Ecotoxicology and Environmental Safety 104 (2014) 373–378
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Toxicity of sediments from a mangrove forest patch in an urban area in Pernambuco (Brazil) D.D. Oliveira a,n, L.P. Souza-Santos a, H.K.P. Silva b, S.J. Macedo a a Universidade Federal de Pernambuco – UFPE, Departamento de Oceanografia, Av. Prof1 Moraes Rêgo, S/N. Cidade Universitária – Recife/PE. CEP. 50670-901, Brazil b Associação Instituto de Tecnologia de Pernambuco – ITEP/OS - Laboratório de Química de Água – LQA; Av. Prof1 Luiz Freire N1 700. Cidade Universitária – Recife/PE. CEP. 50740-540, Brazil
art ic l e i nf o
a b s t r a c t
Article history: Received 6 July 2013 Received in revised form 4 February 2014 Accepted 5 February 2014 Available online 17 April 2014
Industrial and urban residues are discharged every day to the rivers and may arrive at the mangrove forest and prejudice the quality of the environment and the organisms present there. The mangrove forest patch studied is encircled by an urban area of the city of Recife (Brazil) that has approximate 1.5 million inhabitants and is one of the most industrialized centers in Northeast Brazil. The aim of this study was to assess the quality of the sediments of this mangrove patch in terms of metal contamination and ecotoxicology. Samples of surface sediment were collected in six stations for toxicological tests and trace metal determination (Cr, Zn, Mn, Fe, Cu, Pb, Co and Ni), in July and August, 2006 (rainy season); and in January and February 2007 (dry season). Toxicity tests with solid-phase sediments were carried out with the copepod Tisbe biminiensis in order to observe lethal and sub-lethal endpoints and correlate them with chemical data. In June, there were no observed lethal effect, but two stations presented sub-lethal effects. In January, lethal effect occurred in three stations and sub-lethal in one station. The levels for Zn and Cr were at higher levels than international proposed guidelines (NOAA). There was a negative significant correlation between the copepods' fecundity, and Zn and Cr concentrations. Therefore, the studied sediments can be considered to have potential toxic to benthos due to the high content of Zn and Cr. & 2014 Elsevier Inc. All rights reserved.
Keywords: Brazil Pollution Tisbe biminiensis Sediment Trace metals
1. Introduction Mangrove sediments have the capacity to accumulate material released in coastal and marine environments due to their particular physicochemical properties (Harbinson, 1986; MacFarlane and Burchett, 2000). For this reason, high concentrations of trace metals were recorded in sediments of mangroves around the world, and often, it reflects long-term pollution caused by human activities (Perdomo et al., 1998; Harris and Santos, 2000; Tam and Wong, 2000). Contaminated sediments have been recognized as a significant environmental risk, since they usually have strong associations with high concentrations of different classes of anthropogenic pollutants. This contamination may be a source of stress for benthic communities (Zabetoglou et al., 2002). In order to measure such stress, ecotoxicological methods have been developed to
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Corresponding author. E-mail address: [email protected] (D.D. Oliveira).
http://dx.doi.org/10.1016/j.ecoenv.2014.02.004 0147-6513 & 2014 Elsevier Inc. All rights reserved.
assess the effects of polluted sediments at different levels of biological organization (Luoma and Ho, 1992). Recife is a city with an approximate 1.5 million inhabitants and it is the most industrialized center in the northeastern region of Brazil. Capibaribe and Beberibe rivers flow through this city to the Atlantic Ocean. During the years of the city's growth, large mangrove areas were suppressed and nowadays there is only one large remaining mangrove area that is called “Mangrove Park.” It is one of the largest mangroves of Brazil, situated on the city of Recife. The area is encircled by an extremely dense population. The rivers Jordão and Pina that flow into this mangrove received domestic and industrial effluents. This study evaluated the toxicity of the sediments of the aforementioned mangrove forest patch through bioassays, by using the benthic harpacticoid copepod Tisbe biminiensis and by observing lethal and sub-lethal endpoints, as well as the concentration of trace metals in sediments. Marine copepods have been widely used in ecotoxicology to test water and sediment samples (Williams, 1992; Chandler and Scott, 1991; Chandler and Green, 2001; Chandler et al., 2004). Several species of copepods are currently being used in sediment bioassays around the world:
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Tigriopus japonicus, Tigriopus brevicornis, Tigriopus fulvus (Seo et al., 2006; Kwok et al., 2008; Todaro et al., 2001), Amphiascus tenuiremis (Kovatch et al., 1999; Hagopian-Schlekat et al., 2001; Bejarano et al., 2005, 2006), Tisbe holothuriae (ISO 14669, 1999; Miliou et al., 2000; Pounds et al. 2002; Thomas et al., 2007), Tisbe battagliai (Miliou et al., 2000; Taylor et al., 2007), Microarthridion littorale (Kovatch et al., 1999), Nitocra spinipes, Nitocra sp. (Bengtsson, 1978; Lotufo and Abessa, 2002), Schizopera knabeni (Lotufo, 1997), Attheyella crassa (Turesson et al., 2007), and Robertsonia propinqua (Hack et al., 2008; Stringer et al., 2012). The genus Tisbe has been demonstrated to be appropriate for environmental risk assessment since it has a wide geographic distribution and a short life cycle (approximately 12 days to nauplii stage to adult), plus, animals in all stages of development can be cultivated at any time of the year (Williams, 1992; Williams and Jones, 1994; Kusk and Wollenberger, 2007; Araújo-Castro et al., 2009). Tisbe biminiensis is a native species that has been cultivated in the laboratory for years (Pinto et al., 2001) and it has been tested as a toxicity model for sediment samples (AraújoCastro et al., 2009).
2.2. Ecotoxicological bioassay The bioassays were performed after the sampling and followed the method described by Araújo-Castro et al. (2009), modified from Lotufo and Abessa (2002). The sieved sediment (fine fraction) was distributed in three sub-samples that consisted of approximately 2 g of sediment, which was sufficient to form a 0.5 cm layer in each test recipient (glass recipient with 4.5 cm diameter and 6 cm high with a plastic cap and 40-mL capacity). Each recipient received 20 mL of a diatom suspension of Thalassiosira fluviatilis or Chaetoceros gracilis at 0.2 μg Chl-a mL 1 and was incubated at 25 1C under 12-h light/dark photoperiod. Three sub-replicates were created for each of the three sediment samples collected from each sampling site, totaling nine sub-replicates per sampling site. The control consisted of five sub-replicates samples of sediment sampled in Maracaípe mangrove considered to be having no significant pollution (Araújo-Castro et al., 2009). After 24 h of sedimentation, 10 ovigerous females of 12 days old were placed in each test recipient. The experiment lasted seven days, with the addition of 1 mL of concentrated diatom every other day. Dissolved oxygen concentration (D.O.), pH and salinity were determined at the beginning and end of the experiment with an oximeter, a pH meter and a refractometer, respectively. At the end of the bioassay, the entire content of each test recipient was stained with Rose Bengal and fixed with formaldehyde (4 percent) for subsequent counts and determination of the lethal parameter (non-stained adult females were considered dead) and sub-lethal parameter of fecundity, which is the sum of nauplii and copepodites produced during the bioassay.
2.3. Metals analyses 2. Material and methods 2.1. Collecting site The study area is a mangrove forest patch of 225.82 ha wide, encircled by an urban area of Recife, capital of Pernambuco State in Northeast Brazil. This area is bathed by Jordão and Pina rivers and also receives the affluents of Capibaribe river, Jaboatão, Jiquiá and Setúbal Channels (Fig. 1). Surface sediment samples were collected for metal analyses and toxicological tests in June and August 2006 (representing the rainy season) and January and February 2007 (representing the dry season) in six stations. These stations were georeferenciated by a GPS Garmin model Etrex Summit and defined according to geomorphology. Two of them were located on the Jordão river estuary (E and F), three stations on the Pina river (B, C and D) and one was in the point of confluence of both systems (A) (Fig. 1). The superficial sediments were collected to 10 cm depth on the low-tide exposed banks of the river with a stainless steel spatula. The samples were composed of type, as the grain size of these sediments showed a 67 percent silt/ clay and 33 percent fine sand. They were stored in decontaminated plastic containers inside refrigerated boxes until arrival at the laboratory where they were sieved through 64 mm and maintained at 4 1C until bioassays. For the toxicity tests, three sediment samples (replicates) in each station were collected. For metal analysis, only one sample per station was taken.
The extractions of metals (Cr, Ni, Cu, Pb, Zn, Mn, Co, Cd and Fe) from sediment samples were made from drying, 64 mm sieving and a digestion in a microwave (DGT 100 Plus Cost) for 10 min with Nitric Acid (HNO3), Perchloric Acid (HClO4) and Hydrofluoric Acid (HF) adapted (USEPA, 2001). The metals determinations were made using an Inductively Coupled Plasma–Optic Emission Spectrometer (ICP–OES, SPECTRO) (USEPA, 2001). To validate the method we used the standard certificate of Communitary Bureau of Reference (CBR # 625 labeled CRM 277 – Estuarine Sediment). All reagents used were of high analytical grade; working solutions were prepared with corresponding pattern of SPECSOL. The detectation limits were o10 μg g 1 to Cr and Mn and o20 μg g 1 to Fe and Zn. The sediment used to determine the natural levels or background of metals was collected near Navy radio area (081050 58.40 0 Se, 341530 35.010 0 W) in November 2006. This area was chosen because no contamination was observed in the sediment in preliminary studies. One of the Sediment Quality Guidelines (SQG) used to evaluate the biological effects of trace metals in sediments was set by NOAA (1999), and it has two limits: TEL (Threshold Effect Level), the level below which no adverse effect to the biological community was usually observed; and PEL (Probable Effect Level), the level above which adverse effects were likely to be detected. Another criterion was established by Long et al. (1995), whom after conducting field studies with marine and estuarine sediments determined two limits to assess the quality of sediments: the ERL (Effect Range – Low), is threshold concentration below which the
Fig. 1. Map for localization of the mangrove patch and sediment sampling sites.
D.D. Oliveira et al. / Ecotoxicology and Environmental Safety 104 (2014) 373–378 sediments are rarely toxic; and the ERM (Effect Range – Medium), which indicates that the sediments are possibly toxic.
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The fecundity in July 2006 had significant differences in relation to control (ANOVA F¼7.79, p ¼0.0008); the Tukey test indicated lower fecundity in stations E and F. In January 2007, there were also significant differences in relation to control (ANOVA F¼ 8.240, p ¼0.0001), with lower fecundity in station F (Fig. 3). The toxicity observed in the study sites was lethal in January 2007 for A, B and F and sublethal in July 2007 for E and F and in January only to F. The C and D stations showed only the uncontaminated sediment.
2.4. Data processing The data was analyzed with ANOVA to test differences of toxicological endpoints in the sediments at different sampling points and control. Data were tested for normality (Komogorov–Smirnov test) and variance homogeneity (Barlett test). The Kruskal–Wallis non-parametric test was used when the data were not normal or variance was not homogeneous. The subsequent Tukey test was performed to compare pairwise means. The metal contents in the sediments were correlated with ecotoxicological endpoints after normalization to control results using the Pearson correlation analyses. The 95 percent significance level was adopted for all tests.
3.3. Correlation analyses results 3. Results
When metal concentrations in the sediments were correlated with the toxicological data only two significant correlations were found: a negative correlation between Zn and fecundity and a negative correlation between Cr and fecundity (Table 2).
3.1. Trace metals in sediments Only Zn, Mn, Cr and Fe were presented at detectable levels, Ni (o 20 μg g 1), Cu (o20 μg g 1), Co (o 20 μg g 1), Cd (o20 μg g 1) and Pb ( o250 μg g 1) were below the detection limit of the analytical method used. The mean values of detectable trace metal concentrations were compared to the mean background concentrations and to sediment quality guidelines proposed by NOAA (1999) and Long et al. (1995) (Table 1). From July to August 2006, all stations were above guidelines for Zn and Cr and above background for Mn and Fe. From January to February 2007, all stations presented values of Zn above guidelines, and for Cr only station D was below the safety concentration. For Mn and Fe, all stations had higher concentrations than the local background.
4. Discussion According to the data obtained from the surface sediments of Mangrove Park were considered toxic, since we observed lethal and sublethal responses in campaigns. The sediment toxicity may be associated with levels of Zn and Cr present in the sediment, as seen in the correlation analysis. Lewis et al. (2011) reviewed the metal contamination on mangrove areas from the 22 metals reported; the most frequent were Cu, Pb, and Zn. The following ranges were found in μg g 1 dry weight: 0.61-125 (Cr), 0.01-845 (Cu), 1.2-3253 (Mn), 0.3-102 (Ni), 0.08-1950 (Pb), and 0.3-2372 (Zn). The values found in the present study were inside those ranges and varied from the highest to the lowest concentrations as Fe4Zn 4Mn 4Cr. The comparison of our results of Zn with those reported for other protected or urban mangroves showed values relatively similar (Table 3). De Vos and Tarvainen (2006) reported that anthropogenic sources of zinc resulted in levels above preindustrial concentrations in air, soil and water mainly from industrial activities such as mining coal, waste combustion, and
3.2. Ecotoxicological bioassay results The mortality in July 2006 was not significantly different among stations (ANOVA, F¼2.04, p ¼0.077); this ranged from 26 percent to 38 percent. However, in January 2007, there was a significant difference in relation to control (ANOVA, F¼2.649, p ¼0.026); this ranged from 0 percent to 38 percent. In stations A, B and F the mortality values were significantly higher than that in the control station (Fig. 2).
Table 1 Mean values of trace metals in the sediments at Mangrove Park compared with background and guidelines of NOAA (1999) and Long et al. (1995). Mean value (μg g 1dry weight) A
NOAA
Long et al., 1995
B
C
D
E
F
Background
TEL
PEL
ERL
ERM
July/2006 Zn 2427 92 Mn 3387 118 Cr 917 31 Fe 111,990 7 16,508
335 719 193 710 88 72 112,100 736,938
2777 69 220 7 19 867 9 33,0507 1563
– – – –
– – – –
– – – –
41 160 25 5120
124 – 52.3 –
1604 – 271 –
81 – 150 –
370 – 410 –
August/2006 Zn 3397 39 Mn 204 7 66 Cr 93.5 7 2 Fe 47,4407 39,036
365 730 197 785 92 73 48,140 71994
1577 93 1937 6 707 21 30,7607 4722
294 7 22 1937 8 827 5 29,820 7 2630
531 791 1857 16 88 78 33,680 7 892
5707 55 220 7 19 877 2 35,260 72352
41 160 25 5120
124 – 52.3 –
1604 – 271 –
81 – 150 –
370 – 410 –
January/2007 Zn 205 7 14 Mn 1947 30 Cr 807 7 Fe 29,1207 8433
200 713 138 760 77 75 30,440 72479
1337 80 1337 23 527 13 22,230 7 6438
202 7 59 182 723 257 24 24,7607 10,212
322 737 2047 10 78 73 30,0107 1747
366 7 18 194 730 73 710 28,540 7 2105
41 160 25 5120
124 – 52.3 –
1604 – 271 –
81 – 150 –
370 – 410 –
February/2007 Zn 2217 11 Mn 1927 3 Cr 737 4 Fe 31,3107 1825
219 74 201 718 71 73 33,38071334
2707 17 1727 7 747 11 33,3607 866
847 68 3387 90 257 0.5 12,920 7 6872
3597 21 179 725 687 4 31,4907 845
409 7 34 159 721 73 70.4 30,5707 3415
41 160 25 5120
124 – 52.3 –
1604 – 271 –
81 – 150 –
370 – 410 –
Values that exceeded international guidelines are in boldface.
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Fig. 2. Mean 7 standard deviation of the mortality of female Tisbe biminiensis after 7 days of bioassay in July 2006 and January 2007. The letter corresponds to significant differences found by the Tukey test.
Fig. 3. Mean fecundity (Naupliiþ copepodites) of Tisbe biminiensis after 7 days. The letters correspond to significant differences found by the Tukey test and E and F in July 2006 and F in January 2007.
steel processing. A major use of Zn is as an anti-corrosion coating. It is also used as a constituent of brass, as a white pigment (ZnO) in paint and rubber products, and in the manufacture of dry batteries. Chromium concentrations tend to be higher in urban mangroves than in protected ones (Table 3). Still, values reported in the relatively clean urban waterways for fish area in Pichavaram (India) (Ramanathan et al., 1999) showed concentrations above those found in the present study. Chromium is a major component of steel alloys (10–26 percent) and it is used for coating steel as chrome plating. Chromates and dichromates, containing Cr6 þ , are sometimes released in industrial effluents, especially from leather tanning and electroplating operations (De Vos and Tarvainen, 2006). The 21 sediment samples analyzed for Zn were higher than the low suggested guideline, ERL, with half of the values of E and F stations exceeding ERM and PEL. Regarding Cr, only three values were lower than the low suggested guideline, TEL, and were present at stations C and D. ERM or PEL at no time was overcome by Cr. These results indicate that deleterious biological effects would be expected on the basis of these two metals. In accordance with that, toxic lethal or sub-lethal was detected in four of the six seasons. In the same way, the results
Table 2 Results of Pearson correlation analyses between metal data and normalized toxicological endpoints of T. biminiensis in the sediments at Mangrove Park. Endpoints Metal
Mortality
Zn Mn Cr Fe
r ¼ 0.22 r ¼0.006 r ¼ 0.067 r ¼0.18
Fecundity p ¼0.05 p ¼0.98 p ¼0.84 p ¼0.58
r ¼ 0.79 r ¼0.41 r ¼ 0.66 r ¼ 0.19
p ¼ 0.0022n p ¼ 0.19 p ¼ 0.02n p ¼ 0.56
of correlation analysis indicated significant inverse relationships between both metals (Zn, and Cr) and fecundity of T. biminiensis, reinforcing the deleterious effect of both metals in the studied environment. Stations C and D had no lethal or sub-lethal effects upon the tested organisms and had as well the lowest concentrations of trace metals. These stations are located in an area where the influence of industrial and domestic effluents is lower than that in Stations A, B, E, and F. Stations E and F had always sub-lethal effects and high concentrations of zinc, exceeding ERM and PEL in
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Table 3 Comparison of concentrations of metals in mangrove sediments (μg g 1 dry weight). Elements Location
Zn
Cr
Comments
Kumarakam mangrove (India) Mai Po (Hong Kong) Sungei Buloh (Singapore) Pichavaram (India) Cienaga Grande (Colombia) Moreton Bay (Australia) Punta Mala Bay (Panama) Izmit Bay (Turkey) Guanabara Bay (Brazil) Suape Port (Brazil) Mangrove Park (Brazil)
112–466 277–321 51 50–130 91 23–56 105 500–1190 483 27–69 84–409
– – 17 89–186 13 – 23 58–116 42 17–36 25–93
Relatively clean Protected area Protected nature reserve Relatively clean urban waterways for fish Highway construction forestry, urban area Agriculture, aquaculture and national parks Urban area, agriculture Urban area Urban area, industries Industrial and harbor area Urban area
July and in January. Chromium was also between TEL and PEL in these stations located near Jordão river, which receives large volumes of domestic sewage discharges and urban runoff. If we used only the concentration of the metals Zn and Cr on sediment compared Guidelines (NOAA) (Long et al., 1995), all stations studied would be toxic. However, ecotoxicological results differs from that, as stations C and D did not present toxicity. Zinc is a micronutrient which is considered to be essential for animals, plants and humans (WHO, 1996); however, when it is present in concentrations higher than those considered to be optimum, it can be toxic. High levels of zinc may, for instance, affect the formation of the exoskeleton of young crustaceans, which compromises their development (Hagopian-Schlekat et al., 2001). Chromium causes adverse effects on health for more than 180 years. High concentrations of Cr in water and soil have hazardous effects on fish and invertebrates (Eisler, 1986; Lushchak et al., 2009). Sastry and Sunita (1983), exposing the fish Channa punctatus to chromium for 60–120 days observed changes in enzymatic activity in the kidney, brain, liver, gill, intestine and muscle. Wu et al. (2012) studied the exposure of nematodes for 10 days to chromium observing that lethality, mobility and metabolism of organisms were chronically altered. The present results indicated that the benthos community may present deleterious effects in this mangrove area probably due to Zn and Cr contamination.
5. Conclusion The superficial sediments of the “Mangrove Park”, in the middle of the urban area of Recife, which were tested for their ecotoxicological potential, can be characterized as toxic in four out of the six studied stations, as both fecundity and survival of copepod female Tisbe biminiensis were affected. These results most probably reflect the high values found for Zn and Cr. The levels of these metals were higher than proposed international guidelines, something that indicates probable deleterious biological effects. The collection station that showed the best results was station C; this located in a more secluded area of the park and was not influenced by human action due to more restricted access. Unlike stations E and F located in the Jordan river that receive sewage, due to lack of sanitation and garbage on site. Items such as sofas, televisions, computers, beds were viewed during the collection period. Therefore, it is important that more comprehensive studies be carried out in the area for better characterization of possible sources and origins of the elements covered by the study and by other elements, which were not addressed yet.
Badarudeen et al., 1996 Ong Che, 1999 Cuong et al., 2005 Ramanathan et al., 1999 Perdomo et al., 1998 Preda and Cox, 2002 Defew et al., 2005 Pekey et al., 2004 Kehring et al., 2003 Marques et al., 2011 Present study
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Toxicity of sediments from a mangrove forest patch in an urban area in Pernambuco (Brazil) D.D. Oliveira a,n, L.P. Souza-Santos a, H.K.P. Silva b, S.J. Macedo a a Universidade Federal de Pernambuco – UFPE, Departamento de Oceanografia, Av. Prof1 Moraes Rêgo, S/N. Cidade Universitária – Recife/PE. CEP. 50670-901, Brazil b Associação Instituto de Tecnologia de Pernambuco – ITEP/OS - Laboratório de Química de Água – LQA; Av. Prof1 Luiz Freire N1 700. Cidade Universitária – Recife/PE. CEP. 50740-540, Brazil
art ic l e i nf o
a b s t r a c t
Article history: Received 6 July 2013 Received in revised form 4 February 2014 Accepted 5 February 2014 Available online 17 April 2014
Industrial and urban residues are discharged every day to the rivers and may arrive at the mangrove forest and prejudice the quality of the environment and the organisms present there. The mangrove forest patch studied is encircled by an urban area of the city of Recife (Brazil) that has approximate 1.5 million inhabitants and is one of the most industrialized centers in Northeast Brazil. The aim of this study was to assess the quality of the sediments of this mangrove patch in terms of metal contamination and ecotoxicology. Samples of surface sediment were collected in six stations for toxicological tests and trace metal determination (Cr, Zn, Mn, Fe, Cu, Pb, Co and Ni), in July and August, 2006 (rainy season); and in January and February 2007 (dry season). Toxicity tests with solid-phase sediments were carried out with the copepod Tisbe biminiensis in order to observe lethal and sub-lethal endpoints and correlate them with chemical data. In June, there were no observed lethal effect, but two stations presented sub-lethal effects. In January, lethal effect occurred in three stations and sub-lethal in one station. The levels for Zn and Cr were at higher levels than international proposed guidelines (NOAA). There was a negative significant correlation between the copepods' fecundity, and Zn and Cr concentrations. Therefore, the studied sediments can be considered to have potential toxic to benthos due to the high content of Zn and Cr. & 2014 Elsevier Inc. All rights reserved.
Keywords: Brazil Pollution Tisbe biminiensis Sediment Trace metals
1. Introduction Mangrove sediments have the capacity to accumulate material released in coastal and marine environments due to their particular physicochemical properties (Harbinson, 1986; MacFarlane and Burchett, 2000). For this reason, high concentrations of trace metals were recorded in sediments of mangroves around the world, and often, it reflects long-term pollution caused by human activities (Perdomo et al., 1998; Harris and Santos, 2000; Tam and Wong, 2000). Contaminated sediments have been recognized as a significant environmental risk, since they usually have strong associations with high concentrations of different classes of anthropogenic pollutants. This contamination may be a source of stress for benthic communities (Zabetoglou et al., 2002). In order to measure such stress, ecotoxicological methods have been developed to
n
Corresponding author. E-mail address: [email protected] (D.D. Oliveira).
http://dx.doi.org/10.1016/j.ecoenv.2014.02.004 0147-6513 & 2014 Elsevier Inc. All rights reserved.
assess the effects of polluted sediments at different levels of biological organization (Luoma and Ho, 1992). Recife is a city with an approximate 1.5 million inhabitants and it is the most industrialized center in the northeastern region of Brazil. Capibaribe and Beberibe rivers flow through this city to the Atlantic Ocean. During the years of the city's growth, large mangrove areas were suppressed and nowadays there is only one large remaining mangrove area that is called “Mangrove Park.” It is one of the largest mangroves of Brazil, situated on the city of Recife. The area is encircled by an extremely dense population. The rivers Jordão and Pina that flow into this mangrove received domestic and industrial effluents. This study evaluated the toxicity of the sediments of the aforementioned mangrove forest patch through bioassays, by using the benthic harpacticoid copepod Tisbe biminiensis and by observing lethal and sub-lethal endpoints, as well as the concentration of trace metals in sediments. Marine copepods have been widely used in ecotoxicology to test water and sediment samples (Williams, 1992; Chandler and Scott, 1991; Chandler and Green, 2001; Chandler et al., 2004). Several species of copepods are currently being used in sediment bioassays around the world:
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Tigriopus japonicus, Tigriopus brevicornis, Tigriopus fulvus (Seo et al., 2006; Kwok et al., 2008; Todaro et al., 2001), Amphiascus tenuiremis (Kovatch et al., 1999; Hagopian-Schlekat et al., 2001; Bejarano et al., 2005, 2006), Tisbe holothuriae (ISO 14669, 1999; Miliou et al., 2000; Pounds et al. 2002; Thomas et al., 2007), Tisbe battagliai (Miliou et al., 2000; Taylor et al., 2007), Microarthridion littorale (Kovatch et al., 1999), Nitocra spinipes, Nitocra sp. (Bengtsson, 1978; Lotufo and Abessa, 2002), Schizopera knabeni (Lotufo, 1997), Attheyella crassa (Turesson et al., 2007), and Robertsonia propinqua (Hack et al., 2008; Stringer et al., 2012). The genus Tisbe has been demonstrated to be appropriate for environmental risk assessment since it has a wide geographic distribution and a short life cycle (approximately 12 days to nauplii stage to adult), plus, animals in all stages of development can be cultivated at any time of the year (Williams, 1992; Williams and Jones, 1994; Kusk and Wollenberger, 2007; Araújo-Castro et al., 2009). Tisbe biminiensis is a native species that has been cultivated in the laboratory for years (Pinto et al., 2001) and it has been tested as a toxicity model for sediment samples (AraújoCastro et al., 2009).
2.2. Ecotoxicological bioassay The bioassays were performed after the sampling and followed the method described by Araújo-Castro et al. (2009), modified from Lotufo and Abessa (2002). The sieved sediment (fine fraction) was distributed in three sub-samples that consisted of approximately 2 g of sediment, which was sufficient to form a 0.5 cm layer in each test recipient (glass recipient with 4.5 cm diameter and 6 cm high with a plastic cap and 40-mL capacity). Each recipient received 20 mL of a diatom suspension of Thalassiosira fluviatilis or Chaetoceros gracilis at 0.2 μg Chl-a mL 1 and was incubated at 25 1C under 12-h light/dark photoperiod. Three sub-replicates were created for each of the three sediment samples collected from each sampling site, totaling nine sub-replicates per sampling site. The control consisted of five sub-replicates samples of sediment sampled in Maracaípe mangrove considered to be having no significant pollution (Araújo-Castro et al., 2009). After 24 h of sedimentation, 10 ovigerous females of 12 days old were placed in each test recipient. The experiment lasted seven days, with the addition of 1 mL of concentrated diatom every other day. Dissolved oxygen concentration (D.O.), pH and salinity were determined at the beginning and end of the experiment with an oximeter, a pH meter and a refractometer, respectively. At the end of the bioassay, the entire content of each test recipient was stained with Rose Bengal and fixed with formaldehyde (4 percent) for subsequent counts and determination of the lethal parameter (non-stained adult females were considered dead) and sub-lethal parameter of fecundity, which is the sum of nauplii and copepodites produced during the bioassay.
2.3. Metals analyses 2. Material and methods 2.1. Collecting site The study area is a mangrove forest patch of 225.82 ha wide, encircled by an urban area of Recife, capital of Pernambuco State in Northeast Brazil. This area is bathed by Jordão and Pina rivers and also receives the affluents of Capibaribe river, Jaboatão, Jiquiá and Setúbal Channels (Fig. 1). Surface sediment samples were collected for metal analyses and toxicological tests in June and August 2006 (representing the rainy season) and January and February 2007 (representing the dry season) in six stations. These stations were georeferenciated by a GPS Garmin model Etrex Summit and defined according to geomorphology. Two of them were located on the Jordão river estuary (E and F), three stations on the Pina river (B, C and D) and one was in the point of confluence of both systems (A) (Fig. 1). The superficial sediments were collected to 10 cm depth on the low-tide exposed banks of the river with a stainless steel spatula. The samples were composed of type, as the grain size of these sediments showed a 67 percent silt/ clay and 33 percent fine sand. They were stored in decontaminated plastic containers inside refrigerated boxes until arrival at the laboratory where they were sieved through 64 mm and maintained at 4 1C until bioassays. For the toxicity tests, three sediment samples (replicates) in each station were collected. For metal analysis, only one sample per station was taken.
The extractions of metals (Cr, Ni, Cu, Pb, Zn, Mn, Co, Cd and Fe) from sediment samples were made from drying, 64 mm sieving and a digestion in a microwave (DGT 100 Plus Cost) for 10 min with Nitric Acid (HNO3), Perchloric Acid (HClO4) and Hydrofluoric Acid (HF) adapted (USEPA, 2001). The metals determinations were made using an Inductively Coupled Plasma–Optic Emission Spectrometer (ICP–OES, SPECTRO) (USEPA, 2001). To validate the method we used the standard certificate of Communitary Bureau of Reference (CBR # 625 labeled CRM 277 – Estuarine Sediment). All reagents used were of high analytical grade; working solutions were prepared with corresponding pattern of SPECSOL. The detectation limits were o10 μg g 1 to Cr and Mn and o20 μg g 1 to Fe and Zn. The sediment used to determine the natural levels or background of metals was collected near Navy radio area (081050 58.40 0 Se, 341530 35.010 0 W) in November 2006. This area was chosen because no contamination was observed in the sediment in preliminary studies. One of the Sediment Quality Guidelines (SQG) used to evaluate the biological effects of trace metals in sediments was set by NOAA (1999), and it has two limits: TEL (Threshold Effect Level), the level below which no adverse effect to the biological community was usually observed; and PEL (Probable Effect Level), the level above which adverse effects were likely to be detected. Another criterion was established by Long et al. (1995), whom after conducting field studies with marine and estuarine sediments determined two limits to assess the quality of sediments: the ERL (Effect Range – Low), is threshold concentration below which the
Fig. 1. Map for localization of the mangrove patch and sediment sampling sites.
D.D. Oliveira et al. / Ecotoxicology and Environmental Safety 104 (2014) 373–378 sediments are rarely toxic; and the ERM (Effect Range – Medium), which indicates that the sediments are possibly toxic.
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The fecundity in July 2006 had significant differences in relation to control (ANOVA F¼7.79, p ¼0.0008); the Tukey test indicated lower fecundity in stations E and F. In January 2007, there were also significant differences in relation to control (ANOVA F¼ 8.240, p ¼0.0001), with lower fecundity in station F (Fig. 3). The toxicity observed in the study sites was lethal in January 2007 for A, B and F and sublethal in July 2007 for E and F and in January only to F. The C and D stations showed only the uncontaminated sediment.
2.4. Data processing The data was analyzed with ANOVA to test differences of toxicological endpoints in the sediments at different sampling points and control. Data were tested for normality (Komogorov–Smirnov test) and variance homogeneity (Barlett test). The Kruskal–Wallis non-parametric test was used when the data were not normal or variance was not homogeneous. The subsequent Tukey test was performed to compare pairwise means. The metal contents in the sediments were correlated with ecotoxicological endpoints after normalization to control results using the Pearson correlation analyses. The 95 percent significance level was adopted for all tests.
3.3. Correlation analyses results 3. Results
When metal concentrations in the sediments were correlated with the toxicological data only two significant correlations were found: a negative correlation between Zn and fecundity and a negative correlation between Cr and fecundity (Table 2).
3.1. Trace metals in sediments Only Zn, Mn, Cr and Fe were presented at detectable levels, Ni (o 20 μg g 1), Cu (o20 μg g 1), Co (o 20 μg g 1), Cd (o20 μg g 1) and Pb ( o250 μg g 1) were below the detection limit of the analytical method used. The mean values of detectable trace metal concentrations were compared to the mean background concentrations and to sediment quality guidelines proposed by NOAA (1999) and Long et al. (1995) (Table 1). From July to August 2006, all stations were above guidelines for Zn and Cr and above background for Mn and Fe. From January to February 2007, all stations presented values of Zn above guidelines, and for Cr only station D was below the safety concentration. For Mn and Fe, all stations had higher concentrations than the local background.
4. Discussion According to the data obtained from the surface sediments of Mangrove Park were considered toxic, since we observed lethal and sublethal responses in campaigns. The sediment toxicity may be associated with levels of Zn and Cr present in the sediment, as seen in the correlation analysis. Lewis et al. (2011) reviewed the metal contamination on mangrove areas from the 22 metals reported; the most frequent were Cu, Pb, and Zn. The following ranges were found in μg g 1 dry weight: 0.61-125 (Cr), 0.01-845 (Cu), 1.2-3253 (Mn), 0.3-102 (Ni), 0.08-1950 (Pb), and 0.3-2372 (Zn). The values found in the present study were inside those ranges and varied from the highest to the lowest concentrations as Fe4Zn 4Mn 4Cr. The comparison of our results of Zn with those reported for other protected or urban mangroves showed values relatively similar (Table 3). De Vos and Tarvainen (2006) reported that anthropogenic sources of zinc resulted in levels above preindustrial concentrations in air, soil and water mainly from industrial activities such as mining coal, waste combustion, and
3.2. Ecotoxicological bioassay results The mortality in July 2006 was not significantly different among stations (ANOVA, F¼2.04, p ¼0.077); this ranged from 26 percent to 38 percent. However, in January 2007, there was a significant difference in relation to control (ANOVA, F¼2.649, p ¼0.026); this ranged from 0 percent to 38 percent. In stations A, B and F the mortality values were significantly higher than that in the control station (Fig. 2).
Table 1 Mean values of trace metals in the sediments at Mangrove Park compared with background and guidelines of NOAA (1999) and Long et al. (1995). Mean value (μg g 1dry weight) A
NOAA
Long et al., 1995
B
C
D
E
F
Background
TEL
PEL
ERL
ERM
July/2006 Zn 2427 92 Mn 3387 118 Cr 917 31 Fe 111,990 7 16,508
335 719 193 710 88 72 112,100 736,938
2777 69 220 7 19 867 9 33,0507 1563
– – – –
– – – –
– – – –
41 160 25 5120
124 – 52.3 –
1604 – 271 –
81 – 150 –
370 – 410 –
August/2006 Zn 3397 39 Mn 204 7 66 Cr 93.5 7 2 Fe 47,4407 39,036
365 730 197 785 92 73 48,140 71994
1577 93 1937 6 707 21 30,7607 4722
294 7 22 1937 8 827 5 29,820 7 2630
531 791 1857 16 88 78 33,680 7 892
5707 55 220 7 19 877 2 35,260 72352
41 160 25 5120
124 – 52.3 –
1604 – 271 –
81 – 150 –
370 – 410 –
January/2007 Zn 205 7 14 Mn 1947 30 Cr 807 7 Fe 29,1207 8433
200 713 138 760 77 75 30,440 72479
1337 80 1337 23 527 13 22,230 7 6438
202 7 59 182 723 257 24 24,7607 10,212
322 737 2047 10 78 73 30,0107 1747
366 7 18 194 730 73 710 28,540 7 2105
41 160 25 5120
124 – 52.3 –
1604 – 271 –
81 – 150 –
370 – 410 –
February/2007 Zn 2217 11 Mn 1927 3 Cr 737 4 Fe 31,3107 1825
219 74 201 718 71 73 33,38071334
2707 17 1727 7 747 11 33,3607 866
847 68 3387 90 257 0.5 12,920 7 6872
3597 21 179 725 687 4 31,4907 845
409 7 34 159 721 73 70.4 30,5707 3415
41 160 25 5120
124 – 52.3 –
1604 – 271 –
81 – 150 –
370 – 410 –
Values that exceeded international guidelines are in boldface.
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Fig. 2. Mean 7 standard deviation of the mortality of female Tisbe biminiensis after 7 days of bioassay in July 2006 and January 2007. The letter corresponds to significant differences found by the Tukey test.
Fig. 3. Mean fecundity (Naupliiþ copepodites) of Tisbe biminiensis after 7 days. The letters correspond to significant differences found by the Tukey test and E and F in July 2006 and F in January 2007.
steel processing. A major use of Zn is as an anti-corrosion coating. It is also used as a constituent of brass, as a white pigment (ZnO) in paint and rubber products, and in the manufacture of dry batteries. Chromium concentrations tend to be higher in urban mangroves than in protected ones (Table 3). Still, values reported in the relatively clean urban waterways for fish area in Pichavaram (India) (Ramanathan et al., 1999) showed concentrations above those found in the present study. Chromium is a major component of steel alloys (10–26 percent) and it is used for coating steel as chrome plating. Chromates and dichromates, containing Cr6 þ , are sometimes released in industrial effluents, especially from leather tanning and electroplating operations (De Vos and Tarvainen, 2006). The 21 sediment samples analyzed for Zn were higher than the low suggested guideline, ERL, with half of the values of E and F stations exceeding ERM and PEL. Regarding Cr, only three values were lower than the low suggested guideline, TEL, and were present at stations C and D. ERM or PEL at no time was overcome by Cr. These results indicate that deleterious biological effects would be expected on the basis of these two metals. In accordance with that, toxic lethal or sub-lethal was detected in four of the six seasons. In the same way, the results
Table 2 Results of Pearson correlation analyses between metal data and normalized toxicological endpoints of T. biminiensis in the sediments at Mangrove Park. Endpoints Metal
Mortality
Zn Mn Cr Fe
r ¼ 0.22 r ¼0.006 r ¼ 0.067 r ¼0.18
Fecundity p ¼0.05 p ¼0.98 p ¼0.84 p ¼0.58
r ¼ 0.79 r ¼0.41 r ¼ 0.66 r ¼ 0.19
p ¼ 0.0022n p ¼ 0.19 p ¼ 0.02n p ¼ 0.56
of correlation analysis indicated significant inverse relationships between both metals (Zn, and Cr) and fecundity of T. biminiensis, reinforcing the deleterious effect of both metals in the studied environment. Stations C and D had no lethal or sub-lethal effects upon the tested organisms and had as well the lowest concentrations of trace metals. These stations are located in an area where the influence of industrial and domestic effluents is lower than that in Stations A, B, E, and F. Stations E and F had always sub-lethal effects and high concentrations of zinc, exceeding ERM and PEL in
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Table 3 Comparison of concentrations of metals in mangrove sediments (μg g 1 dry weight). Elements Location
Zn
Cr
Comments
Kumarakam mangrove (India) Mai Po (Hong Kong) Sungei Buloh (Singapore) Pichavaram (India) Cienaga Grande (Colombia) Moreton Bay (Australia) Punta Mala Bay (Panama) Izmit Bay (Turkey) Guanabara Bay (Brazil) Suape Port (Brazil) Mangrove Park (Brazil)
112–466 277–321 51 50–130 91 23–56 105 500–1190 483 27–69 84–409
– – 17 89–186 13 – 23 58–116 42 17–36 25–93
Relatively clean Protected area Protected nature reserve Relatively clean urban waterways for fish Highway construction forestry, urban area Agriculture, aquaculture and national parks Urban area, agriculture Urban area Urban area, industries Industrial and harbor area Urban area
July and in January. Chromium was also between TEL and PEL in these stations located near Jordão river, which receives large volumes of domestic sewage discharges and urban runoff. If we used only the concentration of the metals Zn and Cr on sediment compared Guidelines (NOAA) (Long et al., 1995), all stations studied would be toxic. However, ecotoxicological results differs from that, as stations C and D did not present toxicity. Zinc is a micronutrient which is considered to be essential for animals, plants and humans (WHO, 1996); however, when it is present in concentrations higher than those considered to be optimum, it can be toxic. High levels of zinc may, for instance, affect the formation of the exoskeleton of young crustaceans, which compromises their development (Hagopian-Schlekat et al., 2001). Chromium causes adverse effects on health for more than 180 years. High concentrations of Cr in water and soil have hazardous effects on fish and invertebrates (Eisler, 1986; Lushchak et al., 2009). Sastry and Sunita (1983), exposing the fish Channa punctatus to chromium for 60–120 days observed changes in enzymatic activity in the kidney, brain, liver, gill, intestine and muscle. Wu et al. (2012) studied the exposure of nematodes for 10 days to chromium observing that lethality, mobility and metabolism of organisms were chronically altered. The present results indicated that the benthos community may present deleterious effects in this mangrove area probably due to Zn and Cr contamination.
5. Conclusion The superficial sediments of the “Mangrove Park”, in the middle of the urban area of Recife, which were tested for their ecotoxicological potential, can be characterized as toxic in four out of the six studied stations, as both fecundity and survival of copepod female Tisbe biminiensis were affected. These results most probably reflect the high values found for Zn and Cr. The levels of these metals were higher than proposed international guidelines, something that indicates probable deleterious biological effects. The collection station that showed the best results was station C; this located in a more secluded area of the park and was not influenced by human action due to more restricted access. Unlike stations E and F located in the Jordan river that receive sewage, due to lack of sanitation and garbage on site. Items such as sofas, televisions, computers, beds were viewed during the collection period. Therefore, it is important that more comprehensive studies be carried out in the area for better characterization of possible sources and origins of the elements covered by the study and by other elements, which were not addressed yet.
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