Mercury Concentration in the Spectacled Caiman and BlackCaiman (Alligatoridae) of the Amazon: Implicationsfor Human Health

Larissa Schneider • Reinaldo Pacheco Peleja •

Augusto Kluczkovski Jr. • Guilherme Martinez Freire •

Boris Marioni • Richard Carl Vogt • Ronis Da Silveira

Received: 1 February 2012 / Accepted: 2 April 2012 / Published online: 13 May 2012

� Springer Science+Business Media, LLC 2012

Abstract Mercury (Hg) concentrations in the Amazon

are generally high, but no studies have been published on

Hg concentrations in caimans (Alligatoridae) from the

region. Aiming for sizes representative of caimans traded

for food in the Amazon, we measured Hg concentration in

tail muscle of spectacled caiman (Caiman crocodilus cro-

codilus) and black caiman (Melanosuchus niger) from the

Purus River basin. The information on Hg concentration in

caimans from this area is important because of the potential

health risk to humans and other animals that eat them as

well as the potential use of these top-level predators as

bioindicators. There were no significant interspecific or sex

differences in Hg concentrations. The mean Hg concen-

tration was 291.2 lg/kg in C. c. crocodilus and 193.9 lg/kg

in M. niger. A significant positive correlation between Hg

concentration and size was found for M. niger (p = 0.005)

but not for C. c. crocodilus. Our Hg sample from M. niger

corresponded to the size of M. niger collected for com-

mercial trade, but our Hg sample from C. c. crocodilus

turned out to be significantly smaller than the trade samples

(p = 0.004), but this difference is not pertinent in the

absence of a correlation between size and Hg concentration

for this species. Although there are no standards for reptile

meat, both species had mean Hg concentrations lower than

the maximum allowable level of 500 lg/kg Hg recom-

mended by the World Health Organization and by the

Brazilian Health Ministry for fish. However, by calculating

daily consumptions limits and number of meals per month

that can be safely consumed, we found that consumers who

eat caimans frequently may be at risk for Hg-related health

problems.

Mercury (Hg) pollution is a serious environmental problem

in many biomes of the world, and high concentration of

this heavy metal has been found in fish, turtles, and humans

living in Amazonian ecosystems (Belger and Forsberg

2006; Forsberg et al. 1995; Haines et al. 1995; Schneider

et al. 2009; Silva-Forsberg et al. 1999). First, the contam-

inated areas with Hg in the Brazilian Amazon were iden-

tified as the regions where gold mining activities were

intense (Malm et al. 1995; Pfeiffer et al. 1993). However, it

was found that Hg from natural origins can also have a high

L. Schneider (&)

University of Canberra, Kirinari St. Bruce, Canberra, ACT 2617,

Australia

e-mail: Larissa.Schneider@canberra.edu.au

R. P. Peleja

Laboratorio de Biologia Ambiental, Universidade Federal do

Oeste do Para, Av. Marechal Rondon, S/N, Caranazal, Para CEP

68040-070, Brazil

A. Kluczkovski Jr.

Programa de Pos Graduacao em Ciencias dos Alimentos,

Universidade Federal do Amazonas, Av. General Rodrigo

Otavio Jordao Ramos 3000, Manaus, Amazonas CEP

69077-030, Brazil

G. M. Freire � R. Da Silveira

Laboratorio de Zoologia Aplicada a Conservacao, Instituto de

Ciencias Biologicas, Universidade Federal do Amazonas,

Av. General Rodrigo Otavio Jordao Ramos 3000, Manaus,

Amazonas CEP 69.077-030, Brazil

B. Marioni

Caiman Conservation Program, Instituto Piagacu, Rua UZ no 8,

Cj. Morada do Sol, Aleixo, Manaus, Amazonas 69083-000,

Brazil

R. C. Vogt

Coordenacao de Biodiversidade, Instituto Nacional de Pesquisas

da Amazonia, Av. Andre Araujo no 2936, Aleixo, Manaus,

Amazonas CEP 69060-001, Brazil

123

Arch Environ Contam Toxicol (2012) 63:270–279

DOI 10.1007/s00244-012-9768-1

concentration in pristine soil leached into river systems or

freshly dammed reservoirs (Fadini and Jardim 2001; Roulet

et al. 2001). Hg levels in many Amazonian soils are nat-

urally high such that Hg release from soils into the river

system is thought to be greater than the combined input

from all anthropogenic sources (Fadini and Jardim 2001;

Roulet et al. 1998; Zeidemann 1998).

Mercury can be transformed from water and sediment

into methylmercury under both biotic and abiotic condi-

tions (Ravichandran 2004; Steffan et al. 1988). This

transformation is especially important because methyl-

mercury is highly toxic, bioavailable, and persistent in

the environment and can biomagnify in the food chain

(Bisinoti and Jardim 2003; Ullrich et al. 2001). This

transformation is especially common in flooded soils

associated with wetlands because these areas enhance Hg

methylation, thus causing increased accumulation in resi-

dent biota (Porvari and Verta 1995).

The Purus River Basin forms one of the largest flood-

plain areas of all Amazon tributaries (Goulding et al.

2003), and therefore it is expected to be one of the sub-

basins of the Amazon Basin with the highest methyl Hg

content. This river is exploited by commercial fishermen

from Manaus and, in the headwaters, inhabited by Indians

and small communities. Several areas have been designated

for ethnic groups and are protected from extractive activ-

ities (Batista 1998; Goulding et al. 2003; Petrere 1978).

Although there are laws to protect the area, the Piagacu-

Purus Sustainable Development Reserve located in the

lower Rio Purus recently recorded at least 50 tons of dried-

salted caiman meat illegally commercialized annually. This

represents the largest amount of illegal trade of the caiman

wild population in Latin America (Da Silveira 2003;

Marioni et al. 2006).

Mercury is persistent in biological tissues and can bio-

accumulate over time to reach toxic or lethal levels, with the

highest Hg bioaccumulation typically occurring in species of

the highest trophic levels and in long-lived vertebrates.

Crocodilians can live for decades, are generalists and

opportunistic top carnivores (Da Silveira and Magnusson

1999), and usually have high Hg concentrations (Burger et al.

2000; Vieira et al. 2011). The use of caiman meat for human

consumption has been documented since the 1980s (Best

1984; Da Silveira and Thorbjarnarson 1999). Until recently,

all this commerce has been illegal; however, in 2002 a legal

regional and national commerce in caiman meat was estab-

lished from caimans harvested in sustainable development

reserves in Brazil (Mamiraua 2011).

The four crocodilians species that occur in the Amazon

belong to the family Alligatoridae, and they are abundant

throughout the Brazilian Amazon; however, only the two

largest species have historic economic importance (Da

Silveira and Thorbjarnarson 1999; Rebelo and Magnusson

1983; Smith 1981). The black caiman (Melanosuchus

niger) can reach [4.5 m in total length (TL), and the

spectacled caiman (Caiman crocodilus crocodilus) can

reach approximately 2 m TL. The largest populations of

both species occur in the varzea-flooded habitats formed

by Andean rivers, such as the Solimoes and Purus rivers

(Da Silveira et al. 2008).

Although there has been considerable attention devoted

to determining Hg concentrations in fish, turtles, and

humans (Belger and Forsberg 2006; Malm et al. 1995;

Schneider et al. 2009, 2010, 2011; Silva-Forsberg et al.

1999), no data have been published concerning Hg con-

centrations in caimans of the Amazon. This is remarkable

given that caimans are top carnivores, Hg concentrations

are expected to be high, and humans are consuming them.

In this article, we report concentrations of heavy metals

in muscles of two species of crocodilians: the black caiman

(M. niger) and the spectacled caiman (C. c. crocodilus)

from the lower Rio Purus. We were interested in testing the

null hypothesis that there was no difference in Hg con-

centrations between different size classes nor sex bias.

Furthermore, we calculated safe consumption limits for

caiman meat based on fish consumption advisories to

determine if Hg concentrations were high enough to put

consumers of caiman meat at a health risk related to dietary

Hg exposure. These data are pertinent to health issues in

the Rio Purus Basin, which has the highest trade in caiman

meat in Latin America.

Materials and Methods

The Rio Purus is approximately 3000 km long with head-

waters located in the Peruvian Andes that drain into the Rio

Amazonas, 186 km downstream from Manaus, the capital

of the Amazonas State, Brazil (Fig. 1). Most of the lower

Rio Purus Basin is occupied by the Piagacu-Purus Sus-

tainable Development Reserve and two Indian Territories

covering 1,008,167 ha (De Deus et al. 2003). This region

incorporates a large interdigitated mosaic of unflooded

(terra firme) and annually flooded forests inundated by

white (varzea) or black water (igapo). The study area

incorporated a large confluence of floodplain forests under

the influence of both the Rio Amazonas and Rio Purus. The

hydrology of the landscape defines a geochemical mosaic

across the study area and is the primary mechanism to

which this large-scale natural forest mosaic can be attrib-

uted (Haugaasen and Peres 2006).

We collected data from caimans in two different field

studies. The first was from field work throughout 2006,

2007, and 2009 along with the activities of local fisherman

in the Rio Purus. We measured the snout-vent length (SVL)

of live or dead caimans that were being processed to be

Arch Environ Contam Toxicol (2012) 63:270–279 271

123

sold in local markets or transported for commercialization

in big cities of the Amazon area. Our goal was to know the

sizes of caiman that were collected in the Rio Purus to be

traded in the Amazon. We did not collect samples for Hg

analysis at this time because there were no facilities to keep

samples frozen.

The second study was conducted with the goal of col-

lecting samples for the Hg analysis. This second field work

was part of the Bajaquel Project, which had the objective to

develop new technologies for the sustainable management

of caimans. This study was conducted in March and August

2008, corresponding to the midterm of the rising water

season and the end of the rainy season, respectively.

The caimans were captured at night using locking cable

snares and Ketch-all animal restraint poles (IBM, Uni-

versity of Canberra, Canberra, ACT, Australia) (Da

Silveira et al. 1997). They were transported to the Bajaquel

Project floating base where the animals were measured and

killed for the collection of samples for different studies,

including Hg analysis.

Muscle tissue samples of approximately 4 cm3 were

collected from the dorsal part of the tail. This area was

chosen because it is the part of the animal generally used

for human consumption. Each sample was labeled, stored

in plastic bags, and frozen until analysis 6 months later.

Samples were analyzed for Hgtot (organic ? inorganic

Hg) in the Laboratorio de Biologia Ambiental at the Uni-

versidade do Oeste do Para in Santarem, Brazil. Digestion

was performed in tubes washed in 10 % HNO3 solution

and rinsed with deionized water. A 300- to 400-mg sample

was added into a mixture of HNO33 and HCl 6 mol L-1

(10:1, v:v) and heated to 120 �C for 4 h (Malm et al. 1989).

Hgtot concentrations were determined by cold vapour

atomic fluorescence spectroscopy. National Research

Council of Canada–certified reference materials TORT-2

and DORM-2 were used to assess the accuracy of the

method. Concentrations are reported in lg/kg (ppb) on a

wet-weight basis.

The sizes of the caimans were expressed by the SVL

instead of TL (generally double the SVL) because of

injuries that resulted in losing the tip of their tails and

because somatic mass can vary during the seasonal

hydrological pulse.

All statistical analyses used the software PASW sta-

tistics 18. A normality test was performed to determine

whether our data set was modeled by a normal distribu-

tion. To check if the caimans’ lengths were representative

of the caimans used for trade, Student t test was per-

formed using SVL of the caimans. Because Hg data were

not normally distributed, Mann–Whitney test was used to

test for intraspecific and sex-linked differences of Hg

concentration levels. A simple regression was used to

analyze the relation between Hg concentrations and size

of the caimans.

To understand potential human health risks from the

consumption of Hg-contaminated caiman meat, we calcu-

lated the risk-based consumption limits of meat for human

beings. Because no limit of Hg concentration consumption

has been recommended for reptile meat, we used terms

developed for evaluating fish tissue (United States Envi-

ronmental Protection Agency [USEPA] 2000).

We used Eq. 1 from the USEPA (2000) developed for

fish, according to the study performed by Green et al.

(2010), for our calculations. The USEPA characterizes an

analysis by the United States Food and Drug Administra-

tion (USFDA) as follows:

Fig. 1 Location of the Rio

Purus with the Brazilian

location on the right corner

(inset). The study area is circled

in black, and the city of Manaus

is circled in white (main figure)

272 Arch Environ Contam Toxicol (2012) 63:270–279

123

CRlim ¼ RfD� BWð Þ=Cm; ð1Þ

where CRlim = maximum allowable consumption rate (kg/

day), RfD = reference dose (1 9 10-4 mg/kg/day for Hg),

BW = consumer body weight (kg), and Cm = Hg tissue

concentration (mg/kg).

From this, the weekly consumption limit was calculated

using Eq. 2:

CRmm ¼ ðCRlim � TapÞ=MS, ð2Þ

where CRmm = maximum allowable consumption rate

(meals/month), Tap = time averaging period (365.25 days/

12 months = 30.44 days/month), and MS = meal size

(kg).

These limits were calculated using an adult consumer

body mass of 70 kg and an average meal size of 0.200 kg.

Results

Caiman Size

We measured 235 C. c. crocodilus (181 male and 54

female animals) and 113 M. niger (41 male and 70 female

animals) that were being transported from Rio Purus to

larger cities down the Rio Amazonas for illegal trade. The

size of C. c. crocodilus collected for trade ranged from 59

to 115 cm SVL (�x = 89.69 cm; SD = 12.820), and the

size of M. niger specimens ranged from 63 to 140 cm SVL

(�x = 100.80 cm; SD = 16.741).

For Hg analysis, we collected 10 C. c. crocodilus

(6 male and 4 female animals) with SVL measurements

ranging between 62 and 98 cm (mean 75.4 ± 12) and

11 M. niger (6 male and 5 female animals) between 75.3

and 190.9 cm (mean = 107.5 ± 31.44).

The C. c. crocodilus specimens collected for Hg ana-

lyzes were significantly smaller than the animals being

used for trade: t(252) = -3.466, p = 0.00) (Fig. 2a), with

the specimens for Hg analysis being shorter. The M. niger

collected for Hg analysis were similar in size to the animals

being used for trade: t(121) = 1.119, p = 0.065 (Fig. 2b).

Hg Concentrations and Biological Correlates

Hg tot concentration in C. c. crocodilus ranged between

63.2 and 680.6 lg/kg (�x = 291.2 ± 212.8). Individuals

with SVL \80 cm had a great variation in Hg concentra-

tion, whereas larger male and female individuals presented

a lower Hg concentration than smaller male animals

(Fig. 3a). Hg concentration in M. niger ranged from 69.4 to

406.6 lg/kg (�x = 193.9 ± 96.2; Fig. 3b). There was

no significant difference in Hg concentration between

C. c. crocodilus and M. niger U(20) = 43, Z = –0.845

p = 0.398; Fig. 4). Hg concentration cannot be predicted

from C. c. crocodilus SVL (p = 0.519), but it can be

predicted from the size of M. niger (p = 0.013 r2 = 0.514;

Fig. 3).

Calculation of Risk-Based Consumption Limits

From the calculation of risk-based consumption limits, we

determined the threshold for Hg concentration consump-

tion per day, meals per month, and concentrations per meal

in a particular period. A person with a body weight of

70 kg can safely consume 0.024 kg C. c. crocodilus meat

per day. Considering that this person eats a meal size of

200 g of meat, 3.65 meals per month would be the safe

limit for this person. A person with a body weight of 70 kg

can safely consume 0.036 kg of M. niger meat per day.

Considering a meal size of 200 g of meat, a person can

safely consume 5.48 meals per month.

Fig. 2 Boxplot showing SVL (cm) of caimans collected for

Hg analysis in 2008 (Hg) and caimans collected for trade in

2006, 2007 and 2009 (Trade) in the Purus River, Brazilian Amazon.

a C. c. crocodilus. b M. niger

Arch Environ Contam Toxicol (2012) 63:270–279 273

123

Discussion

Size of Caiman for Hg Analysis 9 Size of Caiman

for Trade

One of the objectives of this study was to determine if Hg

concentration in caiman from Rio Purus used for trade pose a

possible health risk for people consuming them. To do this,

we compared the sizes of the caimans collected by fishermen

and the sizes of caiman we collected for Hg analyses. We

strived to have similar sizes between samples so that our

caiman sizes used for Hg analysis would be representative of

the caiman traded in the Amazon. There was no significant

difference in size between M. niger measured from trade

samples and the ones measured from Hg analyses samples.

Thus, our data for Hg analysis reflected what people are

consuming (Fig. 3). Yet, the size of the C. c. crocodilus used

for trade was significantly larger than the ones used for Hg

analysis. However, because there was no relationship

between size and Hg concentration of C. c. crocodilus, our

data might be representative of the amounts of Hg that people

are ingesting when consuming C. c. crocodilus meat.

Although we reported the Hg concentrations from sizes of

caiman traded in the Amazon, more studies are necessary to

include older individuals to gain a better understanding of

bioaccumulation and biomagnification of Hg in these two

species.

Hg Concentration Versus Caiman Size and Sex

Because Hg is well known to accumulate with age in a

number of vertebrates (Burger 1992; Burger and Gochfeld

1997; Park and Curtis 1997), and knowing that caimans are

a top-level predators species, a relationship was expected

between size and Hg for both species. In this study, a

correlation between Hg concentration and size was found

only for M. niger but not for C. c. crocodilus.

Diet may be the cause for the lack of relationship between

C. c. crocodilus Hg concentration and size. Several species

of crocodilians include more terrestrial vertebrates, espe-

cially mammals, in their diet when they attain large sizes

(Blomberg 1977; Giles and Childs 1949; Medem 1981;

McNease and Joanen 1977; 1979). C. c. crocodilus could be

feeding more on terrestrial vertebrates when they are adults,

which would explain why Hg concentrations were the same

or greater in smaller individuals. In the Pantanal region,

C. c. crocodilus presented a correlation between length and

total Hg concentrations but only in specimens captured in

sites with anthropogenic influences (Vieira et al. 2011).

Caimans in the sites where human activities were not intense

Fig. 3 Hg concentration in muscle (lg/kg) and SVL (cm) of

C. c. crocodilus (a) and M. niger (b) sampled in the lower Rio

Purus. Each point represents an individual

Fig. 4 Boxplots showing mean, quartiles, and minimum and

maximum observations for Hg concentration levels in muscle of

C. c. crocodilus and M. niger collected in the Rio Purus Basin,

Amazonia, Brazil

274 Arch Environ Contam Toxicol (2012) 63:270–279

123

(such as the Purus area) presented no significant correlation.

The feeding activity of this species in the Pantanal region is

governed by its habitat instead of its size (Santos 1997).

Studies found a positive correlation between Hg concentra-

tion and size in Alligator mississippiensis (Burger et al. 2000;

Rumbold et al. 2002), but other studies found no relationship

between these two variables (Elsey et al. 1999; Jagoe et al.

1998; Ruckel 1993). Yanochko et al. (1997) found a positive

correlation in A. mississippiensis from Florida but no cor-

relations in the ones from Par Pond, South Carolina. These

conflicts in relationship between Hg concentration and alli-

gator size can be a result of Hg source variations among the

areas studied. In our study, larger sample sizes and larger

individuals must be analyzed to make any assumptions.

In the Amazon, there is a lack of studies on diet of

caimans. Only two studies have reported gut contents of

caimans in the area (Da Silveira and Magnusson 1999;

Horna et al. 2003) and the only reasonable conclusion is

that larger caimans feed on larger prey. There are no data

about frequency of feeding on aquatic and terrestrial spe-

cies of different ages. It is necessary to know both seasonal

and age variations in caiman diets.

It is important to note that the sizes of caiman collected

in this study were not representative of old individuals.

M. niger can reach [4.5 m TL (Da Silveira et al. 2008),

whereas our specimens ranged between 75 and 190.9 cm

(mean 104.5). C. c. crocodilus can reach approximately

2 m in total length (Da Silveira et al. 2008), and our spec-

imens ranged from 62 to 98 cm (mean 75.4). As reported by

Jagoe et al. (1998), there may be dietary differences among

larger, older, and more solitary individuals that result in a

lack of a relationship between Hg in tissues and size. This

observation also suggests that relationships between size and

Hg concentration determined for one size class or location

may not be broadly applicable to other size classes or sites.

We expected to find a difference in Hg concentrations

between male and female individuals. Adult female alli-

gators might exhibit lower levels of contaminants than male

alligators because some reptiles eliminate Hg when eggs are

laid (Delany et al. 1988). However, the difference in Hg

concentration between male and female animals in this

study was not significant. Our data corroborate that for other

species, such as A. mississippiensis (Elsey et al. 1999;

Ruckel 1993; Yanochko et al. 1997), Crocodylus nitolicus

(Almli et al. 2005), C. c. yacare (Vieira et al. 2011)

C. moreletii, and C. acutus (Rainwater et al. 2007). These

alligators could be eliminating Hg from the body tissues at

greater rates reaching equilibrium with ingested Hg.

Hg Concentration Versus Caiman Species

C. c. crocodilus, despite its smaller size, had greater con-

centration of Hg than M. niger. Because M. niger reaches a

larger size than C. c. crocodilus and consequently greater

food consumption, a greater concentration of Hg in

M. niger than C. c. crocodilus was expected. However, the

diet of M. niger in the Rio Purus could be based on ter-

restrial invertebrates or vertebrates in greater proportion

than C. c. crocodilus. That is the case for the Rio Negro

Basin. Terrestrial invertebrates, crabs, and molluscs were

the most frequent categories of prey and were responsible

for 99.5 % of the total mass of M. niger stomach contents

(Da Silveira and Magnusson 1999). However, the sample

included only subadults (15 to 95 cm). Nothing is known

about the diet of the caimans in the Rio Purus specifically.

To evaluate the extent of Hg bioacumulation in these

Amazonian populations, comparisons with other crocodil-

ians species from other parts in the world are listed in

Table 1. There is a paucity of literature regarding Hg

levels in Brazilian caimans: The only study known is of

C. c. yacare in the Pantanal biome (Vieira et al. 2011).

The Hg concentrations for C. c. crocodilus in the

Amazon were similar to those found in C. c. crocodilus in

the Pantanal, a foodplain area located south of the Amazon

in central-west Brazil. Pantanal area, as in the Amazon, has

records of gold mining activities (Lacerda et al. 1991a,

1991b), but they are more restricted and localized.

Among the levels found in worldwide species, M. niger and

C. c. crocodilus presented a concentration high enough to

identify the Purus area as a possible hotspot area for Hg bio-

accumulation. As far as we know, there is no record of mining

activities along the Rio Purus, but this river flows parallel and

close to the Rio Madeira, which has been greatly impacted by

alluvial gold extraction, agriculture, and a hydrolectric res-

ervoir (Dorea and Barbosa 2007). Regarding the Pantanal

biome, how Rio Purus Hg levels link to anthropogenic or

natural processes has yet to be established (Vieira et al. 2011).

We cannot identify if the high Hg concentration in caimans is

related to natural Hg occurring within the basin or if it comes

from the anthropogenic activities in the surrounding area. It is

highly important to study the Hg sources in the Rio Purus, as

well as the local biogeochemical variables influencing meth-

ylation processes, to understand the Hg bioaccumulation in

these caimans.

Health Risk to Human Consumers

Because national or international standards for Hg in rep-

tile meat are still missing, in this study we used the

Brazilian Health Ministry and the World Health Organi-

zation (WHO) consumption limit established for fish flesh

(Brasil 1975; WHO 1976, 1990) of 500 lg/kg. Most of the

caimans in this study had concentrations lower than the

maximum allowable level of 500 lg/kg Hg as recom-

mended WHO (1976) and by the Brazilian Health Ministry

(Brasil 1975). However, two specimens of C. c. crocodilus

Arch Environ Contam Toxicol (2012) 63:270–279 275

123

had Hg levels greater than the maximum criterion level of

500 lg/kg.

Although the mean Hg concentrations for the two cai-

man species were lower than the maximum allowable level

of 500 lg/kg Hg, the most reasonable way to check for Hg

concentrations that can pose a health risk for people con-

suming them is by considering that continuous ingestion of

Hg by the organism will depend on caiman Hg concen-

tration and ingestion rate. Frequent consumption of cai-

mans with Hg concentrations reported in this study is likely

to put consumers at risk for harmful health effects.

Therefore, in this study we measured the ingestion in

terms of meals per month (200 g caiman/meal) for a person

weighing 70 kg according to the acceptable daily intake

concentration of 0.4 lg/kg/day established by the USFDA.

We used for this study a meal size of 0.200 kg as used by

Padovani et al. (1996) to determine the average meal size for

fish. This threshold of 3.65 meals/month calculated for C. c.

crocodilus and 5.48 meals/month for M. niger is especially

important for pregnant women because the developing fetus

is sensitive to Hg’s adverse effects at much lower doses than

adults (Committee on the Toxicological Effects of Methyl-

mercury 2000; Schober et al. 2003).

Considering that this study was performed in the Amazon

where many people do not have access to raising animals and

survive on wildlife protein, the frequency of consumption of

caiman is expected to be greater than the threshold limit

calculated in this study. A shortcoming of this study is that

we do not know the approximate frequency of caiman con-

sumption by local people (especially when considering the

consumption of caiman as an illegal activity; people are more

likely to deny their consumption than to tell the truth), which

precludes us from identifying the potential health risk of Hg

for the local human population. Our point is that the potential

to consume contaminated caimans exists and poses a clear

threat to the health of human consumers.

Health Risk to Caimans Themselves

Levels of Hg in the Rio Purus do not appear to be a threat

to the caiman themselves. Heaton-Jones et al. (1997)

evaluated histopathological material from farm-raised and

wild-caught alligators from the Florida Everglades, which

included some of the highest Hg levels reported to date

(Rumbold et al. 2002). However, no evidence of neruro-

logic, hepatic, or renal toxicosis was observed. Peters

(1983) performed a short-term controlled-dosing study on

20 juvenile alligators (ranging from 95 to 140 cm and

estimated to be approximately 3 to 4 years of age) and

found no clinical or gross pathology attributed to Hg

exposure in any of the animals. The concentration dose

applied in the previously mentioned study was 191 lg/kg,

which remained increased for the duration of the study and

reached 275 lg/kg at the end of the study. The Hg con-

centration in caimans from this study are similar to those

found in the animals under Hg-dose control. However,

because information is lacking on the effects of heavy

metals on crocodilians, it is difficult to speculate on the

biological significance of these concentrations. Data on the

health of caimans in the present study have not been

evaluated, but no gross evidence of problems was observed

at capture or during necropsies (Ronis da Silveira [personal

communication]). Controlled laboratory studies and further

investigations concerning heavy-metal effects on caimans

in the Amazon are needed, especially considering that Hg

in this area is not only from an anthropogenic source but

Table 1 Mean total Hg

concentrations (lg/kg wet

weight) in six species of

crocodilians reported in the

literature

a Original data reported as dry

weight. For this table, they were

divided by a factor of 3.8 (the

wet-to-dry weight ratio

calculated by Jeffree et al. 2001)

for comparison

Species Hg concentration Location Investigator and year

Crocodyilus porosus \0.01 Alligator Rivers Region, Australia Jeffree et al. (2001)a

A. mississippiensis 62.5 Florida, USA Burger et al. (2000)

A. mississippiensis 131 South Louisiana, USA Elsey et al. (1999)

C. c. yacare 145 Pantanal, Brazil Vieira et al. (2011)

M. niger 193 Amazonia, Brazil This study

A. mississippiensis 210.5 Okefenokee, Georgia, USA Jagoe et al. (1998)a

C. c. crocodilus 291 Amazonia, Brazil This study

A. mississippiensis 305 Florida, USA Delany et al. (1988)

A. mississippiensis 316 Florida Everglades, USA Rumbold et al. (2002)a

A. mississippiensis 385 Florida Everglades. USA Jagoe et al. (1998)

A. mississippiensis 480 Georgia. USA Ruckel (1993)

A. mississippiensis 486 Central Florida, USA Jagoe et al. (1998)

A. sinensis 508 Changxing County, China Xu et al. (2006)

A. mississippiensis 1073 Par Pond, South Carolina Yanochko et al. (1997)a

A. mississippiensis 1271 South Carolina, USA Jagoe et al. (1998)

A. mississippiensis 1447 Florida Everglades, USA Yanochko et al. (1997)a

276 Arch Environ Contam Toxicol (2012) 63:270–279

123

also of natural origin. Caimans have faced this high level of

Hg over the long term and could be adapted to face such

high levels of Hg in the future.

Conclusion

Caimans are excellent indicators of metal contamination in

aquatic systems in the Amazon because they are long-

lived; they occur in aquatic systems where Hg often

accumulates; and they are top-level predators. There was

no correlation between body size and Hg concentration for

C. c. crocodilus; however, there was a correlation for

M. niger, perhaps because of diet differences. The caiman

samples used for Hg analysis were representative of the Hg

concentrations amounts that people are consuming. Most of

the caimans in this study had concentrations lower than the

maximum allowable level of 500 lg/kg Hg recommended

by the WHO and by the Brazilian Health Ministry. How-

ever, considering that this study was performed in the

Amazon where many people do not have access to raising

animals and survive on wildlife protein, the frequency

consumption of caiman is expected to be greater than the

threshold limit calculated in this study according to the

acceptable daily intake concentration of 0.4 lg/kg/day

established by the USFDA. Hg concentrations in caimans

from this study are similar to those found in animals under

Hg-dose control, which resulted in no side effects. No gross

evidence of problems was observed at capture or during

necropsies of caimans in this study. Among the levels

found in worldwide species, M. niger and C. c. crocodilus

presented an Hg concentration high enough to identify the

Purus area as a possible hot spot for Hg bioaccumulation.

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