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Nonlinear patterns in mercury bioaccumulation in American alligators are a function of predicted age
Abstract
Mercury is a widespread, naturally occurring contaminant that biomagnifies in wetlands due to the methylation of this element by sulfate-reducing bacteria. Species that feed at the top trophic level within wetlands are predicted to have higher mercury loads compared to species feeding at lower trophic levels and are therefore often used for mercury biomonitoring. However, mechanisms for mercury bioaccumulation in sentinel species are often poorly understood, due to a lack of long-term studies or an inability to differentiate between confounding variables. We examined mercury bioaccumulation patterns in the whole blood of American alligators (Alligator mississippiensis) from a long-term mark-recapture study (1979-2017) in South Carolina, USA. Using a growth model and auxiliary information on predicted age at first capture, we differentiated between age- and size-related variation in mercury bioaccumulation, which are often confounded in alligators due to their determinate growth pattern. Contrary to predictions that the oldest or largest individuals were likely to have the highest mercury concentrations, our best-supported model indicated a peak in mercury concentration at 30-40 years of age, depending on the sex, and lower concentrations in the youngest and oldest animals. To evaluate the robustness of our findings, we re-analyzed data from a previously published study of mercury in alligators sampled at Merritt Island National Wildlife Refuge in Florida. Unlike the South Carolina data, the data from Florida contained minimal auxiliary information regarding age, yet the best supported model similarly indicated a peaked rather than increasing relationship between mercury and body size, a less-precise indicator of age. These findings highlight how long-term monitoring can differentiate between confounding variables (e.g., age and size) to better elucidate complex relationships between contaminant exposure and demographic factors in sentinel species.
... Similarly, marsh periwinkle snails (Littoraria irrorata) dosed with Hg exhibit lower activity levels and reduced speed compared to an unexposed control group (Krull and Newman, 2022). Long-lived apex predators often serve as sentinel species for Hg biomonitoring and evaluating overall environmental health (Lawson et al., 2020), yet the linkages between Hg exposure and movement behavior and home range size in these organisms remains unresolved. ...
... The American alligator (Alligator mississippiensis) inhabits a variety of freshwater and coastal habitats throughout the southeastern United States, and due to their high site fidelity, long lifespan, and high trophic status, alligators serve as bioindicator species for monitoring contaminants within these systems (Milnes and Guillette Jr., 2008;Nifong and Silliman, 2017;Lawson et al., 2020;Kojima et al., 2023). Despite their overall high site fidelity, alligators have been observed to make longrange movements for short periods of time (Joanen and McNease, 1972), likely for foraging or searching for mates. ...
... These findings are not completely unexpected given that we did not find a strong correlation between daily activity and daily distance. Additionally, alligators are territorial and exhibit site fidelity (Fujisaki et al., 2014;Lawson et al., 2020), and based on our results, we suspect that tracked alligators did not move great distances but were instead active within their respective home ranges. Activity data are likely to reflect a range of different behaviors such as moving between basking spots, foraging, and mating. ...
... In addition to licensing fees that subsidize alligator management programs, direct and indirect economic benefits are realized for landowners, guides, and local communities (Louisiana Alligator Advisory Council, 2021;Powell, 2017). Due to their long lifespans (>60 years), high site fidelity, and high trophic status, alligators are an established bioindicator species for monitoring contaminants in aquatic environments (Lawson et al., 2020;Nifong & Silliman, 2017;Rosenblatt & Heithaus, 2011;Wilkinson et al., 2016). These same attributes also convey substantial exposure risks to individuals that consume their meat. ...
... We originally obtained THg concentrations in tail muscle as dry weight (mg/kg), which we converted to wet weight (mg/kg) to account for sample preparation and phase differences (liquid vs. solid) between blood and tail muscle. We used the following formula to estimate the percentage of moisture content (M) for each tail muscle sample (Equation 1; Lawson et al., 2020;Lusk et al., 2005). ...
... Our findings are consistent with Hg being prevalent in aquatic environments throughout the southeastern United States, where consumption of game species harvested through recreational hunting can lead to significant dietary exposures. Prior studies have used blood as a minimally invasive sample to evaluate Hg concentrations in crocodilians (Burger et al., 2007;Eggins et al., 2015;Lawson et al., 2020;Lemaire et al., 2021;Nilsen et al., 2017), and our findings that whole-blood THg concentrations can be used to infer tail muscle THg concentrations are consistent with those studies. For example, Nilsen et al. (2017) observed a similar relationship between concentrations of THg in the blood and muscle of alligators in Florida, and reported that blood concentrations of selenium, rubidium, and zinc are also reflective of those in tail muscle. ...
Mercury is a naturally occurring element but is also considered a widespread contaminant due to global anthropogenic activity. Even in moderate amounts, mercury (Hg) is an established neurotoxin and is associated with a range of adverse outcomes both in humans and wildlife. Humans in the United States are most commonly exposed to Hg through contaminated food or drinking water, and the consumption of game species, particularly those occupying higher trophic levels, has the potential to expose hunters to high concentrations of Hg. In the present study, we determined Hg concentrations in tail muscle and blood from American alligators ( Alligator mississippiensis ) inhabiting a region (Savannah River Site, SC, USA) with known Hg contamination. We then integrated these data with alligator harvest records and previously published surveys of alligator meat consumption patterns to estimate potential exposure risk. We found that the average Hg concentrations in tail muscle (1.34 mg/kg, wet wt) from sampled alligators exceeded the recommended threshold for Hg exposure based on the World Health Organization's guidelines (0.5 mg/kg, wet wt). In addition, based on regional consumption patterns reported for both adults and children, we estimated Hg exposures ( = 0.419 µg/kg/day, = 2.24 µg/kg/day) occurring well above the US Environmental Protection Agency methylmercury reference dose of 0.1 μg/kg/day. Although the two reservoirs sampled in the present study are not currently open to alligator hunting, they are connected to waters that are publicly accessible, and the extent of alligator mobility across these sites is not known. Together, the findings reported in the present study further demonstrate the need for active monitoring of Hg concentrations in game species, which can convey substantial exposure risks to the public. Environ Toxicol Chem 2023;42:525–534. © 2023 The Authors. Environmental Toxicology and Chemistry published by Wiley Periodicals LLC on behalf of SETAC.
... Because of its efficient trophic transfer through aquatic food webs, MeHg constitutes >95% of the total organic mercury in biota with concentrations found in large apex predators that may be millions of times higher than concentrations in surface water (Compeau and Bartha 1985;Lavoie et al. 2013;Wagemann et al. 1998Wagemann et al. , 1997. Such effectual bioaccumulation and biomagnification can result in MeHg accumulating to toxic concentrations in fish and other fish-eating apex predators; the consumption of contaminated fish and wildlife is also a risk for humans, especially exposures occurring during preand perinatal periods of development (Jagoe et al. 1998;Landrigan et al. 2020;Lavoie et al. 2013;Lawson et al. 2020;Nilsen et al. 2017a;Yanochko et al. 1997). Based on the results of numerous studies, the Agency for Toxic Substances and Disease Registry (ATSDR) has established a provisional minimal risk level (MRL) for oral exposure to MeHg of 0.1 mg/kg/day (ATSDR 2022), the US Food and Drug Administration has established a legal action level of 1.0 mg/kg Hg in consumable portions of fish, and the US EPA has set screening values of 0.4 mg/kg and 0.049 mg/kg for fish consumed by recreational and subsistence fishers respectably (Table 1 ( US EPA 2000)). ...
... In crocodilian species the bioaccumulation of anthropogenic toxic metals including Hg has been most well studied in the American alligator (Alligator mississippiensis) of southeastern and south-central United States (Burger et al. 2000;Delany et al. 1988;Elsey et al. 1999;Jagoe et al. 1998;Khan and Tansel 2000;Lawson et al. 2020;Nilsen et al. 2019Nilsen et al. , 2017bRumbold et al. 2002). Along with being a large and long-lived apex and keystone species across its range, American alligators often share rural and urban environments with humans and are important non-migratory sentinels of local adverse impacts from environmental pollutants (Somaweera et al. 2020). ...
... With the exception of the northern most populations of American alligators found in North Carolina, Hg concentrations and potential adverse health impacts of MeHg exposure has been periodically assessed in American alligators (Burger et al. 2000;Delany et al. 1988;Horai et al. 2014;Jagoe et al. 1998;Khan and Tansel 2000;Lawson et al. 2020;Nilsen et al. 2020Nilsen et al. , 2019Nilsen et al. , 2017aNilsen et al. , 2017bRumbold et al. 2002;Yanochko et al. 1997). As is the case elsewhere, Hg is a pervasive pollutant in North Carolina that has resulted in state-wide fish consumption advisories for largemouth bass based upon the presence of unsafe concentrations of Hg. ...
Mercury (Hg) is a widespread and harmful persistent pollutant of aquatic ecosystems. Except for the northern most populations of American alligators (Alligator Mississippiensis) found in North Carolina, the potential adverse health impacts of Hg on ecosystems and humans consuming alligator meat have been studied for over three decades. Now that alligators are being recreationally hunted and consumed across their range, it is especially important to monitor toxic contaminant levels to best understand possible adverse impacts of exposures on alligator populations and human health. In this study, we determined blood Hg concentrations in American alligators from an urbanized site in Wilmington, NC, a nearby site at Lake Waccamaw, NC, and a site on the St Johns River in Florida. Median blood total Hg (tHg) concentrations were particularly high at Lake Waccamaw (526 ng/g, range 152–946 ng/g), resulting in median muscle concentrations (0.48 mg/kg, range 0.13–0.88 mg/kg) well above US EPA screening values for fish consumption. Median concentrations at the Wilmington site (69 ng/g, range 22–336 ng/g) were generally low, and Hg concentrations from the St Johns River site (143 ng/g, range 54–244 ng/g) were comparable to those reported in previous studies. Analysis of relationships between tHg concentrations and a panel of blood chemistry biomarkers found only modest concentration-dependent impact on biomarkers of renal function. The results of this study reveal that local environmental factors greatly impact Hg bioaccumulation in alligators, findings that reaffirm local contaminant biomonitoring in alligator populations will be critical for affective management and determination of guidelines for safe consumption of harvested alligators.
... Because of its e cient trophic transfer through aquatic food webs, MeHg constitutes > 95% of the total organic mercury in biota with concentrations found in large apex predators that may be millions of times higher than in surface water (Compeau and Bartha, 1985;Lavoie et al., 2013;Wagemann et al., 1998Wagemann et al., , 1997. Such effectual bioaccumulation and biomagni cation can result in MeHg accumulating to toxic levels in sh and other sh eating apex predators; the consumption of contaminated sh and wildlife is a potential risk for humans, especially exposures occurring during pre-and perinatal periods of development (Jagoe et al., 1998;Landrigan et al., 2020;Lavoie et al., 2013;Lawson et al., 2020;Nilsen et al., 2017a;Yanochko et al., 1997) In crocodilian species the bioaccumulation of anthropogenic toxic metals including Hg has been most well studied in the American alligator (Alligator mississippiensis) of southeastern and south central United States (Burger et Rumbold et al., 2002). Along with being a large and long-lived apex and keystone species across its range, American alligators often share rural and urban environments with humans and are important non-migratory sentinels of local adverse impacts from environmental pollutants (Somaweera et al., 2020). ...
... ANOVA and Tukey's multiple comparison was used to evaluate differences in SVL between sites, and a Kruskal-Willis test and Dunn's multiple comparison's test was used to evaluate differences individual blood biochemistry endpoints between sites. Estimated tHg concentrations in muscle (mg kg − 1 ) were calculated using the formula and body mass index (BMI) was estimated using the formula (Lawson et al., 2020;Nilsen et al., 2017bNilsen et al., , 2017a. A minimal level of statistical signi cance for differences in values among or between groups was considered p ≤ .05. ...
... In 2018 limited Alligator hunting became legal in North Carolina despite the much lower density of animals compared to populations in more southern states (NCWRC, 2018). To evaluate whether consumption of alligator meat represents a potential threat to consumers we estimated muscle concentrations using previously developed conversion factors that estimate muscles concentrations of tHG in alligator muscle/meat (Lawson et al., 2020;Nilsen et al., 2017bNilsen et al., , 2017a. The calculated average tHg concentrations for the alligators from LW (M = 0.47 mg/kg, SD = 0.23) were found to be well above the US EPA and FDA consumption advisory level for Hg in sh (Table 2 (US EPA, 2022)). ...
Mercury (Hg) is a widespread and potential harmful persistent contaminate of aquatic ecosystems. Except for the northern most populations of American alligators ( Alligator Mississippiensis) found in North Carolina, the potential adverse health impacts of Hg on ecosystems and humans consuming alligator meat has been studied for over three decades. Now that alligators are being recreationally hunted and consumed across their range, it is especially important to monitor toxic contaminant levels to best understand possible adverse impacts of exposures on alligator populations and human health. In this study we evaluated blood Hg levels in American alligators from an urbanized site in Wilmington, NC, a nearby site at Lake Waccamaw, NC, and a site on the St Johns River in Florida. Median blood total Hg concentrations were particularly high at Lake Waccamaw (526 ng/g, range 152–946 ng/g), resulting in median muscle concentrations (0.48 ppm, range 0.13–0.88 ppm) above the US EPA/FDA fish consumption advisory level of 0.3 ppm. Median concentrations at the Wilmington site (69 ng/g, range 22–336 ng/g) were low, and Hg concentrations from the St Johns River site (143 ng/g, range 54–244 ng/g) were comparable to those reported in previous studies. Analysis of relationships between total Hg concentrations and a panel of blood chemistry biomarkers found only modest concentration dependent impact on biomarkers of renal function. The results of this study reveal that local environmental factors greatly impact Hg bioaccumulation in alligators, findings that reaffirm that local contaminant biomonitoring in alligator populations will be critical for affective management and determination of guidelines for safe consumption of harvested alligators.
... Due to the long-term monitoring effort at YWC, we had the unique ability to examine the relationship between Hg concentrations in the maternal female blood and the estimated age and number of nesting years of each female. Estimated age was calculated following the model previously developed for the YWC alligator population (Lawson et al., 2019;Wilkinson et al., 2016). To determine the estimated number of years each female has nested, the estimated age of each female was reduced by 16 (the average age at sexual maturity), and then divided by 2 (two years), the mean nesting frequency for female alligators at YWC (Wilkinson and Rainwater, unpublished data). ...
... Over the three years that nesting female blood and paired egg samples were collected at YWC, nesting females exhibited a mean THg blood concentration of 172 ng/g ± 41 ng/g. This value is similar to those observed in other adult alligators at YWC (Fig. 4, Table S11) (Lawson et al., 2019;Nilsen et al., 2019). While there was inter-and intra-nest variability, the pattern of THg concentrations observed in female blood and yolk THg suggested a consistent amount of THg deposition from maternal females to developing eggs. ...
... Data from long-term alligator research at provided us the ability to estimate the age as well as the number of years (i.e., opportunities to offload Hg) a female may have nested (Lawson et al., 2019;Wilkinson et al., 2016). No statistically significant relationship was observed (r = 0.21; p = 0.44) between age and THg concentrations in nesting females (Tables S2 and S4). ...
American alligators are exposed to mercury (Hg) throughout their natural range and may maternally transfer Hg into their eggs. Wildlife species are highly sensitive to Hg toxicity during embryonic development and neonatal life, and information on Hg transfer into eggs is critical when attempting to understand the effects of Hg exposure on developing oviparous organisms. To examine Hg transfer in alligators, the objectives of the present study were to 1) determine Hg concentrations in yolk (embryonic and neonatal food source) from wild alligator eggs collected from three locations - Yawkey Wildlife Center SC (YWC), Lake Apopka FL (LA), and Lake Woodruff FL (LW); 2) examine the relationship between THg concentrations in wild alligator nest material and egg yolk at Merritt Island National Wildlife Refuge, FL; 3) examine the Hg concentrations in wild maternal female alligators (blood) and the THg in corresponding egg yolks and embryos across three nesting seasons at a single location (YWC), and evaluate the relationship between nesting female THg concentrations (blood) and their estimated age and number of nesting years (YWC); and 4) assess the transfer of biologically-relevant Hg concentrations (based on Hg measured in maternal female blood) into embryos using an egg-dosing experiment. Mean total Hg (THg) concentrations observed at each site were 26.3 ng/g ± 11.0 ng/g (YWC), 8.8 ng/g ± 5.1 ng/g (LA), and 22.6 ng/g ± 6.3 ng/g (LW). No relationship was observed between THg in alligator nest material and corresponding yolk samples, nor between THg in maternal alligator blood and estimated age and number of nesting years of these animals. However, significant positive relationships were observed between THg in blood of nesting female alligators and THg in their corresponding egg yolk. We observed that 12.8% of the maternal blood THg is found in the corresponding egg yolk, and a highly significant correlation was observed between the two sample types (r = 0.66; p < 0.0001). The egg dosing experiment revealed that Hg did not transfer through the eggshell at developmental stage 19. Overall, this study provides new information regarding Hg transfer in American alligators which can improve biomonitoring efforts and may inform ecotoxicological investigations and population management programs in areas of high Hg contamination.
... Mercury, like many other contaminants, bioaccumulates with organismal size and/or age (Haskins et al., 2021a;Lawson et al., 2020;Eggins et al., 2015;Rainwater et al., 2005), and maternal mercury burdens have been shown to, at least in part, be deposited in eggs or otherwise transferred to offspring Scheuhammer et al., 2007). Although much of our current understanding of this phenomenon and its consequences comes from research conducted on birds (Ackerman et al., , 2017Yu et al., 2015;Scheuhammer et al., 2007), maternal transfer of mercury has been demonstrated in numerous herpetofauna as well Lemaire et al., 2021a;Hopkins et al., 2013aHopkins et al., , 2013bChin et al., 2012;Bergeron et al., 2010;Guirlet et al., 2008). ...
... Radionuclide inputs from associated reactors have contributed to the contamination profile of Par Pond (Carlton et al., 1992) but are thought to have minimal consequences for the resident alligator population (Brisbin, 1989;Brisbin et al., 1996Brisbin et al., , 1998. Yawkey is a remote, 6033-ha wildlife management area consisting of three main islands surrounded by brackish and marine habitats (Lawson et al., 2020), and previous research has detected relatively low concentrations of mercury in adult alligator blood (0.1119-0.2535 ppm) and nest material (0.0087-0.0158 ppm) from this site . ...
Mercury is a toxic and pervasive environmental contaminant that can be transferred from mother to offspring during development. Consequences of maternally-transferred mercury have been observed in vertebrate taxa, including reduced clutch viability, reduced offspring size, and behavioral alterations. These sublethal effects have been assumed to decrease survivorship, though this is seldom assessed. Here, we examined how maternally-transferred mercury interacts with incubation temperature to influence reproductive success, offspring behavior, and subsequent survival in the American alligator (Alligator mississippiensis). We collected nine clutches of eggs from a mercury contaminated reservoir on the Savannah River Site, South Carolina, and incubated eggs at either female- or male-promoting temperatures. Clutch-averaged mercury in egg yolk was high relative to other studies in crocodilians and ranged from 0.248 to 0.554 ppm compared to 0.018-0.052 ppm at a site with low levels of mercury contamination; mercury levels in hatchling blood ranged from 0.090 to 0.490 ppm (x¯ = 0.240 ppm, n = 158). We found few, mostly negligible correlations between life history traits and mercury but noted a positive relationship with egg mass, possibly mediated by correlated maternal effects such as resource provisioning. Incubation temperature exerted strong effects on hatchling phenotypes, with warmer, male-promoting temperatures producing larger and bolder hatchlings. Presumptive females, produced from cooler incubation temperatures, spent more time in warm areas during behavior trials. Hatchlings were released 10-15 days post-hatch and surveyed over eight months to assess survival. Survivorship was positively correlated with hatchling size and negatively correlated with proportional time spent in warm areas. Presumptive females had much lower survival, and overall survivorship for the eight-month period was 0.185-0.208, depending on the modelling approach. Our study suggests that, within the range of concentrations we observed, incubation temperature has a stronger effect on offspring behavior and survival than maternally-transferred mercury pollution in American alligators.
... Our sampling area included tidal marsh (2524 ha) and managed impounded wetlands (hereafter impoundments; 1012 ha) in which the salinity ranged from 0 to 35 ppt (Wilkinson et al., 2016). See Lawson et al. (2020) for a complete description. ...
... Captured adults (>180-cm total length [TL]) were uniquely marked using the methods and materials described in Lawson et al. (2020). For individuals >120-cm TL, we determined the sex through cloacal examination (Chabreck, 1963) and recorded two standard body measurements (AE0.5 cm): TL and snout-vent length (SVL). ...
Population models often require detailed information on sex-, age-, or size-specific abundances, but population monitoring programs cannot always acquire data at the desired resolution. Thus, state uncertainty in monitoring data can potentially limit the demographic resolution of management decisions, which may be particularly problematic for stage-or size-structured species subject to consumptive use. American alligators (Alligator mississippiensis; hereafter alligator) have a complex life history characterized by delayed maturity and slow somatic growth, which makes the species particularly sensitive to overharvest. Though alligator populations are subject to recreational harvest throughout their range, the most widely used monitoring method (nightlight surveys) is often unable to obtain size class-specific counts, which limits the ability of managers to evaluate the effects of harvest policies. We constructed a Bayesian integrated population model (IPM) for alligators in Georgetown County, SC, USA, using records of mark-recapture-recovery, clutch size, harvest, and nightlight survey counts collected locally, and auxiliary information on fecundity, sex ratio, and somatic growth from other studies. We created a multistate mark-recapture-recovery model with six size classes to estimate survival probability, and we linked it to a state-space count model to derive estimates of size class-specific detection probability and abundance. Because we worked from a count dataset in which 60% of the original observations were of unknown size, we treated size class as a latent property of detections and developed a novel observation model to make use of information where size could be partly observed. Detection probability was positively associated with alligator size and water temperature, and negatively influenced by water level. Survival probability was lowest in the smallest size class but was relatively similar among the other five size classes (>0.
... While the toxicological risks of Pb to wildlife health are welldocumented for birds (De Francisco et al., 2003;Williams et al., 2017a), relatively few studies have focused on reptiles, despite growing concerns surrounding the impact of anthropogenic pollutants on reptile populations (Dos Santos et al., 2021;Mingo et al., 2016). Crocodilians are especially susceptible to contaminant exposure due to their high trophic status and long lifespan, with various metals having been detected in crocodilians from numerous localities throughout their global range (e.g., Xu et al., 2006;Rainwater et al., 2007;Du Preez et al., 2016;Cedillo-Leal et al., 2018;Lawson et al., 2020). Similar to birds, crocodilians are susceptible to Pb exposure through inadvertent ingestion of pellets, bullet fragments and fishing weights. ...
... Demographic factors such as sex and body size (a proxy for age) are generally known to influence bioaccumulation and untangling these effects can be difficult, particularly in studies that are limited in temporal scope or sample size. Lawson et al. (2020) demonstrated that Hg bioaccumulation in American alligators differed among size classes, with total Hg concentrations peaking in individuals of intermediate size (and age). Male Nile crocodiles reach larger sizes than females and we are unable to account for potential differences in exposure among age classes related to shifts in diet, movement or habitat use patterns. ...
Lead (Pb) exposure is a widespread wildlife conservation threat, but impacts on reptile populations remain poorly documented. In this study, we examined Pb exposure and accumulation in a wild population of Nile crocodiles (Crocodylus niloticus) at Lake St Lucia, South Africa. Recreational angling has occurred in the area since the 1930s and incidental ingestion of Pb fishing weights has previously been identified as a major source of Pb poisoning in the local crocodile population. In 2019, we sampled blood and tail fat tissues from wild (n = 22) and captive (n = 3) crocodiles at Lake St Lucia to investigate potential impacts of chronic Pb exposure on crocodilian health. Lead was detected in blood samples of all wild crocodiles, although concentrations varied widely between individuals (86–13,100 ng ml⁻¹). The incidence of Pb poisoning was higher in male crocodiles, with mean blood lead (BPb) concentrations in males (3780 ± 4690 ng ml⁻¹) significantly (p < 0.001) higher compared to females (266 ± 230 ng ml⁻¹). Blood Pb concentrations were correlated with concentrations measured in tail fat tissue (n.d – 4175 ng g⁻¹ wet wt.). Although most of the crocodiles sampled appeared to be in good physical condition, highly elevated BPb concentrations (>6000 ng ml⁻¹) were associated with markedly suppressed packed cell volumes (4.6–10.8%) and severe deterioration in tooth condition. These findings suggest that anaemia and tooth loss may be clinical signs of long-term environmental exposure to Pb. Although previously undocumented in crocodilians, these symptoms are consistent with Pb poisoning observed in birds and mammals, and suggest that crocodilians may be more susceptible to the long-term toxic effects of Pb than previously thought. In light of these findings, we suggest that the impact of accumulated Pb on crocodilian fitness, reproduction and mortality requires urgent attention.
... While the toxicological risks of Pb to wildlife health are welldocumented for birds (De Francisco et al., 2003;Williams et al., 2017a), relatively few studies have focused on reptiles, despite growing concerns surrounding the impact of anthropogenic pollutants on reptile populations (Dos Santos et al., 2021;Mingo et al., 2016). Crocodilians are especially susceptible to contaminant exposure due to their high trophic status and long lifespan, with various metals having been detected in crocodilians from numerous localities throughout their global range (e.g., Xu et al., 2006;Rainwater et al., 2007;Du Preez et al., 2016;Cedillo-Leal et al., 2018;Lawson et al., 2020). Similar to birds, crocodilians are susceptible to Pb exposure through inadvertent ingestion of pellets, bullet fragments and fishing weights. ...
... Demographic factors such as sex and body size (a proxy for age) are generally known to influence bioaccumulation and untangling these effects can be difficult, particularly in studies that are limited in temporal scope or sample size. Lawson et al. (2020) demonstrated that Hg bioaccumulation in American alligators differed among size classes, with total Hg concentrations peaking in individuals of intermediate size (and age). Male Nile crocodiles reach larger sizes than females and we are unable to account for potential differences in exposure among age classes related to shifts in diet, movement or habitat use patterns. ...
... Water salinity in impoundments ranges from 0 to 35 parts per trillion (ppt), depending on rainfall and water management practices (Wilkinson 1983;Wilkinson et al. 2016). Because of its protected status, YWC has been the site of multiple long-term (.40-yr) studies on alligator reproduction (Wilkinson 1983;McCoy et al. 2015;Zajdel et al. 2019;Bock et al. 2020) and ecotoxicology (Cobb et al. 1997;Bangma et al. 2017;Lawson et al. 2020;Nilsen et al. 2020) in coastal habitats. ...
Among the Crocodylia, maternal females of most species are known to attend their nests during the egg incubation period.
However, the ecological and environmental factors driving nest attendance in these reptiles remain poorly understood. In 2019, we conducted a
study in coastal South Carolina, USA, to examine temporal patterns of nest attendance by American Alligators (Alligator mississippiensis),
investigate the site and environmental factors influencing nest attendance, and characterize behaviors exhibited by attending females. We used
automated game cameras to monitor American Alligator nests throughout the incubation period and collected a suite of physical and
environmental measurements at nest sites and associated habitat. Female attendance was modeled using generalized linear mixed-effects
models with a binomial error distribution. Overall, nest attendance occurred for only a brief portion (1%) of the nesting period. The primary
factors influencing nest attendance were day since oviposition, time of day, rainfall, and distance of nests to nearest water, with most attendance
occurring during the first week postoviposition, at the end of incubation preceding hatchling emergence, at nighttime, shortly following rain
events, and when nests were closer to water. Salinity of nearest water exhibited a weak effect, with the probability of nest attendance slightly
decreasing as salinity increased. Maternal females exhibited four primary behaviors associated with nest attendance: crawling on the nest
(16.2%), guarding the nest from a distance (62.2%), defending the nest (2.5%), and opening the nest and transporting young to water (19.0%),
although temporal and behavioral patterns of nest attendance varied among individual females. At 8 (80%) of 10 nests predated by Raccoons
(Procyon lotor), the maternal female returned and attempted to repair the nest. Nest defense by female American Alligators was low relative to
the number of nest visits by egg and hatchling predators and other mammals. Collectively, our study reveals both environmental and nest site–
level factors influence female nest attendance and, more broadly, demonstrates the importance of spatial and temporal scales of observation in
studies of crocodilian maternal care.
... Secondly, for mothers, maternal transfer presents a potentially relevant pollution offloading route. Such offloading can decrease the concentration of pollutants in females and contribute to explain differences in body burdens of some pollutants between males and females (Humphries et al., 2021), although other processes also contribute to these differences such as differences in metabolic rates, lipid storage and allocation, and habitat usage as observed in wildlife (Binnington and Wania (2014), Lawson et al. (2020)) and humans (Salihovic et al., 2012). Finally, for egg predators, this might lead to a source of dietary exposure (Warwick et al., 2013). ...
We aimed to address two common challenges for scientists working with observational data: ''how to quantify the relationship between two observed (or measured) variables'', and, ''how to account for censored values'' (i.e., observations or measures whose value is only known to fall within a range). Quantifying the relationship between observed variables, and predicting one variable from the other (and vice versa), violates the assumption of standard regression regarding the existence of an independent, explanatory variable that is observed with no (or limited) uncertainty. To overcome this challenge, we developed and tested a Bayesian error-in-variables, EIV, regression model which accounts for uncertainty in variables orthogonally. Moreover, parameter estimation using Bayesian inference allowed the full parameter uncertainty to be propagated into probabilistic model predictions suitable for decision making. Alternative model formulations were applied to a dataset containing measured concentrations of organic pollutants in mothers and their eggs from the freshwater turtle Malaclemys terrapin and validated against an independent dataset of the turtle Chelydra serpentina. The best performing EIV model was then applied to the dataset again after censoring measurements in one or both variables. Here, independent likelihoods for both censored and uncensored data were formulated and then easily combined following the Bayesian implementation of the model. The EIV model performed well, as revealed by posterior predictive checks around 85%, and obtained comparable parameter estimates in both censored and uncensored cases. The resulting model allows scientists and decision-makers to quantitatively link variables, and make predictions from one variable to the next while accounting for uncertainties and censored data.
... We divided tortoises into juvenile and adult classes by size; we did not separate adults further by relative age (young, middle-aged, old) or size. The complexity of age in bioaccumulation is exemplified by a long-term, mark-recapture study of Hg in American alligators, Alligator mississippiensis (68). The accumulation of Hg peaked at an age of 30 to 40 years and was lower in young and old individuals. ...
Background
Desert tortoise (Gopherus agassizii) populations have continued to decline due to infectious and other diseases, predation, and habitat alteration. The potential contribution of minerals and heavy metals to tortoise health and susceptibility to disease remains uncertain.
Objective
The objective of this study was to evaluate the results of elemental analysis on trace minerals, macrominerals, and heavy metals in scute keratin, kidney, and liver from ill and dying desert tortoises salvaged for necropsy between 1993 and 2000.
Methods
Salvaged tortoises were categorized by size (adult, juvenile), geographic location, and primary disease based on necropsy findings. A subset of tortoises that were injured or killed by vehicular trauma or predation but with no notable pathologic abnormalities was used for comparison with diseased tortoises. The panel of elements was analyzed in scute keratin, kidney, and liver samples by inductively-coupled plasma spectrometry and atomic absorption spectrophotometry.
Results
Necropsies were done on 46 tortoises, including 9 juveniles, salvaged from 5 regions in the Colorado and Mojave Deserts of California. Primary diseases were cutaneous dyskeratosis (n = 9), infection/inflammation (n = 8), malnutrition (n = 7), mycoplasmosis (n = 5), and urolithiasis (n = 3); 14 tortoises died of trauma. Concentrations of elements differed by tissue, size, desert region, and disease status (p < 0.05). Tortoises with cutaneous dyskeratosis had higher Se concentrations, primarily in keratin and liver, than tortoises with other diseases (p < 0.001). Juveniles were more likely than adults to have high Pb, Sn, and Zn levels (p < 0.05). All tortoises had detectable levels of more than one potentially toxic heavy metal, including As, Cd, Cr, Hg, Ni, Pb, Sn, and V.
Conclusion
Potentially toxic elements are frequently found in tissues from tortoises in desert regions of California, with higher concentrations in diseased tortoises. Metal exposure from soils, mining, historic and ongoing military activities, and other human activities could increase susceptibility to disease in desert tortoises.
... Size is often used as a proxy for age in fish (Bermejo, 2007;Coggins et al., 2013), but little is known about the ages of wild plethodontid salamanders. Age impacts Hg bioaccumulation in other taxa (see Lavigne et al., 2010;Lawson et al., 2020;Sandheinrich & Drevnick, 2016), so it may affect Hg concentrations in salamanders as well. Snout-vent length was not related to δ 15 N or δ 13 C in E. bislineata, so size is not influencing the prey types that these salamanders are consuming. ...
Salamanders serve as bioindicators of mercury (Hg) in both terrestrial and aquatic habitats and are an important link in the food web between low‐trophic prey and higher‐trophic predators. We investigated the drivers of methylmercury (MeHg) exposure in three common plethodontid salamander species in New York State, USA, including comparisons among regions, habitat types (terrestrial and semiaquatic), and color morphs of Plethodon cinereu s (striped and unstriped). Nonlethal tail samples were collected from one terrestrial species ( P. cinereus ) and two semiaquatic species ( Eurycea bislineata and Desmognathus spp.) in the Adirondack Mountains (ADK) and the Finger Lakes National Forest (FLNF) regions. Samples were analyzed for MeHg and stable isotopes, including δ ¹⁵ N and δ ¹³ C which are proxies of trophic position and diet, respectively. Despite elevated biota Hg concentrations typically found in the ADK, salamander MeHg concentrations did not differ by region in the terrestrial species and one of the semiaquatic species. In addition, diet and trophic level did not explain MeHg exposure in salamanders. Semiaquatic salamanders exhibited higher MeHg concentrations than terrestrial salamanders in the FLNF only. Within species, only snout–vent length predicted MeHg concentrations in E. bislineata with few other variables significant as predictors of MeHg concentrations in path models. Among P. cinereus individuals in the FLNF, the striped morph had greater MeHg concentrations than the unstriped morph, and food web tracers were not different between morphs. Overall, New York State salamander Hg concentrations were elevated compared to other locations where these species are present. The present study establishes baseline Hg data in salamanders for future assessments of changes in Hg bioavailability to forests of New York State. Environ Toxicol Chem 2024;00:1–13. © 2024 SETAC
... Among the elements in all age groups, a positive correlation was observed between mercury and the risk of noncarcinogenicity, and this relationship was a negative correlation for body weight. Lawson et al.'s study in 2020 also showed that mercury bioaccumulation in the body of people in Florida was inversely related to body size (Lawson et al., 2020). Carcinogenesis risk assessment also confirmed that consumption rate was the most influential parameter and negatively correlated with body weight (Fig. 6). ...
... Some studies on the effects of age using body length as a proxy for bioaccumulation of Hg in crocodilians have shown that larger animals have higher concentrations in tissues than smaller ones, such as in muscle, liver, and blood of the caiman Melanosuchus niger in the Amazon (Eggins et al., 2015;Schneider et al., 2013). However, middle-aged Alligator mississippiensis exhibited higher Hg concentrations in whole blood than younger and older animals at the same study site, contrary to bioaccumulation predictions (Lawson et al., 2020). Sex, in turn, seems to be a factor that directly influences Hg concentrations in American alligators, with females losing up to 2.5% of their body mass during the reproductive period, which reflects a loss of 1.6% to 5.7% of the total body load of Hg/year (Schneider et al., 2013). ...
Studies on the bioaccumulation and toxicity of contaminants in Crocodylians are scarce. We evaluated alterations in concentrations of the nondestructive biomarkers butyrylcholinesterase (BChE), glutathione‐S‐transferase (GST), superoxide dismutase (SOD), and reduced glutathione (GSH), together with bioaccumulation of the metals iron (Fe), copper (Cu), zinc (Zn), manganese (Mn), chronium (Cr), aluminium (Al), and lead (Pb) in Caiman latirostris captured in Tapacurá Reservoir (TR; São Lourenço da Mata, Pernambuco, Brasil), in urbanized areas of Pernambuco State (UA; Brasil) and from the AME Brasil caiman farm (AF; Marechal Deodoro, Alagoas, Brasil); the latter was used as a potential reference with low levels of contamination. For metal analysis, 500 µL of blood was digested in 65% HNO 3 and 30% H 2 O 2 . The samples were analyzed by inductively coupled plasma–optical emission spectrometry. For analysis of biomarkers, an aliquot of blood was centrifuged to obtain plasma in which biochemical assays were performed. Blood concentrations of metals analyzed in animals from AF were lower compared with TR and UA, confirming that animals from the caiman farm could be used as references with low levels of contamination. Iron, Cu, Mn, Al, and Pb exceeded toxic levels for other vertebrates in animals from TR and UA. Butyrylcholinesterase activity showed significant reduction in adults from UA and TR compared with AF. An increase in the activity of GST and GSH, in adults of TR and UA in relation to AF, was verified. Superoxide dismutase activity showed a significant reduction in adults of TR in relation to AF, and the concentrations of Cu and Mn were negatively correlated with SOD activity. Animals from UA and TR showed greater concentrations of the analyzed metals compared with reference animals, and changes in biomarkers were seen, confirming the potential of these nondestructive chemical and biological parameters in blood of C. latirostris for biomonitoring of pollution. Environ Toxicol Chem 2024;00:1–18. © 2024 SETAC
... In this order, ontogenetic dietary shift between juveniles and adults greatly influences measured total Hg concentration in blood, leading to a high variability in the relation between size and MeHg concentration. This ontogenetic shift explains why the relationship between blood Hg and body size is variable and was found in some studies (Eggins et al. 2015;Buenfil-Rojas et al. 2018;Lemaire et al. 2021a), but not in others (Yanochko et al. 1997;Eggins et al. 2015;Lawson et al. 2020). Therefore, when comparing Hg concentrations between different geographic areas, it is important to consider size of individuals. ...
Mercury contamination is a widespread phenomenon that impacts ecosystems worldwide. Artisanal Small Scale Gold Mining (ASGM) activities are responsible for more than a third of atmospheric Hg emission. Due to Hg toxicity and its broad and elevated prevalence in the environment resulting from ASGM activities in the tropics, its biomonitoring is essential to better understand the availability of its methylmercury (MeHg) form in the environment. The Minamata Convention was ratified with the objective to “protect human health and the environment from anthropogenic emissions and releases of mercury compounds”. Biomagnification of MeHg occurs through the trophic food web, where it biomagnifies and bioaccumulates in top predators. To monitor environmental MeHg contamination, studies have evaluated the use of living organisms; however, reptiles are among the least documented vertebrates regarding MeHg exposure. In this review we evaluate the use of crocodylians for Hg biomonitoring in tropical ecosystems. We found that out of the 28 crocodiles species, only 10 have been evaluated regarding Hg contamination. The remaining challenges when using this taxon for Hg biomonitoring are inconsistencies in the applied methodology (e.g., wet versus dry weight, tissues used, quantification method). However, due to their life history traits, crocodylians are particularly relevant for monitoring MeHg contamination in regions where ASGM activities occur. In conclusion and given their ecological and socio-economic importance, crocodylians are at great risk of MeHg contamination and are excellent bioindicators for tropical ecosystems.
... Blood slides were further deidentified to mask sample identity for whole blood cell counts. Samples used for each analysis were randomly selected based only on availability of sufficient material for analysis, and when possible to balance analysis for comparable numbers of males and females, life stage (adult SVL >90 cm; juvenile SVL <90 cm, and body mass index (BMI) estimated using the formula BMI Tail Girth/(SVL x 2) (Lawson et al., 2020). To control for possible effects of seasonality samples were date matched. ...
Surface and groundwater of the Cape Fear River basin in central and coastal North Carolina is contaminated with high levels of per- and polyfluoroalkyl substances (PFAS). Elevated levels of PFAS have also been found in blood of fish and wildlife from the Cape Fear River, and in the blood of human populations reliant on contaminated well or surface water from the Cape Fear River basin as a source of drinking water. While the public and environmental health impacts of long-term PFAS exposures are poorly understood, elevated blood concentrations of some PFAS are linked with immunotoxicity and increased incidence of some chronic autoimmune diseases in human populations. The goal of this One Environmental Health study was to evaluate PFAS exposure and biomarkers related to immune health in populations of American alligators (Alligator mississippiensis), a protected and predictive sentinel species of adverse effects caused by persistent toxic pollutants. We found that serum PFAS concentrations in alligator populations from the Cape Fear River were increased compared to a reference population of alligators from the adjoining Lumber River basin. The elevated serum PFAS concentrations in the Cape Fear River alligators were associated with increased innate immune activities, and autoimmune-like phenotypes in this population. In addition to evidence of significantly higher double stranded-DNA binding autoantibodies in adult Cape Fear River alligators, our qRT-PCR analysis found remarkably high induction of Interferon-α signature genes implicated in the pathology of human autoimmune disease. We interpret the association of increased PFAS exposure with disrupted immune functions to suggest that PFAS broadly alters immune activities resulting in autoimmune-like pathology in American alligators. This work substantiates and extends evidence from experimental models and human epidemiology studies showing that some PFAS are immune toxicants.
... Because of the longevity of alligators and their ectothermic nature, we anticipated potentially important effects of alligator age, season, and time of day on alligator tolerance of humans, even though these factors were not the primary focus of our investigation. To account for their potential effects, we included alligator length (a general proxy for age ;Wilkinson et al. 2016, Lawson et al. 2020), a quadratic (x + x 2 ) form of day of year (a proxy for season), and time of day (a proxy for ambient temperature) in all of the candidate models, and the simplest (base) model assumed these were the only factors associated with the response (model 1, Table 2). Seven additional models expanded on the base model by including various combinations of treatment and survey exposure (Table 2). ...
As anthropogenic impacts on ecosystems increase, novel solutions are needed to mitigate increasing human–wildlife conflict. Aversive conditioning is one strategy that can reduce the risks of humans living alongside wildlife by modifying the behavior of animals through their experiences with humans. Although considered rare, American alligator (Alligator mississippiensis) attacks on humans most often occur in human‐dominated landscapes and can be fatal. Our goal was to determine if capture and release protocols might serve as a form of aversive conditioning to reduce alligator tolerance of humans. Specifically, we compared the behavioral response of alligators to an approaching human for animals with 3 different levels of capture experience: alligators from a reference site where no captures occurred, alligators from a site where captures occurred that directly experienced capture and release, and alligators from the site where captures occurred that indirectly experienced capture and release (never captured but likely observed capture of others). We used a hurdle model and information‐theoretic approach to evaluate support for 8 hypotheses regarding factors that influence alligator probability of flight in response to an approaching human and the flight initiation distance (FID) of alligators that did flee. Our hypotheses considered the effects of capture experience, exposure to non‐capture (visual) surveys, alligator size, ambient temperature, and season. The best‐supported models provided strong evidence that capture experience increased the probability of flight and, to a lesser extent, increased FID of alligators that did flee, but that the strength of the effect varied with alligator size or some correlate. Furthermore, the effect of capture may extend beyond animals with direct experience. Capture and release protocols can result in an aversive conditioning response in alligators, effectively reducing habituation to humans. Given the geographic limitations of our study, more work is necessary to determine whether the utility of aversive conditioning may be site‐dependent, or similarly effective across a wider selection of developed landscapes. Alligators that indirectly and directly experience capture events are less tolerant of humans than alligators that do not experience capture by humans, though effects of capture are stronger for large alligators than smaller alligators. Capture events might be useful as a form of aversive conditioning to increase public safety and facilitate coexistence in landscapes shared by humans and alligators.
... Burger et al. 2000), no significant correlation (Table S2) was found among our samples. Changes in Hg concentrations with size or age (Lawson et al. 2020), or changes in diet (Schneider et al. 2012;Lázaro et al. 2015) may explain such inconsistency. Rivera et al. (2016) showed that there was significant correlation between Hg in muscle and animal size and weight, but the size range of Rivera and this study is too narrow for any further analysis. ...
Caiman yacare is considered one of the top predators in the Amazon basin, and understanding pollutant distribution within its tissues may help its sustainable management. As a top predator, C. yacare should have the highest mercury concentrations, but has lower Hg concentrations than carnivorous fish (Rivera et al. 2016), which are part of their diet. We compared total Hg among liver, kidney, fat, and muscle of C. yacare, and whether trends in the distribution of Hg among tissues were like other crocodilians, aquatic birds, omnivorous, and carnivorous fish. Fat had the lowest concentrations (0.025 ± 0.03 mg kg⁻¹) followed by muscle (0.15 ± 0.06 mg kg⁻¹), kidney (0.57 ± 0.30 mg kg⁻¹) and liver (1.81 ± 0.80 mg kg⁻¹). Such preferential accumulation makes C. yacare meat a safer alternative for human consumption than carnivorous fish. The relation between Hg accumulation in liver and muscle is highest in crocodilians, which has evolutive and environmental implications.
Contaminant body burdens are determined by complex interactions between contaminant inputs into the environment, local ecological dynamics, and organismal ontogeny. Although a naturally occurring element, mercury (Hg) is a potent neurotoxin, commonly assessed in contaminant body burdens. Anthropogenic activity has impacted its spatial distribution, resulting in regional ‘hotspots’ with elevated Hg concentrations. Due to the propensity of methylated Hg to bioaccumulate within individuals over time and biomagnify across trophic levels, long-lived apex predators can carry substantial body burdens in affected ecosystems. Still, the role of an organism's ontogeny and habitat in shaping individual Hg concentrations, especially within and across species, is not well understood. We assessed total Hg, carbon (δ13C), and nitrogen (δ15N) isotopic ratios in whole blood samples (n = 133) across three distinct habitats in the Southeastern U.S. to investigate how size and dietary shifts in the American alligator (Alligator mississippiensis) influence Hg accumulation. Mercury concentrations were approximately 8-fold higher in alligators inhabiting the Okefenokee Swamp, Georgia (mean = 0.62 mg/kg) compared to those inhabiting coastal habitats (Jekyll Island, Georgia and Yawkey Wildlife Center, South Carolina). Whereas individual size and nitrogen isotope signatures generally displayed positive relationships with Hg concentrations, model selection approaches revealed these relationships varied across populations, likely in response to site-specific differences in environmental Hg concentrations and life history attributes of the alligators. Collectively, our findings demonstrate that although Hg concentrations in A. mississippiensis are highly influenced by differences between sites, diet and body size can sometimes additionally affect individual variation within populations, suggesting that organismal ontogeny interacts with site-specific contamination and ecological factors to affect Hg body burdens.
Despite the general lack of studies that use reptiles as bioindicators, the value of freshwater turtles and crocodilians in ecotoxicology has been proven, due to their importance as sentinel species. The aim of this study was to compile information on the use of freshwater turtles and crocodilians as environmental biomonitors of inorganic element contamination. We searched for articles in databases using specific keywords. A total of 104 studies published between the years 1970 and 2020 were collected. We noted a general increase in the number of studies involving turtles and crocodilians during the study time period. The Order Testudines were the subjects of 46% of the analysed publications, and the Order Crocodylia accounted for 54%. Within these studies, we counted 39 species (turtles n=29 and crocodilians n=10). Forty chemical elements were evaluated in the analysed articles, of which the majority represented non-essential elements (Hg, Cd, Pb). Although internal organs constituted the main biological matrix chosen for each group (37%), we observed an increase in the use of non-destructive matrices in both groups (scale, blood, tail muscle, carapace). The majority of analysed studies used HNO3 for the sample decomposition, with the majority of analyses being per-
formed using atomic absorption spectroscopy (53%). Mainly blank controls (19%), analyte recovery (18%) and replicates (18%) were used as methods of validating analytical procedures. Furthermore, the studies used certified reference materials, which measure the accuracy of the methods used. We conclude that the increase in the use of aquatic reptiles in environmental monitoring research is mainly due to their ability to reveal integrated changes in ecosystems, aiding
in environmental public policy decision-making and effective management plans.
Mercury (Hg) is a global environmental contaminant that affects ecosystems. It is known to biomagnify through food webs, and to bioaccumulate especially in the tissues of top predators. Large scale comparisons between taxa and geographic areas are needed to reveal critical trends related to Hg contamination and its deleterious effects on wildlife. Yet, the large variety of tissues (keratinized tissues, internal organs, blood) as well as the variability in the units used to express Hg concentrations (either in wet- or dry-tissue weight) limits straightforward comparisons between studies. In the present study, we assessed the moisture content that could influence the total Hg (THg) concentrations measured in several tissues (claws, scutes, total blood and red blood cells) of three caiman species. First, we aimed to evaluate the moisture content from the different tissues, and second to provide information on THg concentrations in various matrices. Our results show a difference of THg concentrations between the tissues and intra- and interspecific variations of moisture content, with the highest THg values found in keratinized tissues (scute keratinized layers and claws). For the three species, we found positive relationships between body size and THg concentration in keratinized tissues. In the blood, the relationship between body size and THg concentration was species-dependent. Our results emphasize the need for a standardized evaluation of THg concentration and trace elements quantification based on dry weight analytical procedures. In addition, the use of both blood and keratinized tissues offers the possibility to quantify different time scales of THg exposure by non-lethal sampling.
Toxic trace element exposure occurs through release of the ubiquitous and naturally occurring elements arsenic (As), cadmium (Cd), lead (Pb), and mercury (Hg). The unique environmental conditions of the wetland ecosystems along the southeastern Atlantic coast of the United States lead to the accumulation of Hg which is greater than in most other ecosystems in the country. There are also point sources of As, Cd, and Pb in this region. To effectively monitor trace element concentrations, and consequently the potential human exposure, accessible local sentinel species are needed. In this study, concentrations of As, Cd, Pb, Hg and six other trace elements (Al, Ni, Cu, Zn, Se, Mo) were examined in American alligators (Alligator mississippiensis) from seven wetland sites in South Carolina and Florida and assessed for their utility as a sentinel species for human trace element exposure. Alligators were chosen as a potential sentinel as they share a common exposure with the local human population through their aquatic diet, and they are directly consumed commercially and through recreation hunting in this region. Sex was significantly related to the concentration of Zn, Mo, and Al, but not As, Pb, Hg, Cd, Se, or Cu. Site specific differences in element concentrations were observed for As, Pb, Hg, Cd, Se, Zn, and Mo. Size/age was significantly related to the element Hg and Pb concentrations observed. The observed concentration ranges for the four toxic elements, As (6-156 ng/g), Cd (0.3-1.3 ng/g), Pb (3-4872 ng/g), and Hg (39-2765 ng/g), were comparable to those previously reported in diverse human populations. In this region alligators are hunted recreationally and consumed by the local community, making them a vehicle of direct human toxic element exposure. We propose that the similarity in As, Cd, Pb, and Hg concentrations between alligators observed in this study and humans underscores how alligators can serve as a useful sentinel species for toxic element exposure.
Scarcity of site-specific consumption rates for use in contaminant exposure modeling has resulted in a lack of formal guidance for assessing risk of exposure to contaminants via consumption of wild game in the United States. Consequently, numerical estimation of what species hunters harvest, consume, and share is important for human health risk assessment, especially in areas with elevated risk of contaminant exposure. To address these information gaps, we designed and administered questionnaires to 260 hunters at two hunting expos in South Carolina and inquired about their harvesting, sharing, and consumption habits with respect to wild game and wild fish. Of the 11 game and fish we included in our survey, respondents reported hunting and consuming an average of 5.3 and sharing 3.5. We found a significant difference in number of wild game and fish meals eaten per year across a rural–urban gradient, with respondents from low population density counties consuming more than those from medium or high population density counties. Additionally, hunters in our survey reported sharing a considerable portion of the game they procure, and often consume more fish and game than they hunt. Thus, future surveys would benefit from asking more directed questions related to who is receiving harvested game and portion size shared. Additionally, 90% of surveyed hunters also reported consuming fish. Thus, our results also highlight the importance of considering cumulative wild game and fish consumption in future risk assessment analysis for the southeastern United States and other comparable populations, especially for high-risk groups such as children and pregnant women.
Concentrations of mercury (Hg) are not well studied in free-ranging wildlife. Atmospheric deposition patterns of Hg have been studied in detail and have been modeled for both global and specific locations and often correlate to environmental impact. However, monitoring the impact of Hg deposition in wildlife is complicated due to local environmental conditions that can affect the transformation of atmospheric Hg to the biologically available forms (e.g., rainfall, humidity, pH, the ability of the environment to methylate Hg), as well as affect the accessibility to organisms for sampling. In this study, Hg concentrations in blood samples from a population of American alligators (Alligator mississippiensis) at Merritt Island National Wildlife Refuge (MINWR), FL, USA, over a seven-year period (2007 to 2014; n=174 individuals) were examined to assess Hg variation in the population, as well as the difference in Hg concentration as a function of health status. While most of this population is healthy, 18 individuals with low body mass indices (BMI, defined in this study) were captured throughout the sampling period. These alligators exhibited significantly elevated Hg concentrations compared to their age/sex/season matched counterparts with normal BMI, suggesting that health status should be taken into account when examining Hg concentrations and effects. Alligator blood Hg concentrations were related to the interaction of age/size, sex, and season. This study illustrates the value of a routinely monitored population of large predators in a unique coastal wetland ecosystem, and illuminates the value of long-term environmental exposure assessment.
Cross-ecosystem movements of mobile consumers are a primary mechanism by which energy and nutrients are exchanged between disparate ecosystems. While factors influencing variation in bottom–up subsidies between ecosystems have been well studied, much less is known regarding how biotic and abiotic factors influence the dynamics of mobile consumer-driven connectivity. In a literature survey, we found only 14% of studies examined factors contributing to variation in cross-ecosystem marine foraging by freshwater-adapted consumers. Here, we examine the relationships between abiotic factors and cross-ecosystem movements of a highly mobile freshwater-adapted top predator, Alligator mississippiensis (American alligator). As alligators lack physiological adaptations to survive in marine environments, we predict this linkage would be affected by factors that modify the ability to cope with high salinities. Our results reveal that multiple abiotic factors (e.g., relative humidity, temperature, total precipitation) are key explanatory variables of the duration of cross-ecosystem foraging trips by alligators, and that the absence of salt glands does not preclude them from performing long forays into marine environments. More broadly, our results expand our understanding of mobile consumer-driven ecosystem connectivity at the land–sea interface by demonstrating connectivity is highest when physical stressors are relaxed, and access to and availability of resources are maximized.
Routine monitoring of contaminant levels in wildlife is important for understanding chemical exposure and ultimately the link to ecosystem and human health. This is particularly important when the monitored species is recreationally hunted for human consumption. In the southeastern United States, recreational alligator harvesting takes place annually and in locations that are known to be contaminated with environmental pollutants. In this study, we investigated the biodistribution of trace elements in the American alligator (Alligator mississippiensis) from five sites in Florida, USA. These sites are locations where annual recreational alligator harvesting is permitted and two of the sites are identified as having high mercury contamination with human consumption advisories in effect. We utilized routinely collected monitoring samples (blood and scute), a commonly consumed tissue (muscle), and a classically analyzed tissue for environmental contaminants (liver) to demonstrate how the trace elements were distributed within the American alligator. We describe elemental tissue compartmentalization in an apex predator and investigate if noninvasive samples (blood and scute) can be used to estimate muscle tissue concentrations for a subset of elements measured. We found significant correlations for Hg, Rb, Se, Zn and Pb between noninvasive samples and consumed tissue and also found that Hg was the only trace metal of concern for this population of alligators. This study fills a gap in trace elemental analysis for reptilian apex predators in contaminated environments. Additionally, comprehensive elemental analysis of routinely collected samples can inform biomonitoring efforts and consumption advisories.
Mercury (Hg) is a pervasive heavy metal that often enters the environment from anthropogenic sources such as gold mining and agriculture. Chronic exposure to Hg can impair immune function, reducing the ability of animals to resist or recover from infections. How Hg influences immunity and susceptibility remains unknown for bats, which appear immunologically distinct from other mammals and are reservoir hosts of many pathogens of importance to human and animal health. We here quantify total Hg (THg) in hair collected from common vampire bats (Desmodus rotundus), which feed on blood and are the main reservoir hosts of rabies virus in Latin America. We examine how diet, sampling site and year, and bat demography influence THg and test the consequences of this variation for eight immune measures. In two populations from Belize, THg concentrations in bats were best explained by an interaction between long-term diet inferred from stable isotopes and year. Bats that foraged more consistently on domestic animals exhibited higher THg. However, relationships between diet and THg were evident only in 2015 but not in 2014, which could reflect recent environmental perturbations associated with agriculture. THg concentrations were low relative to values previously observed in other bat species but still correlated with bat immunity. Bats with higher THg had more neutrophils, weaker bacterial killing ability and impaired innate immunity. These patterns suggest that temporal variation in Hg exposure may impair bat innate immunity and increase susceptibility to pathogens such as bacteria. Unexpected associations between low-level Hg exposure and immune function underscore the need to better understand the environmental sources of Hg exposure in bats and the consequences for bat immunity and susceptibility.
This paper provides an up-to-date assessment of global mercury emissions from anthropogenic and natural sources. On an annual basis, natural sources account for 5207 Mg of mercury released to the global atmosphere, including the contribution from re-emission processes, which are emissions of previously deposited mercury originating from anthropogenic and natural sources, and primary emissions from natural reservoirs. Anthropogenic sources, which include a large number of industrial point sources, are estimated to account for 2320 Mg of mercury emitted annually. The major contributions are from fossil-fuel fired power plants (810 Mg yr−1), artisanal small scale gold mining (400 Mg yr−1), non-ferrous metals manufacturing (310 Mg yr−1), cement production (236 Mg yr−1), waste disposal (187 Mg yr−1) and caustic soda production (163 Mg yr−1). Therefore, our current estimate of global mercury emissions suggests that the overall contribution from natural sources (primary emissions + re-emissions) and anthropogenic sources is nearly 7527 Mg per year, the uncertainty associated with these estimates are related to the typology of emission sources and source regions.
The extinction vortex is a theoretical model describing the process by which extinction risk is elevated in small, isolated populations owing to interactions between environmental, demographic, and genetic factors. However, empirical demonstrations of these interactions have been elusive. We modelled the dynamics of a small mountain lion population isolated by anthropogenic barriers in greater Los Angeles, California, to evaluate the influence of demographic, genetic, and landscape factors on extinction probability. The population exhibited strong survival and reproduction, and the model predicted stable median population growth and a 15% probability of extinction over 50 years in the absence of inbreeding depression. However, our model also predicted the population will lose 40–57% of its heterozygosity in 50 years. When we reduced demographic parameters proportional to reductions documented in another wild population of mountain lions that experienced inbreeding depression, extinction probability rose to 99.7%. Simulating greater landscape connectivity by increasing immigration to greater than or equal to one migrant per generation appears sufficient to largely maintain genetic diversity and reduce extinction probability. We provide empirical support for the central tenet of the extinction vortex as interactions between genetics and demography greatly increased extinction probability relative to the risk from demographic and environmental stochasticity alone. Our modelling approach realistically integrates demographic and genetic data to provide a comprehensive assessment of factors threatening small populations.
Significance
Anthropogenic mercury poses risks to humans and ecosystems when converted to methylmercury. A longstanding conundrum has been the apparent disconnect between increasing global emissions trends and measured declines in atmospheric mercury in North America and Europe. This work shows that locally deposited mercury close to coal-fired utilities has declined more rapidly than previously anticipated because of shifts in speciation from air pollution control technology targeted at SO 2 and NO x . Reduced emissions from utilities over the past two decades and the phase-out of mercury in many commercial products has led to lower global anthropogenic emissions and associated deposition to ecosystems. This implies that prior policy assessments underestimated the regional benefits of declines in mercury emissions from coal-fired utilities.
Mercury is a widespread environmental contaminant with exposures eliciting a well-documented catalog of adverse effects. Yet, knowledge regarding the underlying mechanisms by which mercury exposures are translated into biological effects remains incomplete. DNA methylation is an epigenetic modification that is sensitive to environmental cues, and alterations in DNA methylation at the global level are associated with a variety of diseases. Using a liquid chromatography tandem mass spectrometry-based (LC-MS/MS) approach, global DNA methylation levels were measured in red blood cells of 144 wild American alligators (Alligator mississippiensis) from 6 sites with variable levels of mercury contamination across Florida's north-south axis. Variation in mercury concentrations measured in whole blood was highly associated with location, allowing the comparison of global DNA methylation levels across different "treatments" of mercury. Global DNA methylation in alligators across all locations was weakly associated with increased mercury exposure. However, a much more robust relationship was observed in those animals sampled from locations more highly contaminated with mercury. Also, similar to other vertebrates, global DNA methylation appears to decline with age in alligators. The relationship between age-associated loss of global DNA methylation and varying mercury exposures was examined to reveal a potential interaction. These findings demonstrate that global DNA methylation levels are associated with mercury exposure, and give insights into interactions between contaminants, aging, and epigenetics.
Total mercury (Hg) concentrations of muscle, liver, blood, and epidermal keratin were measured in typically consumed, economically and culturally important species of turtle (Podocnemis unifilis and Podocnemis expansa) and caiman (Melanosuchus niger and Caiman crocodilus) from the Rio Purus in the Amazon basin, Brazil. Methylmercury (MeHg) concentrations were also measured in muscle tissue, representing the first analysis of MeHg concentrations in Amazonian reptile species. In muscle tissues Hg was mostly MeHg (79–96%) for all species. No correlations existed between animal size and total Hg or MeHg concentrations for any species other than M. niger, possibly as a result of growth dilution or the evolution of efficient Hg elimination mechanisms. Significant linear correlations were found between total Hg concentrations in all pairs of nonlethally sampled tissues (keratin and blood) and internal tissues (muscle and liver) for M. niger and between keratin and internal tissues for P. expansa, indicating that nonlethally sampled tissues can be analyzed to achieve more widespread and representative monitoring of Hg bioaccumulation in Amazonian reptiles. Although mean Hg concentrations in muscle for all species were below the World Health Organization guideline for safe consumption (500 µg kg–1), mean concentrations in caiman liver were above the safe limit for pregnant women and children (200 µg kg–1). No significant differences were found between total Hg and MeHg concentrations in tissues from wild-caught and farm-raised P. expansa, suggesting that farming may not reduce Hg exposure to humans. Environ Toxicol Chem 2015;9999:1–11. © 2015 SETAC
American alligators Alligator
mississippiensis undergo major transformations in morphology and ecology during development. These include several thousand-fold changes in body mass, modified snout and dental proportions, and shifts in diet from small, delicate foodstuffs to the inclusion of increasingly larger, more robust prey. How these changes in anatomical form contribute to actual physical performance and niche use is largely unknown. In the present study, bite-force measurements for 41 specimens of A.
mississipiensis, were made throughout ontogeny (hatchling–older adults) using a series of precision force transducers. How this performance indicator scaled with respect to cranial and whole-body measurements was determined. Bite-force production throughout development was contrasted with ontogenetic changes in trophic ecology. The influences of this performance measure on these changes were then analysed. The results showed a 800-fold range (12–9452 N) of bite forces with values positively correlating with increases in body size. Scaling of biting forces through ontogeny showed positive allometry with respect to body mass, head length, jaw length, snout–vent length and total length. These patterns may be attributable to allometric growth of individual skeletal elements (and associated musculature), and/or progressive fusion and ossification of skull and jawbones during development. The overall pattern of force increase throughout ontogeny did not vary in association with major shifts in diet. Notably, the bite-force values for adult A.
mississippiensis are the highest measured for any living animal and represent the first measures for a large crocodilian. Additionally, these data provide the first documentation of how bite force changes during ontogeny in a reptile. By bridging the rich morphological and ecological databases for these animals, this study opens the door to a comprehensive understanding of feeding in A.
mississippiensis. Furthermore, it provides groundwork for standardized comparative studies of feeding among crocodilian, reptilian, or other gnathostome vertebrates.
The estuarine crocodile (Crocodylus porosus) is an apex predator across freshwater, estuarine and coastal environments. The impact of a changing C. porosus population upon the ecosystem is unknown, but due to large ontogenetic changes in body mass (>1000-fold) their impact may be wide reaching and substantial. Here we investigated the relationship between diet, movement and body size in a population of C. porosus inhabiting a tidal river in northern Australia. Subcutaneous acoustic transmitters and fixed underwater receivers were used to determine the activity space and movement patterns of 42 individuals (202–451 cm in total length). There was no size-related spatial partitioning among different sized crocodiles. Large individuals (snout–vent length (SVL): 160 cm < SVL < 188.5 cm) did, however, exhibit a much larger activity space than other size classes. Diet and individual specialization was assessed using the composition of stable carbon (δ13C) and nitrogen (δ15N) isotopes in tissues with different turnover rates. There was a quadratic relationship between body size and δ15N, suggesting that medium-sized individuals (110 cm < SVL < 160 cm) incorporated a greater proportion of high trophic prey into their diets than small (SVL < 110 cm) or large individuals (SVL > 160 cm). Tissue δ13C composition on the other hand was positively correlated with body size, indicating that different size classes were trophically linked to primary producers in different habitats. Individual-level analyses showed that small crocodiles were generalist feeders while medium and large size classes specialized on particular prey items within the food webs they fed. The findings further our understanding of ontogenetic variation in C. porosus diet, and suggest that change in C. porosus population size or demographics may be influential at various levels across the local food web.
Large-bodied apex predators (e.g., sharks, wolves, crocodilians) are believed to regulate food web structure and drive ecosystem processes, but there remains relatively little experimental evidence. Here we use field surveys and a mesocosm experiment to evaluate the cascading effects of an apex predator (American alligator) on a salt marsh food web. Consistent with previous studies (n. = 10), field surveys revealed blue crabs (Callinectes sapidus Rathbun 1896), an important marsh mesopredator, were a frequent component of estuarine-occurring alligators' diet (mean. ±. SD, 47. ±. 20%, n. = 1384). In mesocosms, we examined potential consequences of this interaction in a simplified salt marsh community. We experimentally isolated alligator effects on the abundance (consumptive effect) and behavior (non-consumptive effect) of blue crabs and on blue crab consumption of plant-grazing snails and ribbed mussels. Alligators reduced blue crab abundance by ~. 40% over 3. days and induced behavioral changes, resulting in decreased foraging activity and increased refuge use by blue crabs. The combined effects of reduced crab abundance and altered behavior translated into increased survival of both a keystone grazer (snails) and a mutualist (mussels) within the salt marsh food web. Our findings experimentally demonstrate that a large-bodied, apex predator has the potential to 1) generate a trophic cascade, 2) elicit behavioral changes (i.e., non-consumptive effects) in mesopredator prey, and 3) indirectly affect the potential for both grazing and mutualism to occur in this food chain. Our results generate testable hypotheses regarding the broad-scale effects of alligator presence and top-down forcing in salt marsh ecosystems.
A higher proportion of long‐lived animals die from senescence than short‐lived animals, yet many long‐lived homeotherms show few signs of physiological ageing in the wild. This may, however, differ in long‐lived diving homeotherms that frequently encounter hypoxic conditions and have very high metabolic rates.
To examine ageing within a long‐lived diving homeotherm, we studied resting metabolism and thyroid hormones ( N = 43), blood oxygen stores ( N = 93) and foraging behaviour ( N = 230) of thick‐billed murres ( U ria lomvia ). Because murres dive exceptionally deep for their size and have a very high metabolism, we expected that ageing murres would show signs of physiological senescence. We paid particular attention to resting metabolism as we argue that these maintenance costs reflect those experienced during deep dives.
Blood oxygen stores (haematocrit), resting metabolic rate and thyroid hormone levels all declined significantly with age in incubating murres 3–30 years of age. In birds measured longitudinally 3 years apart, thyroid hormone levels and haematocrit were both significantly lower, suggesting progressive changes within individuals rather than selective disappearance of individuals with high metabolic rates. Within our longitudinal data set, we found no effect of age on dive depth, dive shape or behavioural aerobic dive limit.
A meta‐analysis of changes in resting metabolism with age across 15 animal species demonstrated that such declines are pervasive across most of the kingdom. The rate of decline was highest in species with high energy expenditure supporting a linkage between metabolism and senescence.
Physiological changes occurred in tandem with advancing age in murres, but offset each other such that there was no detectable decline in behavioural performance.
The post-occipital sinus of the spinal vein is often used for the collection of blood samples from crocodilians. Although this sampling method has been reported for several crocodilian species, the technique and associated anatomy has not been described in detail in any crocodilian, including the Nile crocodile (Crocodylus niloticus). The anatomy of the cranial neck region was investigated macroscopically, microscopically, radiographically and by means of computed tomography. Latex was injected into the spinal vein and spinal venous sinus of crocodiles to visualise the regional vasculature. The spinal vein ran within the vertebral canal, dorsal to and closely associated with the spinal cord and changed into a venous sinus cranially in the post-occipital region. For blood collection, the spinal venous sinus was accessed through the interarcuate space between the atlas and axis (C1 and C2) by inserting a needle angled just off the perpendicular in the midline through the craniodorsal cervical skin, just cranial to the cranial borders of the first cervical osteoderms. The most convenient method of blood collection was with a syringe and hypodermic needle. In addition, the suitability of the spinal venous sinus for intravenous injections and infusions in live crocodiles was evaluated. The internal diameter of the commercial human epidural catheters used during these investigations was relatively small, resulting in very slow infusion rates. Care should be taken not to puncture the spinal cord or to lacerate the blood vessel wall using this route for blood collection or intravenous infusions.
We studied growth of the caiman, Caiman crocodilus yacare, in the Brazilian Pantanal for 27 years between 1987 and 2013.We recaptured 647 of 7769 C. c. yacare initially marked in an area of 50 km(2), in two ranches. We were able to determine size at age accurately for 24 male and17 female caimans that had been marked at hatching or less than 1 year old, and recaptured over periods of 5 to 24 years. The other 606 caimans were used to evaluate short-term growth rates. Age-size relationships were estimated using growth models from the Richards family of curves (full model, von Bertalanffy and monomolecular). The form of the relationships differed between analyses based on caimans of known age and analyses based on integration of growth rate on size relationships for caimans whose ages were not known. Individuals showed large variation in short-term growth rates, but data on known-age animals indicated little between-individual variability in long-term growth rates. There was evidence of a small effect of rainfall, but not temperature, on short-term growth of small caimans, but most variation in growth rates was unexplained by variables other than age and sex. Data on known-age individuals indicated that female C. c. yacare generally reach sexual maturity between 10 and 15 years of age. Because of the asymptotic relationship between age and size, deviations of observations from the model for age are larger than for size, and estimates of age at a given size have greater errors than estimates of size at a given age. Integration of growth rate on size relationships may be adequate for estimating size from age in many cases, but accurate estimates of age from size require data on known-age individuals over the size range of the species.
Although evidence that reptiles exhibit indeterminate growth remains equivocal and based on inadequate data, the assumption that they do is still widely accepted as a general trait of reptiles. We examined patterns of variation in adult growth using long-term mark-recapture data on 13 populations of 9 species representing 3 families of freshwater turtles located in South Carolina, Michigan, and Arizona in the USA and in Ontario, Canada. Across 13 study populations, growth rates of all adults and only those that grew averaged 1.5 and 1.9 mm/yr respectively. Sources of variation in growth rates included species, population, sex, age, and latitude. Most adults of both sexes with recapture intervals greater than 10 years grew, but across all populations an average of 19 % of individuals did not grow (some with recapture intervals up to 30 years). For known-age adults of three species, the highest growth rates occurred during the 10 years following sexual maturity, and the proportions of non-growing individuals increased with age. Growth rates of adults were on average 92 % lower than those of juveniles. Based on linear relationships of clutch size and body size of females at average juvenile and adult growth rates it would take 0.7 (0.2–1.2) years and 8.6 (min–max = 2.3–18.5) years, respectively, to grow enough to increase clutch size by one egg. The majority of within population variation in adult body size in 3 species appeared to be a combination of differences in ages at maturity and juvenile and early adult growth, rather than indeterminate growth. The results from our study populations indicate that increases in body size (and associated reproductive output) that results from indeterminate growth are not substantial enough to represent a major factor in the evolution of life histories in general or the evolution of longevity and aging specifically.
We studied the mercury contamination of 13 species of seabirds breeding on Bird Island, South Georgia, in 1998. Total mercury concentrations in body feather samples of birds caught at their breeding colonies were determined. Among the species, grey-headed albatross (8933 ng g(-1)) and southern giant petrel (7774 ng g(-1)) showed the highest, and gentoo penguin (948 ng g(-1)) the lowest body feather mercury concentrations. Mercury levels were negatively correlated with the proportion of crustaceans (mainly krill) in the species' diets, suggesting that the trophic level is the most important factor in explaining the variation of mercury concentrations in Antarctic seabirds. In 4 species studied for age effects among adult birds (grey-headed and black-browed albatross, northern and southern giant petrel), no age-dependent variation in mercury levels was found. Sex differences were also assessed: female gentoo penguins had lower mercury levels than males, which may be related to the elimination of part of the mercury body burden by females into eggs. In contrast, northern giant petrel males had lower levels than females, which may be related to a higher consumption by males of carrion from Antarctic fur seals. In grey-headed albatrosses, mercury levels were 113 % higher than in 1989, when this species was investigated at the same site, indicating a possible increase in mercury pollution of the Southern Ocean during the last decade.
The movements of 100 crocodiles (0.3–4.3 m) were followed over 3 years by mark-recapture, spotlight survey and radiotelemetry at Ngezi, Zimbabwe. Home ranges were based on frequency of occurrence of animals in 100 m grid squares. Most crocodiles were nocturnal, but adults occasionally moved in daylight. Animals 0.4–2.2 m had home ranges of similar sizes, but dispersed at 1.2 m. Smaller crocodiles were restricted to the river (the only nesting area) whereas all larger animals occupied the lake into which the river flowed. From 2.2 m the range of movement increased until large subadult females (2.7 m) travelled widely without distinct home ranges. Subadults were still largely excluded from the river and the smallest nesting female migrated out of the river after each breeding season. Large breeding females (>2.8 m) had small home ranges near prime nest sites. There appeared to be no difference in the behavior of the sexes up to 2.2 m. There are few data on larger males, but four mature animals (>3.2 m) had distinct home ranges. Home ranges of small juveniles increased in size in the hot season, but for adults the effects of climate and breeding were confused. The different behavior of the various categories of crocodiles resulted in the marked separation of breeding females with their last few season's offspring from immature animals 1.2–2.2 m. Dispersal appears to occur at the same stage in other crocodilians with similar scaling parameters because adults become increasingly intolerant of intermediate-sized animals. It is suggested that size-class separation is part of a general density-dependent regulating mechanism in crocodilian populations.
With few exceptions, crocodilians must be counted and caught for studies of their ecology. Most methods of finding and catching crocodilians in use today are modifications of methods for harvesting crocodilians (Chabreck 1963; Jones 1966). These methods have been adapted to suit the target species, or local habitat conditions and to minimize risk of injury to the crocodile and the investigator (Webb and Messel 1977; Hutton et al.1987; Walsh 1987; McDaniel and Hord 1990). Any particular situation will likely require innovations on methods used by others. This document is Circular 1451, one of a series of the Wildlife Ecology and Conservation Department, Florida Cooperative Extension Service, Institute of Food and Agricultural Sciences, University of Florida. First published: November, 2004. CIR1451/UW198: Counting and Capturing Crocodilians (ufl.edu)
The Atlantic Goliath Grouper Epinephelus itajara is currently a protected species in the southeastern United States waters of the Atlantic and the Gulf of Mexico and is considered vulnerable throughout its geographic range. In this study, I evaluated mercury concentrations in their tissues (muscle, liver), which revealed high concentrations (μg/g ww) of mercury (mean ± SE) in liver (6.18 ± 0.86) and muscle (1.12 ± 0.06) tissue that increased with size and age. Mercury concentrations were highest in fish caught off Florida's Atlantic coast, but varied on a finer regional scale. Mercury concentrations in muscle tissue were generally greater near urbanized areas with known mercury sources and environmental conditions appropriate for higher methylation rates. This suggests that management should consider improving the water quality in these areas to reduce the risk of health effects to human consumers and to the fish themselves.
The American alligator (Alligator mississippiensis) is a keystone species that exhibits strong top-down effects on both ecosystem structure and function. As a highly mobile predator, alligators can link spatially segregated food webs and influence prey abundance, composition, and behavior across space and time. Therefore, understanding alligator movement patterns has relevant applications to alligator ecology and management, as well as the study of communities or ecosystems across the alligator’s range. We provide a brief review that highlights several of the challenges of studying alligator movement patterns. We then describe recent advancements in animal tracking technology that are relevant to the study of crocodilians, including reductions in transmitter size, improved battery longevity and location fix precision, and the ability to pair movement data with animal-borne sensor information (e.g., temperature, velocity). Given the rapidly expanding transmitter options now available, we discuss some of the benefits and drawbacks of the major transmitter platforms (radio, satellite, and acoustic) and analytical frameworks, as guidance for future studies. Next, we review the existing literature and discuss potential drivers of variation in movement patterns including demographic, environmental, and behavioral factors, and how they may interact. We then synthesize our knowledge of alligator movement behaviors and discuss their potential community- and ecosystem-level implications. We conclude our chapter by delineating specific research needs that could add both breadth and depth to our understanding of alligator movements, including future studies that focus on adult females and inland or northern-latitude populations, as well as the need for longer-term datasets to evaluate site-fidelity patterns or the lack thereof.
Stable isotope analysis is a widespread tool in ecological studies of diet composition and habitat use. In deserts, freshwater environments constitute threatened local hotspots of biodiversity. In these environments, stable isotopes may help to describe trophic ecology of top-predators. We examined stable carbon (δ¹³C) and nitrogen (δ¹⁵N) isotopes from scute keratin samples of 33 Crocodylus suchus and muscle samples from 39 potential prey collected in Southern Mauritania. Isotope ratios were compared among crocodiles according to size (non-adult and adult), and habitat (rock pools and floodplains). There was a significant interaction effect of habitat and size on crocodile δ¹³C values. Whereas δ¹³C was similar for all crocodiles collected in rock pools, adults had lower signatures than non-adults in seasonal floodplains. δ¹⁵N indicated an ontogenetic dietary shift with adult crocodiles foraging on prey from higher trophic level. Standard ellipse areas showed wider isotopic niches for adult than non-adult crocodiles, and within adults, for those from floodplains than those from rock pools. These environments are small, seasonal, overexploited for livestock watering, and polluted. They support very small and isolated crocodile populations. This study is aimed to provide conservation authorities with baseline information to strictly protect water-bodies where these predators subsist in arid environments.
The perception that crocodilians exhibit indeterminate growth is common in the general reptilian literature. However, this assumption is frequently based on observations of immature and young adult animals and therefore lacks a complete understanding of adult growth patterns. Long-term mark-recapture studies appear to be the most certain method of determining growth patterns of adult crocodilians. From 1979–2015, we conducted a mark-recapture study of an American Alligator (Alligator mississippiensis) population on the Tom Yawkey Wildlife Center (YWC) in coastal South Carolina to examine long-term growth patterns and the influence of age on multiple reproductive parameters. We found no discernible linear growth in 19 of 31 adult female and 7 of 19 adult male alligators over periods of 5–33 years. The mean maximum reproductive lifespan for female alligators on the study site was 46 years, and females continued to reproduce for an extended period of time after reaching maximum size. The Schnute growth model predicted that male alligators grew at a faster rate and attained a greater estimated mean terminal snout–vent length (SVL) than females (males = 186.9, CI0.95 = 184.5, 189.3 cm; females = 135.9, CI0.95 = 134.1, 137.8 cm) at the hypothetical age 75. In addition, the model predicted that males exhibited a greater estimated mean size (SVL = 182.0, CI0.95 = 179.6, 184.4 cm) and age (43 years) at which growth essentially ceased when compared to females (SVL = 131.4, CI0.95 = 129.5, 133.2 cm; 31 years). However, actual growth records of individual alligators suggested that the growth model may have overestimated the age at which male alligator growth ceased. The estimated mean earliest age at sexual maturity was 11.6 years (CI0.95 = 10.5, 12.8) for males and 15.8 years (CI0.95 = 14.5, 17.1) for females. We also documented that alligators on the site commonly live to 50 and can possibly live to >70 years of age. This study provides evidence that both male and female American Alligators in a population in coastal South Carolina exhibit a pattern of determinate growth and adds to a growing list of studies suggesting crocodilians as a group exhibit this growth pattern rather than indeterminate growth. Our findings are important for modeling population growth and determining sustainable harvest rates, particularly for alligators living near their northern distributional limit where growing seasons may be shorter and onset of sexual maturity later than in more southern portions of their range.
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 μg g(-1)Hg 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 μg g(-1)Hg w.w. moreover, most were above the limit recommended by WHO (0.5 μg g(-1)Hg w.w.); except for Leiarius marmuratus, which presented a mean of 0.353 ± 0.322 μg g(-1)Hg 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 μg g(-1)Hg w.w., respectively. Finally, recommendations on the consumption habits of Tacana communities are discussed.
Tools for performing model selection and model averaging. Automated model selection through subsetting the maximum model, with optional constraints for model inclusion. Model parameter and prediction averaging based on model weights derived from information criteria (AICc and alike) or custom model weighting schemes.
[Please do not request the full text - it is an R package. The up-to-date manual is available from CRAN].
Methylmercury is a bioaccumulative contaminant that biomagnifies in aquatic food webs and adversely affects the health of freshwater fish. Previous studies have documented an inverse relation between fish condition and concentration of mercury in fish. However, this relation may be a result of slow-growing fish accumulating large amounts of methylmercury rather than the effects of methylmercury on fish condition and growth. We evaluated the relation among fish condition, growth, and mercury concentration in northern pike Esox lucius from 26 lakes in the western region of the Laurentian Great Lakes. The relative weight (an index of fish condition) of northern pike was inversely related to mercury concentration in the axial muscle. The concentration of mercury in standard-size northern pike increased with fish age and suggested that fast-growing fish accumulated less mercury than slow-growing fish. However, there was no relation between the mean relative weight of northern pike in each population and mean age or mercury concentration of standard-size northern pike. These results suggest that the relation between mercury and fish condition is not due to the effects of mercury on rate of growth. Rather, slow-growing fish bioaccumulate greater concentrations of mercury than fast-growing fish of the same length. This article is protected by copyright. All rights reserved.
In this study, we evaluated the effect of temperature on the long-term stability of three mercury species in bovine blood.
We used inductively coupled plasma mass spectrometry (ICP-MS) analysis to determine the concentrations of inorganic (iHg),
methyl (MeHg) and ethyl (EtHg) mercury species in two blood pools stored at temperatures of −70, −20, 4, 23°C (room temperature)
and 37°C. Over the course of a year, we analyzed aliquots of pooled specimens at time intervals of 1, 2, 4 and 6 weeks and
2, 4, 6, 8, 10 and 12 months. We applied a fixed-effects linear model, step-down pairwise comparison and coefficient of variation
statistical analysis to examine the temperature and time effects on changes in mercury species concentrations. We observed
several instances of statistically significant differences in mercury species concentrations between different temperatures
and time points; however, with considerations of experimental factors (such as instrumental drift and sample preparation procedures),
not all differences were scientifically important. We concluded that iHg, MeHg and EtHg species in bovine whole blood were
stable at −70, −20, 4 and 23°C for 1 year, but blood samples stored at 37°C were stable for no more than 2 weeks.
Alligator mississippiensis is a keystone species within the Everglades and other marsh systems, acting as predator and prey and structuring plant communities. Alligators are dependent on spatial and temporal patterns of water fluctuations. Deep water is required for alligator courtship and mating, and water levels help to determine availability of food and therefore patterns of growth and survival. Alligators adjust the height of the nest egg cavity based on spring water levels, which historically indicated whether water levels later in the nesting season (July and August) would be high or low. Historically alligators were abundant in peripheral marshes of the Everglades. Now they are most abundant in central sloughs, but until recently recommendations regarding managing hydrological conditions for alligators focused on maintaining alligators in central slough habitats. Hydrological management for alligators should be based on restoring alligators to habitats where they were formerly abundant, rather than maintaining them in habitats where they were not. -from Authors
We conducted a study of black caiman (Melanosuchus niger) growth rates using data from a long-term mark-recapture study carried out in the Rupununi region of Guyana between 2005 and 2015. In contrast to previous studies, growth rates of black caiman declined with increasing size and this decline occurred more rapidly for females. Size-at-age models predicted that males and females reach asymptotic sizes of 178.2-189.0 cm SVL and 140.1-143.4 cm SVL, respectively. Our results suggest that growth rates of black caiman in the Rupununi region follow the same general patterns as for other crocodilians, and that disparities with previous black caiman studies may be largely related to density-dependent factors, among other possibilities. However, future studies that include large black caiman of known ages are needed to validate our findings.
Wild caught, captive alligators (Alligator mississippiensis) over a seven-year period exhibited a successful nesting rate of 48 percent in six pens maintained on Rockefeller Refuge. Hatching success in pens (56 percent) closely correlated the 58 percent determined for wild alli-gators inhabiting natural marsh. Pen construction methods, stocking rates, and maintenance techniques were implemented to simulate natural marsh conditions, thereby en-couraging breeding and contributing to the well being of the alligators. Diseases posed no problem during this investigation although fighting did cause some concern during the early stages of the study. Courtship activities, nest construction techniques and maternal duties following egg laying were highly variable among the various alligators under study. Also, courtship behavior was highly ritualized. Behavior of pen reared alligators as compared to wild captured adult alligators were compared. Stocking rates were found to differ greatly. Pen reared adult animals could be maintained in much closer confine-ment and under less stress when compared to wild captured adults. INTRODUCTION Alligators have been kept in captivity throughout Louisiana for many years. However, only on rare occasions do they reproduce under captive conditions. As alligators are easily maintained in captivity and fairly disease free, in the past they were sold by the thousands in Louisiana as pets. Also, alligator hunters would capture young alligators at a nest site and return home to confine them to some type of make shift pen under the pretense of starting an "alligator farm".
As use of Akaike's Information Criterion (AIC) for model selection has become increasingly common, so has a mistake involving interpretation of models that are within 2 AIC units (ΔAIC ≤ 2) of the top-supported model. Such models are <2 ΔAIC units because the penalty for one additional parameter is 2 AIC units, but model deviance is not reduced by an amount sufficient to overcome the 2-unit penalty and, hence, the additional parameter provides no net reduction in AIC. Simply put, the uninformative parameter does not explain enough variation to justify its inclusion in the model and it should not be interpreted as having any ecological effect. Models with uninformative parameters are frequently presented as being competitive in the Journal of Wildlife Management, including 72 of all AIC-based papers in 2008, and authors and readers need to be more aware of this problem and take appropriate steps to eliminate misinterpretation. I reviewed 5 potential solutions to this problem: 1) report all models but ignore or dismiss those with uninformative parameters, 2) use model averaging to ameliorate the effect of uninformative parameters, 3) use 95 confidence intervals to identify uninformative parameters, 4) perform all-possible subsets regression and use weight-of-evidence approaches to discriminate useful from uninformative parameters, or 5) adopt a methodological approach that allows models containing uninformative parameters to be culled from reported model sets. The first approach is preferable for small sets of a priori models, whereas the last 2 approaches should be used for large model sets or exploratory modeling.
This chapter talks about some specific statistical procedures for selecting variables in regression. It discusses: all possible regressions using three criteria: R2, s2, and the Mallows Cp\, and the best subset regression using R2, R2 (adjusted), and Cp\. The chapter also focuses on stepwise regression, backward elimination, and some variations on previous methods. It explains the uses of the R2 statistic, residual mean square and Mallows Cp Statistic. The stepwise regression procedure starts off by choosing an equation containing the single best X variable and then attempts to build up with subsequent additions of X”s one at a time as long as these additions are worthwhile. The Hald data is used to illustrate the workings of the stepwise procedure. The backward elimination method is also an economical procedure. It tries to examine only the “best” regressions containing a certain number of variables.
(1) Great skuas Catharacta skua Brunnich have among the highest tissue mercury concentrations of British seabirds, and many of the birds breeding on Foula, Shetland in 1988 and 1989 had concentrations well in excess of those known to affect reproduction adversely in some terrestrial bird species. Comparison of mercury concentrations in feathers of great skuas collected before 1900 and in 1988-89 indicates a significant increase during this century, which is assumed to be due to anthropogenic activities (Thompson 1989). (2) Mercury in muscle tissues of great skuas was entirely methyl mercury, whereas approximately half the mercury in liver and kidney tissue was inorganic. Feather mercury concentrations correlated with total mercury concentrations in soft tissues of birds culled during incubation. (3) Mercury concentrations in feathers of adult great skuas on Foula, Shetland were found to be higher than those in feathers of chicks, but were independent of adult age and sex. (4) There was no evidence of accumulation of inorganic mercury in soft tissues with age. This suggests that dietary variation and specialization are more important than age as determinants of mercury concentrations in this species. (5) There was no relationship between diet during the breeding season and feather mercury concentration, either comparing mercury concentrations in different years covering a period of major change in diet at the colony, or comparing different birds with markedly different diets in the same year. Great skuas disperse widely during the winter, and differences in exposure to mercury during this period may be more important than differences in diet during the breeding season. (6) Despite evidence of increased mercury pollution (Thompson 1989), there was no evidence of a relationship between the mercury concentrations of individuals and their breeding performance or survival.
We examined stomach contents from 219 American alligators (Alligator mis-sissippiensis) collected from 4 Florida lakes. Fish, mostly shad (Dorosoma spp.), bow-fin (Amia calva), and gar (Lepisosteus spp.) occurred in 55.3% of the stomachs and was the most important food group (57.5%) by volume. Apple snails (Pomacea paludosa) and crayfish (Procambarus spp.) were important invertebrate prey (66.7% occurrence and 6.6% by volume). Of the 195 stomachs having a dominant food type (>50% of the total food volume), most (72%) contained one food type exceeding 90% of the total food volume. The predominant food type differed by lake (P< 0.001), sex (P= 0.056), and size (P< 0.001) of the alligator. In general, the dominant food type changed from invertebrate to vertebrate with an increase in alligator size. Alligator length-weight re-lationships (condition) were examined for variation associated with diet. For large alli-gators (2.89 m total length [TL]), increasing probability of dominance by the fish food type was associated with better condition. Fish were more likely to be the dominant food for alligators in lakes with the highest chlorophyll a concentrations. Food re-sources limitations may affect alligator diet and condition at some locations. Informa-tion on dietary constraints and condition may be useful in managing American alliga-tors for commercial and conservation purposes.
Large‐bodied, top‐predators are often highly mobile, with the potential to provide important linkages between spatially distinct food webs. What biological factors contribute to variation in cross‐ecosystem movements, however, have rarely been examined.
Here, we investigated how ontogeny (body size), sex and individual‐level behaviour impacts intrapopulation variation in cross‐ecosystem foraging (i.e. between freshwater and marine systems), by the top‐predator Alligator mississippiensis .
Field surveys revealed A. mississippiensis uses marine ecosystems regularly and are abundant in estuarine tidal creeks (from 0·3 to 6·3 individuals per km of creek, n = 45 surveys). Alligator mississippiensis captured in marine/estuarine habitats were significantly larger than individuals captured in freshwater and intermediate habitats.
Stomach content analysis (SCA) showed that small juveniles consumed marine/estuarine prey less frequently (6·7% of individuals) than did large juveniles (57·8%), subadult (73%), and adult (78%) size classes. Isotopic mixing model analysis ( SIAR ) also suggests substantial variation in use of marine/estuarine prey resources with differences among and within size classes between sexes and individuals (range of median estimates for marine/estuarine diet contribution = 0·05–0·76).
These results demonstrate the importance of intrapopulation characteristics (body size, sex and individual specialization) as key determinants of the strength of predator‐driven ecosystem connectivity resulting from cross‐ecosystem foraging behaviours. Understanding the factors, which contribute to variation in cross‐ecosystem foraging behaviours, will improve our predictive understanding of the effects of top‐predators on community structure and ecosystem function.
During the late 1980s, the upper trophic-level biota of the Everglades (FL, USA) was recognized as being highly contaminated with mercury (Hg). However, the timing and pattern of that increase is poorly known, and no information is available about mercury contam ination in Everglades wildlife prior to 1974. We measured methylmercury concentrations in feathers of white ibises (n = 33), great egrets (n = 7), anhingas (n = 21), and great blue herons (n = 12) from museum specimens collected from 1910 through 1980 and combined them with more recent feather samples collected from live birds (1985–2000, n = 98, 37, 49, and 7, respectively). We found no evidence of contamination of museum samples with inorganic mercuric preservatives (0.01–0.28% of total Hg in feathers). All species showed relatively low concentrations of mercury through the 1970s (<5 μl/L dry wt for anhingas, ibises, and egrets, <10 μl/L for herons). Samples from all species taken during the 1990s showed a large and significant increase (4–5X) in MeHg concentration. This evidence suggests that most of the increase in Hg deposition during the 20th century in south Florida occurred during the last two to three decades, which is consistent with information about local source deposition. Contamination levels prior to the 1970s appear to have been associated with normal reproduction in these birds, suggesting partial evidence for a threshold of reproductive impairment.
The control of mercury in the air emissions from coal-fired power plants is an ongoing challenge. The native unburned carbons in fly ash can capture varying amounts of Hg depending upon the temperature and composition of the flue gas at the air pollution control device, with Hg capture increasing with a decrease in temperature; the amount of carbon in the fly ash, with Hg capture increasing with an increase in carbon; and the form of the carbon and the consequent surface area of the carbon, with Hg capture increasing with an increase in surface area. The latter is influenced by the rank of the feed coal, with carbons derived from the combustion of low-rank coals having a greater surface area than carbons from bituminous- and anthracite-rank coals.The chemistry of the feed coal and the resulting composition of the flue gas enhances Hg capture by fly ash carbons. This is particularly evident in the correlation of feed coal Cl content to Hg oxidation to HgCl2, enhancing Hg capture. Acid gases, including HCl and H2SO4 (at small concentrations) and the combination of HC1 and NO2, in the flue gas can enhance the oxidation of Hg.In this presentation, we discuss the transport of Hg through the boiler and pollution-control systems, the mechanisms of Hg oxidation, and the parameters controlling Hg capture by coal-derived fly ash carbons.
The relationship between mercury (Hg) concentrations in fish muscle and fish growth rates was assessed for 54 walleye Sander vitreus, 52 northern pike Esox lucius, and 35 lake trout Salvelinus namaycush populations throughout the Province of Quebec, Canada. We used the von Bertalanffy growth model to estimate the ages of fish specimens for a given length, and Hg concentrations in fish specimens at standardized length were determined via a quadratic regression model. Measured values of Hg concentrations in walleyes, northern pike, and lake trout were then correlated to the estimated age at standardized length for each population (375, 675, and 550 mm, respectively). A model-II regression was performed to describe the existing relationships. Growth rates were positively related to Hg concentrations in walleyes and northern pike (when three outliers were excluded), whereas no correlation was observed for lake trout. Our findings demonstrate that slower-growing walleyes and northern pike have higher Hg concentrations at standardized length. For these fish species, growth rate could be used as an integrated proxy to predict Hg concentration in fish muscle on a regional scale. Our findings support the contention that biodilution can be an important factor regulating mercury concentrations in fish. Thus, our findings suggest that proper control of fish growth rate through fishing pressure, lake ecology, and watershed management could be used by fisheries management authorities to minimize the toxic risk associated with Hg exposure from fish consumption.