Bull Environ Contam Toxicol (2014) 92:274–278 DOI 10.1007/s00128-014-1208-7
Differences in Methylmercury and Inorganic Mercury Biomagnification in a Tropical Marine Food Web Te´rcia G. Seixas • Isabel Moreira • Salvatore Siciliano Olaf Malm • Helena A. Kehrig
•
Received: 3 April 2013 / Accepted: 16 January 2014 / Published online: 23 January 2014 Ó Springer Science+Business Media New York 2014
Abstract Methylmercury (MeHg), inorganic mercury (Hginorg) and their biomagnification factors (BMF) were evaluated along a non-degraded Brazilian bay food web. Highly significant differences (p \ 0.0001) were found between MeHg and Hginorg concentrations among all organisms (microplankton, shrimp, fish and dolphin). MeHg increased with increasing trophic position while Hginorg did not present the same pattern. BMF values for MeHg were higher than 1 for all trophic interactions from source to consumer, indicating that MeHg was transferred more efficiently and biomagnified over the entire web. Only one BMF exceeding one was observed for Hginorg (27) between microplankton and their consumer, planktivorous fish. BMF values for Hginorg were significantly different than those found for MeHg (20) at the base of the food web.
T. G. Seixas (&) I. Moreira Dep. de Quı´mica, Pontifı´cia Universidade Cato´lica do Rio de Janeiro, 22453-900 Rio de Janeiro, Brazil e-mail: [email protected] S. Siciliano Dep. de Endemias, Escola Nacional de Sau´de Pu´blica/Fiocruz, 21041-210 Rio de Janeiro, Brazil O. Malm H. A. Kehrig Lab. de Radioiso´topos Eduardo Penna Franca, IBCCFUniversidade Federal do Rio de Janeiro, Rio de Janeiro, RJ 21949-900, Brazil H. A. Kehrig Lab. de Cieˆncias Ambientais, Universidade Estadual do Norte Fluminense, Campos dos Goytacazes, RJ 28013-602, Brazil
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Keywords Trophic transfer Tropical ecosystem Marine biota South Atlantic Ocean Oligotrophic ecosystem
Mercury in its more toxic organic form, methylmercury (MeHg), biotransfers along marine food webs (Kehrig et al. 2011), from base to higher trophic levels via both benthic and pelagic pathways (Chen et al. 2009). Primary producers (microplankton) can represent an important exposure route for mercury (Watras et al. 1998) to primary consumers, such as zooplankton and planktivorous fish (Okay et al. 2000). Biomagnification is the increase in mercury concentrations between two subsequent trophic levels, that is, between the prey and the consumer (Barwick and Maher 2003). According to Watras et al. (1998) this process results from trophic transport when consumers absorb contaminants from carbon sources (food) and then respire carbon at a rate faster than they depurate the contaminant. Since mercury has the ability to undergo biomagnification along food webs, environmental exposure, particularly for higher trophic level consumers, including humans, can be significant (Agusa et al. 2007). Furthermore, its organic form can affect productivity, reproduction and survival of coastal and marine organisms, and can be hazardous to human and wildlife health (WHO 1990). For these reasons, this metal has been recognized as a serious pollutant of aquatic ecosystems. There are several globally documented cases regarding the biomagnification of total mercury in freshwater and marine ecosystems. However, a limited number of studies are available for comparison across marine systems in coastal regions of the south-eastern Atlantic Ocean (Corbisier et al. 2006; Pereira et al. 2010; Kehrig et al. 2011,
Bull Environ Contam Toxicol (2014) 92:274–278
2013; Bisi et al. 2012; Di Beneditto et al. 2012). No previous studies are available regarding methylmercury and inorganic mercury biomagnification at Ilha Grande Bay (Fig. 1). Thus, the present study makes an initial contribution to this task by presenting methylmercury (MeHg) and inorganic mercury (Hginorg) concentrations in one size class of plankton, microplankton (C25 lm), and in muscle tissues of pinkspot shrimp (Farfantepenaeus brasiliensis), four fish species with different feeding habits (Mugil liza, Citharichthys spilopterus, Micropogonias furnieri and Trichiurus lepturus), and a coastal dolphin (Sotalia guianensis) from Ilha Grande Bay. The aims were to compare the possible differences in MeHg and Hginorg biomagnification among the trophic positions, as well as along the marine food web from the base level (planktonic comunity) to its top level, represented by the predator S. guianensis. In addition, the calculation of biomagnification factors (BMF) was conducted in the more conventional way to compare MeHg and Hginorg concentrations in consumer to those in source (prey) along the coastal food web.
Materials and Methods Ilha Grande Bay (3,100 Km2; 23°S 44°W) located in the southern coast of the Rio de Janeiro State, Brazil is considered a biodiversity hotspot and includes a high number of protected areas (Creed et al. 2007). Despite the presence of some potential pollution sources, this bay can be considered a non-contaminated area, since low levels of metals such as Ni, Cu, Cr, Mn, Zn and Hg have been found in
Fig. 1 Area where marine organisms were collected for MeHg and Hginorg analysis in the Rio de Janeiro coast, South-eastern Brazil
275
sediments (Lacerda et al. 1981; Cardoso et al. 2001) and fish (Kehrig et al. 1998) in the last decades. Planktonic organisms were collected at three sampling stations on May 2011 by horizontal hauls at the water surface, using planktonic conical nets of 25 lm mesh size (microplankton). The plankton samples were stored in precleaned Teflon bottles, separated per site and identified. At the laboratory these samples were freeze-dried and stored in hermetic vessels until chemical analysis. Pinkspot shrimp and fish were collected with the help of local fishermen between 2009 and 2011 at Ilha Grande Bay from the same area as the planktonic organisms (Fig. 1). After sampling, biological characteristics of the specimens were obtained, and sub-samples of dorso-lateral muscle were removed, except for F. brasiliensis (shrimp), that had all muscle tissue removed. Marine group, scientific name, number of sampling locations or individuals (N), common name, feeding habit and the range of organism length of all species are presented in Table 1. Sotalia guianensis (dolphin) found dead and stranded along the shores of the bay were collected by Dr. Salvatore Siciliano (ENSP/Fiocruz). All samples were freeze-dried and sheltered from light until analysis. After the lyophilization procedure the muscle samples lost around 75 % of their water content. For the total mercury (Hg) analyses, dried samples (0.05 g) were digested in a sulphuric-nitric acid mixture. Hg was determined by CV-AAS, using NaBH4 as a reducing agent. A detailed description of the method used is given elsewhere (Kehrig et al. 2008). The MeHg analysis in the samples was conducted by digesting samples with an alcoholic potassium hydroxide solution followed by dithizone–toluene extraction. MeHg dithizonate was identified and quantified in the toluene layer by GC-ECD. A detailed description of the method used is given elsewhere (Kehrig et al. 2008). The values corresponding to the concentrations of inorganic mercury (Hginorg) were calculated as the difference between the values found for Hg and MeHg concentrations. The limits of detection were 0.007 and 0.004 lg g-1 for Hg and MeHg, respectively. Quality control was performed by a strict blank control, the analysis of replicates and certified reference materials. Accuracy was assessed through the analysis of certified material DORM-2 (Hg: 4.64 ± 0.26 lg g-1) from the National Research Council-Canada and IAEA 350 (MeHg: 3.65 ± 0.35 lg g-1) from the International Atomic Energy Agency. Average recovery values were always C90 % of the certified values. Reproducibility was evaluated using the coefficient of variation of the replicates, which was always less than 10 %. Statistical analyses were performed using STATISTICAÒ 7.0 for Windows (StatSoft, Inc., 1984–2004, USA). Data was tested for normal distribution (Shapiro–Wilk’s
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Bull Environ Contam Toxicol (2014) 92:274–278
Table 1 Marine group, scientific name, number of sampling locations or individuals (N), common name, feeding habit, the range of organism length and methylmercury (MeHg) and inorganic mercury (Hginorg) mean concentrations (on a dry weight basis) of all species Species
Group
Pooled species
Microplankton
F. brasiliensis
Crustacean
N 6 90
Common name
Feeding habit
Length (lm or cm)
Phytoplankton
Primary producer
C25 lm
Pinkspot shrimp
Omnivorous
(7.0–20.0)
[MeHg] (lg kg-1)
[Hginorg] (lg kg-1)
1.75 ± 0.23
1.17 ± 0.16
73.19 ± 28.75
8.08 ± 6.41 31.88 ± 17.08
M. liza
Fish
30
Lebranche mullet
Planktivorous
(29.0–50.0)
35.09 ± 19.66
C. spilopterus
Fish
16
Bay whiff
Benthic-feeder
(9.0–17.0)
127.25 ± 70.42
3.21 ± 2.81
M. furnieri
Fish
40
Whitemouth croaker
Benthic-feeder
(26.0–46.0)
271.56 ± 100.45
2.82 ± 1.60
T. lepturus
Fish
21
S. guianensis
Cetacean
6
Atlantic cutlassfish
Carnivorous
(75.0–130.0)
349.91 ± 94.22
8.82 ± 5.35
Guiana dolphin
Carnivorous
(133.0–191.0)
1,812.21 ± 806.54
4.57 ± 3.09
test) and non-parametric tests were then applied. The analysis of variance was conducted by the Kruskal–Wallis test. ANOVA was followed by a post hoc test (Mann– Whitney U test) in order to define significant differences in MeHg and Hginorg concentrations among the trophic levels, as well as along the marine food web. A p value of less than 0.05 was chosen to indicate statistical significance.
Results and Discussion Methylmercury (MeHg) and inorganic mercury (Hginorg) concentrations (on a dry weight basis) in the sampled microplankton, shrimp, fish and dolphin are summarized in Table 1. The Kruskal–Wallis ANOVA test demonstrated the presence of highly significant differences (p \ 0.0001) between the MeHg and Hginorg concentrations among the studied coastal biota, from microplankton, omnivorous shrimp (pinkspot shrimp – F. brasiliensis), planktivorous fish (M. liza), carnivorous fish (C. spilopterus, M. furnieri and T. lepturus) to the top predator of the food web, S. guianensis. MeHg concentrations increased successively with increasing trophic position (Table 1), from microplankton, shrimp, planktivorous fish, carnivorous fish to the toppredator, corresponding to a transfer between trophic positions from the lower trophic position to the top level. However, Hginorg concentrations displayed a trend of not increasing with the increase in trophic position (Table 1), indicating that MeHg was indeed the biomagnified Hg species. Food web biomagnification is defined as the increase in chemical concentration (MeHg and Hginorg) with increasing trophic position of organisms in a food web (Lavoie et al. 2010). This is calculated for simple consumer-source interactions (Riget et al. 2007) as a ratio of a chemical concentration between the consumer and source. The values along the studied coastal food web are presented in Fig. 2.
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The muscle tissue of the top-predator (S. guianensis) presented the highest MeHg concentration, followed by T. lepturus, M. furnieri, C. spilopterus and M. liza, which correspond to dolphin preferential food items (Bisi et al. 2012). MeHg concentrations in S. guianensis muscle were 5, 7, 14 and 51 times higher than those found in the same tissue of T. lepturus, M. furnieri, C. spilopterus and M. liza, respectively (Fig. 2). On the other hand, T. lepturus that feed mainly on pelagic and demersal prey species and have cannibalistic feeding behavior (Bittar and Di Beneditto 2009) presented muscular MeHg concentrations higher than their prey, M. furnieri, C. spilopterus and M. liza (about 1, 3 and 10 times higher, respectively). MeHg concentrations in M. furnieri and C. spilopterus muscle tissue were approximately 4 and 2 times the amount found in their preferred prey, F. brasiliensis (Vazzoler 1975; Vasconcelos-Filho et al. 2007). M. liza, that feeds mainly on sediment organic detritus and filamentous algae (microplankton) (Blaber 1997), presented muscular MeHg concentrations about 20 times higher than its preferred diet, microplankton. Our data clearly show that MeHg increased with increasing trophic position at Ilha Grande Bay, since MeHg biomagnified from source to top-predator dolphin in all trophic interactions (eight interactions) (Fig. 2). This finding is consistent with earlier observations on the biota of two different areas in the Rio de Janeiro coast (Kehrig et al. 2010, 2013), Gulf of Maine (Chen et al. 2009), North Sea and Scheldt Estuary (Baeyens et al. 2003) and Papua New Guinea (Bowles et al. 2001). Regarding inorganic mercury (Hginorg), almost all of the links of the Ilha Grande Bay food web presented a biomagnification factor (BMF) \ 1, since prey (sources) presented higher Hginorg concentrations than their consumers (Fig. 2). Only one BMF for Hginorg [ 1 was observed, between planktivorous fish M. liza and their source, microplankton (Fig. 2). Mercury (MeHg and Hginorg) enters the food chain via phytoplankton (microplankton) and is bioaccumulated by the other links in the web, via trophic transfer (Kehrig et al. 2011; Costa et al. 2012).
Bull Environ Contam Toxicol (2014) 92:274–278
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Fig. 2 Biomagnification factor (BMF) of methylmercury and inorganic mercury through a coastal food web. Numbers in the circle are BMF
It is noteworthy that, according to Fig. 2, more Hginorg was available at the base of the web than MeHg, since the BMF for Hginorg (27) was higher and significantly different (Mann–Whitney U test; p \ 0.0001) than that found for MeHg (20) in this food web. However, the BMF values for MeHg in the subsequent links of the web were higher than those found for Hginorg, indicating that methylmercury was more efficiently transferred over the entire web, from source to top-predator dolphin. These observations suggest that MeHg biomagnification processes are occurring along the Ilha Grande Bay aquatic food web. The BMF values for MeHg and Hginorg in this study between the consumer, M. liza, and their diet, microplankton (20 and 27, respectively) were higher than those found (4.7 and 1.5, respectively) in a previous study (Kehrig et al. 2010) with the same fish species and microplankton from an impacted coastal area in Rio de Janeiro State, Guanabara Bay. This suggests that Hginorg and MeHg are more available for the biota at Ilha Grande Bay, an oligotrophic ecosystem, when compared to Guanabara Bay, an eutrophic ecosystem. According to Seixas et al. (2013), the bioproduction at Guanabara Bay is greater than at Ilha Grande Bay. Guanabara Bay presents higher biomass in it ecosystem than that found in the Ilha Grande Bay ecosystem, which may subsequently dilute mercury and reduce its availability to the biota; i.e., influencing Hginorg and MeHg availability throughout the food web. Consequently, more MeHg is available in the Ilha Grande Bay environment. Acknowledgments The authors would like to thank the financial support of the Fundac¸a˜o de Amparo a` Pesquisa do Estado do Rio de
Janeiro (FAPERJ Proc 101976/2009), Coordenac¸a˜o de Aperfeic¸oamento de Pessoal de Nı´vel Superior (CAPES) and Conselho Nacional de Desenvolvimento Cientı´fico e Tecnolo´gico (CNPq).
References Agusa T, Kunito T, Sudaryanto A, Monirith I, Kan-Atireklap S, Iwata H, Ismais A, Sanguansin J, Muchtar M, Tana TS, Tanabe S (2007) Exposure assessment for trace elements from consumption of marine fish in Southeast Asia. Environ Pollut 145:766–777 Baeyens W, Leermakers M, Papina T, Saprykin A, Brion N, Noyen J, De Gieter M, Elskens M, Goeyens L (2003) Bioconcentration and biomagnification of mercury and methylmercury in North Sea and Scheldt Estuary fish. Arch Environ Contam Toxicol 45:498–508 Barwick M, Maher W (2003) Biotransference and biomagnification of selenium, copper, cadmium, zinc, arsenic and lead in a temperate seagrass ecosystem from lake Macquarie Estuary, NSW, Australia. Mar Environ Res 56:471–502 Bisi TL, Lepoint G, Azevedo AF, Dorneles PR, Flach L, Das K, Malm O, Lailson-Brito J (2012) Trophic relationships and mercury biomagnification in Brazilian tropical coastal food webs. Ecol Indic 18:291–302 Bittar VT, Di Beneditto APM (2009) Diet and potential feeding overlap between Trichiurus lepturus (Osteichthyes, Perciformes) and Pontoporia blainvillei (Mammalia, Cetacea) in northern Rio de Janeiro, Brazil. Zoologia 26:374–378 Blaber SJM (1997) Fish and fisheries in tropical estuaries. Fish and Fisheries Series v. 22, Chapman Hall, London Bowles KC, Apte SC, Maher WA, Kawei M, Smith S (2001) Bioaccumulation and biomagnifications of mercury in Lake Murray, Papua New Guinea. Can J Fish Aquat Sci 58:888–897 Cardoso AGA, Boaventura GR, Silva Filho EV, Broad J (2001) Metal distribution in sediments from the Ribeira Bay, Rio de JaneiroBrazil. J Braz Chem Soc 6(12):767–774 Chen CY, Dionne M, Mayes BM, Ward DM, Sturup S, Jackson BP (2009) Mercury bioavailability and bioaccumulation in estuarine
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278 food webs in the Gulf of Maine. Environ Sci Technol 43:1804–1810 Corbisier TN, Soares LSH, Petti MAV, Muto EY, Silva MHC, McClelland J, Valiela I (2006) Use of isotopic signatures to assess the food web in a tropical shallow marine ecosystem of Southeastern Brazil. Aquat Ecol 40:381–390 Costa MF, Landing WM, Kehrig HA, Barletta M, Holmes CD, Barrocas PRG, Evers DC, Buck DG, Vasconcellos AC, Hacon SS, Moreira JC, Malm O (2012) Mercury in tropical and subtropical coastal environments. Environ Res 119:88–100 Creed JC, Oliveira AES, Pires DO, Figueiredo MAO, Ferreira CEL, Ventura CRR, Brasil ACS, Young PS, Absala˜o RS, Paiva PC, Castro CB, Serejo CS (2007) RAP Ilha Grande—um levantamento da biodiversidade: histo´rico e conhecimento da biota. In: Creed JC, Pires DO, Figueiredo MAO (eds) Biodiversidade Marinha da Baı´a da Ilha Grande. MMA/SBF, Brası´lia Di Beneditto APM, Bittar VT, Camargo PB, Rezende CE, Kehrig HA (2012) Mercury and nitrogen isotope in a marine species from a tropical coastal food web. Arch Environ Toxicol 62:264–271 Kehrig HA, Malm O, Moreira I (1998) Mercury in a widely consumed fish Micropogonias furnieri (Demarest, 1823) from four main Brazilian estuaries. Sci Total Environ 213:263–271 Kehrig HA, Seixas TG, Palermo EA, Di Beneditto APM, Souza CMM, Malm O (2008) Different species of mercury in the livers of tropical dolphins. Anal Lett 41:1691–1699 Kehrig HA, Seixas TG, Baeˆta AP, Malm O, Moreira I (2010) Inorganic and methylmercury: do they transfer along a tropical coastal food web? Mar Pollut Bull 60:2350–2356 Kehrig HA, Seixas TG, Palermo EA, Baeˆta AP, Malm O, Moreira I (2011) Bioconcentration and biomagnification of methylmercury in Guanabara Bay, Rio de Janeiro. Quim Nova 34:377–384 Kehrig HA, Seixas TG, Malm O, Di Beneditto APM, Rezende CE (2013) Mercury and selenium biomagnification in a Brazilian coastal food web using nitrogen stable isotope analysis: a case study in an area under the influence of the Paraiba do Sul River plume. Mar Pollut Bull 75:283–290
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Bull Environ Contam Toxicol (2014) 92:274–278 Lacerda LD, Pfeiffer WC, Fiszman M (1981) Nı´veis naturais de metais pesados em sedimentos marinhos da Baı´a da Ribeira, Angra dos Reis. Cienc Cult 34(7):921–924 Lavoie RA, Hebert CE, Rail J-F, Braune BM, Yumvihoze E, Hill LG, Lean DRS (2010) Trophic structure and mercury distribution in a Gulf of St. Lawrence (Canada) food web using stable isotope analysis. Sci Total Environ 408:5529–5539 Okay OS, Donkin P, Peters LD, Livingstone DR (2000) The role of algae (Isoochrysis galbana) enrichment on the bioaccumulation of benzo[a]pyrene and its effects on the blue mussel Mytilus edulis. Environ Pollut 110:103–113 Pereira AA, van Hattum B, de Boer J, van Bodegom PM, Rezende CE, Salomons W (2010) Trace elements and carbono and nitrogen stable isotopes in organisms from tropical coastal lagoon. Arch Environ Contam Toxicol 5:464–477 Riget F, Moller P, Dietz R, Nielsen TG, Asmund G, Strand J, Larsen MM, Hobson KA (2007) Transfer of mercury in the marine food web of West Greenland. J Environ Monit 9:877–883 Seixas TG, Moreira I, Malm O, Kehrig HA (2013) Ecological and biological determinants of methylmercury accumulation in tropical coastal fish. Environ Sci Pollut Res 20:1142–1150 Vasconcelos-Filho AL, Neumann-Leita˜o S, Ramos-Porto M, Almeida ZS (2007) Biologia alimentar de Citharichthys spilopterus (Paralichthyidae) em um estua´rio tropical, Pernambuco, Brasil. Rev Bras Enga Pesca 2(2):6–12 Vazzoler G (1975) Distribuic¸a˜o da fauna de peixes demersais e ecologia dos sciaenidae da plataforma continental Brasileira, entre as latitudes 29°210 S (Toˆrres) e 33°410 S (Chuı´). Bol Inst Oceanogr 24:85–169 Watras CJ, Back RC, Halvorsen S, Hudson RJM, Morrison KA, Wente SP (1998) Bioaccumulation of mercury in pelagic freshwater food webs. Sci Total Environ 219:183–208 WHO (1990) Methylmercury. Environ Health Criteria No 101. World Health Organisation, Geneva
Differences in Methylmercury and Inorganic Mercury Biomagnification in a Tropical Marine Food Web Te´rcia G. Seixas • Isabel Moreira • Salvatore Siciliano Olaf Malm • Helena A. Kehrig
•
Received: 3 April 2013 / Accepted: 16 January 2014 / Published online: 23 January 2014 Ó Springer Science+Business Media New York 2014
Abstract Methylmercury (MeHg), inorganic mercury (Hginorg) and their biomagnification factors (BMF) were evaluated along a non-degraded Brazilian bay food web. Highly significant differences (p \ 0.0001) were found between MeHg and Hginorg concentrations among all organisms (microplankton, shrimp, fish and dolphin). MeHg increased with increasing trophic position while Hginorg did not present the same pattern. BMF values for MeHg were higher than 1 for all trophic interactions from source to consumer, indicating that MeHg was transferred more efficiently and biomagnified over the entire web. Only one BMF exceeding one was observed for Hginorg (27) between microplankton and their consumer, planktivorous fish. BMF values for Hginorg were significantly different than those found for MeHg (20) at the base of the food web.
T. G. Seixas (&) I. Moreira Dep. de Quı´mica, Pontifı´cia Universidade Cato´lica do Rio de Janeiro, 22453-900 Rio de Janeiro, Brazil e-mail: [email protected] S. Siciliano Dep. de Endemias, Escola Nacional de Sau´de Pu´blica/Fiocruz, 21041-210 Rio de Janeiro, Brazil O. Malm H. A. Kehrig Lab. de Radioiso´topos Eduardo Penna Franca, IBCCFUniversidade Federal do Rio de Janeiro, Rio de Janeiro, RJ 21949-900, Brazil H. A. Kehrig Lab. de Cieˆncias Ambientais, Universidade Estadual do Norte Fluminense, Campos dos Goytacazes, RJ 28013-602, Brazil
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Keywords Trophic transfer Tropical ecosystem Marine biota South Atlantic Ocean Oligotrophic ecosystem
Mercury in its more toxic organic form, methylmercury (MeHg), biotransfers along marine food webs (Kehrig et al. 2011), from base to higher trophic levels via both benthic and pelagic pathways (Chen et al. 2009). Primary producers (microplankton) can represent an important exposure route for mercury (Watras et al. 1998) to primary consumers, such as zooplankton and planktivorous fish (Okay et al. 2000). Biomagnification is the increase in mercury concentrations between two subsequent trophic levels, that is, between the prey and the consumer (Barwick and Maher 2003). According to Watras et al. (1998) this process results from trophic transport when consumers absorb contaminants from carbon sources (food) and then respire carbon at a rate faster than they depurate the contaminant. Since mercury has the ability to undergo biomagnification along food webs, environmental exposure, particularly for higher trophic level consumers, including humans, can be significant (Agusa et al. 2007). Furthermore, its organic form can affect productivity, reproduction and survival of coastal and marine organisms, and can be hazardous to human and wildlife health (WHO 1990). For these reasons, this metal has been recognized as a serious pollutant of aquatic ecosystems. There are several globally documented cases regarding the biomagnification of total mercury in freshwater and marine ecosystems. However, a limited number of studies are available for comparison across marine systems in coastal regions of the south-eastern Atlantic Ocean (Corbisier et al. 2006; Pereira et al. 2010; Kehrig et al. 2011,
Bull Environ Contam Toxicol (2014) 92:274–278
2013; Bisi et al. 2012; Di Beneditto et al. 2012). No previous studies are available regarding methylmercury and inorganic mercury biomagnification at Ilha Grande Bay (Fig. 1). Thus, the present study makes an initial contribution to this task by presenting methylmercury (MeHg) and inorganic mercury (Hginorg) concentrations in one size class of plankton, microplankton (C25 lm), and in muscle tissues of pinkspot shrimp (Farfantepenaeus brasiliensis), four fish species with different feeding habits (Mugil liza, Citharichthys spilopterus, Micropogonias furnieri and Trichiurus lepturus), and a coastal dolphin (Sotalia guianensis) from Ilha Grande Bay. The aims were to compare the possible differences in MeHg and Hginorg biomagnification among the trophic positions, as well as along the marine food web from the base level (planktonic comunity) to its top level, represented by the predator S. guianensis. In addition, the calculation of biomagnification factors (BMF) was conducted in the more conventional way to compare MeHg and Hginorg concentrations in consumer to those in source (prey) along the coastal food web.
Materials and Methods Ilha Grande Bay (3,100 Km2; 23°S 44°W) located in the southern coast of the Rio de Janeiro State, Brazil is considered a biodiversity hotspot and includes a high number of protected areas (Creed et al. 2007). Despite the presence of some potential pollution sources, this bay can be considered a non-contaminated area, since low levels of metals such as Ni, Cu, Cr, Mn, Zn and Hg have been found in
Fig. 1 Area where marine organisms were collected for MeHg and Hginorg analysis in the Rio de Janeiro coast, South-eastern Brazil
275
sediments (Lacerda et al. 1981; Cardoso et al. 2001) and fish (Kehrig et al. 1998) in the last decades. Planktonic organisms were collected at three sampling stations on May 2011 by horizontal hauls at the water surface, using planktonic conical nets of 25 lm mesh size (microplankton). The plankton samples were stored in precleaned Teflon bottles, separated per site and identified. At the laboratory these samples were freeze-dried and stored in hermetic vessels until chemical analysis. Pinkspot shrimp and fish were collected with the help of local fishermen between 2009 and 2011 at Ilha Grande Bay from the same area as the planktonic organisms (Fig. 1). After sampling, biological characteristics of the specimens were obtained, and sub-samples of dorso-lateral muscle were removed, except for F. brasiliensis (shrimp), that had all muscle tissue removed. Marine group, scientific name, number of sampling locations or individuals (N), common name, feeding habit and the range of organism length of all species are presented in Table 1. Sotalia guianensis (dolphin) found dead and stranded along the shores of the bay were collected by Dr. Salvatore Siciliano (ENSP/Fiocruz). All samples were freeze-dried and sheltered from light until analysis. After the lyophilization procedure the muscle samples lost around 75 % of their water content. For the total mercury (Hg) analyses, dried samples (0.05 g) were digested in a sulphuric-nitric acid mixture. Hg was determined by CV-AAS, using NaBH4 as a reducing agent. A detailed description of the method used is given elsewhere (Kehrig et al. 2008). The MeHg analysis in the samples was conducted by digesting samples with an alcoholic potassium hydroxide solution followed by dithizone–toluene extraction. MeHg dithizonate was identified and quantified in the toluene layer by GC-ECD. A detailed description of the method used is given elsewhere (Kehrig et al. 2008). The values corresponding to the concentrations of inorganic mercury (Hginorg) were calculated as the difference between the values found for Hg and MeHg concentrations. The limits of detection were 0.007 and 0.004 lg g-1 for Hg and MeHg, respectively. Quality control was performed by a strict blank control, the analysis of replicates and certified reference materials. Accuracy was assessed through the analysis of certified material DORM-2 (Hg: 4.64 ± 0.26 lg g-1) from the National Research Council-Canada and IAEA 350 (MeHg: 3.65 ± 0.35 lg g-1) from the International Atomic Energy Agency. Average recovery values were always C90 % of the certified values. Reproducibility was evaluated using the coefficient of variation of the replicates, which was always less than 10 %. Statistical analyses were performed using STATISTICAÒ 7.0 for Windows (StatSoft, Inc., 1984–2004, USA). Data was tested for normal distribution (Shapiro–Wilk’s
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Table 1 Marine group, scientific name, number of sampling locations or individuals (N), common name, feeding habit, the range of organism length and methylmercury (MeHg) and inorganic mercury (Hginorg) mean concentrations (on a dry weight basis) of all species Species
Group
Pooled species
Microplankton
F. brasiliensis
Crustacean
N 6 90
Common name
Feeding habit
Length (lm or cm)
Phytoplankton
Primary producer
C25 lm
Pinkspot shrimp
Omnivorous
(7.0–20.0)
[MeHg] (lg kg-1)
[Hginorg] (lg kg-1)
1.75 ± 0.23
1.17 ± 0.16
73.19 ± 28.75
8.08 ± 6.41 31.88 ± 17.08
M. liza
Fish
30
Lebranche mullet
Planktivorous
(29.0–50.0)
35.09 ± 19.66
C. spilopterus
Fish
16
Bay whiff
Benthic-feeder
(9.0–17.0)
127.25 ± 70.42
3.21 ± 2.81
M. furnieri
Fish
40
Whitemouth croaker
Benthic-feeder
(26.0–46.0)
271.56 ± 100.45
2.82 ± 1.60
T. lepturus
Fish
21
S. guianensis
Cetacean
6
Atlantic cutlassfish
Carnivorous
(75.0–130.0)
349.91 ± 94.22
8.82 ± 5.35
Guiana dolphin
Carnivorous
(133.0–191.0)
1,812.21 ± 806.54
4.57 ± 3.09
test) and non-parametric tests were then applied. The analysis of variance was conducted by the Kruskal–Wallis test. ANOVA was followed by a post hoc test (Mann– Whitney U test) in order to define significant differences in MeHg and Hginorg concentrations among the trophic levels, as well as along the marine food web. A p value of less than 0.05 was chosen to indicate statistical significance.
Results and Discussion Methylmercury (MeHg) and inorganic mercury (Hginorg) concentrations (on a dry weight basis) in the sampled microplankton, shrimp, fish and dolphin are summarized in Table 1. The Kruskal–Wallis ANOVA test demonstrated the presence of highly significant differences (p \ 0.0001) between the MeHg and Hginorg concentrations among the studied coastal biota, from microplankton, omnivorous shrimp (pinkspot shrimp – F. brasiliensis), planktivorous fish (M. liza), carnivorous fish (C. spilopterus, M. furnieri and T. lepturus) to the top predator of the food web, S. guianensis. MeHg concentrations increased successively with increasing trophic position (Table 1), from microplankton, shrimp, planktivorous fish, carnivorous fish to the toppredator, corresponding to a transfer between trophic positions from the lower trophic position to the top level. However, Hginorg concentrations displayed a trend of not increasing with the increase in trophic position (Table 1), indicating that MeHg was indeed the biomagnified Hg species. Food web biomagnification is defined as the increase in chemical concentration (MeHg and Hginorg) with increasing trophic position of organisms in a food web (Lavoie et al. 2010). This is calculated for simple consumer-source interactions (Riget et al. 2007) as a ratio of a chemical concentration between the consumer and source. The values along the studied coastal food web are presented in Fig. 2.
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The muscle tissue of the top-predator (S. guianensis) presented the highest MeHg concentration, followed by T. lepturus, M. furnieri, C. spilopterus and M. liza, which correspond to dolphin preferential food items (Bisi et al. 2012). MeHg concentrations in S. guianensis muscle were 5, 7, 14 and 51 times higher than those found in the same tissue of T. lepturus, M. furnieri, C. spilopterus and M. liza, respectively (Fig. 2). On the other hand, T. lepturus that feed mainly on pelagic and demersal prey species and have cannibalistic feeding behavior (Bittar and Di Beneditto 2009) presented muscular MeHg concentrations higher than their prey, M. furnieri, C. spilopterus and M. liza (about 1, 3 and 10 times higher, respectively). MeHg concentrations in M. furnieri and C. spilopterus muscle tissue were approximately 4 and 2 times the amount found in their preferred prey, F. brasiliensis (Vazzoler 1975; Vasconcelos-Filho et al. 2007). M. liza, that feeds mainly on sediment organic detritus and filamentous algae (microplankton) (Blaber 1997), presented muscular MeHg concentrations about 20 times higher than its preferred diet, microplankton. Our data clearly show that MeHg increased with increasing trophic position at Ilha Grande Bay, since MeHg biomagnified from source to top-predator dolphin in all trophic interactions (eight interactions) (Fig. 2). This finding is consistent with earlier observations on the biota of two different areas in the Rio de Janeiro coast (Kehrig et al. 2010, 2013), Gulf of Maine (Chen et al. 2009), North Sea and Scheldt Estuary (Baeyens et al. 2003) and Papua New Guinea (Bowles et al. 2001). Regarding inorganic mercury (Hginorg), almost all of the links of the Ilha Grande Bay food web presented a biomagnification factor (BMF) \ 1, since prey (sources) presented higher Hginorg concentrations than their consumers (Fig. 2). Only one BMF for Hginorg [ 1 was observed, between planktivorous fish M. liza and their source, microplankton (Fig. 2). Mercury (MeHg and Hginorg) enters the food chain via phytoplankton (microplankton) and is bioaccumulated by the other links in the web, via trophic transfer (Kehrig et al. 2011; Costa et al. 2012).
Bull Environ Contam Toxicol (2014) 92:274–278
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Fig. 2 Biomagnification factor (BMF) of methylmercury and inorganic mercury through a coastal food web. Numbers in the circle are BMF
It is noteworthy that, according to Fig. 2, more Hginorg was available at the base of the web than MeHg, since the BMF for Hginorg (27) was higher and significantly different (Mann–Whitney U test; p \ 0.0001) than that found for MeHg (20) in this food web. However, the BMF values for MeHg in the subsequent links of the web were higher than those found for Hginorg, indicating that methylmercury was more efficiently transferred over the entire web, from source to top-predator dolphin. These observations suggest that MeHg biomagnification processes are occurring along the Ilha Grande Bay aquatic food web. The BMF values for MeHg and Hginorg in this study between the consumer, M. liza, and their diet, microplankton (20 and 27, respectively) were higher than those found (4.7 and 1.5, respectively) in a previous study (Kehrig et al. 2010) with the same fish species and microplankton from an impacted coastal area in Rio de Janeiro State, Guanabara Bay. This suggests that Hginorg and MeHg are more available for the biota at Ilha Grande Bay, an oligotrophic ecosystem, when compared to Guanabara Bay, an eutrophic ecosystem. According to Seixas et al. (2013), the bioproduction at Guanabara Bay is greater than at Ilha Grande Bay. Guanabara Bay presents higher biomass in it ecosystem than that found in the Ilha Grande Bay ecosystem, which may subsequently dilute mercury and reduce its availability to the biota; i.e., influencing Hginorg and MeHg availability throughout the food web. Consequently, more MeHg is available in the Ilha Grande Bay environment. Acknowledgments The authors would like to thank the financial support of the Fundac¸a˜o de Amparo a` Pesquisa do Estado do Rio de
Janeiro (FAPERJ Proc 101976/2009), Coordenac¸a˜o de Aperfeic¸oamento de Pessoal de Nı´vel Superior (CAPES) and Conselho Nacional de Desenvolvimento Cientı´fico e Tecnolo´gico (CNPq).
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