Journal of Fish Biology (2016) doi:10.1111/jfb.12999, available online at wileyonlinelibrary.com
Effects of dredging operations on the demersal fish fauna of a South American tropical–subtropical transition estuary M. Barletta*†, F. J. A. Cysneiros‡ and A. R. A. Lima* *Laboratório de Ecologia e Gerenciamento de Ecossistemas Costeiros e Estuarinos (LEGECE), Departmento de Oceanografia, Universidade Federal de Pernambuco, Cidade Universitária, 50740-550 Recife, Pernambuco, Brazil and ‡Departamento de Estatística, Universidade Federal de Pernambuco, Cidade Universitária, 50740-550, Recife, Pernambuco, Brazil
Changes in the environment and in the composition of fish assemblages in the Paranaguá Estuary (South Brazil) were assessed by comparisons made before, during and after dredging operations, in the same months and areas studied in the previous year. Interactions between year and month were observed for salinity. During the dredging year fish total density was 2 individuals m−2 and with a total biomass of 104 g m−2 (among 31 species captured). For the same period the year before, 0·3 individuals m−2 and 3 g m−2 were captured (38 species). The number of species showed significant time v. month interactions, assuming that fish species composition varied for both year and month. Total mean density and biomass showed significant differences for interaction time v. month, and density and biomass in the dredging month September 2001 in the main channel were scientifically different from other months. Interaction times v. area were significant for Cathorops spixii (increased biomass), Aspistor luniscutis (increased density), Menticirrhus americanus (decreased biomass) and Cynoscion leiarchus (decreased density and biomass). This suggests that during the dredging process there is a change in the structure of the demersal fish assemblage. The impact (damage and mortality) induced by dredging on the macrobenthic animals along the dredge path attracted adults of C. spixii that reached densities 10 times greater than in the year before. On the other hand, sciaenid species practically disappeared. To contribute to the conservation of the estuarine fish fauna, and maintain fisheries production of the Paranaguá Estuary and surrounding areas, it is recommended that, dredging should be done from the late rainy season to the early dry season. Decisions must take into account the ecological cycles of socio-economically important fish species and prioritize the safe disposal of dredged spoils. © 2016 The Fisheries Society of the British Isles
Key words: anthropogenic interventions; estuarine waterways; habitat change; Paranaguá Estuary; port facilities; shipping channels.
INTRODUCTION Estuaries have historically been strategic for economic growth because they are sheltered waters, hence they are usually exposed to significant anthropogenic impacts (Barletta et al., 2010). Such impacts are caused by a large number of different factors, including the construction and maintenance of ports and shipping terminals. In addition, land reclamation, real-estate development and industrial estates have ecologically harmful impacts on estuaries. These impacts are part of a non-sustainable economic †Author to whom correspondence should be addressed. Tel.:+55 81 2126 7223; email:
[email protected]
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(a)
(b)
(c)
(d)
50 m
Menthicirrhus americanus (total length: 27 cm)
Fig. 1. (a) Dredger, (b) cutter head and suction pipe, (c) spoil disposal and (d) example of injuries caused to a fish (e.g. Menticirrhus americanus, Sciaenidae) by the dredging process.
model which, so far, has failed to take into consideration any ecological limits of estuarine environments (Kennish, 1998). One of the most significant, and often neglected, ecological impacts on these systems is the initial and/or maintenance dredging of shipping channels (Fig. 1), which provide access to port and terminal facilities (Kennish, 1992). Dredging, although essential for shipping, is usually in direct conflict with almost all legitimate uses of the sea (MEMG, 2003), and has both direct and indirect impacts on the local ecology. Estuarine organisms, particularly in benthic habitats, are directly impacted. Changes in water quality and circulation patterns indirectly affect other groups. Considering all the potentially harmful impacts caused by activities in ports and terminals, dredging poses the highest environmental concern (Peris-Mora et al., 2005). It is directly responsible for decreases in water quality, generation of vast amounts of contaminated wastes that build up over the years, alteration of the sea floor, coastal habitats, littoral dynamics and impacts on the landscape. It may also affect land use and cause soil contamination incompatible with other uses (Peris-Mora et al., 2005). Effects from dredging operations have immediate and long-term effects, both from dredging and dumping actions (MEMG, 2003). The unplanned dumping of dredged spoils [Fig. 1(c)] may have an even more severe effect than the removal of the material itself (MEMG, 2003). Direct impacts include the physical removal of the sediments where benthic organisms live, leading to their death by the mechanical action of the dredge [Fig. 1(b), (c)] and destruction of their habitat [Fig. 1(c)] (Hoffmann & Dolmer, 2000; Torres, 2000). The indirect effects are related to re-suspension of the bottom sediments and include increased turbidity, limited light penetration, dissolved oxygen consumption
© 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.12999
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and a decrease in primary productivity. The nature and extent of the environmental impacts associated with physical disturbance of sediments can include direct destruction of benthic habitat, and decreased water quality as a result of sediment resuspension. The effect of clam dredging off Lagos (south Portugal) on bottom structure has been estimated and the damage inflicted on the benthic macrofauna left on the dredge path evaluated (Gaspar et al., 2003). The sediment suspended during dredging rapidly resettled both on sand and sandy-mud bottoms, and the impact (damage and mortality) induced by dredging on the macrobenthic animals left on the dredge path rapidly attracted Ophiura albida. Immediately after the tow, ophiuroids reached densities eight times greater in the track area than in the background. Another example is from the Thames Estuary (U.K.) where the disposal of dredged material from port expansion caused, as consequence large amounts of material, redution of benthic fauna biodiversity (MEMG, 2003). Other impacts on organisms are caused by changes in the pattern of currents and tides within estuaries. Depth changes lead to further and deeper salt wedge penetrations and consequently new patterns and variations in salinity. Wave action and sediment transport alterations will result in new erosion and sedimentation processes. Although dredging may bring some benefits in terms of improved water circulation, and in the medium term (few years), better water quality in semi-enclosed water bodies, this is not usually the case in larger estuaries where ports are located (Peris-Mora et al., 2005). The type of dredge and the way it is operated can greatly influence the potential damage in terms of dispersal of material being re-located (MEMG, 2003). Therefore, the form and magnitude of dredged spoil plumes are governed by the dredging technique employed, sensitivity of the dredged material to re-suspension, and the hydrodynamics of the overlying water. Plumes vary in horizontal extent from a few 100 m to tens of km. There is also a vertical gradient associated with these plumes in which the bottom waters are the most impacted. Re-suspension of the deposited material is very likely to occur, causing a ‘hopping effect’ of the deposited dredged material across the sea floor. As a consequence, fine sediments can reach far further and spread over much larger areas. The life span of a plume is measured on a scale of hours, but bottom transport of deposited sediments can last for weeks after disposal (Smith et al., 2008). The use of response indicators to evaluate the consequences of decisions from port authorities (Peris-Mora et al., 2005) is one of the most frequently recommended approaches (MEMG, 2003). Indicators are signals which allow data to become available for management purposes (Peris-Mora et al., 2005), including conservation of nature and traditional ways of life. Therefore, to ensure that dredging activities do not result in unacceptable environmental degradation, indicators of physico-chemical, biological and socio-economic impact, capable of detecting the ‘dredging signal’ (MEMG, 2003) should be chosen. In other words, indicators should be representative of the ecological sensitivity of the dredging and disposal sites, as well as surrounding areas. Studies discussing the effects of dredging operations on temperate estuarine communities are usually based on information from benthic communities (Kennish, 1992, 1998). Likewise, in tropical estuaries most of the attention has been focussed on the impacts on benthic invertebrates (Flood et al., 2005; Vivan et al., 2009), seagrass (McMahon et al., 2011), phytoplankton and bacteria (Nayar et al., 2003). Research on the effects of habitat fragmentation by deepening of channels and removal of wetland vegetation in Lake Huron (Uzarski et al., 2009), damage to commercial fisheries from marine sand mining in Korea (Kim & Grigalunas, 2009),
© 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.12999
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the response of the fish community to the dredging operations of coastal rivers in the BioBio region in Chile (Ortiz-Sandoval et al., 2009), the response of tidal creek fishes to dredging and coastal development pressures in Lynnhaven River (Chesapeake Bay) (Bilkovic, 2011), interannual changes in benthic fish populations in the eastern region of the English Channel after sand and gravel mining (Drabble, 2012), and harbour construction effects on reef fish communities in north-east Brazil (Freitas et al., 2009), are types of indicators reported. Experiments evaluating the risks of prolonged exposure to high concentrations of suspended sediment (SS) in orange-spotted grouper Epinephelus coioides (Hamilton 1822), an important mariculture species that has a wide distribution in the Indo-Pacific, showed that damages to gill structure were evident and strongly correlated with SS concentration (Au et al., 2004). Additionally, experiments evaluating the sublethal effects of SS in Pacific herring Clupea pallasii Valenciennes 1847 eggs and larvae from San Francisco Bay estuary, U.S.A. (Griffin et al., 2009), reported that dredge SS increased self-aggregation of the eggs and led to significant sublethal and lethal effects (e.g. increases in precocious larval hatch, higher percentages of abnormal larvae and increases in larval mortality) during the first 2 h in water at SS of 250 or 500 mg l−1 . The study of the ecology of estuaries through their fish communities has been shown to be fundamental for the understanding of the functioning of the entire ecosystem (Yáñez-Arancibia et al., 1985; Cyrus & Blaber, 1992; Barletta-Bergan et al., 2002a, b; Barletta et al., 2005, 2008; Barletta & Blaber, 2007; Barletta & Barletta-Bergan, 2009; Dantas et al., 2010, 2015; Lima et al., 2015, 2016; Ramos et al., 2016). All these studies have emphasized the importance of the estuarine ecosystem for marine, estuarine and freshwater fish species at each phase of their lives. Some these fishes have socio-economic importance for the local populations (Barletta & Costa, 2009; Barletta et al., 2010). The use of suitable methods (sample design and sample effort) for describing and predicting the fish communities may be an important tool for detecting, describing and quantifying the effects of dredging activities in estuarine ecosystems. Also, data from pre-dredging studies are important environmental records and can be used to detect spatio-temporal changes. The use of this approach for detecting the effects of dredging activities on fish communities has not previously been attempted. The aim of the present study was to assess the impact of dredging in estuaries, especially on the demersal fish assemblages using before–after and impact-control approaches. Characteristics of the demersal fish communities from the main channel of Paranaguá Estuary were compared before (May 2001), during (September 2001) and after (March 2002) dredging. Moreover, comparisons using these same months of the year before dredging (Barletta et al., 2008) were also made in order to quantify possible differences between years on the fish assemblages.
MATERIALS AND METHODS S T U DY A R E A The main channel of the east–west axis of the Paranaguá Estuary (depth range between 5 and 18 m) (25∘ 15′ –25∘ 35′ S; 48∘ 45′ –48∘ 45′ W) can be divided into three sectors (upper, middle and lower estuary) according to the salinity gradient and geomorphology (Barletta et al., 2008). The upper estuary has mesohaline and oligohaline characteristics without vertical stratification during the dry season (winter), with partial or strong stratification during the rainy season
© 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.12999
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D R E D G I N G E F F E C T S O N F I S H A S S E M B L AG E S N
(b)
(a)
Study area 0
0°
2
4 km
Brazil P. do Felix
Guaraqueçaba Bay
Deposit area
Study area Dredged area
tic lan
Control area
At
N
Oc
ea
n
–25° 0·5ʹ
0
5
10 km
–48° 0·0ʹ
Fig. 2. (a) Paranaguá Estuary on the southern coast of Brazil. Portion of the estuary where the main channel was dredged is represented by . Samples from Barletta et al. (2008) are represented by 216 dots ( ). (b) Shipping channel of the east–west axis of Paranaguá Estuary which was dredged to improve access to Ponta do Felix port facilities. Continuous line ( ) marks the dredged channel area and dashed line (white) the adjacent area where dredged spoils were disposed. (b)The samples taken before ( ), during ( ) and after ( ) the dredging process are shown. (a) The control area is represented by .
(summer) (Barletta et al., 2008; Figs 2 and 3). The middle estuary has intermediate salinities, and during the rainy season the area becomes meso- and oligohaline because it is influenced by freshwater run off. During the dry season, sea water is the main influence on this area. The lower estuary is dominated by marine waters throughout the year. The Paranaguá Estuary and its adjacent areas also form an important nature conservation zone (Guebert-Bartholo et al., 2011). The dredging process studied here has deepened the main channel of the east–west axis of Paranaguá Estuary, between the end of the upper estuary and the head of the middle estuary [Fig. 2(a)]. The dredged spoils were disposed of in the area adjacent to the dredged channel [Fig. 2(b)].
E N V I R O N M E N TA L VA R I A B L E S Before each fish sample was taken, samples of surface and bottom water were collected for dissolved oxygen (mg l−1 ), water temperature (∘ C) (Wissenschaftlich Technische Werkstätten, WTW OXI 325; www.wfw.com) and salinity (WTW LF 197) mesurements. The Secchi depth (cm) was also taken. FISH SAMPLES Eighteen fish samples were taken before (May 2001), during (September 2001) and after (March 2002) dredging (Fig. 2). For each time period three samples were taken from the dredged channel and three from the adjacent area where the dredge spoils were dumped [Fig. 2(b)]. In order to analyse the seasonal and interannual effects on the fish species distribution in the estuary, comparisons were done at the same place using the same months of the year prior to the dredging (Barletta et al., 2008). Samples taken downstream from the dredged area (area 2, middle estuary, Barletta et al., 2008) were considered as a control [Fig. 2(a)]. In the present study, the fish samples were taken using the same net and methods described in Barletta et al. (2008).
© 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.12999
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700 600
Rainfall (mm)
500 400 300 200 100 0
h y y il uar bruar Marc Apr Fe
Jan
Ma
y
e
Jun
t r r r r y Jul ugus embe ctobe embe embe A ept c v O e o D N S
Fig. 3. Rainfall (monthly totals in mm) for Paranaguá Estuary [year: 2000 ( ), 2001 ( ), 2002 ( )] (Departamento Nacional de Meterologia do Estado do Paraná) and historical rainfall patterns ( : 1961/1990) (DNM, 1992). May 2001: before dredging, September 2001: during the dredging process and March 2002: after the dredging process.
Samples were taken with an otter trawl 7·7 m long, with a mesh size between-knots of 35 mm in the body, 22 mm at the codend and 6 mm at the codend cover. The length of the ground rope was 8·5 m and the head rope was 7·1 m. Fish biomass and density were calculated following the criteria adopted by Barletta et al. (2005, 2008). For each sample, the swept area (A) was estimated from: A = DhX2 (1) where, D is the legth of the path, h is the length of the head rope and X 2 is that fraction of the head rope (hX 2 ), which is equal to the width of the path swept by the trawl, the wing spread (Sparre et al., 1989). According to Barletta et al. (2005) the ideal towing speed, at which the otter trawl has the optimal width, was recorded between 3·7 km h−1 (2·0 knots) (h = 3·4 m; X 2 = 0·4787) and 6·5 km h−1 (3·5 knots) (h = 3·8 m; X 2 = 0·5352). In this study, the samples were taken at speeds between 4 and 5·5 km h−1 , and it was assumed that the fraction of the head rope which was close to the width of the swept area was X 2 = 0·5. The catch per unit area (CPUA) was used for the estimation of density (D) and biomass (B), which were calculated by dividing the catch by the swept area (A): ( ) D = CN A−1 individuals m−2 ( ) B = CM A−1 g m−2
(2) (3)
where CN is the catch in number and CM is the catch in mass of fishes. The abundances are relative, as the gear efficiency has not been built into the density and biomass calculations.
S TAT I S T I C A L A N A LY S I S Three-way ANOVA was used to determine whether significant differences in environmental variables (water temperature, dissolved oxygen, salinity and Secchi depth) occurred in time [control, dredging year and year before the dredging process (Barletta et al., 2008)], space (dredged channel and adjacent area) and position of the water column (surface and botton).
© 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.12999
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All these variables, except Secchi depth, were also analysed for significant differences in the water column (surface and bottom). In order to test the influence of the dredging process and seasonality on fish species distribution (number of species, density, biomass and components), three-way ANOVA was used to determine whether significant differences occurred in time [control, year before the dredging process (Barletta et al., 2008)] and dredging year, months [May 2001 and June 2000; September 2001 (when the dredging process was occurred) and September 2000; March 2002 and March 2001)] and sites (dredged channel and adjacent area). One of the assumptions to apply the ANOVA is the normality and homecedasticity of the response variable. When the normal distribution is not adequate for the dataset (y1 , … , yn ) a transformation to obtain normality is necessary. The Box-Cox transformation (Box & Cox, 1964) consist of a search method to find a value 𝜆 such that transformed data Z 1 , … , Z n tend to a normal distribution and assume a homoscedastic variance. Box–Cox transformation (Box & Cox, 1964) was used for the biotic (number of species, total biomass, density and components) variables as follows: Z𝜆 =
{
(Ln 𝜆(y) if) 𝜆 = 0 y – 1 ∕𝜆 if 𝜆 ≠ 0,
(4)
where Z𝜆 is the transformed variable, y is an original untransformed data. Lambda (𝜆) is the known value that minimize the sum of squares of the transformed observation, Se (𝜆), in a grid of values. Cochran’s test was used to check the homogeneity of variances. Since it showed that the variance was still often heterogenous, conclusions from the results of ANOVA have concentrated on those cases where significance levels were 3% in all samples) was conducted to investigate the structure of the fish assemblage and particularly its variation in different years (year before and dredging year) in terms of the environmental variables measured during sampling [i.e. direct gradient analysis; ter Braak (1986)]. In this analysis, the environmental variables (salinity, dissolved oxygen, water temperature and Secchi depth) were introduced to the main matrix as descriptors (Legendre & Legendre, 1998). With this procedure, statistical association among fish assemblage patterns and environmental variables for each year were quantified. The CCA was run with 100 iterations with randomized site locations to facilitate Monte-Carlo tests between the eigenvalues and species-environment correlations for each axis that resulted from CCA and those expected by chance. The CCA produces a biplot where environmental variables are represented as arrows (vectors) radiating from origin of the ordination. The length of an environmental vector is related to strength of the relationship between the environmental variable that the vector represents and the species assemblages for each year.
RESULTS E N V I R O N M E N TA L VA R I A B L E S
Water temperature (surface and bottom) showed the same annual trends (Fig. 4). Significant differences were observed in March for both years (F 2,36 = 840·06, P < 0·01) (Fig. 4). Dissolved oxygen showed significant differences for months (F 2,36 = 12·941, P < 0·01) and throughout the water column (F 1,36 = 25·591, P < 0·01). Interactions between the factors year and month (F 4,36 = 5·4314, P < 0·01) were observed for salinity (Fig. 4) and suggests that this area of the estuary was previously characterized by a stratified estuarine salt wedge. During the year of the dredging,
© 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.12999
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M . B A R L E T TA E T A L.
(a)
Surface
30
Bottom
Water temperature (° C)
28 26 24 22 20 18 16
Dissolved oxygen (mg l−1)
(b)
8·0 7·5 7·0 6·5 6·0 5·5 5·0 4·5
(c)
35 30
Salinity
25 20 15 10 5 0 1
2
3
1
2
3
Month Fig. 4. Surface and bottom mean ± s.d. values of (a) water temperature, (b) dissolved oxygen and (c) salinity for control ( ), the year before ( ) and year of the dredging process ( ).
however, water stratification was not detected. This indicates that the dredging processes for deepening the main channel dislodged the estuarine salt wedge to inner parts of the estuary, causing an increase in salinity, mainly at the end of the rainy season (month 3 dredging year) (Fig. 4). In addition, the variable Secchi depth showed significant interactions between the factors year and month (F 4,18 = 13·391, P < 0·01) (Fig. 5). © 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.12999
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180 160
Secchi depth (cm)
140 120 100 80 60 40 20 0 1
2
3
Month Fig. 5. Mean ± s.d. Secchi depth (cm) for control ( ), the year before ( ) and year of dredging ( ).
C O M P O S I T I O N O F T H E F I S H A S S E M B L AG E
During the dredging year, 31 species were captured from the dredged area with absolute mean density and biomass values of 2 individuals m−2 and 104 g m−2 , respectively (Appendix I). After the dredging process, 15 species were captured from the dredged area with absolute mean density and biomass values of 0·27 individuals m−2 and 4·05 g m−2 (Appendix I). For the same period in the year before, however, 38 species were captured, with 0·3 individuals m−2 and 3 g m−2 (Appendix II). These differences between years is a consequence of the increase in catfish (Ariidae) species densities and biomass, which concentrated in the dredged channel. Cathorops spixii (Agassiz 1829) and Stellifer rastrifer (Jordan 1889) were the most important species in density and biomass for both years (Appendices I and II). D R E D G I N G P R O C E S S E F F E C T S V. S E A S O N A L VA R I AT I O N S O N T H E F I S H A S S E M B L AG E
During the dredging year, number of species showed significant differences for the factors time (before, during and after dredging process) and site (dredged channel and adjacent area which received the dredging materials) (Table I and Fig. 6). Time v. site interactions were also significant, assuming that fish species composition varied in both time and space. This indicates that estuary’s physico-chemical characteristics changed, and therefore fish assemblage composition changed as well. The source of variance was the decrease in number of species after the dredging process in both the dredged channel and the adjacent area where the dredge materials were deposited (Fig. 6). Total mean density showed significant differences for the variable site, given that the density found in the September dredging month in the main channel was significantly different from that found in other months independent of site (channel and adjacent area which received the dredged materials during this month) (Table I and Fig. 6). Total
© 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.12999
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M . B A R L E T TA E T A L.
Table I. Summary of the ANOVA results for number of species, total (and components) density and biomass for time: before dredging (BD), during dredging (DD) and after dredging (AD), for site: dredged channel (DC) and adjacent area (AA) Source of variance Parameters Number of species Density (individuals m−2 ) Total Genidens barbus Menticirrhus americanus Stellifer rastrifer Genidens genidens Cathorops spixii Aspistor luniscutis Cynoscion leiarchus Biomass (g m−2 ) Total G. barbus M. americanus S. rastrifer G. genidens C. spixii A. luniscutis C. leiarchus
Time (1)
Site (2)
Interactions
* BD DD AD
** DC AA
1 × 2**
NS
* DC AA * DC AA NS
NS NS NS NS NS
* DC AA * DC AA NS * DC AA * DC AA
NS
* BD AD DD * BD DD AD * BD DD AD * DD BD AD NS * DD AD BD * BD AD DD
1 × 2* 1 × 2* NS NS
* DD BD AD * * BB DD AD *
* DC AA NS NS
NS
* DC AA
NS
* DD BD AD * DD BD AD *
* DC AA * DC AA NS
1 × 2*
1 × 2*
* BD AD DD
NS
NS
NS
1 × 2*
NS, non-significant differences (P > 0·05); *, P < 0·05; **, P < 0·01; differences among time and sites were determined by Bonferroni test (P < 0·05) post hoc comparisons.
mean biomass showed significant differences for time (September dredging month) and site (dredged channel). The results suggest that the fish assemblage which remained in the estuary during the dredging process (Appendix I) were concentrated in density and biomass in the main channel. This explains the increase in total mean density and biomass during the September dredging month. During this time, most of the fish species, avoided the adjacent area where the dredge spoils were deposited.
© 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.12999
(a)
20
Number of species
D R E D G I N G E F F E C T S O N F I S H A S S E M B L AG E S
15
11
10
5
0
(b)
25
Bio mass (g m–2)
20 15 10 5 0
Density (individuals m–2)
(c)
1 0·8 0·6 0·4 0·2 0 BD
DD
AD
Phases of dredging process Fig. 6. Mean + s.d. (a) number of species, (b) total biomass and (c) density for dredged channel ( ) and adjacent area ( ).
When the dredging year is compared with year before it was detected that fish composition and total mean density showed significant differences between years (Table II and Fig. 7). Total mean biomass showed significant differences between year and months. Interactions between both factors also was detected indicating that the source of variance between years was September of the dredging year (Table II and Fig.7).
© 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.12999
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Table II. Summary of the ANOVA results for the variables number species, total (and components) density and biomass Source of variance Parameters
Year (1)
Month (2)
Interactions
*
NS
NS
** C YB YD **
NS
NS
*
1 × 2**
Menticirrhus americanus
* C YB YD
*
NS
Stellifer rastrifer
* C YB YD **
NS
1 × 2*
NS
NS
Number of species Density (individuals m−2 ) Total Genidens barbus
Genidens genidens Cathorops spixii
* YD C YB
*
NS
Aspistor luniscutis
* YD C YB *
NS
NS
NS
1 × 2*
* S Ma M/J * S Ma M/J ** M/J S Ma NS
1 × 2*
Cynoscion leiarchus Biomass (g m−2 ) Total G. barbus M. americanus S. rastrifer G. genidens C. spixii A. luniscutis C. leiarchus
* YD YB C * YD YB C NS * C YB YD ** C YB YD NS * C YB YD * C YB YD
1 × 2** 1 × 2*
NS
NS
NS NS
1 × 2* NS
NS
1 × 2**
YB, year before; C, control; YD, year of dredging process; M/J, May and June; S, September; Ma, March; NS, non-significant (P > 0·05); *, P < 0·05; **, P < 0·01. Differences between year and months were determined by Bonferroni test (P < 0·05) post hoc comparisons.
© 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.12999
D R E D G I N G E F F E C T S O N F I S H A S S E M B L AG E S
Number of species
(a)
20 18 16 14 12 10 8 6 4 2 0
(b)
12
13
Bio mass (g m–2)
10 8 6 4 2 0
Density (individuals m–2)
(c)
0·9
0·6
0·3
0
1
2
3
Month Fig. 7. Mean + s.d. (a) number of species, (b) total mean biomass and (d) density for control ( ), year before dredging ( ) and dredging year ( ) of the main channel and its adjacent area used for dredged materials disposal.
From the 31 species sampled during the dredging year (Appendix I), for at least seven of them it was possible to detected some sensitivity to dredging (Table I and Figs 8 and 9). Significant interaction between time v. site was detected for C. spixii (density and biomass), Aspistor luniscutis (Valenciennes 1840) (biomass) and Genidens genidens (Cuvier 1829) (density and biomass). During the dredging process (September of the dredging year) the density and biomass of these species increased in the dredged channel. When these species are compared between years (dredging year v. year before) it is clear that the source of variance between years was the month when the dredging process took place (September of dredging year) (Table II and
© 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.12999
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M . B A R L E T TA E T A L.
0·002
(a)
0·008
0·0015
0·006
0·001
0·004
0·0005
0·002
0
0
Density (individuals m–2)
0·4
(c)
0·08
0·3
0·06
0·2
0·04
0·1
0·02
0
0
1
(e)
0·07 0·06 0·05 0·04 0·03 0·02 0·01 0
0·8 0·6 0·4 0·2 0
(b)
(d)
(f)
BD 0·03
DD
AD
(g)
0·02 0·01 0 BD
DD
AD
Phases of dredging process
Fig. 8. Mean ± s.d. density of (a) Genidens barbus, (b) Menticirrhus americanus,(c) Stellifer rastrifer, (d) Genidens genidens, (e) Cathorops spixii, (f) Aspistor luniscutis and (g) Cynoscion leiarchus in the main channel ( ) and its adjacent area used for dredged material disposal ( ).
Figs 10 and 11). In addition, density and biomass of Genidens barbus (Lacépède 1803) increased mainly where the reject sediment was deposited during the dredging process (September of the dredging year), had (Table I and Figs 8 and 9). It was the main source of variance between years (dredging year and year before) (Table II and Figs 10 and 11). On the other hand, significant differences were detected for Menticirrhus americanus (L. 1758) for time (density and biomass); S. rastrifer for time and site (density and biomass) and Cynoscion leiarchus (Cuvier 1830) for time (density and biomass) and site (density) (Table I and Figs 8 and 9). For these species, the dredging process decreased significantly their density and biomass within and between years (Table II and Figs10 and 11). CCA ordination biplot diagrams of species scores (Fig. 12), as well as regression statistics (Table III), permitted an interpretation of the distribution of the fish species
© 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.12999
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D R E D G I N G E F F E C T S O N F I S H A S S E M B L AG E S
0·2
0·4
(a)
0·3
0·15
0·2
0·1 0·05
0·1
0
0
0·8
(b)
10
(c)
(d)
8
0·6
6 0·4 4
Biomass (g m–2)
0·2
2
0 40
0 1·5
(e)
(f)
1·2 30
0·9
20
0·6
10
0·3
0
0 BD
0·5
DD
AD
(g)
0·4 0·3 0·2 0·1 0 BD
DD
AD
Phases of dredging process
Fig. 9. Mean ± s.d. biomass of (a) Genidens barbus, (b) Menticirrhus americanus,(c) Stellifer rastrifer, (d) Genidens genidens, (e) Cathorops spixii, (f) Aspistor luniscutis and (g) Cynoscion leiarchus in the main channel ( ) and its adjacent area used for dredged material disposal ( ).
groups per month and area for each year, in relation to environmental variables. The CCA output detected that, for both years, axis I was represented by the salinity gradient. In addition, during the year before dredging, water temperature and dissolved oxygen (both P < 0·01) were the most important variables. These variables were responsible for structuring patterns of the fish assemblages and the formation of axes I and II. The second factorial axis best represents the seasonality of the water temperature, but during the dredging year, no environmental variable was responsible for structuring patterns of the fish assemblages and formation of axes I and II. It suggests that some other forcing factor, such as anthropogenic perturbations, has influenced the distribution pattern of the fish assemblages. For example, G. barbus occurred in the adjacent areas, mainly during the dredging operations (Figs 8 and 9). On the other hand, during the same period, C. spixii, A. luniscutis and G. genidens showed the highest mean density and biomass values, both in the dredged channel. Moreover, S. rastrifer almost disappeared in density and biomass from the dredged channel, and M. americanus
© 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.12999
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M . B A R L E T TA E T A L.
0·002
(a)
0·008
0·0015
0·006
0·001
0·004
0·0005
0·002
0
0
0·2
(c)
0·05
(b)
(d)
0·04
0·15
Density (individuals m–2)
0·03 0·1
0·02
0·05
0·01
0
0
1
(e)
0·04
0·8
(f)
0·03
0·6
0·02
0·4 0·01
0·2 0
0 1
0·025
2
3
(g)
0·02 0·015 0·01 0·005 0
1
2
3
Month Fig. 10. Mean ± s.d. density of (a) Genidens barbus, (b) Menticirrhus americanus,(c) Stellifer rastrifer, (d) Genidens genidens, (e) Cathorops spixii, (f) Aspistor luniscutis and (g) Cynoscion leiarchus for control ( ), year before dredging ( ) and dredging year ( ) of the main channel and its adjacent area used for dredged materials disposal.
from both sites (dredged channel and adjacent area where the dredged sediment was deposited) after the dredging operations (Figs 8, 9 and 12). In addition, during the dredging year, Etropus crossotus Jordan & Gilbert 1882, Citharichthys spilopterus Günther 1862, Citharichthys arenaceus Evermann & Marsh 1900, Sphoeroides testudineus (L. 1758) and Symphurus tessellatus (Quoy & Gaimard 1824) were mostly captured in the month before the start of dredging (June 2001). After that, these species were seldom captured [Appendix I and Fig. 12(c)]. DISCUSSION F I S H A S S E M B L AG E S U N D E R S E A S O NA L A N D A N T H RO P O G E N I C E F F E C T S
Areas that are more environmentally varied may be more able to withstand the effects of anthropogenic perturbations and are said to be in ‘environmental homeostasis’,
© 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.12999
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D R E D G I N G E F F E C T S O N F I S H A S S E M B L AG E S
(a)
0·4
(b)
0·1 0·08
0·3
0·06
0·2
0·04 0·1
0·02 0
0·8
0
(c)
5
(d)
4 0·6
3
Biomass (g m–2)
0·4
2
0·2
1
0
0
25
(e)
1·2 1·0 0·8 0·6 0·4 0·2 0
20 15 10 5 0
(f)
1 0·3
2
3
(g)
0·2 0·1 0 1
2
3
Month Fig. 11. Mean ± s.d. biomass of (a) Genidens barbus, (b) Menticirrhus americanus,(c) Stellifer rastrifer, (d) Genidens genidens, (e) Cathorops spixii, (f) Aspistor luniscutis and (g) Cynoscion leiarchus for control ( ), year before dredging ( ) and dredging year ( ) of the main channel and its adjacent area used for dredged materials disposal.
becoming more resilient (Elliott & Quintino, 2007). In such cases, a low signal (anthropogenically driven change) to noise (natural changes) ratio makes it difficult to detect man-induced changes in estuaries, unless the anthropogenic stress is severe, leading to the ‘estuarine quality paradox’ (Elliott & Quintino, 2007). Also, the structural attributes of estuaries, such as community diversity and structure, population abundance and reproduction, and species distribution, exist as expected, under natural prevailing conditions, and may be more resilient to natural disturbances than previously thought (Borja & Elliott, 2007). These concepts and limits should be considered when developing descriptors of reference conditions for regional seas (Barletta et al., 2010).
© 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.12999
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M . B A R L E T TA E T A L.
(a)
3
Stestu
2
Ggeni
Axis II (24%)
YB2a
1
YB1c
YB1a
YB2c Sal
Mamer Secchi Gluteus Cspix Dradia YB3a
0
Stessel
Slunis
Cleiarc Ecross Gbarb
Temp**
O2 **
YB3c
–1
Srast Cspil
Cfaber
–2 –2
–1
0
1
2
3
4
Axis I (60%)
(b)
(c)
3
4 Gbarb
Stestu
Ggeni
2
2
Slunis
C2a
Axis II (23%)
Axis II (26%)
1
DY3a C2c
Gluteus Sal C1c
0
C1a
Secchi
Mamer C3a Cleiarc Dradia
Temp*
–1
Slunis
Cspix
Stessel
Ecross
O2**
DY2a Ggeni DY2c DY3c Cspix O2 Dradia
0
Temp
Secchi* Sal*
Srast Cfaber
Cleiarc
Gluteus Cfaber Mamer
–2
C3c
DY1c Srast
DY1a
Gbarb
Ecross
Cspil
Stessel Cspil
–2 –2
–1
0
1
Axis I (59%)
2
3
–4
–2
–1
0
Stestu
1
2
3
Axis I (55%)
Fig. 12. Canonical correspondent analysis ordination biplot showing species (see Appendices I and II) centroids in relation to environmental variables (temp., bottom water temperature; O2, bottom dissolved oxygen; Sal, bottom salinity; Secchi, Secchi depth) for each year: (a) year before dredging, (b), control and (c) dredging year. , species: Cspix, Cathorops spixii; Alunis, Aspistor luniscutis; Gluteus, Geniatremus luteus; Stessel, Symphurus tessellatus; Cleiarc, Cynoscion leiarchus; Cspil, Citharichthys spilopterus; Ecross, Etropus crossotus; Ggeni, Genidens genidens; Gbarb, Genidens barbus; Mamer, Menticirrhus americanus; Dradia, Diplectrum radialis; Cfaber, Chaetodipterus faber; Srast, Stellifer rastrifer; Stestu, Sphoeroides testudineus. , year month, area: YB1c, year before dredging month 1 (June 2000), channel; YB1a, year before dredging month 1 (June 2000), adjacent area; YB2c, year before dredging month 2 (September/2000), channel; YB2a, year before dredging month 2 (September/2000), adjacent area; YB3c, year before dredging month 3 (March 2001), channel; YB3a year before dredging month 3 (March 2001), adjacent area; C1c, control month 1 (June 2000), channel; C1a, control month 1 (June 2000), adjacent area; C2c, control month 2 (September 2000), channel; C2a, control month 2 (September 2000), adjacent area; C3c, control month 3 (March 2001), channel; C3a, control month 3 (March 2001), adjacent area; DY1c, dredging year month 1 (May 2001), channel; DY1a, dredging year month 1 (May 2001), adjacent area; DY2c, dredging year month 2 (September 2001), channel; DY2a, dredging year month 2 (September 2001), adjacent area; DY3c, dredging year month 3 (March 2002), channel; DY3a, dredging year month 3 (March 2002), adjacent area.
© 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.12999
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D R E D G I N G E F F E C T S O N F I S H A S S E M B L AG E S
Table III. Summary of canonical correspondence analysis (CCA) ordination biplot using species biomass (see CCA diagram in Fig. 12) in relation to environmental variables (bottom water temperature, bottom dissolved oxygen, bottom salinity and Secchi depth for each year: (a) year before dredging, (b) control and (c) dredging year. Correlation with environmental variables are shown: *, P < 0·05; **, P < 0·01
(a) Year before dredging Total inertia Eigenvalues Species–environmental correlations (Pearson) Cumulative % variance Species data Species environmental relation Environmental variables Salinity Dissolved oxygen (mg l−1 ) Water temperature (∘ C) Secchi depth (cm) (b) Control Total inertia Eigenvalues Species–environment correlations (Pearson) Cumulative % variance Species data Species environmental relation Environmental variables Salinity Dissolved oxygen (mg l−1 ) Water temperature (∘ C) Secchi depth (cm) (c) Dredging year Total inertia Eigenvalues Species–environment correlations (Pearson) Cumulative % variance Species data Species environmental relation Environmental variables Salinity Dissolved oxygen (mg l−1 ) Water temperature (∘ C) Secchi depth (cm)
Axis I
Axis II
0·32 0·994
0·128 1
59·8 69·2
83·8 96·9
0·617 0·92 ** −0·78 0·801
0·6304 −0·29 0·51 * 0·351
0·355 0·995
0·169 0·997
55·7 61·7
82·2 91·1
0·327 0·971 ** −0·575 0·878
0·799 −0·006 −0·711 0·157
0·196 0·961
0·083 0·989
55·5 62·8
79 89·4
0·614* −0·6713 0·1361 0·665*
−0·707 −0·179 0·572 −0·289
0·535
0·638
*
0·353
*
Salinities showed a clear seasonal pattern, especially in the upper reaches of Paranaguá Estuary (Barletta et al., 2008). The lowest salinity values (0–12) were observed between January and March (early rainy season). This also explains the greater species density and biomass in the middle estuary, where salinity is stable even at the end of the rainy season, and remained so in the year before the dredging
© 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.12999
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M . B A R L E T TA E T A L.
Dredging Process
During
?
Cynoscion leiarchus Stellifer rastrifer Cathorops spixii
Before
After Menticirrhus americanus
Aspistor luniscutis
Fig. 13. Conceptual model developed based on the main results and conclusion of this study. In the first situation (before dredging, May 2001), the system is characterized by a stratification of the water column, diversity of fish species and equilibrium among the different groups and guilds. During the dredging process (September 2001, there is no longer water stratification in relation to salinity, turbidity increases and the fish assemblage is dominated by Ariidae (principally Cathorops spixii), with a clear drop in diversity and a rise in biomass. Following, in the after dredging situation (March 2002), there is a dominance of neritic processes, with only slight salinity stratification. At this time, the fish assemblage resumes a biomass similar to the before dredging levels, but with changed composition. Finally, it is not known if the system recovers to acceptable water quality and fish assemblages.
process began. Seasonal changes in the composition of fish assemblages of tropical estuaries are often attributed to the seasonal fluctuation of salinity, reproduction and recruitment patterns (Barletta-Bergan et al., 2002a, b; Barletta et al., 2003, 2005; Barletta & Blaber, 2007; Dantas et al., 2010, 2015; Lima et al., 2015; Ramos et al., 2016). The Paranaguá Estuary is not an exception to this model, but the middle and lower portions of the estuary have stable salinities even during the peak of the rainy season (Barletta et al., 2008). The Sciaenidae had the greatest species diversity in the area before and during the dredging operations. These species are frequently dominant in estuarine environments of tropical and sub-tropical regions (Barletta et al., 2005, 2008; Barletta & Blaber, 2007), and the decrease in the species diversity of sciaenids after dredging is therefore important information (Fig. 13 and Table IV). According to Chao (2002), sciaenids feed mainly on live prey on the bottom and in the water column. These prey and sciaenid species themselves [e.g. M. americanus, Fig. 1(d)] were affected by the mechanical action of the dredge. Another factor that may cause a decrease in diversity of fish species after dredging is the release of toxic substances and elements from the sediments (Nayar et al., 2003; Flood et al., 2005; Souza et al., 2007; Griffin et al., 2009).
© 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.12999
D R E D G I N G E F F E C T S O N F I S H A S S E M B L AG E S
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Table IV. Comparison between the sensibility (the ability to feel and react to something) and responses (an answer or reaction to something that has been done) of the main species in this study to the dredging process Species
Sensibility
Cynoscion leiarchus
High
Stellifer rastrifer
High
Menticirrhus americanus High Cathorops spixii
Low
Aspistor luniscutis
Low
Genidens genidens
Low
Genidens barbus
Medium
Response Avoids dredging area and dredged material deposit. Migrate to another area. Avoids dredging area and dredged material deposit. Migrate to another area. Avoids dredging area and dredged material deposit. Migrate to another area. Attracted by increased food availability (invertebrates and carcasses), especially in the dredged channel. Attracted by increased food availability (invertebrates and carcasses), especially in the dredged channel. Attracted by increased food availability (invertebrates and carcasses), especially in the dredged channel. Attracted to dredged material deposit. Not present in the main channel after dredging.
Suspended particles and dissolved elements or substances in equilibrium with them can re-settle at different speeds, smothering, suffocating and poisoning fish eggs, larvae (Griffin et al., 2009) and benthic organisms, compelling the motile ones to migrate to other regions and killing the sessile (Vivan et al., 2009). Dredging can also alter the structure of food chains, causing death of some fish species for lack of food (Pombo et al., 2002). Other environmental and socio-economic studies similar to this have shown that the level of contaminants in port sediments in Brazil is critical, the sources of contamination are multiple (Souza et al., 2007). Channels are permanently dredged, but remain contaminated since contaminant sources are not adequately treated. Sediment contaminants can effectively be transferred to the water column (elutriate effect) at the dredge spoil disposal site and then transported (Souza et al., 2007), spreading the pollution far and wide. Suspended or dissolved organic matter can consume all the available dissolved oxygen from the water column and temporarily stress aquatic organisms (Kennish, 1998). This suggests that, with the increase of turbidity during and immediately after dredging, and a decreased dissolved oxygen supply, fish species may be forced to migrate to other areas (Table IV). In this study, the lowest Secchi depth (mean ± s.d. 50 ± 26 cm) was recorded during the dredging processes in September 2001 (Fig. 13). Six months after dredging operations, the water transparency and salinity of the water column increased singnifically when compared with year before (dredge area and control). Moreover, dissolved oxygen did not show significant diferences between years (before and dredging years). This study indicates that the total density of fishes in the estuary increased from c. 0·30 individuals m−2 the year before dredging to c. 2·00 individuals m−2 in the year of dredging. Similarly, biomass increased from c. 3–104 g m−2 over this time period. Migration of adults of Ariidae to where the dredging was being conducted was responsible for the increments in density and biomass (Fig. 13). When the total density and biomass of dredging month (September 2001: 0·60 individuals m−2 and
© 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.12999
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M . B A R L E T TA E T A L.
70 g m−2 ) and the same period the year before (September 2000: 0·02 individuals m−2 and 1 g m−2 ) are compared with periods before dredging (June 2000: 0·01 individuals m−2 and 0·2 g m−2 ) and after dredging (March 2000: 1·00 individuals m−2 and 7 g m−2 ) year before, and before dredging (May 2000: 0·80 individuals m−2 and 18 g m−2 ) and after dredging (March 2001: 0·50 individuals m−2 and 8 g m−2 ), it is clear that differences between and within years are not caused exclusively by the dredging process. Seasonal and interannual sources of variability may also be responsible for some of these changes. Non-significant differences occurred in rainfall patterns from 2000 to 2002 in the study area. Accordingly, this series of years did not differ from the climatic average (Fig. 2). In spite of the impact caused by the action of the dredge, there was an increase in density and biomass of some Ariidae (e.g. C. spixii, G. genidens and A. luniscutis) (Fig. 13). These were present at all different times in this study (before, during and after dredging). These species use the upper and middle reaches of the estuary for reproduction, spawning and recruitment between the end of the dry season and the beginning of the rainy season (October to March) (Barletta et al., 2008). At the specific level, C. spixii remained, and G. genidens and A. luniscutis moved from the lower portion of the estuary to the area where dredging was being performed (Fig. 13 and Table IV). These species were responsible for the increase in density (sevenfold) and biomass (35-fold) in the area. This suggests that these species are attracted to the dredged area by an increase in food supply [e.g. dead prey carcasses, Fig. 1(d)] from the dredged materials disposal and by the enlargement of the neritic zone in the inner portion of the estuary. In this case, the trophic guilds were represented by almost 100% benthophagous and hyper-benthophagous fish species (Ariidae) (Fig. 13). It must be highlighted, however, that all benthic and epibenthic prey (polychaetes, shellfishes and crustaceans) and benthic and demersal fishes (Ariidae, Sciaenidae and Achiridae), were available as a dead organisms squashed or triturated by the cutter suction dredger. For that reason, all these triturated animals are carcases, and these predators are opportunistic carcass feeders or scavengers. After dredging operations, however, S. rastrifer and C. leiarchus almost disappeared from the dredged channel, and M. americanus from both habitats (dredged channel and adjacent area) (Fig. 13 and Table IV). For these six species, it is clear that the source of variation between and within years is related to the dredging process. In addition, during the dredging year, E. crossotus, C. spilopterus, C. arenaceus, S. testudineus and S. tessellatus were mainly captured in the month before the start of dredging. This suggests that the changes in fish assemblage composition between the months and within years was not caused by seasonality alone. Barletta et al. (2005) suggested that seasonal changes of the estuarine fish assemblage in the Caeté Estuary (eastern Amazon) are determined by a combination of temporal fluctuations in rainfall, reproduction and recruitment-induced abundances of marine, estuarine and freshwater species. Corrêa (2001) detected intense to moderate reproductive activity between the end of the dry season (October, November and December) and the beginning of the rainy season (January, February and March) for C. spixii, S. testudineus, S. rastrifer, Isopisthus parvipinnis, A. luniscutis and G. genidens at Guaraqueçaba Bay [Fig. 2(a)]. The greatest capture frequencies of mature specimens of these species were recorded from the end of the rainy to the end of the dry season. Adults migrate to Guaraqueçaba Bay for reproduction between the end of the dry and the beginning of the rainy season. The peak of recruitment occurs at the end of the rainy season. Thus, the large quantity of fishes in Paranaguá Estuary in March 2001
© 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.12999
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(early rainy season) and why these species decreased in March 2002, is probably due to dredging that coincides with the reproduction period (September 2001, early dry season) for many of them. All the above evidence explains the lower number of species in March 2001 at the beginning of the rainy season in the year of dredging in the main channel of the Paranaguá Estuary. At this time the number of species in the region should have been statistically similar to the same period of the previous year, but were not. According to the present study and Barletta et al. (2008), the number of species, density and biomass during dredging increased in the main channel, probably because the species that were in the adjacent area (where the dredged materials was dumped) migrated to the main channel. Only G. barbus showed a different behaviour, and apparently is not much affected by the disposal of dredge materials in the water column (Table IV). On the other hand, as a consequence of dredging activities, total fish habitat loss was observed during the harbour construction at Pecém Beach (São Gonçalo do Amarante – Ceará, north-east Brazil) where the beachrock tidal pools were covered by the dredge spoil (Freitas et al., 2009). This suggests that the dredging process impact is inversely proportional to the size and complexity of the stressed habitat or ecosystem, as proposed by Elliott & Quintino (2007). According to Kennish (1998), the increase in water turbidity caused by the action of the dredging can promote changes in the life cycles of organisms, negatively affecting the fishing activity of an estuarine region and coastal waters. Plankton, benthos and nekton species suffer tissue damage or, in cases in which there is possible chemical contamination, there is bioaccumulation and poisoning. According to Corrêa (2001), the fishery resources of Guaraqueçaba Bay [e.g. C. spixii, G. genidens, A. luniscutis, G. barbus, Harengula clupeola (Cuvier 1829), Bairdiella ronchus (Cuvier 1830), M. americanus and Cynoscion leiarchus (Cuvier 1830)] are important sources of financial and food security for the local traditional populations. For that reason it is suggested that the different ontogenetic phases of these species that use the estuary should be considered as bioindicators of heavy metals (e.g. mercury) bioavailability (Bloom & Lasorsa, 1999; Lewis et al., 2001). SUGGESTIONS FOR THE PLANNING OF DREDGING O P E R AT I O N S I N E S T U A R I N E E C O S Y S T E M S
Future dredging operations for maintenance of the shipping channel, providing access to the port facilities of the east–west axis of the Paranaguá Estuary, should be avoided during the reproductive season of most fishes (October to December) and during recruitment, which peaks at the end of the rainy season (April to June) (Corrêa, 2001). This strategy would help to conserve important fishery species which are sensitive to the impact of dredging, without totally prohibiting the operation. This would be a mitigatory strategy, but the lesser impact of planned dredging must be integrated to other conservation actions, specially if periodical dredging is required. Intervals between dredging years should be as long as possible to assure the system’s resilience. Efforts to decrease the accretion process of the estuary by controlling deforestation and encouraging better land use practices are also necessary. On the other hand, the expansion of port facilities in this area will create a larger and more frequent demand for dredging operations, which will need adequate management and law enforcement.
© 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.12999
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M . B A R L E T TA E T A L.
Hence, to promote sustainable fishery management practices, dredging in this estuary should take place during the dry season (July to September), but it is important to stress that the beginning and end of each season varies from one year to another. Thus, the above recommendation may change according to rainfall patterns of a particular year. To allow planning of dredging, it is important to closely follow the trends in rainfall for the region, in order to predict continental drainage and salinity variations within the estuary, which in turn trigger important ecological processes in relation to the fishes within the estuary. According to Barletta et al. (2005), salinity controls fish assemblages across time and space in estuaries free from direct intervention. Dredging might alter the salinity patterns and consequently fish assemblage distribution and composition as observed in this study. Seasonal rainfall patterns and other environmental variables vary greatly along the South American coast (Barletta et al., 2010). If similar measures regarding dredging or any other large anthropogenic interventions are to be implemented in other regions of South America and other countries around the tropical and sub-tropical belt, the seasonal regimes and their consequences for estuarine communities should be well documented prior to decision making. The group of sensitive species and their respective life cycles can vary from one estuary to another. For these reasons it is important to undertake similar studies and monitoring wherever there is a need for periodical dredging of shipping and access channels in estuaries. Complementary studies of dredging impacts on other groups of organisms that use the estuary as protection, feeding and reproduction areas involving keystone (Barletta et al., 2008) and flag (Guebert-Bartholo et al., 2011) species in the estuarine ecosystem and adjacent coastal areas are equally necessary. Since some of these species are viewed as important natural resources for traditional populations, assessments based on the local ecological knowledge must also be taken into consideration. Hopefully, results from this study will help managerial decisions regarding dredging necessities and estuarine conservation, at the same time providing support to local populations which depend on estuarine living resources. Moreover, it is recommended studies using multiple regression models should be conducted to highlight the biological and the environmental variables determining the fish assemblage affected by the dredging process in estuarine ecosystems as highlighted in this study. This work resulted from a cooperation between Zentrum fur Marine Tropenoekologie (ZMT), Bremen, Germany and the Centro de Estudos do Mar (CEM – UFPR), Pontal do Paraná – PR, Brazil under the Governmental Agreement on Cooperation in the Field and Scientific Research and Technological Development between Germany and Brazil. It was funded by the German Ministry for Education Science, Research and Technology (BMBF) (Project number: 03F0154A, Mangrove Management and Dynamics – MADAM) and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq N∘ . 30041900–7). The authors thank S. J. M. Blaber, M. F. Costa and two anonymous referees for the important contributions to earlier versions of this manuscript. M.B. and F.J.A.C. are CNPq fellows.
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Species
Achirus lineatus Genidens barbus Cathorops spixii Genidens genidens Aspistor luniscutis Carangidae Oligoplites saurus Selene vomer Trachinotus falcatus Clupeidae Pellona harroweri Cyneglossidae Symphurus tessellatus Dasyatidae Dasyatis guttata Engraulidae Lycengraulis grossidens Cetengraulis edentulus Ephipidae Chaetodipterus faber Paralichthydae Etropus crossotus Paralichthys brasiliensis Citharhichthys arenaceus Citharichthys spilopterus Pomadasydae Geniatremus luteus Sciaenidae Cynoscion microlepdotus Stellifer rastrifer Cynoscion leiarchus Micropogonias furnieri Menticirrhus americanus Cynoscion acoupa Isopistus parvipinis
Achiridae Ariidae
Family