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Tracing Waterbird Exposure to Total Mercury and Selenium: A Case Study at the Solar Saltworks of Thyna (Sfax, Tunisia) Francisco Ramírez,*,† Aida Abdennadher,‡ Carola Sanpera,† Lluís Jover,§ Keith A. Hobson,|| and Leonard I. Wassenaar|| †
Dept. de Biologia Animal, Universitat de Barcelona, Avda. Diagonal 645, Barcelona 08028, Spain Laboratory of Aquatic Resources & Ecosystems (UR03AGRO1), National Agronomic Institute of Tunisia, 43, Avenue Charles Nicolle 1082, Tunis, Tunisia § Dept. de Salut Publica, Universitat de Barcelona, Casanova 143, Barcelona 08036, Spain Environment Canada, 11 Innovation Boulevard, Saskatoon, Saskatchewan S7N 3H5, Canada
)
‡
bS Supporting Information ABSTRACT: Saltworks have emerged as important alternative/complementary feeding habitats for avifauna. However, the consequences of such habitat shifts in terms of changes in exposure to contaminants are poorly understood. We evaluated the exposure of the waterbird community breeding at the saltworks of Thyna (Tunisia) to total Hg (THg) and Se according to their differential use of saltworks dietary resources, as revealed by δ13C and δ15N values in their eggs (included species [n] -sorted according to increasing reliance on saltworks resources: Yellow-legged Gull Larus michahellis [12], Common Tern Sterna hirundo [12], Slender-billed Gull Larus genei [15], Little Egret Egretta garzetta [20], and Pied Avocet Recurvirostra avosetta [22]). Concentrations of THg and Se were under the threshold points for deleterious effects. Egg THg concentrations significantly decreased as the dietary contribution of saltworks resources increased (mean: 3.23, 1.66, 0.76, 0.4, and 0.27 μg/g dw, respectively). Conversely, egg Se concentrations did not vary according to foraging habitats (2.49, 2.96, 2.61, 3.27, and 1.5 μg/g dw, respectively). Tracing waterbird exposure to THg and Se at saltworks was feasible through the use stable isotopic assays of eggs. Birds using saltworks are not exposed to higher concentrations of THg and Se than in adjacent marine habitats.
’ INTRODUCTION Anthropogenic activities have resulted in the contamination of aquatic systems with several inorganic pollutants (e.g., Hg or Se15). Previously, monitoring of inorganic contaminants has focused on marine and freshwater systems (e.g., refs 4 and 5). In contrast, monitoring of man-made systems such as low-latitude solar saltworks are few6,7 but could become crucial for wildlife management and conservation since saltworks have emerged as important alternative or complementary feeding habitats for estuarine species, particularly migrant and resident avifauna.8 The challenge remains that it is difficult to quantify the relative use by waterbirds of saltworks compared with adjacent, lower salinity environments and to develop a convenient proxy for assay. Fortunately, the application of naturally occurring stable isotopes of carbon (13C/12C, expressed as δ13C) and nitrogen (15N/14N, expressed as δ15N) is a useful tool to derive the origin of pollutants allocated to animals’ tissues through their diets (e.g., refs 4 and 9). Transforming isotopic information into dietary proportions of isotopically distinct dietary sources is feasible through the use of multisource isotope mixing models.10 This quantitative isotope approach can provide more reliable information on pollutant pathways within natural systems in general and within saltworks-ascribed r 2011 American Chemical Society
food webs in particular. However, poor isotopic delineation of main dietary sources as well as the use of inappropriate isotopic discrimination factors linking diet with consumer tissues may introduce uncontrolled biases in dietary reconstructions.10,11 An alternative to classical isotope mixing models is the use of the δ-spaces defined and delimited by the isotopic composition of predators known to feed on particular food resources.12 These species can act as isotopic end-points in mixing models instead of the isotopic composition of potential dietary sources. In this way, a more realistic dietary reconstruction of wild communities is expected since diet-specific isotopic niches integrate the isotopic variability of dietary sources while accounting for assimilation efficiencies, diet-tissue discrimination factors, and possible metabolic routing. We report on the results of an investigation of inorganic contaminant concentrations in the waterbird community breeding at the saltworks of Thyna (Sfax, Tunisia). These saltworks are classified as a RAMSAR site and Important Bird Area (IBA) since Received: January 4, 2011 Accepted: May 10, 2011 Revised: May 6, 2011 Published: May 23, 2011 5118
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Environmental Science & Technology they are considered one of the most important crossroads of migratory birds that come from Europe and Sub-Saharan Africa.13,14 In particular, we aimed to investigate the exposure of waterbirds to total Hg (THg) and Se according to actual use of prey from the saltworks. Since pollutant bioavailabilities have been reported to decrease across salinity gradients as a consequence of several geochemical processes,15,16 we expected that the exposure to THg and Se should be lower for those waterbirds feeding largely on saltworks food resources. We measured concentrations of THg and Se in eggs of five bird species: Little Egret (Egretta garzetta), Slender-billed Gull (Larus genei), Yellow-legged Gull (Larus michahellis), Common Tern (Sterna hirundo), and Pied Avocet (Recurvirostra avosetta); whose diets were reconstructed based on egg δ13C and δ15N values and using our alternative (isotopic niche) mixing model approach. We also report THg and Se concentrations of main fish species coming from saltworks (the Mediterranean Toothcarp Aphanius fasciatus) and the adjacent marine system (Bogues Boops boops and Sardines Sardina pilchardus).
’ EXPERIMENTAL SECTION Study Area and Field Methods. The saltworks of Thyna are located in the Gulf of Gabes (central-eastern coast of Tunisia, 34°390 N 10°420 E) and are subjected to the influence of residues from industrial activity in the surrounding area (see the Supporting Information). As a result, the exposure of birds to pollutants in the Gulf of Gabes is higher with respect to other Tunisian marine ecosystems (e.g., the Gulf of Tunis,4,7). During the peak egg laying of the 2006 breeding season, we sampled one egg per nest of five bird species breeding within the saltworks but feeding differentially on diets from marine and saltworks resources (see the Supporting Information for details on sampling strategy). In particular, we sampled eggs of Yellow legged Gull, Little Egret, and Pied Avocet, whose diets at this locality exclusively depend on the consumption of marine fish, saltworks fish, and saltworks invertebrates, respectively,4,7,17,18 but also eggs of bird species with unknown diets such as Slenderbilled Gull and Common Tern. In addition to egg sampling, fish species from saltworks and the adjacent marine environment were collected in May 2008. In particular, Mediterranean Toothcarps (main saltworks fish species found in Little Egret fledgling regurgitates18) were sampled within the Thyna saltworks using fyke nets (2.5 mm mesh) placed in eight ponds of differing salinities for 12 h (Supporting Information; Figure S1). Regarding the marine environment, we obtained Bogues and Sardines (main marine fish species found in Yellow-legged Gull fledgling regurgitates4) collected by commercial fishing fleets operating in the Gulf of Gabes. Samples were placed in sealed bags and frozen pending stable isotope and THg and Se determinations. Chemical Analysis. Egg contents were separated from shells, and saltworks fish were randomly selected and pooled (10 individuals per pool) as a function of sampling station (see Table 1 for the number of pools per sampling station). Samples (i.e., egg contents or fish) were freeze-dried, homogenized, and separated in two pools for stable isotope and THg and Se determinations. Subsamples for stable isotope analyses were lipid-extracted with several rinses of chloroformmethanol (2:1).19 Isotope analyses were carried out at the Serveis Científico-Tecnics of the University of Barcelona (Spain) by means of elemental analysisisotope ratio mass spectrometry using a ThermoFinnigan Flash 1112 (CE Elantech, Lakewood, NJ, USA) elemental analyzer
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coupled to a delta isotope ratio mass spectrometer via a CONFLOIII interface (Thermo Finnigan MAT, Bremen, Germany). Stable isotope ratios were expressed in the standard δ-notation (%) relative to Vienna Pee Dee Belemnite (δ13C) and atmospheric N2 (δ15N). Replicate assays of IAEA standards indicated analytical measurement errors of (0.1% for δ13C and (0.2% for δ15N. THg and Se concentrations were determined at the Serveis Científico-Tecnics of the University of Barcelona (Spain) by means of ICP-MS (Induction Coupled Plasma-Mass Spectrometer, Perkin-Elmer Optima 6000). The accuracy of the analysis was checked by measuring CRM certified reference tissues (Human Hair CRM 397, Lobster hepatopancreas Tort-2 and Dogfish liver Dolt-3; National Research Council Canada). Mean recoveries on reference tissues account for 102% for THg and 101% for Se, and no corrections were applied to the original results. THg and Se concentrations are expressed in μg/g dw. ICP-MS LOD values were 0.2 ppb for THg and 1 ppb for Se, which correspond approximately to 0.18 μg/g dw (THg) and 0.95 μg/g dw (Se) in the tissue samples analyzed. For further information on methodologies see the Supporting Information. Data Analysis. SPSS 15.0 for Windows (SPSS Inc., Chicago, IL, USA) was used for statistical analyses. Normality checks for distributions of δ13C and δ15N values and concentrations of THg and Se were visually inspected using Q-Q plots. No severe deviations from normality were found, so no data transformation was performed, and we used parametric tests throughout. Among birds, comparisons of isotopic values and THg and Se concentrations were done using one-way ANOVA and applying Welch0 s correction to account for the heterogeneity of variances. Posthoc pairwise analyses were carried out using Tamhane0 s tests procedure. Trends across the salinity gradient for concentrations of inorganic pollutants in fish were evaluated by assessing their relationship with salinity. We used least-squares estimation to fit several simple models. Model selection was based on adjusted r-squared and residual distributions. Reconstructing Bird Diets through Isotopic Mixing Models. Dietary reconstructions for Common Terns and Slenderbilled Gulls were performed at the individual level through a dualisotope (δ13C-δ15N), three end-point (marine fish, saltworks fish, and saltworks invertebrates) mixing model.20 Average isotopic values for predators of marine fish, saltworks fish, and saltworks invertebrate (i.e., Yellow-legged Gulls, Little Egrets, and Pied Avocets, respectively) were incorporated as isotopic end-points instead of the isotopic composition of potential dietary sources. To ensure the reliability of our mixing paradigm, we estimated 95% confidence intervals (95% CI) for individual dietary contributions (Supporting Information). We considered that individual dietary reconstructions would be unreliable whenever estimated 95% CI for the lowest and highest contributions were 100%, respectively (which would indicate that consumer isotopic values fell significantly outside of the mixing triangle). Otherwise, negative contributions predicted by the model would be readjusted by setting the most negative values to 0% and re-estimating the other percentages according to the original proportions.21 Tracing Bird Exposure to THg and Se. Lineal models (LM) were used to evaluate variations in bird exposure to THg and Se according to dietary exploitation of saltworks resources. In particular, we evaluated the relationship between measured concentrations of THg and Se in birds’ eggs and individual dietary contribution of saltworks resources (estimated by adding 5119
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Table 1. Concentrations of Total Hg (THg) and Se for Birds’ Eggs and Fish Sampled within the Saltworks of Thyna and the Adjacent Marine Biomea THg (μg/g dw) salinity (g/L)
n
43 50
3 9
63 70
Sig.
b
Det. Rate
Se (μg/g dw)
mean
SD
(0/3) (0/9)
-
12
(0/12)
9
(0/9)
75
12
85
b
Sig.
Det. rate
mean
SD
-
(3/3) (9/9)
1.33 1.42
0.15 0.33
-
-
(12/12)
1.60
0.17
-
-
(9/9)
0.14
0.21
(0/12)
-
-
(11/12)
1.23
0.16
11
(0/11)
-
-
(9/11)
0.12
0.11
90
12
(0/12)
-
-
(12/12)
1.26
0.15
102
9
(0/9)
-
-
(9/9)
2.13
0.32
Gulf of Gabes Bogues
34
4
(0/4)
-
-
(4/4)
3.28
0.43
Sardines
34
4
(0/4)
-
-
(4/4)
2.33
0.43
(12/12)
3.23
1.11
1
(12/12)
2.49
0.44
(12/15)
0.76
0.44
1
2
(15/15)
2.61
0.65
(12/12)
1.66
0.71
1
2
(12/12)
2.96
0.44
2
(20/20)
3.27
0.69
(16/22)
1.50
0.34
Fish saltworks Toothcarpsc
Birds Laridae Yellow-legged Gull
12
Slender-billed Gull
15
1 3
Sternidae Common Tern Ardeidae Little Egret
12
2
20
3
(9/20)
0.40
0.09
22
3
(3/22)
0.27
0.14
Recurvirostridae Pied Avocet
3
a
Detection rates (Det. Rate: values over the limit of detection/sample size -n-), mean and standard deviation (SD) have been used to summarize THg and Se concentrations. Among bird species pair-wise comparisons (Sig.) were done through Tamhane’s test procedure while maintaining the overall alpha level = 0.05. b Numbers denote groups of bird species not significantly different for their THg and Se concentrations. c Sample size represents the number of pools per sampling station.
predicted relative contributions of saltworks fish and saltworks invertebrates to birds’ diets) through least-squares lineal regressions. In addition, we investigated bird exposure to THg and Se according to dietary exploitation of habitats varying in salinity. In this regard, variations in biota δ13C values associated with changes in salinity (mean ( SD for Mediterranean Toothcarps δ13C values: 5.9% ( 0.7% for salinities 60 g/L,18) suggested egg δ13C values to be particularly useful to trace birds’ dietary exploitation of different salinity ranges. We therefore used LM to evaluate the relationship between egg δ13C values and concentrations of THg and Se. This analysis was limited to Little Egrets and Pied Avocets as they were the only bird species that exclusively feed within saltworks, thereby avoiding uncontrolled variability in egg δ13C values due to the influence of other isotopically distinct dietary sources.
’ RESULTS AND DISCUSSION Overall, both THg and Se were detected in most egg samples with the exception of Little Egret for THg (detected in 9 of 20 eggs) and Pied Avocets, for which detection rates were 3/22 for THg and 16/22 for Se (Table 1). However, concentrations of THg and Se were under the threshold points for deleterious effects (2.54 μg/g dw for Hg22 and 67 μg/g dw and Se23) and lower than those detected in eggs of birds breeding at other
Western-Mediterranean areas (e.g., the Spanish-Mediterranean coast24,25 or the Chafarinas Is., near Moroccan coast26) and at other hypersaline systems (e.g., the Salton Sea, California27). In particular, significant differences in concentrations of THg and Se were found among species (FWelch 4, 12 = 12.2, p < 0.001 for THg and FWelch 4, 33 = 32.9, p < 0.001 for Se, see Table 1 for pairwise comparisons). THg was not detected in fish samples (Table 1) suggesting lower concentrations than those observed in bird eggs, which was consistent with biomagnification of Hg throughout food webs (e.g., refs 1 and 28). Regarding fish0 s Se concentrations, a quadratic trend across the salinity gradient was observed (F2, 79 = 48.5, p < 0.001): fish0 s Se concentrations largely decrease between marine and saltworks environments, reaching minimum thereafter and with a final slight increase in the highest-salinity ponds (Supporting Information; Figure S2). Bird Dietary Reconstructions. Isotopic differences observed for bird species breeding in sympatry at the saltworks of Thyna (FWelch 4, 35.2 = 61.7, p < 0.001 for δ13C and FWelch 4, 36.4 = 212.2, p < 0.001 for δ15N, Table 2) revealed a broad discrimination among their feeding habits. Whereas Yellow-legged Gulls, Little Egrets, and Pied Avocets were assumed to have fed exclusively on marine fish, saltworks fish, and saltworks invertebrates, respectively,4,7,17,18 predicted individual feeding strategies for Slender-billed Gulls and Common Terns revealed a differing contribution of these dietary resources to the diet of individuals 5120
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(see Figure 1 and the Supporting Information; Table S1), with average relative contributions accounting for 24%, 50%, 26% and 47%, 50%, 3%, respectively. Trophic segregation also occurred at the intraspecific level. While Pied Avocets and Yellow-legged Gulls showed a high degree of population-level specialization (as revealed by their low isotopic variability, 29,30), the relatively high δ13C variability observed for Little Egrets was interpreted as a likely reflection of individual feeding strategies based on the use of differing salinity ranges. Intraspecific trophic segregation was also detected for Slender-billed Gulls and Common Terns, whose individual diets greatly differ in the relative contribution of saltworks dietary Table 2. Isotopic Composition (δ13C and δ15N) of Eggs of Birds Breeding at the Saltworks of Thynaa δ13C (%) n
Sig.b
δ15N (%)
mean SD
Sig.b
mean SD
Laridae Yellow-legged Gull 12 1 Slender-billed Gull 15 Sternidae Common Tern
12
3
15.7 0.8 1
9.1
0.9
2 12.5 1.5 1
9.3
1.1
2
10.7
0.6
2
11.4
1.2
14.3 1.2
Ardeidae Little Egret
20
2 11.4 1
22
2 12
Recurvirostridae Pied Avocet a
0.7
3 5.6
0.6
Mean and standard deviation (SD) have been used to summarize isotopic data. Among bird species pair-wise comparisons (Sig.) were done through Tamhane’s test procedure while maintaining the overall alpha level = 0.05. b Numbers denote groups of bird species not significantly different for egg δ13C and δ15N values
resources. In particular, the relationship between contributions of saltworks invertebrates and marine fish for Slender-billed Gulls suggested that both prey types were present in similar relative proportions in diets of most individuals, whereas the contribution of saltworks fish was highly variable within the population. For Common Terns, individual feeding strategies consisted of a variable relative contribution of fish from saltworks and the marine environment (Figure 1). Bird Exposure to Contaminants. Trophic segregation within this waterbird community, but also expected differences in concentrations of THg and Se among potential foraging habitats (refs 15 and 16 and the Supporting Information; Figure S2), provided us with an exceptional framework to assess variations in the exposure of birds to these contaminants as a function of actual use of prey from the saltworks. According to previous works showing THg bioavailability to decrease across salinity gradient,15,16 the higher contribution of saltworks resources to bird diet resulted in lower concentrations of THg in their eggs (F1, 68 = 41.5, p < 0.001). This was observed both at the population (Figure 2A) and at the individual level (Figure 3). In contrast, concentrations of Se in eggs were not related to saltworks-resource exploitation (F1, 95 = 1.9, p = 0.175, Figure 2B), despite the lower availability of this element within saltworks (as revealed by observed differences in concentrations of Se for fish from saltworks and the adjacent marine system, Table 2 and the Supporting Information; Figure S2). Female to egg Se transfer depends on female dietary intake,3133 although phylogeny might also play an important role in modulating the amount of Se allocated to eggs.34 Developing embryos require certain amount of Se in order to synthesize selenoproteins, which are vital for cell viability and function. However, excessive concentrations of Se produce embryotoxic and teratogenic effects resulting in embryonic malformations and increasing mortalities.35,36 Thus, observed concentrations of Se in birds’
Figure 1. (A) Bivariate plot of δ13C and δ15N values for Slender-billed Gulls and Common Terns. Rectangles represent the isotopic composition (mean ( SD) of predators feeding on marine fish -MF-, saltworks fish -SWF-, and saltworks invertebrates -SWI- (Yellow-legged Gull, Little Egret, and Pied Avocet, respectively), which were incorporated as dietary end-points in the isotopic mixing model to reconstruct the diet of Slender-billed Gulls and Common Terns at the individual level (B) (see Experimental Section and the Supporting Information). 5121
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Figure 3. Bivariate plot of saltworks resource exploitation by birds (estimated by adding individual relative consumption of saltworks fish and saltworks invertebrates) vs concentrations of total mercury (THg) in their eggs. For bird species mainly feeding on particular food resources (i.e., Yellow-legged Gull, Little Egret, and Pied Avocet) error bars (mean and 95% confidence interval) are represented. For Slender-billed Gull and Common Tern (species with mixed diets) we represent individual feeding strategies.
Figure 2. Error bars (mean and 95% confidence interval) for (A) THg and (B) Se concentrations measured in eggs of bird species breeding in the saltworks of Thyna. The relative contributions of marine fish -MF-, saltworks fish -SWF-, and saltworks invertebrates -SWI- to the diet of each species have been also represented.
eggs are likely not simply a passive reflection of those in the maternal diet but might also reflect phylogenetic and speciesspecific differences that have evolved to provide some adjustment between dietary supply and embryonic demand. In addition to observed differences in waterbird exposure to THg and Se according to dietary exploitation of saltworks vs adjacent marine environment, the relationship between δ13C values and Se concentrations measured in eggs of Little Egret (F1, 18 = 4.5, p = 0.047) can be interpreted as the result of an increasing exposure to Se of birds feeding largely on higher hypersaline ponds. Although Pied Avocet also fed within saltworks, the low egg δ13C variability (Table 2) suggested that most individuals were feeding on similar salinity ranges (probably on invertebrates from shallow and high hypersalinity ponds, 17), which might explain the lack of a significant relationship between δ13C values and Se concentrations for this species (F1, 15 = 0.5, p = 0.48, Figure 4). Solar saltworks will become more critical to wildlife as natural feeding habitats progressively decrease as a result of human activities on coastal and estuarine environments.8 Within this
Figure 4. Bivariate plot of Se concentrations for Little Egrets and Pied Avocets vs δ13C values measured in their eggs (which have been used as a proxy to dietary exploitation of different salinity ranges).
framework, monitoring animal exposure to pollutants derived from dietary exploitation of saltworks resource is crucial to evaluate the actual impact of such pollution on saltworks-dependent wildlife communities, which may have important implications in management and conservation policies. Dietary exploitation of saltworks resources may result in a lower exposure of birds to inorganic contaminants (e.g., THg). However, the exposure of saltworks-dependent birds to particular inorganic pollutants (e.g., Se) may vary according to dietary exploitation of different salinity ranges. We underscore the necessity of accurate information on feeding habits to properly interpret pollutant concentrations in animals’ tissues. In this regard, dietary reconstructions at the intraspecific level are particularly interesting since differing 5122
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Environmental Science & Technology individual feeding strategies may appear within populations resulting in a differential exposure to pollutants. Our proposed isotopic framework is a suitable and reliable approach for such individual-level dietary reconstructions.
’ ASSOCIATED CONTENT
bS
Supporting Information. Details on the study area, sampling strategy, analytical methods and on the mass-balanced mixing model applied in this study. Figure S1 (the saltworks of Thyna and detail of the eight different points where Mediterranean Toothcarps were sampled), Figure S2 (trends for fish concentrations of Se across the salinity gradient), and Table S1 (output of the mixing model). This material is available free of charge via the Internet at http://pubs.acs.org.
’ AUTHOR INFORMATION Corresponding Author
*Phone: þ3493-4021041. Fax: þ3493-4035740. E-mail: ramirez@ ub.edu.
’ ACKNOWLEDGMENT We thank the members of “L’Association des Amis des Oiseaux” for their precious help during the fieldwork and Ra€ul Ramos and Joan Navarro for their valuable comments on an early version of this manuscript. Fran Ramírez was supported by FPU grant (AP-2004-3715). Funds were provided by AECI-PCI Spanish-Tunisian projects A/2907/05 and A/6165/06, the MEyC project CGL2004-02238/BOS and Environment Canada. This work is devoted to the memory of Xavier Ruiz who died on April 27, 2008. ’ REFERENCES (1) Atwell, L.; Hobson, K. A.; Welch, H. E. Biomagnification and bioaccumulation of mercury in an Arctic marine food web: Insights from stable nitrogen isotope analysis. Can. J. Fish. Aquat. Sci. 1998, 55, 1114–1121. (2) Boncompagni, E.; Muhammad, A.; Jabeen, R.; Orvini, E.; Gandini, C.; Sanpera, C.; Ruiz, X.; Fasola, M. Egrets as monitors of trace-metal contamination in wetlands of Pakistan. Arch. Environ. Contam. Toxicol. 2003, 45, 399–406. (3) Fisk, A. T.; de Wit, C. A.; Wayland, M.; Kuzyk, Z. Z.; Burgess, N.; Robert, R.; Braune, B.; Norstrom, R.; Blum, S. P.; Sandau, C.; Lie, E.; Larsen, H. J. S.; Skaare, J. U.; Muir, D. C. G. An assessment of the toxicological significance of anthropogenic contaminants in Canadian Arctic wildlife. Sci. Total Environ. 2005, 351, 57–93. (4) Abdennadher, A.; Ramírez, F.; Romdhane, M. S.; Ruiz, X.; Jover, L.; Sanpera, C. Biomonitoring of coastal areas in Tunisia: Stable isotope and trace element analysis in the Yellow-legged Gull. Mar. Pollut. Bull. 2009, 60, 440–447. (5) Vest, J. L.; Conover, M. R.; Perschon, C.; Luft, J.; Hall, J. O. Trace element concentration in wintering waterfowl from the Great Salt Lake, Utah. Arch. Environ. Contam. Toxicol. 2009, 56, 302–316. (6) Tavares, P. C.; Kelly, A.; Maia, R.; Lopes, R. J.; Santos, R. S.; Pereira, M. E.; Duarte, A. C.; Furness, R. W. Variation in the mobilization of mercury into Black-winged Stilt Himantopus himantopus chicks in coastal saltpans, as revealed by stable isotopes. Estuar. Coast. Shelf. Sci. 2008, 77, 65–76. (7) Abdennadher, A.; Ramírez, F.; Romdhane, M. S.; Ruiz, X.; Jover, L.; Sanpera, C. Little Egret (Egretta garzetta) as a bioindicator of trace element pollution in Tunisian aquatic ecosystems. Environ. Monit. Assess. 2011, 175, 677–684.
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