Arch. Environ. Contam. Toxicol. 42, 319 –324 (2002)
DOI: 10.1007/s00244-001-0020-7
A R C H I V E S O F
Environmental
Contamination
a n d Toxicology
© 2002 Springer-Verlag New York Inc.
Mercury in Morelet’s Crocodile Eggs from Northern Belize
T. R. Rainwater,1 B. M. Adair,1 S. G. Platt,2 T. A. Anderson,1 G. P. Cobb,1 S. T. MCMurry1
1
The Institute of Environmental and Human Health, Department of Environmental Toxicology, Texas Tech University, Box 41163, Lubbock, Texas
79409-1163, USA
2
Wildlife Conservation Society, P.O. Box 1620, Phnom Penh, Cambodia
Received: 2 August 2001 /Accepted: 24 October 2001
Abstract. Recent studies have examined mercury accumulation in crocodilians. However, though most researchers have
focused on tissue concentrations, few have examined mercury
levels in crocodilian eggs. In July 1995, we analyzed mercury
in 31 nonviable Morelet’s crocodile (Crocodylus moreletii)
eggs collected from eight nests across three localities in northern Belize. All eggs were found to contain mercury. Based on
an individual egg basis, mean concentration of mercury for all
three localities was among the lowest reported for any crocodilian species. When localities were examined separately,
mean concentrations for Laguna Seca and Gold Button Lagoon
were comparable to those observed in other studies, and the
mean for Sapote Lagoon was the lowest ever reported. Based
on mean nest concentrations, mercury in eggs from Laguna
Seca was approximately two- and tenfold higher than for Gold
Button Lagoon and Sapote Lagoon, respectively. Variability in
mercury concentrations among localities is likely the result of
site-specific differences in mercury input, bioavailabilty, and
bioaccumulation. Mercury concentrations were relatively uniform in eggs from the same nest and among nests from the
same localities. The presence of mercury in Morelet’s crocodile eggs suggests exposure in adult females, developing embryos, and neonates. However, crocodiles in these areas show
no overt signs of mercury toxicity, and no indication of population decline is evident. A paucity of data on the effects of
mercury on crocodilians precludes meaningful speculation as
to the biological significance of tissue and egg concentrations.
Controlled laboratory studies and long-term population monitoring are needed to address these questions.
Over the last decade, studies describing the exposure and
response of crocodilians to environmental contaminants have
increased substantially. This is largely the result of extensive
research showing population declines and reproductive impairment in American alligators (Alligator mississippiensis) inhabiting contaminated lakes in Florida, USA (Jennings et al. 1988;
Correspondence to: T. R. Rainwater; email: thomas.rainwater@
tiehh.ttu.edu
Woodward et al. 1993; Guillette et al. 1994, 1996; Crain et al.
1998), as well as numerous reports of pesticide and polychlorinated biphenyl exposure in various crocodilian species worldwide (Best 1973; Ogden et al. 1974; Vermeer et al. 1974;
Wheeler et al. 1977; Hall et al. 1979; Wessels et al. 1980;
Matthiessen et al. 1982; Phelps et al. 1986, 1989; Delany et al.
1988; Heinz et al. 1991; Skaare et al. 1991; Cobb et al. 1997,
2002; Bargar et al. 1999; Guillette et al. 1999; Wu et al. 2000a,
2000b). Most of these studies have focused on organochlorine
chemicals, but additional concern has been raised concerning
the exposure and impacts of heavy metals, particularly mercury, on crocodilians (Brazaitis et al. 1996, 1998; Brisbin et al.
1998).
Mercury contamination is a global concern (Eisler 1987;
Rudd 1995; Brisbin et al. 1998; Hanisch 1998) and is currently
considered the most serious environmental threat to wildlife in
the southeastern United States (Facemire et al. 1995). Mercury
is introduced into the environment through a variety of natural
and anthropogenic sources (Facemire et al. 1995; Eisler 1987;
Hanisch 1998) and readily accumulates in wildlife (Wolfe et al.
1998). Conditions including low pH and low dissolved oxygen
(Miskimmin et al. 1992; Driscoll et al. 1994) enhance the
formation of methylmercury (the most bioavailable form of
mercury; Surma-Aho et al. 1986; Grieb et al. 1990) in lowland
swamps, rivers, lakes, and other wetlands typically inhabited
by crocodilians (Ruckel 1993; Jagoe et al. 1998), and mercury
is believed to be the heavy metal of greatest concern to these
animals (Brisbin et al. 1998; Burger et al. 2000). Several
researchers have reported mercury levels in crocodilian tissues
(Vermeer et al. 1974; Delany et al. 1988; Hord et al. 1990;
Ware et al. 1990; Yoshinaga et al. 1992; Ruckel 1993; Facemire et al. 1995; Heaton-Jones et al. 1994, 1997; Yanochko et
al. 1997; Jagoe et al. 1998; Brisbin et al. 1998; Rhodes 1998;
Elsey et al. 1999; Burger et al. 2000), but fewer have examined
mercury concentrations in crocodilian eggs (Ogden et al. 1974;
Stoneburner and Kushlan 1984; Phelps et al. 1986; Heinz et al.
1991; Bowles 1996). Because wildlife species are highly sensitive to mercury toxicity during embryonic development and
neonatal life (Eisler 1987; Wolfe et al. 1998), information on
mercury concentrations in eggs is critical when attempting to
ascertain the effects of mercury exposure on developing oviparous organisms.
Morelet’s crocodile (Crocodylus moreletii) is a medium-
320
T. R. Rainwater et al.
sized freshwater crocodile found in the Atlantic and Caribbean
lowlands of Mexico, Guatemala, and Belize (Ross 1998). It is
currently recognized as endangered under the U.S. Endangered
Species Act (Code of Federal Regulations 1977) and is listed
on Appendix I of the Convention on International Trade in
Endangered Species of Flora and Fauna (CITES) (Ross 1998).
By the late 1960s, Morelet’s crocodile was nearly extirpated in
Belize as the result of overharvesting for the commercial skin
trade (Charnock-Wilson 1970; Frost 1974). However, following legal protection under the Wildlife Protection Act of 1981,
populations in northern Belize have made a substantial recovery (Platt 1996; Platt and Thorbjarnarson 2000).
Although Morelet’s crocodile populations in northern Belize
seemingly face no immediate threats (Platt and Thorbjarnarson
2000), exposure to environmental pollutants may present a
subtle yet significant long-term threat to populations in contaminated areas (Gibbons et al. 2000). Wu et al. (2000a,
2000b) found numerous organochlorine pesticides in Morelet’s
crocodile eggs from Belize, many of which are believed to be
linked to reproductive failure in Florida alligators (Guillette et
al. 1994, 1996; Crain et al. 1998). The purpose of this study
was to examine levels of mercury in Morelet’s crocodile eggs
from different localities in northern Belize. We hypothesized
that crocodile eggs from remote areas of Belize would contain
mercury, based on the propensity of mercury to accumulate in
crocodilian habitats and the occurrence of mercury in alligator
eggs collected from remote areas of the southeastern United
States (Ogden et al. 1974; Stoneburner and Kushlan 1984;
Bowles 1996).
Materials and Methods
Fig. 1. Map of Belize showing localities from which Morelet’s crocodile eggs were collected in July 1995 (GB ⫽ Gold Button Lagoon,
LS ⫽ Laguna Seca, SL ⫽ Sapote Lagoon)
Study Sites and Sample Collection
In July 1995, 31 nonviable Morelet’s crocodile eggs were collected
from eight undisturbed, naturally incubating nests found at three
nonalluvial lagoons (Platt and Thorbjarnarson 2000) in northern Belize
(Figure 1). Sixteen eggs were collected from three nests at Sapote
Lagoon (18°19⬘N, 88°33⬘W), located approximately 20 km southwest
of Corozal Town and part of the Ramonal and Sapote Agricultural
Reserve. Twelve eggs were collected from four nests at Gold Button
Lagoon (17°55⬘N, 88°45⬘W), located on a private cattle ranch approximately 25 km southwest of Orange Walk Town. Three eggs were
collected from one nest from Laguna Seca (17°37⬘N, 89°05⬘W),
located on Gallon Jug Farm within the protected Rio Bravo Conservation and Management Area, approximately 90 km west of Belize
City. Nonviable eggs were identified by the absence of an opaque
patch or band on the eggshell (Ferguson 1985), assigned unique
identification numbers, placed on ice for shipment to the United States,
and stored at –20°C until analysis.
Mercury Analysis
Content (shell not included) of each egg was homogenized, and three
aliquots digested for total mercury analysis using the method of Adair
and Cobb (1999). Samples (approximately 0.15 to 0.2 g) were placed
into acid-washed, 8-ml glass vials (loosely capped) and predigested
overnight at room temperature in 1 ml of concentrated acid (1:1 metals
grade HNO3/H2SO4). Next, samples were digested for 2 h in an 80°C
water bath and then placed into a freezer (–20°C) to cool for 10 min.
A total of 200 l of hydrogen peroxide was added to each vial in 25-l
increments over a period of 2 h, after which vials were placed back
into the cooled water bath until the water temperature reached 80°C
(approximately 1 h). Digested samples and three vial rinsates were
filtered through glass fiber filter paper into 10-ml volumetric flasks.
The samples were brought to volume with Milli-Q water and stored in
15-ml centrifuge tubes until analysis. Samples were analyzed by cold
vapor atomic absorption for total mercury (method limit of detection ⫽ 0.05 g/g in a 200 mg egg sample; qualitative range ⫽
0.02– 0.05 g/g). Mean mercury concentrations were expressed as
g/g wet mass.
Results
Mercury was detected in all 31 crocodile eggs examined in this
study. Mean (⫾ SE) concentrations (g mercury/g egg, wet
mass) were based on nest means rather than individual eggs.
Mean concentration of mercury for all localities (n ⫽ 8 nests)
was 0.11 ⫾ 0.05 (range ⫽ 0.02– 0.21). Mean concentrations for
Gold Button Lagoon and Sapote Lagoon were 0.11 ⫾ 0.02
(range ⫽ 0.06 – 0.14, n ⫽ 4) and 0.02 ⫾ 0.01 (range ⫽
⬍0.02– 0.03, n ⫽ 3), respectively, and the concentration for the
single nest at Laguna Seca was 0.21. Although small sample
sizes precluded statistical analysis, some trends in mercury
concentrations among nests and sites were noted. Mercury
Hg in Crocodile Eggs from Belize
levels appeared to be relatively uniform among eggs from the
same nest (although variability increased as concentrations
approached the limit of detection) and, with the possible exception of a single nest at Gold Button Lagoon (GB3), among
nests within each site (Figure 2). Among sites, however, the
mercury concentration for Laguna Seca was approximately
two- and tenfold higher than means for Gold Button Lagoon
and Sapote Lagoon, respectively.
Most reports of mercury levels in crocodilian eggs present
concentrations in individual eggs or means based on individual
eggs. For comparative purposes, we calculated means for Morelet’s crocodile eggs examined in this study based on individual eggs as well. Mean concentration of mercury for all localities (0.07 ⫾ 0.01, range ⫽ ⬍0.02– 0.23) was among the lowest
reported for any crocodilian (Table 1), while the levels for
Laguna Seca (0.21) and Gold Button Lagoon (0.11 ⫾ 0.01)
were comparable to those reported in other studies. Mean
mercury concentration for Sapote Lagoon (0.02 ⫾ 0.002) was
the lowest reported for eggs in any species, excluding those
examined by Heinz et al. (1991), in which mercury was not
detected (Table 1).
Discussion
Jagoe et al. (1998) reported considerable variation in mercury
concentrations in alligator tissue among four localities in the
southeastern United States and speculated this to be a reflection
of differences in local and atmospheric mercury inputs as well
as site-specific variations in mercury bioavailability. This is
likely the case in Belize as well. Although the sources of
mercury in crocodile eggs examined in this study are unknown,
we suspect the occurrence of mercury in these wetlands results
primarily from natural processes and atmospheric deposition
(Miskimmin et al. 1992; Driscoll et al. 1994; Rudd 1995),
given the remoteness of the collection sites and relatively few
anthropogenic mercury sources in Belize (Hartshorn et al.
1984). The among-site variation observed in this study may be
an artifact of small sample sizes, but we speculate that any true
site-related differences in egg mercury levels can be attributed
to site-specific differences in mercury input, bioavailability,
and bioaccumulation. Mercury contamination in crocodilian
eggs likely results from maternal transfer. Direct environmental contamination from nest media may be another possible
route of exposure (Sahoo et al. 1996; Linder and Grillitsch
2000), but this process has not been specifically examined. Wu
et al. (2000a) found multiple organochlorine pesticides in Morelet’s crocodile nest material from one of the sites examined in
this study (Gold Button Lagoon), but mercury levels were not
determined.
Although the effects of mercury on mammals and birds are
well documented (Eisler 1987; Wolfe et al. 1998), virtually
nothing is known concerning the effects of mercury on reptiles
(Hall 1980; Wolfe et al. 1998; Linder and Grillitsch 2000).
Indeed, numerous reports of mercury exposure in crocodilians
exist, but most focus primarily on human health hazards related
to the consumption of crocodilian meat (Peters 1983; Delany et
al. 1988; Hord et al. 1990; Yoshinaga et al. 1992; Ruckel 1993;
Elsey et al. 1999). Peters (1983) dosed captive juvenile American alligators with methylmercury chloride (5.0 mg/kg) and
321
Fig. 2. Mean concentrations (⫾ SE, g/g wet mass) of mercury in
Morelet’s crocodile eggs from eight nests in northern Belize. Numbers
above error bars indicate the number of eggs analyzed per nest. GB ⫽
Gold Button Lagoon, LS ⫽ Laguna Seca, SL ⫽ Sapote Lagoon
concluded, “it does appear that the alligator is capable of
carrying such levels without toxic manifestations.” Likewise,
no clinical signs of mercury toxicity were observed in 24
wild-caught alligators from Florida, despite the fact that each
animal contained mercury in various tissues (ranges in ppm wet
mass: tail muscle ⫽ 0.04 – 4.28; kidney ⫽ 0.15– 65.33; liver ⫽
0.14 –99.48) (Heaton-Jones et al. 1997). Burger et al. (2000)
found low concentrations of mercury (similar to those observed
in the present study) in alligator tissues from multiple lakes in
Florida and speculated these levels likely posed no threat to
alligator health. Conversely, Heaton-Jones et al. (1994) found
mercury in optic lobes, optic nerves, and retinas of Everglades
alligators and concluded mercury accumulation in these tissues
was impacting the alligator visual system. However, no clinical
effects were examined. More recently, Brisbin et al. (1998)
reported elevated mercury concentrations (ppm wet mass: muscle ⫽ 3.48, kidney ⫽ 33.55, liver ⫽ 158.85) in a large adult
alligator found dead in a mercury-contaminated pond in South
Carolina. Because these concentrations exceeded mercury levels shown to be lethal in various birds, mammals, and amphibians under laboratory conditions (Wolfe et al. 1998), and due to
the animal’s emaciated condition at the time of death, Brisbin
et al. (1998) suggested this may be the first documented case of
mercury-related mortality in a crocodilian.
Despite numerous reports of mercury in crocodilian habitats,
tissues, and eggs, no clinical effects on crocodilians at the
individual or population levels have been documented. Brisbin
et al. (1998) emphasized the need for controlled laboratory
studies to determine the toxicological impacts of mercury and
other metals on crocodilians and cautioned against attributing
crocodilian mortality or morbidity to these compounds until
such information is available. Similarly, Linder and Grillitsch
(2000) stated, “the presence of a substance in an organism is
not an adverse biological effect in and of itself.” Although
mercury concentrations were found in alligator tissues from the
Florida Everglades, populations there are stable with no indication of decline, suggesting no significant impact on repro-
322
T. R. Rainwater et al.
Table 1. Mercury concentrations (ppm wet mass) in crocodilian eggs
Species
American alligator
(Alligator mississippiensis)
American crocodile
(Crocodylus acutus)
Morelet’s crocodile
(Crocodylus moreletii)
Nile crocodile
(Crocodylus niloticus)
Location
n
Mean (⫾ SE) Mercury
Concentration
Range
Reference
Florida, USA
Florida, USA
South Carolina, USA
4
34
10
0.54 ⫾ 0.06
ND
NR
0.41–0.71
ND
0.01–0.02
Ogden et al. 1974
Heinz et al. 1991
Bowles 1996
5
9
0.09 ⫾ 0.01
0.13 ⫾ 0.01
0.07–0.14
NR
Ogden et al. 1974
Stoneburner and Kushlan 1984
Belize
31
0.07 ⫾ 0.01
⬍0.02–0.23
This study
Zimbabwe
26
0.23 ⫾ 0.03a
Florida, USA
Florida, USA
0.02–0.54
Phelps et al. 1986
a
Based on dry mass.
ND ⫽ Not detected, NR ⫽ Not reported.
duction (Heaton-Jones et al. 1997). Likewise, although virtually every river in coastal South Carolina is contaminated with
mercury (Facemire et al. 1995), alligator population densities
there are equal to or exceed those of other states within the
animal’s range (Rhodes 1998). The limited data from the
present study indicate mercury contamination in Morelet’s
crocodile eggs in northern Belize, suggesting chemical exposure in adult females, developing embryos, and neonates. However, Morelet’s crocodiles in these areas have shown no overt
signs of mercury toxicity (e.g., emaciation, abnormal motor
coordination; Eisler 1987) and no indication of population
decline is evident (Rainwater et al. 1998; Platt and Thorbjarnarson 2000). Because mercury may have latent, chronic effects on wildlife (Eisler 1987; Wolfe et al. 1998), long-term
monitoring and sampling of crocodilian populations are essential for detecting contaminant-induced impacts over time.
In this study, 31 (100%) Morelet’s crocodile eggs from three
localities in northern Belize were found to contain mercury.
This constitutes the first report of mercury in crocodilian eggs
from Central America and, to our knowledge, only the fifth
report of mercury in crocodilian eggs worldwide (4 of 23 extant
species; Ross 1998). Mean concentrations were among the
lowest reported for crocodilians, but certain eggs contained
levels comparable to those observed in other species. However,
a paucity of information on the effects of mercury on crocodilians makes it difficult to speculate on the biological significance of these concentrations (Stoneburner and Kushlan 1984).
Controlled laboratory studies and long-term population monitoring are warranted to fully understand the relevance of mercury in crocodilian eggs and the effects of mercury on crocodilians at both the individual and population levels.
Acknowledgments. We thank Barry Bowen (Gallon Jug) and Robert
Noonan (Gold Button Ranch) for providing access to their property.
We also thank Colin, Mark, and Monique Howells (Lamanai Outpost
Lodge/Lamanai Field Research Center); Bruce and Carolyn Miller
(Wildlife Conservation Society, Gallon Jug); and Robert Noonan
(Gold Button Ranch) for generously providing accommodations in
Belize during this project. Thomas Rhott and Travis Crabtree assisted
in egg collections. This project was supported by Lamanai Field
Research Center, Indian Church, Belize, the Royal Geographical So-
ciety, and U.S. EPA (grant no. R826310 to STM). SGP was supported
by Wildlife Conservation Society. Additional support for TRR was
provided by the ARCS Foundation, Lubbock, Texas.
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