Low total mercury in Caiman yacare (Alligatoridae) as

Environmental Pollution xxx (2016) 1e6

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Low total mercury in Caiman yacare (Alligatoridae) as compared to carnivorous, and non-carnivorous fish consumed by Amazonian indigenous communities* c, *, C.I. Molina c, d, G. Miranda-Chumacero a, d S.J. Rivera a, L.F. Pacheco b, D. Acha a

Wildlife Conservation Society, Greater Madidi-Tambopata Landscape Conservation Program, La Paz, Bolivia n Boliviana de Fauna, Instituto de Ecología, Universidad Mayor de San Andr Coleccio es, P.O. Box 10077, La Paz, Bolivia Unidad de Calidad Ambiental, Instituto de Ecología, Universidad Mayor de San Andr es, P.O. Box 10077, La Paz, Bolivia d Instituto de Ecología, Unidad de Limnología, Universidad Mayor de San Andr es, P.O. Box 10077, La Paz, Bolivia b c

a r t i c l e i n f o

a b s t r a c t

Article history: Received 10 April 2016 Received in revised form 4 July 2016 Accepted 4 July 2016 Available online xxx

Mercury contamination in the River Beni basin is an important health risk factor, primarily for indigenous communities that live along the river. Among them are the Tacana, living in their original territory with sustainable use of their natural resources, consuming fish, Caiman yacare, and other riverine resources as their main source of protein. To assess mercury exposure to Tacana people, total mercury (THg) was evaluated in the muscle of seven commercial fish, and Caiman yacare (yacare caiman) during 2007 and 2008. THg was extracted by acid digestion and concentrations were determined by atomic absorption spectrometry. Mean mercury concentrations in C. yacare was 0.21 ± 0.22 mg g1Hg w.w. (wet weight), which is lower than expected given its high trophic level, and its long life-span. It is possible that mercury in C. yacare is accumulated in other organs, not included in this study; but it is also possible that physiological mechanisms are involved that help caimans get rid of ingested mercury, or simply that C. yacare’s diverse diet reduces THg accumulation. Carnivorous fishes (Pygocentrus nattereri, Pseudoplatystoma tigrinum, Zungaro zungaro, Plagioscion squamosissimus, and Leiarius marmoratus) had the highest total mercury concentrations, ranging from 0.35 to 1.27 mg g1Hg w.w. moreover, most were above the limit recommended by WHO (0.5 mg g1Hg w.w.); except for Leiarius marmuratus, which presented a mean of 0.353 ± 0.322 mg g1Hg w.w. The two non-carnivorous fish species (Prochilodus nigricans, and Piaractus brachypomus) present mean concentrations of 0.099 ± 0.027, and 0.041 ± 0.019 mg g1Hg w.w., respectively. Finally, recommendations on the consumption habits of Tacana communities are discussed. © 2016 Elsevier Ltd. All rights reserved.

Keywords: Bioaccumulation Biomagnification Health of indigenous peoples Mercury exposure

1. Introduction Mercury pollution in the Amazon basin is a growing concern, mainly for indigenous riparian populations for whom fisheries are their major sources of protein (Barbieri et al., 2009; Benefice et al., 2008; Maurice-Bourgoin et al., 2000). Mercury in the Amazon is naturally abundant in soils, and erosion is thought to be an important source of inorganic mercury (Roulet et al., 1998), together with artisanal gold mining (Maurice-Bourgoin et al., 2000) and deforestation (Roulet et al., 1998). Methylmercury (MeHg), an organic form of mercury, is one of

* This paper has been recommended by Von Hippel Frank A. * Corresponding author. ). E-mail addresses: [email protected], [email protected] (D. Acha

the most toxic chemical species (Lebel et al., 1998; Tamm et al., 2006), produced by the transformation of the inorganic mercury via biotic and abiotic processes. Sulfate-reducing bacteria (SRB) are frequently the main (though not the only) mercury methylators et al., 2011; King et al., 2000; Macalady et al., 2000). Mercury (Acha methylation in Amazonian Lakes takes place predominantly in the periphyton associated with different macrophytes (Acha et al., 2005; Guimar~ aes et al., 2000a, 2000b). Periphyton is an important carbon source and could be the main entrance of MeHg to the food chain (Molina et al., 2010). In the aquatic food web, Hg is mainly found as MeHg. Methylmercury is easily bioaccumulated and biomagnified through the food chain (Barbosa, 2003; Molina et al., 2010; Pouilly et al., 2013). Therefore, long-lived (Khan and Tansel, 2000), larger organisms (McArthur et al., 2003; Watras et al., 1998) and species higher in the food chain tend to have higher concentrations of

http://dx.doi.org/10.1016/j.envpol.2016.07.013 0269-7491/© 2016 Elsevier Ltd. All rights reserved.

Please cite this article in press as: Rivera, S.J., et al., Low total mercury in Caiman yacare (Alligatoridae) as compared to carnivorous, and noncarnivorous fish consumed by Amazonian indigenous communities, Environmental Pollution (2016), http://dx.doi.org/10.1016/ j.envpol.2016.07.013

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S.J. Rivera et al. / Environmental Pollution xxx (2016) 1e6

mercury (Da Silva et al., 2005; Pouilly et al., 2013; Trudel and Rasmussen, 2001). Consequently, top predators may have the highest mercury concentrations (Cabana et al., 1994; Duvall and Barron, 2000; Rumbold et al., 2002) and potentially show the highest risk for human exposure to Hg. At the Amazon, mercury exposure is mostly related to fish consumption (Maurice-Bourgoin et al., 2000) and in particular to the consumption of carnivorous fish species (Passos et al., 2003), but little is known about the risk of Caiman yacare meat consumption. This information is particularly valuable for control methylmercury exposure in human populations since there are strong relationships between the quantity, frequency and type of fish consumed and mercury concentrations in human hair (Dolbec et al., 2001; Passos et al., 2003). Caiman yacare (Yacare from now on) is considered as a top predator in the Amazon basin because it feeds mostly at the top of the food web (Table S1) and is almost free from predators (Sergio et al., 2014). Adults can reach ~2.5 m of total length and feed mainly on fish; although they are highly opportunistic predators that may also consume water birds and small mammals (Santos et al., 1996). Yacare populations are managed under a sustainable harvesting program in Bolivia (CIPTA and WCS, 2010). Yacare and other caiman species constitute an important source of meat for indigenous communities (Constantino et al., 2008; Figueiredo et al., 2015). Caiman consumption is growing so much that there is research on how to better process the meat (Romanelli et al., 2002; Telis et al., 2003). Yacare meat is rich in proteins, and it may be an important source of Omega-3 fatty acids (IBCE, 2010). Its position in the trophic chain generates a high concern of potential Hg exposure for the consumers, as high mercury concentrations have already been reported in other species of South American crocodilians (Schneider et al., 2015; Vieira, 2011). Here we investigate the concentrations of total mercury in Caiman yacare and compare it to the mercury concentration in seven fish species (five carnivorous and two non-carnivorous), which are all common in the diet of the Tacana people in the Beni river basin (Miranda-Chumacero et al., 2011). Under the hypotheses that Yacare occupies the highest trophic level, we expected to find the highest level of THg in Caiman yacare, followed by carnivorous fishes and non-carnivorous species. 2. Methods

captured during commercial hunting, between September and October of 2007 and 2008. Only animals larger than 1.8 m were sampled, since harvesting regulations only allow the capture of those individuals, under the assumption that most are males (Llobet et al., 2004). Capture site (GPS location, habitat type), and standard measurements (total length, sex, and weight) were recorded for each sampled individual. Samples were about 2 cm3, and their collection was as clean as possible, removing any fat, bone, and skin. Samples were placed into Teflon tubes and immediately cryo-frozen using liquid nitrogen for cryo-conservation. 2.3. Fish samples Fish samples were obtained from specimens brought for sale by Tacana fishermen to Rurrenabaque, a small town close to the study site. A total of 35 muscle samples from seven different fish species were collected and grouped into carnivorous/piscivorous (C: Pygocentrus nattereri, Pseudoplatystoma tigrinum, Zungaro zungaro, Plagioscion squamosissimus, and Leiarius marmoratus) and not carnivorous (NC: Prochilodus nigricans, and Piaractus brachypomus). NC species includes herbivorous and omnivorous species that ~ ez et al., 2007; Pouilly et al., consume little or no other fish (Iban 2004). 2.4. Total Hg determination Samples were weighed both before, and after freeze-drying (lyophilized) to calculate the percentage of water content in each sample. Lyophilized tissues were ground and homogenized in an agate mortar. Mercury was extracted from 100 mg of the dry sample by acid digestion with 5 mL of HNO3 (65%) and 0.5 mL of HCl (6 N), at 100 C for 2 h. After cooling down, the extracts were further digested with 1 mL of H2O2 (50%) for 2 h. The final extract was completed to 30 mL with ultrapure water. Samples were digested alongside with reference samples (BCR: tuna fish and Tortrez, 2000). Total Hg was 2: lobster hepatopancreas NRCC) (Pe detected after acidification with HCl (3%) and reduction with SnCl2 (1.5%) with an Atomic Absorption Spectrophotometer (AAS, Perkin Elmer 3110). Concentrations were determined using a standard curve and stability of the instrument was monitored with a standard every five sample readings.

2.1. Study area 2.5. Data analyses All the sampling was conducted in the area of sustainable management of the indigenous Tacana land “Tierra Comunitaria de Origen Tacana I” (TCO Tacana I, Fig. 1). The area encompasses ~3719 km2 within the Beni river basin. Legal harvesting of Yacare takes places within an area of about 1300 km2 (CIPTA and WCS, 2002). A total of 17 locations were sampled, including a large river (Beni River), three smaller rivers and nine small lakes. The number of samples per location varied from one to nine. The Beni is a “white waters” large river, characterized by neutral pH, low oxygen concentrations, and high concentrations of suspended particles (Gautier et al., 2007). The hydrological and geomorphological dynamics of the river generate a large number of small and medium-sized oxbow lakes, inhabited by Yacare, other common large reptiles like the black caiman (Melanosuchus niger), and yellow-spotted river turtles (Podocnemis unifilis) as well as a high diversity of fish species. 2.2. Yacare sampling Since people consume mainly the tail of Yacare, all samples were collected from this part of the body. A total of 64 muscle samples were collected from individuals immediately after they were

Each set of data was evaluated for normality with Shapiro-Wilk test. Since most of our data sets fail to pass the normality test total mercury (THg) concentrations among carnivorous, noncarnivorous and Yacare were normalized applying the natural logarithm to compare them using one way ANOVA, followed by Tukey’s post hoc pairwise comparison. The same procedure without normalization was applied to compare THg among the different species studied, assuming a normal distribution. Data transformation is always risky when using ANOVA. Therefore, we also performed Kruskal-Wallis one way ANOVA followed by Dunn’s post hoc pairwise comparison. We used an a ¼ 0.05 for all tests. All analyses were conducted in PASW SPSS® version 19.0 for Windows (SPSS Inc. Chicago, IL, USA) or SigmaPlot 12.0. 3. Results and discussion All 64 Yacare samples had detectable concentrations of THg (mean 0.21 ± 0.22 mg g1Hg w.w., Table 1). Among them, about most had concentrations below the recommended limit of Hg content in freshwater fish meat for human consumption (0.5 mg g1Hg w.w.; WHO, 1991). Only 6 had concentrations higher



Fig. 1. Sampling locations inside the sustainable management area in the Bolivian Amazon.


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Table 1 Muscle Total Hg concentration (mean ± standard deviation) for C. yacare and carnivorous and non-carnivorous fish species consumed by local people at Tacana I indigenous territory, Bolivia. Maximum concentration recommended by WHO in muscle for human consumption is 0.5 mg g1 Hg w.w. Species

Local name

Feeding habit

N

THg (mean ± SD in mg/g ww)

Caiman yacare Pygocentrus nattereri Pseudoplatystoma tigrinum Zungaro zungaro Plagioscion squamosissimus Leiarius marmoratus Prochilodus nigricans Piaractus brachypomus

Lagarto ~a Piran Pintado

carnivore carnivore carnivore

64 4 5

0.21 ± 0.22 1.27 ± 1.16 0.85 ± 0.49

Bagre Corvina

carnivore carnivore

7 4

0.75 ± 0.31 0.66 ± 0.31

Tujuno balo Sa Pacú

carnivore Non carnivorous Non carnivorous

6 4 5

0.35 ± 0.32 0.10 ± 0.03 0.04 ± 0.2

than 0.5 mg g1Hg w.w. and up to 1.20 mg g1 Hg w.w. Unlike Yacare, four out of the five carnivorous fish species had muscle THg concentrations above the limits recommended by the WHO, while all specimens of non-carnivorous fish had concentrations below WHO recommended levels (Table 1). The number of fish samples collected is low to characterize THg content in each fish species but provides a solid set of data for placing Yacare THg concentrations in its food web context. THg concentrations in our fish samples were in the same range as previous studies in the region (Lebel et al., 1997; Lechler et al., 2000; Maurice-Bourgoin et al., 2000; Pouilly et al., 2013). Mean THg were significantly different among the Yacare and the carnivorous and non-carnivorous fish (F2,96 ¼ 28.2; p < 0.05; Tukey p ¼ 0.05; Fig. 1S; H ¼ 35.9 p < 0.001). Dunn pairwise comparison showed a significant difference between carnivorous and noncarnivorous fish (p < 0.05), as well as between Yacare and carnivorous fish (p < 0.05) but no difference between Yacare and noncarnivorous fish (Fig. 2S). A more detailed comparison by species (Fig. 2) shows a significant difference among mean values (F ¼ 10.7; p < 0.001) and median values (H ¼ 40.2; p < 0.001). The post hoc ~ a and analysis shows significant differences between Yacare, Piran Pacu (Tukey p < 0.001), but no difference between Yacare and the remaining fish species (Tukey p > 0.05). Such differences would place Caiman yacare at about the same level of non-carnivorous fish

Fig. 2. Total mercury concentrations among different fish species and Caiman yacare (Yacare), error bars are 95% confidence intervals for each group of data. The horizontal line at 0.5 mg g1 indicates the recommended limit by the WHO.

(Fig. 2). Overall, carnivorous fish presented a higher THg and thus represent a significantly higher health risk than non-carnivorous fish (Fig. S1). However, contrary to our expectations, the supposed top predator Yacare presented intermediate values (Fig. 2). The public health implication of these results is that local communities may preferably administrate their menu according to feeding habits of the consumed species to minimize their potential exposition to mercury. When a choice is possible, a preference for non-carnivorous species may reduce this risk. Also, Yacare meat seems to be relatively safe for human consumption and may constitute another alternative to carnivorous fish consumption. Caiman yacare muscle was expected to have the highest levels of THg, because of its top predator status, and its long life span. Such assumption was held for other studies including crocodilians studies (Jagoe et al., 1998; Khan and Tansel, 2000; Rainwater et al., 2007), probably because of the high Hg concentrations found in some locations (Heaton-Jones et al., 1997). Modeling studies also suggested that alligators presented a high risk of mercury contamination (Duvall and Barron, 2000). Our results suggest that this hypothesis may be unwarranted, at least for our study sites. Previous studies have focused on either determining mercury concentrations in crocodilians from different locations, or comparing concentrations among different organs or structures of the same animals. To our knowledge, no other study compared mercury concentration in crocodilians and other aquatic vertebrates of the same system. We found that most of the Yacare diet in our research area is fish (Table S1), which makes it a top predator (Sergio et al., 2014) without the expected Hg load. One possible explanation to these relative lower concentrations is that THg does not accumulate preferentially in the muscles of crocodilians, but elsewhere in their bodies. For example, preferential accumulation of Hg in both American alligator (Alligator mississipiensis), and Caiman crocodilus seem to be in the liver (Jagoe et al., 1998; Rumbold et al., 2002). In any event, since meat for human consumption comes from the tail, our sampling was representative from a public health perspective. It has also been suggested that juvenile American alligators have higher bioconcentration factors (Khan and Tansel, 2000). Our samples were collected only from large adult individuals, meaning that we may have missed the peak of THg accumulation for C. yacare, if it occurs in juvenile stages. However, this would be only an unexpected plus on the management strategy for C. yacare since selecting large individuals for consumption should help preserve the Yacare population and reduce the exposure of human populations to mercury. Furthermore, despite the small data range, our results show negative (though weak) correlations between THg, and individual total length (r ¼ 0.26: p ¼ 0.04) and weight (r ¼ 0.30; p ¼ 0.02). Such correlation coincides with the observation of higher concentrations in juvenile alligators (Khan and Tansel, 2000), and Melanosuchus niger. However, the correlation was not found for C. crocodilus in a recent study in Brazilian Amazonia (Eggins et al., 2015) and the opposite was found for Alligator mississippiensis (Nilsen et al., 2016). Like most reptiles, crocodilians have low energetic requirements and are highly efficient in transforming food into biomass (Vitt and Caldwell, 2013; P. 222). Therefore, adult crocodilians may consume a small number or biomass of prey, take a long time to digest them, and spend long periods without feeding. All of this might reduce the bioaccumulation of Hg by C. yacare. Finally, Yacare diet within our study site (Table 1S) shows that this crocodilian feeds mainly on fish species (68.3%), both carnivorous and non-carnivorous, which places Yacare at least at the same level as carnivorous fish. However, unlike carnivorous fish, Yacare feeds in many other things that may dilute or reduce Hg accumulation.



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Table 2 Total mercury concentrations obtained in Caiman yacare for this study and those reported for other crocodilians. Location

Reference

Species

Muscle (n)

Caudal scutes

Everglades Central Florida Okefenokee SRS; South Carolina South Carolina Everglades Pantanal, Brazil Paraguay River Bento Gomes Cuiba Nhecol^ andia Belize and Costa rica Belize and Costa rica Purus River Purus River Purus River TCO Tacana I

Jagoe et al., 1998 Jagoe et al., 1998 Jagoe et al., 1998 Jagoe et al., 1998 (Yanochko et al., 1997) Rumbold et al., 2002 Vieira, 2011

A. mississippiensis A. mississippiensis A. mississippiensis A. mississippiensis A. mississippiensis A. mississippiensis C. crocodilus yacare

5.57 ± 0.47a (18) 1.85 ± 0.35a (21) 0.0 ± 0.12a (9) 4.83 ± 0.88a (17) 4.08 ± 0.46 (44) 0.10e1.80 b(28) 0.05 ± 0.01 (8) 0.27 ± 0.08 (27) 0.14 ± 0.04 (36) 0.12 ± 0.10 (7)

5.83 ± 1.04 0.137 0.076

Rainwater et al., 2007 Rainwater et al., 2007 Schneider et al., 2012 Eggins et al., 2015 Eggins et al., 2015 This study

Crocodylus moreletii Crocodylus acutus C. crocodilus crocodilus C. crocodilus Melanosuchus niger C. yacare

a b

b

4.58 ± 0.63

0.099 ± 0.022 0.093 ± 0.027

0.29 ± 0.21 (10) 0.362 ± 0.231b 0.176 ± 0.097b 0.21 ± 0.22b (64)

Mercury concentrations in mg g1Hg dry weight Hg and. Wet weight, reported as mean and standard deviation (SD).

Although C. yacare samples had significantly lower concentration of THg than the carnivorous fish species sampled, this does not mean that they present an absolute low concentration of THg. When comparing with crocodilians from other places the THg concentrations observed in C. yacare from the Beni river appeared to be intermediate (Table 2). 4. Conclusions Total mercury concentrations are higher in carnivorous fishes than in non-carnivorous species. Mercury concentrations in Caiman yacare were intermediate between those groups of fishes and were below the FAO/WHO recommended a limit of 0.5 mg g1. Our results allow us to recommend that human populations consume preferably non-carnivorous fishes and Yacare tail meat, particularly to avoid adverse effects of Hg during critical periods such as pregnancy. Acknowledgement The Wildlife Conservation Society through the Greater MadidiTambopata Landscape Conservation Program funded this research with support from Gordon and Betty Moore Foundation, John D. and Catherine T. MacArthur Foundation and the blue moon fund. We extend our particular thanks to fishermen and caiman managers in local communities. We would also like to thank Jaime Chincheros of the Institute of Ecology and Environmental Quality Laboratory (LCA), and Jean Louis Duprey of Institut de Recherche veloppement (IRD) for their support in the execution of pour le De this study. Marc Pouilly commented on an earlier version of this manuscript. Appendix A. Supplementary data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.envpol.2016.07.013. References , D., Hintelmann, H., Yee, J., 2011. Importance of sulfate reducing bacteria in Acha mercury methylation and demethylation in periphyton from Bolivian Amazon region. Chemosphere 82, 911e916. Acha, D., Iniguez, V., Roulet, M., Guimaraes, J.R., Luna, R., Alanoca, L., Sanchez, S., 2005. Sulfate-reducing bacteria in floating macrophyte rhizospheres from an Amazonian floodplain lake in Bolivia and their association with Hg methylation.

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