Titles should never contain abbreviations, e

1182
Palma, et al.
Zooplankton spatial and temporal distribution in an equatorial
estuary (Amazon littoral, Brazil)
Marília Borges Palma†, Kelli Garbosa da Costa†, André Magalhães†, Manuel de Jesus Flores Montes‡, Luci
Cajueiro Carneiro Pereira† and Rauquírio Marinho da Costa†
†Instituto de Estudos Costeiros,
Universidade Federal do Pará,
Bragança, 68600-000, Brazil.
[email protected]
[email protected]
[email protected]
[email protected]
[email protected]
‡Departamento de Oceanografia Química,
Universidade Federal de Pernambuco,
Recife, 50670-901, Brazil.
[email protected]
www.cerf-jcr.org
ABSTRACT
Palma, M.B., Costa, K.G. da, Magalhães, A., Flores Montes, J., Pereira, L.C.C. and Costa, R.M. da, 2013. Zooplankton
spatial and temporal distribution in an equatorial estuary (Amazon littoral, Brazil) . In: Conley, D.C., Masselink, G.,
Russell, P.E. and O’Hare, T.J. (eds.), Proceedings 12th International Coastal Symposium (Plymouth, England), Journal
of Coastal Research, Special Issue No. 65, pp. 1182-1187, ISSN 0749-0208.
www.JCRonline.org
Few data are available on the zooplankton communities of the Amazonian littoral zone. Given this, the present study
investigated the structure and spatial-temporal variation in these organisms in the Taperaçu estuary. Samples were taken
at three different stations during neap flood tides in rainy and dry seasons. Samples were taken from the subsurface
water with a plankton net coupled to a flowmeter. Additional water samples were collected from the sub-surface in
order to determine the chlorophyll-a concentrations. Salinity and pH were measured in situ. The lowest salinity (3.25)
was recorded in the innermost station in February (2011), favouring the development of a number of oligohaline
species, such as Bosmina sp., Daphnia sp., and Diaphanossoma sp. The highest salinity recorded at this station was
27.88. A total of 68 taxa were identified. The copepods were the most important group. Oithona oswaldocruzi and
Acartia lilljeborgii were the predominant species in the rainy and dry seasons, respectively. The highest mean
zooplankton densities were recorded during the rainy season at the innermost station (4,459,354.58±7,666,682.09 ind.m3
). While the Taperaçu estuary was dominated by saline waters throughout the study period, both coastal and estuarine
species were able to develop during the rainy season. A limited freshwater pulse was observed in the rainy season, when
adjacent marshes fed into the estuary, indicating that salinity (influenced by rainfall rates) was the main factor
controlling the composition and density of the local zooplankton community.
ADDITIONAL INDEX WORDS: Plankton dynamics, rainfall, salinity, Amazon littoral.
INTRODUCTION
Estuarine ecosystems provide shelter and feeding resources for
a wide variety of aquatic and terrestrial species (Aveline, 1980;
Kaiser et al., 2005), and represent a major supply of fishery
resources. The high biological productivity of these systems –
including phytoplankton, zooplankton, and fish – is related to the
retention and efficient recycling of nutrients between benthic and
pelagic habitats, and the adjacent vegetation (Lam-Hoai et al.,
2006).
In these environments, zooplanktonic organisms play a
fundamental role in the transfer of energy between primary
producers and other components of the aquatic food web (Lenz,
2005), such as commercially-important fish species. These
organisms are also highly sensitive to environmental change, with
impacts resulting in marked alterations in the density and
composition of the zooplanktonic fauna (Neumann-Leitão et al.,
1992). Given their role in the ecosystem, the response of these
organisms to negative impacts on the environment, may provoke
alterations throughout the aquatic food web of the aquatic
ecosystems.
The Amazon coastal region is strongly influenced by seasonal
variation in rainfall levels, fluvial discharge, and the action of
tides, winds, and currents (Lara and Dittmar, 1999). In this region,
____________________
DOI: 10.2112/SI65-200.1 received 07 December 2012; accepted 06
March 2013.
© Coastal Education & Research Foundation 2013
most of the research on zooplankton has focused on the effects of
salinity on the distribution of these organisms in estuarine
environments affected by fluvial conditions (Krumme and Liang,
2004; Magalhães et al., 2009, 2010; Costa et al., 2009). Given
this, the present study investigates the spatial-temporal variation in
the density, abundance, and diversity of the zooplankton of an
atypical Amazonian estuary – the Taperaçu estuary in northern
Brazil – which is characterized by the absence of any major fluvial
discharge, and a minimal input of freshwater.
METHODS
Study area
The Taperaçu estuary (00º50’-00º57’S, 46º42’-46º45’W: Figure
1) is located in the municipality of Bragança, approximately 200
km east of the mouth of the Amazon River. This ecosystem is
considered to be atypical due to the lack of fluvial discharge,
although there is some input of freshwater from the surrounding
marshes during the rainy season (Asp et al., 2012), as well as from
the Caeté estuary through the Taici tidal creek during the flood
tide (Araujo Junior, 2012). The Taperaçu is considered to be a
permanently open estuary, characterized by high levels of
turbidity (mean = 378.1 NTU), shallow depths (mean = 4.2 m),
and strong tidal currents, of up to 2.04 m.s-1 (Asp et al., 2012).
Journal of Coastal Research, Special Issue No. 65, 2013
Zooplankton spatial and temporal distribution in an equatorial estuary (Amazon littoral, Brazil)
Like the rest of the northern coast of Brazil, the Taperaçu estuary
is subject to semidiurnal macrotides, with heights of around 5 m,
increasing to up to 6 m during the equinoctial spring tides (SouzaFilho et al., 2009). The local climate is hot equatorial, with a
marked rainy season between January and July, and a dry (or less
rainy) season between August and December (Moraes et al.,
2005), with relative humidity of the air ranging between 80% and
91% (Martorano et al., 1993). Mean temperatures are around 26ºC
and mean annual precipitation is approximately 2,500 mm
1183
(DO) concentrations were obtained in situ using a CTDO (model
XR-420), while pH was measured using a PHS-3B pHmeter.
In the laboratory, the samples were fractioned using a Folsom
apparatus (McEwen et al., 1954). The subsamples were then
identified to the lowest possible taxonomic level and counted,
using a Zeiss stereoscopic microscope and gridded Petri dishes.
The zooplanktonic organisms were identified based on the
literature available for the taxa of the South Atlantic (Boltovskoy,
1981, 1999) and classified taxonomically (WoRMS, 2012).
These data were used to calculate the frequency of occurrence,
absolute (ind.m-3) and relative density, as well as the indices of
ecological diversity (Shannon, 1948) and evenness (Pielou, 1969).
Given the large number of taxa present in the samples, all noncopepod zooplanktonic organisms were allocated to the category
“others”.
The Kruskal-Wallis (H) and Mann-Whitney (U) tests (Zar,
1999) were used to evaluate the existence of temporal and spatial
differences in the physical-chemical characteristics of the water,
total zooplankton density and the density of the most abundant
taxa, and species richness, diversity, and evenness. Spearman’s
correlation coefficient was used to assess possible relationships
between physical-chemical and biological factors. All the analyses
were run in STATISTICA, version 6.0.
A cluster analysis was also run based on the zooplankton
density data, using the Bray and Curtis index (1957), with the
dendrogram being produced using the WPGMA (Weighted Pair
Group Method of Arithmetic Averages) method. An analysis of
similarity (ANOSIM) was subsequently applied to test the
significance of the differences observed among the groups formed
by the dendrogram. A similarity percentage (SIMPER) analysis
was also run in order to identify the species that most contributed
to the similarity among the groups. These analyses were run in the
PRIMER, version 6.1.6 (Plymouth Routines Multivariate
Ecological Research) following Clarke and Warwick (1994).
RESULTS AND DISCUSSION
Figure 1. Study area: (a) South America; (b) Location of the
Taperaçu estuary on the Amazonian coast of northern Brazil; (c)
Positions of the sampling stations in the upper (1), middle (2),
and lower (3) sectors of the Taperaçu estuary, with the black
arrow indicating the position of Taici creek, which connects the
Taperaçu and Caeté estuaries (Modified from Mehlig, 2001).
(INMET, 1992).
Sampling and laboratory procedures
Data were collected during neap flood tides at three fixed
stations (Figure 1: S1 – inner sector, S2 – middle sector, and S3 –
outer sector, at the mouth of the estuary) during the rainy season
(February, April, and June, 2011) and the dry season (October,
2010, August and October, 2011). The samples were collected
from the subsurface water in horizontal 3-minute trawls of
conical-cylindrical plankton nets (120 μm), coupled to mechanical
flowmeters (General Oceanics Inc.) to determine the total volume
of water filtered. Additional 400-ml samples of subsurface were
collected for the determination of potential hydrogenionic (pH)
and chlorophyll-a concentrations. Salinity and dissolved oxygen
During the present study, salinity varied significantly between
seasons (U = 3.00, p < 0.01), with values ranging from 10.94±7.65
at S1 during the rainy season to 35.21±3.54 at S3 in the dry
season. This variation appeared to be related to that in local
precipitation levels, which increased from 38.1±21.5 mm in the
dry season to 343.0±138.5 mm in the rainy season. Similar
seasonal variation was observed in pH (U = 14.0, p < 0.05), with
mean values ranging from 6.88±0.24 at S1 in the rainy season to
7.86±0.11 at S3 during the dry season, while mean dissolved
oxygen concentrations also varied significantly (U = 8.50, p <
0.01), from 4.22±1.18 mg/L in the rainy season to 8.41±0.46 mg/L
in the dry season. By contrast, turbidity (U = 18.00, p < 0.05) and
chlorophyll-a concentrations (U = 14.50, p < 0.05) were
significantly higher during the rainy season. Mean turbidity was
18.56±11.74 NTU at S1 in the dry season and 77.63±72.66 NTU
at S2 in the rainy season, while the chlorophyll-a concentration
increased from 6.58±4.00 mg.m-3 at S3 in the dry season to
37.04±15.81 mg.m-3 at S1 in the rainy season. No significant
pattern was observed in any of the hydrological variables within
seasons (Figure 2).
In tropical estuaries in Brazil (Thüllen and Berger, 2000;
Magalhães et al., 2009) and other parts of the world (Capo et al.,
2006; Lam-Hoai et al., 2006), temporal variation in hydrological
parameters, in particular salinity, tend to be related primarily to
rainfall levels. In the specific case of the Taperaçu estuary, in
addition to precipitation, the absence of ant continuous fluvial
discharge also has a major influence on these parameters,
permitting a greater influx of marine waters into this ecosystem, in
Journal of Coastal Research, Special Issue No. 65, 2013
1184
Palma, et al.
Figure 2. Mean (±SD) salinity, pH, turbidity, DO and
chlorophyll-a concentrations recorded at Taperaçu estuary,
northern Brazil.
particular during the dry season, with an attenuating effect on the
spatial gradients in hydrological variables. The data collected
during the present study indicate that the Taperaçu estuary is
spatially homogeneous in relation to salinity levels.
The higher pH values recorded during the dry season were
associated with the buffering effect of the marine waters that
penetrate the estuary mainly during this part of the year
(Schmiegelow, 2004). The high dissolved oxygen concentrations
recorded during the dry season may be related to the strong
hydrodynamics observed in the region during this period, when
the winds and tidal currents are at their strongest, provoking
higher levels of oxygenation of the water, which is typical of
shallow and relatively turbulent coastal systems with a strong
marine influence (Losada et al., 2003; Sousa et al., 2009). The
increase in dissolved oxygen concentrations during this period
may also be related to the greater penetration of solar radiation
into the water column and the consequent increase in the primary
productivity of the local phytoplankton (Sousa et al., 2008).
The high turbidity and chlorophyll-a levels recorded at the inner
(S1) and middle (S2) stations during the rainy season may be
related to the increase in the availability of suspended particulate
matter and nutrients derived from the input of the surrounding
floodplain during this period, as observed in other estuarine
ecosystems of Northern and Northeast Brazil (Lara and Dittmar,
1999; Pereira-Filho, 2001), and in other countries around de world
(Osore et al., 2004; Duggan et al., 2008). An additional factor may
be the re-suspension of the bottom sediments and phytobenthic
organisms provoked by the hydrodynamics of the system (Losada
et al., 2003; Matos et al., 2011).
Dissolved oxygen (DO) concentrations normally decrease when
turbidity increases. While this juxtaposition was observed in the
Taperaçu estuary, DO concentrations were relatively high at S2
during the rainy season. This may have been related to the rapid
circulation of the water related to the strong local hydrodynamics,
which was more intense at S2, which leads to an increase in
turbidity, but also a more intense level of interaction between the
water and the atmosphere, favouring an increase in the DO
concentrations in the water column.
The zooplankton community recorded during the present study
was highly diverse, with a total of 68 taxa being identified,
including members of the phyla Ciliophora, Sarcomastigophora,
Cnidaria, Nematoda, Platyhelminthes, Annelida, Mollusca,
Arthropoda, Bryozoa, Chaetognatha, Echinodermata, and
Chordata. However, the copepods were the most diverse, with just
over half (55%) of the total number of taxa (38). A predominance
of copepods is typical of the mesozooplankton of estuarine
environments (Villate and Orive, 1981; Turner, 2004), except
during periods when certain benthic and nektonic organisms, such
as decapods and mollusks, breed and produce large numbers of
larvae (Osore et al., 2004; Leite et al., 2009).
Of the species recorded, only Oithona oswaldocruzi Oliveira,
1945 and Oithona hebes Giesbrecht, 1891 were classified as very
frequent (≥ 70%), and were present in 100% of the samples
analyzed. Other frequent species included Paracalanus quasimodo
Bowman, 1971 (94% of the samples), Acartia tonsa Dana, 1849
(89%), Acartia lilljeborgii Giesbrecht, 1889 (89%),
Pseudodiaptomus acutus (Dahl F., 1894) (83%), Parvocalanus
crassirostris (Dahl F., 1894) (78%), and Euterpina acutifrons
(Dana, 1847) (78%). These species are tolerant of major
oscillations in salinity (Bradford-Grieve et al., 1999), and are
common in estuaries from Brazil (Costa et al., 2011; Muxagata et
al., 2012) and worldwide (Maruthanayagam and Subramanian,
2000; Brugnoli-Olivera et al., 2004).
Mean
total
zooplankton
density
varied
from
24,240.83±13,836.54 ind.m-3 at S3 in the dry season to
4,459,354.58±7,666,682.09 ind.m-3 at S1 in the rainy season.
Mean copepod densities ranged from 18,746.62±9,754.08 ind.m-3
at S3 in the dry season to 4,440,778.62±7,667,291.30 ind.m-3 at S1
Journal of Coastal Research, Special Issue No. 65, 2013
Zooplankton spatial and temporal distribution in an equatorial estuary (Amazon littoral, Brazil)
in the rainy season. The mean density of the “other” zooplankton
varied from 3,039.17±4,272.39 ind.m-3 at S3 in the rainy season to
24,143.95±35,848.33 ind.m-3 at S2 in the dry season (Figure 3).
Despite this variation, no significant spatial or temporal
differences were found in the densities of the zooplankton
community. The outlying high densities recorded in the present
Figure 3. Mean (±SD) density of total zooplankton, copepods
and “other taxa at Taperaçu estuary, northern Brazil.
study may be related to the presence of localized zooplankton
“patches”, as observed by Magalhães (2012) in the same estuary.
In the Taperaçu estuary, as well as in other Amazonian
estuarine ecosystems (Costa et al., 2009; Costa et al., 2012) the
highest zooplankton densities are recorded in the rainy season.
Duggan et al. (2008), which studied the seasonal and interannual
variability in the composition and abundance of the zooplankton
community in a tropical estuary (Darwin Harbour, Australia),
pointed out that the highest average abundance occurred during
the dry season, and that its distribution could be better explained
by the balance between food concentration and predation pressure
(Ueda, 1991), instead of salinity. In the present study, salinity
apparently was not the major determinant of zooplankton and
copepod dynamics, since a significant correlation was only found
between dissolved oxygen concentrations and species diversity (rs
1185
= 0.49, p < 0.05). This may have been due to the influx of more
oxygenated marine water into the estuary, resulting in the
recruitment of coastal species from adjacent ecosystems.
In the case of total zooplankton, copepod nauplii were the most
abundant organisms throughout the study period, with mean
relative abundance ranging from 16% (9.525,33±7,473.92 ind.m-3)
at S2 in the dry season to 58% (721,530.7±1,187,823.94 ind.m-3)
at S1 in the rainy season, followed by O. oswaldocruzi (3%–21%),
A. lilljeborgii (0%–19%), P. quasimodo (2%–14%), cirriped
nauplii (2%–13%), and Oikopleura dioca (0%–12%). The relative
high abundance of copepod nauplii throughout the study period
indicates that copepods reproduce throughout the annual cycle,
which is possibly related to the temperature of the water
(Edmonson, 1965), which tends to vary little over the course of
the year in tropical estuaries, favouring the reproduction of these
organisms. The size of the mesh (120 μm) employed in the present
study may have underestimated the abundance of nauplii stages.
Even so, the estimates of mean nauplii density were higher than
those recorded in most tropical and temperate estuaries around the
world (e.g. Vieira et al., 2003; Duggan et al., 2008), despite the
use of plankton nets with smaller meshes than those used here.
With a similarity of 78%, the cluster analysis resulted in the
formation of two well-defined groups (Figure 4a) – group 1 (dry
season – 81% similarity) and group 2 (rainy season – 72%
similarity). These two groups are separated primarily by the
variation in rainfall, which had a direct effect on the salinity
gradient and, in turn, the occurrence and distribution of the
principal taxa recorded in this study. The SIMPER analysis
indicated that A. lilljeborgii (5.09%) and the copepod nauplii
(5.76%) were the organisms that contributed most to the similarity
within groups 1 and 2, respectively.
The results of the ANOSIM analysis confirmed that the two
groups were significantly different (Global R = 0.519, p < 0.01).
The rainy season samples from S1 did not group with the others
due to the exclusive presence of cladocerans such as Bosmina sp.,
Daphnia sp., and Diaphanossoma sp. in these samples, when there
was a considerable reduction in salinity. These taxa had not been
recorded previously in the Taperaçu estuary, given that salinity is
normally very high in this system throughout the year. These
Figure 4. (a) Cluster analysis and (b) contribution (%) of the main zooplankton taxa recorded in the Taperaçu estuary, northern Brazil.
The “others” category corresponds to the taxa with a relative abundance of less than 5%.
Journal of Coastal Research, Special Issue No. 65, 2013
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Palma, et al.
organisms may have been introduced into the Taperaçu estuary
through the influx of freshwater from the adjacent marshes during
the rainy season. Another source of these organisms may be the
influx of oligohaline waters from the neighbouring Caeté estuary
through the Taici tidal creek (Magalhães et al., 2011). The highest
survey. The first author is grateful to Coordenação de
Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the
concession of a Postgraduate scholarship. Co-authors Luci Pereira,
Rauquírio Costa and Manuel Flores Montes are grateful to
Conselho Nacional de Desenvolvimento Científico e Tecnológico
CNPq for research grants (#308379/2011-0, #306061/2011-2 and
#558106/2009-9, respectively). We are also indebted to Stephen
Ferrari for his careful correction of the English.
LITERATURE CITED
Figure 5. Spatial and seasonal mean (±SD) variations in species
diversity (H’), evenness (J’) and richness of the zooplankton
community at Taperaçu estuary, northern Brazil.
abundance of the dominant zooplanktonic taxa was recorded at S1
and S2 during the rainy season, when salinity was at its lowest
levels (Figure 4b).
Mean species richness (S) varied from 11±3 during the rainy
season to 12±2 in the dry season. Evenness (J’) ranged from
0.67±0.09 in the rainy season to 0.70±0.05 in the dry season,
while diversity (H’) varied from 2.27±0.32 bits.ind-1 in the rainy
season to 2.47±0.35 bits.ind-1 in the dry season (Figure 5).
Overall, then, the dry season samples were richer in species, more
even, and diverse, possibly due to the greater flow of marine water
into the estuary during this period. The opposite tendency was
observed in the rainy season samples due to the dominance of
copepod nauplii and the other taxa during this period.
CONCLUDING REMARKS
In the present study, the Taperaçu estuary was characterized by
a greater diversity of zooplankton taxa during the dry season,
although density was much higher during the rainy season. The
increase in diversity observed during the dry season may be
related to the greater flow of marine water into the estuary during
this part of the year. The increase in the density of zooplankton
during the rainy season was related to the abundance of copepod
nauplii observed in this period. O. oswaldocruzi was the most
abundant and frequent species, occurring in all the samples
analyzed, throughout the study period (annual cycle). This species
is typical of estuarine and marine environments, and is well
adapted to major fluctuations in salinity. The predominance of this
species throughout the year reflects the continuous influence of
marine waters on the study estuary. The presence of limnic
organisms in the estuary during the rainy season may have been
the result of the influx of freshwater from neighbouring marshes,
although they may also have been transported from the oligohaline
waters of the neighbouring Caeté estuary through the Taici tidal
creek.
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