67
3.68
2.66
1.75
25.2
25.8
25.9
0.8
1.7
1.4
>0.8
>1.7
>1.4
0.37
0.74
0.40
0.03
0.02
0.00
362.40
261.30
243.30
16.24
15.57
40.92
51.33
43.93
41.07
1.77
1.72
4.13
1
1
1.5
0.07
0.10
1.00
0.01
0.00
0.03
549.70
415.08
863.87
32.26
4.76
13.41
44.70
33.83
51.07
3.15
2.50
1.91
1.5
1.6
1.8
2.00
3.88
4.91
0.05
0.07
0.11
569.90
653.87
816.07
31.16
111.33
200.75
46.17
49.60
57.87
1.68
7.01
11.85
27.9
27.9
30.4
24.8
24.8
24.3
3
1.7
2.5
24.8
25.9
26.7
2
3
1
0.9
1.4
>1
1.56
0.86
1.02
0.05
0.02
0.03
406.27
372.67
286.17
4.62
16.85
15.04
54.57
48.43
53.27
2.05
1.96
0.38
29.5
28.8
30.35
2.7
2.3
3.8
2.2
>2.3
3
1.84
1.18
2.20
0.02
0.25
0.15
534.40
431.90
387.33
86.15
53.38
18.29
58.18
44.05
45.98
3.41
1.36
2.46
1
2.5
0.87
3.90
3.99
0.05
0.12
1.30
1727.78
762.28
648.40
100.56
29.86
23.23
98.68
67.55
63.00
7.18
2.92
2.99
26.1
29.8
29.2
25.1
25.1
24.9
0.5
2.5
1.2
>0.5
1
1.1
1.52
4.78
4.17
0.07
0.06
0.19
843.53
681.40
818.37
130.19
58.20
15.32
58.03
43.57
77.60
4.73
9.44
2.50
24.5
24.9
24.3
3.4
3
2.2
0.9
1.2
>2.2
1.51
1.62
1.36
0.20
0.03
0.04
575.23
649.23
282.10
28.51
33.97
35.54
53.97
74.90
49.60
0.79
7.97
4.86
30.8
29.5
29.8
2.7
3.6
3
0.6
1.2
>3
7.00
2.44
0.62
0.14
0.06
0.03
2306.23
666.40
260.55
83.82
38.73
33.49
159.05
62.60
28.88
6.44
1.27
2.39
Sest N
g l 1
Bacteria
cells ml
1
9.71E + 05
1.20E + 06
1.42E + 06
222.74
156.45
160.36
7.06
1.95
10.27
17.94
14.29
19.70
2.30
1.35
1.91
1.20E + 06
1.49E + 06
9.07E + 05
1.40E + 06
2.10E + 06
1.87E + 06
152.11
173.30
142.97
8.83
8.60
12.72
11.14
14.83
13.74
1.00
2.04
1.19
2.10E + 06
2.63E + 06
2.01E + 06
2.77E + 06
3.17E + 06
3.77E + 06
131.77
142.15
153.33
26.77
16.25
21.93
18.27
15.74
15.84
4.86
2.32
1.93
2.54E + 06
2.45E + 06
1.58E + 06
hydr3992.tex; 8/06/1998; 20:36; v.5; p.12
139
Table 3. Continued.
Stn
Sal. Temp. Depth Secchi Chlorophyll
˚C
m
m
g l 1
3-Feb-96
1
7.5
2
13
3
35
Daintree River
1-Jun-93
1
0.2
2
14.7
3S
17.2
3D
24.1
20-Jun-95
1
2.6
2
16.3
3
20.4
29
29.1
PC
g l
PN
g l
1
Sest C
g l 1
1
15.70
8.88
1.08
1.92
0.77
0.02
1608.63
1122.58
154.68
146.46
97.04
12.71
159.45
124.95
360.40
23.58
13.69
4.00
23.3
24.3
24.3
24.2
2.5
2.5
6.5
1.5
1.20
1.67
1.89
1.84
0.08
0.26
0.06
0.08
792.87
366.93
459.50
501.53
31.97
14.42
25.69
21.28
90.33
25.90
29.73
33.40
3.25
2.06
1.49
1.96
21.9
22.2
21.5
2
3
4.5
1.8
2.2
2
3.78
3.94
‘4.83
0.09
0.05
0.05
413.80
440.13
517.43
37.52
14.57
32.88
59.80
69.47
67.67
3.33
2.69
2.46
The dominance of Oithona spp. was a consistent
feature of the zooplankton communities in all river
systems, but there was no consistent pattern of zooplankton abundance along the three station transects
in any river system (Figure 10). Stations immediately
inside the mouths of each river had a sizeable component of coastal species, whereas stations further
inside the rivers had a less diverse estuarine assemblage. In the Pascoe, Claudie and Lockhart Rivers
Pseudodiaptomus griggae was an important component of the upstream (low salinity) area, but in the
McIvor and Daintree Rivers P. griggae did not occur;
instead Gladioferens pectinatus was abundant in low
salinities. Similarly, the species of Oithona present
in these two groups of rivers differed. Oithona sp. 2
was the dominant oithonid north of the Daintree River,
and appeared to have a contiguous distribution with
Oithona sp. 1, which was dominant in the Daintree
and Haughton Rivers. However, a few individuals of
Oithona sp. 1 did co-occur with Oithona sp. 2 in the
Lockhart River in Dec-95. O. aruensis occurred in all
river systems. Acartia sinjiensis was also an important
component of the McIvor and Daintree Rivers, but was
rare in the other rivers. In December 1995, after a hot
dry period, paracalanid copepods penetrated throughout the McIvor River, but generally paracalanids were
common only at the seaward end of the rivers. The
large contribution of paracalanids to the zooplankton
communities within the Daintree River estuary in June
1995 was due to high abundances of Bestiolina similis, but near the mouth the paracalanid community
Sest N
g l 1
Bacteria
cells ml
1
2.31E + 06
2.46E + 06
1.99E + 06
2.34E + 06
43.83
133.87
174.50
11.68
18.96
14.92
11.25
20.10
17.70
2.59
3.29
2.94
2.11E + 06
1.99E + 06
2.01E + 06
comprised a mixture of B. similis and Parvocalanus
crassirostris. Similarly, these species accounted for
the appreciable paracalanid community in the Lockhart River in February 1996.
Discussion
Environment
The river systems described in this paper differ in their
hydrography. The Cape York rivers have appreciable freshwater input for most of the year, though in
December 1995 even the McIvor and Lockhart Rivers
became hypersaline after a period of drought. Nonetheless, these rivers represent different physical settings
from that of the Haughton, which in addition to being
located in the dry tropics, also has fresh water diverted
from it. The Haughton River is more similar to a tidally
driven inlet than to the more riverine systems of Cape
York. However, all these systems are characterised by
high tidal flows, with the consequent turbulence resulting in the water column being well mixed and turbid. In
fact, in the Haughton River turbidity depended on the
velocity of tidal flow as indicated by maximum tidal
height at that time.
Chlorophyll concentration in the Great Barrier Reef
lagoon rarely exceeds 1.0 g l 1 (Furnas & Mitchell,
1986). By comparison, the Haughton River represents
a chlorophyll rich environment, typically with values
4.0 g l 1 (Figure 3). Moreover, 25% of this chloro-
hydr3992.tex; 8/06/1998; 20:36; v.5; p.13
140
phyll is > 10 m, and therefore directly available to
copepods as food. Though we made no attempt to
characterise phytoplankton communities, we observed
many chain-forming diatoms in the plankton samples.
Similarly, chlorophyll values within the Cape York
rivers rivers usually exceeded what would be expected
in coastal waters, and sometimes spectacularly so, as in
the case of the McIvor River in February 1996, where
a concentration in excess of 15 g l 1 was recorded.
Particulate carbon values are typically 5-fold higher within the Haughton River than those observed in
nearby coastal waters (McKinnon, 1996, unpublished
data). Though particulate carbon and nitrogen are not
necessarily correlated with chlorophyll concentration
in coastal waters (Roman, 1980), both were strongly
correlated with chlorophyll in the Cromarty Landing
series, implying that the same physical processes are
important in determining these measurements. However, the generally high C:N ratios in combination with
the low chlorophyll: phaeopigment ratios of particulate matter indicates the prevalence of detritus in the
particle environment of mangrove rivers. How much
of this detrital material originates from the mangroves
themselves is unknown.
Sampling of seston carbon and nitrogen was
designed to represent > 37 m zooplankton biomass,
but it is impossible using screens alone to eliminate
non-living particles. Seston N was positively correlated with zooplankton abundance but seston C was
not, possibly because particulate detritus with a high
C:N ratio disproportionally inflated the C measurement. The presence of detritus in the seston is evident
from the C:N ratios (grand mean of 7), relative to the
value of 4:1 typical of zooplankton (Roman, 1980).
The < 37 m particulate matter, on the other hand, had
a grand mean C:N ratio of 12.5.
Detritus may be important in the nutrition of estuarine copepods (e.g. Heinle et al., 1977), and the associated bacterial cells may enhance the nutritional value
of detrital particles. Indeed, the abundance of bacterial flora in our samples was correlated with particulate
load. However, the number of bacterial cells observed
in our samples is at the low end of abundances listed for estuarine waters (0.5–35 106 cells ml 1 ) by
Ducklow & Shiah (1993), and we did not observe welldeveloped bacterial films on the surface of detrital particles. We conclude therefore that if bacteria are important in copepod nutrition in mangrove estuaries, it is
more likely to occur via intermediary organisms such
as protozoa than directly from detrital particle uptake.
Plankton abundance
Our sampling strategy targeted Oithona species and
small calanoid copepods such as Parvocalanus and
Bestiolina. As expected, larger species such as Acartia and Paracalanus were rarer, and the resulting error
terms in density measurements larger. Genera such as
Pseudodiaptomus and Gladioferens, though comparatively large-bodied, were under-sampled because of
their strong demersal behaviour. The range in summer
abundances of crab larvae (up to 5 l 1 ) originating
from species of crab resident in mangrove forests was
similar to that observed by Robertson et al. (1988) in
their nearby mangrove forest sites. However, our data
indicate that the abundance of zoea is highly variable,
and therefore the importance of crab zoea in the diet of
fish may be transitory.
It is difficult to compare zooplankton abundances
derived from studies which use different plankton net
mesh-sizes, since many small species of tropical zooplankton pass undetected through the mesh of the traditional 200 m plankton net (see Hopcroft et al., in press
for a graphical example). The use of all but the most
fine-meshed plankton nets fails to sample the abundant developmental stages of copepods. This study, by
measuring zooplankton abundance from water samples
which were poured through a 37 m sieve, captured all
copepod life stages from egg to adult. The zooplankton
abundances we observed were high, with the McIvor
and Lockhart Rivers having the highest abundances
of zooplankton (up to 1400 l 1 in the McIvor River,
June 1995). These abundances are higher than those
observed in most previous studies of mangrove zooplankton by about an order of magnitude (see Robertson & Blaber, 1992, Table 3). However, where similar
collection methods have been used, abundances similar to those of our study have been recorded even in
temperate areas; Mallin (1991) obtained abundances
of 178 organisms l 1 with a 73 m mesh and a plankton pump in the Neuse Estuary, North Carolina, and
Lonsdale et al. (1996) obtained abundances of up to
658 l 1 around Long Island, New York, in water samples collected with buckets and passed through a 64 m
screen.
Highest zooplankton abundances in the Cromarty
Landing series occurred after freshwater had entered
the system, and conversely, the lowest abundances
occurred during the dry season. In fact, the time lag
in abundance since the period of flood in 1994 is similar to that shown in adjacent coastal waters following
a flood period (McKinnon & Thorrold, 1993). Our
hydr3992.tex; 8/06/1998; 20:36; v.5; p.14
141
observation of different patterns of abundance on each
of the transects implies that zooplankton abundance at
any one station within the Haughton River estuary is
dependent on tidal state.
Despite strong tidal currents in the Haughton river, vertical patterns of zooplankton abundance persisted. Nauplii are commonly aggregated near the surface
(e.g. Dagg & Whitledge, 1991), but it is surprising
that supposedly weak swimmers such as paracalanid
and acartiid juveniles and Oithona sp. 1 adults were
significantly more abundant in our near-bottom samples. It is unclear, however, whether the vertical distribution patterns of the copepodites arise from active
swimming of the copepods, or some physical process.
Zooplankton can utilize current shear to maintain horizontal position in estuaries (Bosch & Taylor, 1973;
Orsi, 1986; Kimmerer & McKinnon, 1987), and this
may be the case in mangrove rivers. Oithona sp. 1 is
rare in coastal waters neighbouring the Haughton River, suggesting it has some behavioural mechanism for
limiting washout. This does not appear to be the case
for Acartia sinjiensis and Bestiolina similis, both of
which were distributed throughout the water column,
and do occur in neighbouring coastal waters.
Plankton community structure
Our goal in this study was to understand planktonic
processes within the true estuarine community, since
in terms of the mangrove ecosystem this community
is more important than the exchange fauna found near
river mouths, which by definition includes many nonresident coastal species. In the Haughton River tidal
oscillations were of sufficient size to confound spatial
sampling, but the transects still indicated an estuarine community distinct from that at the mouth. By
sampling at Cromarty Landing, we reasoned that we
could repeatedly sample the estuarine component of
the Haughton River system irrespective of tidal state.
Nevertheless, community structure appeared to correspond more closely with tidal state than with the
seasonal patterns typically observed in neighbouring
coastal plankton communities.
In all the rivers we studied, Oithona species comprised most of the zooplankton, and this seems to
be characteristic of mangrove zooplankton worldwide
(see Robertson & Blaber, 1992). Oithona can form
swarms around mangrove prop roots, with densities as
high as 21 ml 1 (Ambler et al., 1991). Unfortunately,
the similarity between the species of Oithona in our
study precludes identification of their developmental
stages to species level and conclusions about the distribution of each species must be restricted to the adult
stage, which comprise only a small fraction of the total
population. However, it is apparent that Oithona sp.
1 and Oithona sp. 2 are euryhaline, since they thrive
in low salinities, as well as occurring in hypersaline
conditions at other times of the year.
The zooplankton communities encountered in the
Haughton River can be directly compared with those
from nearby Alligator Creek, a mangrove system
just north of the Haughton River system (Robertson
et al., 1988). Coastal zooplankton communities in
north Queensland are characterised by seasonal patterns of abundance with minima in August-September
and maxima in April-May (Robertson et al., 1988;
McKinnon & Thorrold, 1993; McKinnon, unpublished). This, together with the location of Robertson et al.’s (1988) mangrove mainstream site near
the mouth of Alligator Creek, probably accounts for
their conclusion of marked seasonality in mangrove
zooplankton abundances. Mangrove zooplankton can
be divided into four components (Grindley, 1984); a
stenohaline marine component near the mouth, a euryhaline marine component, a true estuarine component,
and a freshwater component. The estuarine and freshwater components of the Alligator Creek system were
under-represented in Robertson et al. (1988) study
because they sampled close to the mouth of the river. However, representatives of all four components
were found in each of the rivers described in this study,
though not on all sampling occasions. The Haughton
River lacked a freshwater component except during
the flood of February 1994, when freshwater species
were washed into the River. The Cape York rivers typically had representatives of all components, though
the Lockhart and McIvor rivers had a distinctly marine
fauna at all stations in December 1994 after a period
of low rainfall.
The most common copepod species occurring in
coastal plankton communities of the Great Barrier
Reef lagoon are Oithona attenuata, Parvocalanus crassirostris, Paracalanus spp., Acrocalanus gibber and
Euterpina acutifrons (McKinnon & Thorrold, 1993;
McKinnon, unpublished). Of these taxa, only P. crassirostris appears to occur in mangrove systems with
any consistency. Fulton (1984) found that small copepods such as Oithona and P. crassirostris were ‘avoided’ by fish predators, which preferred the larger bodied Acartia and Euterpina. Visual predators could
be important mediators of community composition in
mangroves, since most newly recruited fish in man-
hydr3992.tex; 8/06/1998; 20:36; v.5; p.15
142
grove systems are zooplanktivores (Robertson & Duke,
1990). However, some factor other than body size, such
as competition from the mangrove resident species,
must prevent the intrusion of O. attenuata and O. nana
into the upper reaches of these estuaries. Bestiolina
similis and Acartia sinjiensis, though often found in
coastal waters, thrive in the higher turbidity water of
the mangroves and appear to establish resident populations there. Freshwater plankton, when it occurred,
was ephemeral, and comprised salt-intolerant taxa.
Low salinity waters in the Cape York rivers were
characterised by the presence of Pseudodiatomus griggae in the Pascoe, Claudie and Lockhart Rivers, and
by Gladioferens pectinatus in the McIvor and Daintree Rivers. P. griggae was originally described from
Papua New Guinea (Walter, 1987), and was dominant
in the inner reaches of the Fly River Delta (Robertson
et al., 1990), and therefore can be regarded as tropical
in affinity. In contrast, G. pectinatus is the dominant
calanoid in low salinity estuaries in south-eastern Australia and New Zealand (Arnott et al., 1986), and therefore has cold-temperate affinities. This is the northernmost record of this species to date. Interestingly, the
faunal shift occurring between the Pascoe, Claudie,
and Lockhart Rivers and the McIvor and Daintree
Rivers was also apparent in the occurrence of Oithona
species, with Oithona sp. 1 dominant in the southern
rivers, and Oithona sp. 2 dominant in the northernmost
rivers. G. pectinatus has not yet been recorded from
the Haughton River or Alligator Creek, but may well
occur in systems in the area where low salinity waters
persist.
Conclusions
This study emphasises the importance of copepods in
general, and the genus Oithona in particular, in the formation of distinct zooplankton communities in mangrove estuaries. The water column is rich in particulate
matter of low food quality, as indicated by the C:N
ratio and pigment composition. On the other hand, the
phytoplankton biomass in all rivers examined is considerable when compared to the generally low standing stocks in neighbouring coastal waters. The size
distribution of these cells ought to render a considerable fraction of this community directly available to
copepods. The effect of physical forcing on plankton
communities in mangrove estuaries is dominant over
all the biological variables we measured. For example,
the degree of mixing, determined by tidal state, and the
extent of freshwater input into these systems appears to
drive both the quantity and quality of particulate material available to higher consumers, and the distribution
of zooplankton communities within the estuary.
Acknowledgements
We thank Alistar Robertson for the encouragement to
undertake this study, and the many people who assisted
with field collections, notably Craig Humphrey, Sheryl
Fitzpatrick, Steven Boyle and the ex-crew of the AIMS
vessels. We particularly want to thank Peter Gair for
great seamanship and co-operation in the cruises to
the Cape York Rivers. Janet Ley and Paul Dixon collected samples for us in December 1995 and February
1996, and Alan Mitchell provided chlorophyll and carbon and nitrogen measurements from those dates. The
Department of Primary Industries at Ayr provided flow
data for the Haughton River. We thank Dan Alongi and
Miles Furnas for comments on the manuscript.
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