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Organizational Changes to Thyroid Regulation in Alligator mississippiensis: Evidence for Predictive Adaptive Responses

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PLOS One
Authors:
Ashley Boggs at National Institute of Standards and Technology
Ashley Boggs
Russell H Lowers at National Aeronautics and Space Administration
Russell H Lowers
Jessica Cloy-McCoy at Medical University of South Carolina
Jessica Cloy-McCoy
Louis J Guillette at Medical U of South Carolina
Louis J Guillette
  • Medical U of South Carolina
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Abstract and Figures

During embryonic development, organisms are sensitive to changes in thyroid hormone signaling which can reset the hypothalamic-pituitary-thyroid axis. It has been hypothesized that this developmental programming is a 'predictive adaptive response', a physiological adjustment in accordance with the embryonic environment that will best aid an individual's survival in a similar postnatal environment. When the embryonic environment is a poor predictor of the external environment, the developmental changes are no longer adaptive and can result in disease states. We predicted that endocrine disrupting chemicals (EDCs) and environmentally-based iodide imbalance could lead to developmental changes to the thyroid axis. To explore whether iodide or EDCs could alter developmental programming, we collected American alligator eggs from an estuarine environment with high iodide availability and elevated thyroid-specific EDCs, a freshwater environment contaminated with elevated agriculturally derived EDCs, and a reference freshwater environment. We then incubated them under identical conditions. We examined plasma thyroxine and triiodothyronine concentrations, thyroid gland histology, plasma inorganic iodide, and somatic growth at one week (before external nutrition) and ten months after hatching (on identical diets). Neonates from the estuarine environment were thyrotoxic, expressing follicular cell hyperplasia (p = 0.01) and elevated plasma triiodothyronine concentrations (p = 0.0006) closely tied to plasma iodide concentrations (p = 0.003). Neonates from the freshwater contaminated site were hypothyroid, expressing thyroid follicular cell hyperplasia (p = 0.01) and depressed plasma thyroxine concentrations (p = 0.008). Following a ten month growth period under identical conditions, thyroid histology (hyperplasia p = 0.04; colloid depletion p = 0.01) and somatic growth (body mass p
Thyroid gland histology from neonatal alligators. Thyroids were rated from 0 to 3 according to hyperplasia severity, hyperplasia area, and hypertrophy. A. All ratings of 1 (mild). B. All ratings of 2 (moderate). C. All ratings of 3 (severe). D. An example of follicular cell involution. F  =  follicular cell, C  =  colloid, L  =  lumen, IN  =  involution.
Thyroid gland histology from neonatal alligators. Thyroids were rated from 0 to 3 according to hyperplasia severity, hyperplasia area, and hypertrophy. A. All ratings of 1 (mild). B. All ratings of 2 (moderate). C. All ratings of 3 (severe). D. An example of follicular cell involution. F  =  follicular cell, C  =  colloid, L  =  lumen, IN  =  involution.
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Thyroid gland histology from neonatal alligators. Thyroids were rated from 0 to 3 according to hyperplasia severity, hyperplasia area, and hypertrophy. A. All ratings of 1 (mild). B. All ratings of 2 (moderate). C. All ratings of 3 (severe). D. An example of follicular cell involution. F = follicular cell, C = colloid, L = lumen, IN = involution. doi:10.1371/journal.pone.0055515.g001
Thyroid gland histology from neonatal alligators. Thyroids were rated from 0 to 3 according to hyperplasia severity, hyperplasia area, and hypertrophy. A. All ratings of 1 (mild). B. All ratings of 2 (moderate). C. All ratings of 3 (severe). D. An example of follicular cell involution. F = follicular cell, C = colloid, L = lumen, IN = involution. doi:10.1371/journal.pone.0055515.g001
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Mean classification for thyroid histological markers of American alligators.
Mean classification for thyroid histological markers of American alligators.
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Thyroid follicular cell hyperplasia. Mean proportions of follicular cell layers per thyroid gland of alligators from three sites in Florida. Merritt Island = black, Lake Woodruff = white, Lake Apopka = gray. A. Neonatal alligators. (AP: N = 16; MINWR: N = 11; LWNWR: N = 13) B. Juvenile alligators (N = 18 for all sites). Error bars are 6 SEM. Letters represent significant differences among sites within follicular cell layer classifications. doi:10.1371/journal.pone.0055515.g002
Thyroid follicular cell hyperplasia. Mean proportions of follicular cell layers per thyroid gland of alligators from three sites in Florida. Merritt Island = black, Lake Woodruff = white, Lake Apopka = gray. A. Neonatal alligators. (AP: N = 16; MINWR: N = 11; LWNWR: N = 13) B. Juvenile alligators (N = 18 for all sites). Error bars are 6 SEM. Letters represent significant differences among sites within follicular cell layer classifications. doi:10.1371/journal.pone.0055515.g002
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Thyroid follicular cell hyperplasia. Mean proportions of follicular cell layers per thyroid gland of alligators from three sites in Florida. Merritt Island  =  black, Lake Woodruff  =  white, Lake Apopka  =  gray. A. Neonatal alligators. (AP: N = 16; MINWR: N = 11; LWNWR: N = 13) B. Juvenile alligators (N = 18 for all sites). Error bars are ± SEM. Letters represent significant differences among sites within follicular cell layer classifications.
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Thyroid follicular cell hyperplasia. Mean proportions of follicular cell layers per thyroid gland of alligators from three sites in Florida. Merritt Island  =  black, Lake Woodruff  =  white, Lake Apopka  =  gray. A. Neonatal alligators. (AP: N = 16; MINWR: N = 11; LWNWR: N = 13) B. Juvenile alligators (N = 18 for all sites). Error bars are ± SEM. Letters represent significant differences among sites within follicular cell layer classifications.
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... Beginning in 2006, the late Dr. L. J. Guillette Jr. (a summary of Dr. Guillette Jr.'s accomplishments can be found in McCoy et al. 2016) in collaboration with researchers from the Kennedy Space Center-Ecological Program and individuals from several universities, commenced a comprehensive population-scale study of alligator reproductive physiology and behavior, ecotoxicology, health, and ecology within the Merritt Island National Wildlife Refuge and greater Cape Canaveral Peninsula located along the mid-Atlantic coast of Florida (Boggs et al. 2011, Boggs et al. 2013, Bowden et al. 2014a, Bowden et al. 2014b, Horai et al. 2014, Tellez and Nifong 2014, Rosenblatt et al. 2015, Bangma et al. 2017a, Bangma et al. 2017b, Nifong and Lowers 2017. While the Cape Canaveral Peninsula is not a true barrier island, the majority of upland areas along the peninsula are surrounded by saline waters and are ecologically analogous to barrier islands. ...
... Boggs et al. (2011) hypothesized that altered iodide, a vital structural component of thyroid hormones, linked to differences in iodine content within the diet, likely contributed to the perpetually elevated thyroid hormone concentrations observed in alligators from MINWR. Boggs et al. (2013) further investigated the relationship between and the potential implications (i.e., adult metabolic diseases) of iodine exposure to thyroid functioning and morphology in developing (i.e., embryonic) alligators. Boggs et al. (2013) demonstrated that embryonic exposure to elevated iodine and other endocrine disrupting chemicals can alter the morphology and function of the thyroid gland, which could potentially lead to the development of harmful thyroid syndromes later in life (i.e., thyrotoxicosis, hyper-or hypo-thyroidism). ...
... Boggs et al. (2013) further investigated the relationship between and the potential implications (i.e., adult metabolic diseases) of iodine exposure to thyroid functioning and morphology in developing (i.e., embryonic) alligators. Boggs et al. (2013) demonstrated that embryonic exposure to elevated iodine and other endocrine disrupting chemicals can alter the morphology and function of the thyroid gland, which could potentially lead to the development of harmful thyroid syndromes later in life (i.e., thyrotoxicosis, hyper-or hypo-thyroidism). Iodine content is much higher in the tissues of estuarine-versus freshwater-and terrestrial-inhabiting prey, thus the degree to which coastal alligators consume estuarine prey could potentially influence thyroid hormone production and metabolism. ...
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... American alligators (Alligator mississippiensis) inhabiting Lake Apopka (Orange county, Florida, USA), a site contaminated with OCPs (Guillette Jr. et al., 1999;Heinz et al., 1991), exhibit altered thyroidal phenotypes that include diminished neonatal plasma TH concentrations, altered thyroidal histomorphology, and impaired growth (Boggs et al., 2013), as well as disrupted reproductive physiology, including gonadal transcription, steroidogenesis, and systemic steroid hormone homeostasis (Crain et al., 1998;Guillette et al., 1994Guillette et al., , 1995Guillette et al., , 1996Guillette et al., , 1999Moore et al., 2012). Importantly, these effects are persistent; Boggs et al. (2013) and Moore et al. (2012) demonstrated that these impaired thyroidal and gonadal phenotypes, respectively, remain present in Lake Apopka animals raised under controlled laboratory conditions for months, indicating that in ovo OCP exposure induces organizational effects with long-lasting consequences on the alligator endocrine system. ...
... American alligators (Alligator mississippiensis) inhabiting Lake Apopka (Orange county, Florida, USA), a site contaminated with OCPs (Guillette Jr. et al., 1999;Heinz et al., 1991), exhibit altered thyroidal phenotypes that include diminished neonatal plasma TH concentrations, altered thyroidal histomorphology, and impaired growth (Boggs et al., 2013), as well as disrupted reproductive physiology, including gonadal transcription, steroidogenesis, and systemic steroid hormone homeostasis (Crain et al., 1998;Guillette et al., 1994Guillette et al., , 1995Guillette et al., , 1996Guillette et al., , 1999Moore et al., 2012). Importantly, these effects are persistent; Boggs et al. (2013) and Moore et al. (2012) demonstrated that these impaired thyroidal and gonadal phenotypes, respectively, remain present in Lake Apopka animals raised under controlled laboratory conditions for months, indicating that in ovo OCP exposure induces organizational effects with long-lasting consequences on the alligator endocrine system. Thus, the Lake Apopka alligator population presents a unique opportunity to examine the effects of steroid hormone disruption on both short-and long-term thyroid physiology under realistic exposure conditions. ...
... Using an ecologically relevant model in which persistent thyroidal abnormalities have been linked to OCP exposure, we describe both the native transcriptional patterns of genes related to thyroid function and steroid hormone signaling in the alligator embryo, as well as the functional consequences of embryonic exposure to exogenous steroid hormones on transcription of these genes later in life. While embryonic stages are critical windows of thyroid hormone activity in vertebrates, previous studies of American alligator thyroidal physiology have not described embryonic life stages (Bermudez et al., 2011;Boggs et al., 2013Boggs et al., , 2016. In this study we test two competing hypotheses regarding the roles that steroid hormones play in mediating OCP-induced thyroid disruption. ...
Assessing Impacts of Precocious Steroid Exposure on Thyroid Physiology and Gene Expression Patterns in the American Alligator (Alligator mississippiensis)
Article
  • Nov 2018
The thyroid gland is sensitive to steroid hormone signaling, and many thyroid disrupting contaminants also disrupt steroid hormone homeostasis, presenting the possibility that thyroid disruption may occur through altered steroid hormone signaling. To examine this possibility, we studied short-term and persistent impacts of embryonic sex steroid exposure on thyroid physiology in the American alligator. Alligators from a lake contaminated with endocrine disrupting contaminants (Lake Apopka, FL, USA) have been shown to display characteristics of thyroid and steroid hormone disruption. Previous studies suggest these alterations arise during development and raise the possibility that exposure to maternally deposited contaminants might underlie persistent organizational changes in both thyroidal and reproductive function. Thus, this population provides a system to investigate contaminant-mediated organizational thyroid disruption in an environmentally-relevant context. We assess the developmental expression of genetic pathways involved in thyroid hormone biosynthesis and find that expression of these genes increases prior to hatching. Further, we show that nuclear steroid hormone receptors are also expressed during this period, indicating the developing thyroid is potentially responsive to steroid hormone signaling. We then explore functional roles of steroid signaling during development on subsequent thyroid function in juvenile alligators. We exposed alligator eggs collected from both Lake Apopka and a reference site to 17β-estradiol and a non-aromatizable androgen during embryonic development, and investigated effects of exposure on hatchling morphometrics and thyroidal gene expression profiles at 5 months of age. Steroid hormone treatment did not impact the timing of hatching or hatchling size. Furthermore, treatment with steroid hormones did not result in detectable impacts on thyroid transcriptional programs, suggesting that precocious or excess estrogen and androgen exposure does not influence immediate or long-term thyroidal physiology.
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... While no relevant studies were reported in birds, in a study investigating the impact of embryonic sex steroid exposure on thyroid physiology in the American alligator (Alligator mississippiensis) from the EDCcontaminated Lake Apopka, results suggested that estradiol exposure did not impact thyroid physiology in these alligators (Galligan et al., 2019). This indicated that the effect of in ovo organochlorine pesticide exposure on the organization of the thyroid reported in a related study on this species (Boggs et al., 2013) was not mediated through estrogens. ...
... Analyses from Lake Apopka alligators demonstrated that embryonic androgen (dihydrotestosterone) exposure did not impact thyroid physiology (Galligan et al., 2019). This indicated that the effect of in ovo organochlorine pesticide exposure on the organization of the thyroid reported in a related study on this species (Boggs et al., 2013) was not mediated through steroid hormones. The authors could therefore not conclude that thyroidal physiology in the American alligator is sensitive to steroid hormone signaling at early life stages. ...
Disruption by stealth - Interference of endocrine disrupting chemicals on hormonal crosstalk with thyroid axis function in humans and other animals
Article
Full-text available
  • Aug 2021
  • ENVIRON RES
Thyroid hormones (THs) are important regulators of growth, development, and homeostasis of all vertebrates. There are many environmental contaminants that are known to disrupt TH action, yet their mechanisms are only partially understood. While the effects of Endocrine Disrupting Chemicals (EDCs) are mostly studied as “hormone system silos”, the present critical review highlights the complexity of EDCs interfering with TH function through their interactions with other hormonal axes involved in reproduction, stress, and energy metabolism. The impact of EDCs on components that are shared between hormone signaling pathways or intersect between pathways can thus extend beyond the molecular ramifications to cellular, physiological, behavioral, and whole-body consequences for exposed organisms. The comparatively more extensive studies conducted in mammalian models provides encouraging support for expanded investigation and highlight the paucity of data generated in other non-mammalian vertebrate classes. As greater genomics-based resources become available across vertebrate classes, better identification and delineation of EDC effects, modes of action, and identification of effective biomarkers suitable for HPT disruption is possible. EDC-derived effects are likely to cascade into a plurality of physiological effects far more complex than the few variables tested within any research studies. The field should move towards understanding a system of hormonal systems’ interactions rather than maintaining hormone system silos.
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... A further well-known case of endocrine disruption in a wild population is the American alligators, Alligator mississippiensis, inhabiting the polluted Lake Apopka, Florida, United States, where both males and female alligators were shown to exhibit developmental abnormalities in their reproductive systems (Guillette et al., 1994;Guillette et al., 1996). Moreover, the thyroid systems of juvenile Lake Apopka alligators were also significantly impacted with abnormal thyroid anatomy and thyroid hormone levels being observed in hatchlings (Boggs et al., 2013;Crain et al., 1998) The potential sources of EDCs in the CRC include WWTW, agriculture (crops, livestock, aquaculture), forestry, landfills, paper and pulp effluent, trace metals and mining and metallurgy. ...
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... Increased salinity also appears to influence thyroid development and thyroid hormone (TH) secretion in alligators, which unlike many species of crocodiles, do not have extrarenal salt glands. Neonatal American alligators hatched from eggs collected from an estuarine barrier island population exhibited thyroid hyperplasia and higher triiodothyronine (T 3 ) concentrations than neonates from an inland population (Boggs et al., 2013). Although these differences do not persist in hatchlings maintained in freshwater conditions, juvenile alligators from the barrier island population have higher TH concentrations and lower plasma inorganic iodide (pI À ) in comparison to the inland population (Boggs et al., 2011). ...
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... Given that snapping turtles were studied a few days after hatching, longer-term studies will be required to distinguish whether these effects are simply due to thermal acclimation or are the result of developmental programming of metabolic phenotype. Nevertheless, studies of American alligators do suggest that disruption of thyroid hormone signaling during embryogenesis can program functioning of the hypothalamic-pituitary-thyroid axis as long as 10 months after hatching (Boggs et al., 2013). ...
Embryonic Temperature Programs Phenotype in Reptiles
Article
Full-text available
  • Jan 2020
Reptiles are critically affected by temperature throughout their lifespan, but especially so during early development. Temperature-induced changes in phenotype are a specific example of a broader phenomenon called phenotypic plasticity in which a single individual is able to develop different phenotypes when exposed to different environments. With climate change occurring at an unprecedented rate, it is important to study temperature effects on reptiles. For example, the potential impact of global warming is especially pronounced in species with temperature-dependent sex determination (TSD) because temperature has a direct effect on a key phenotypic (sex) and demographic (population sex ratios) trait. Reptiles with TSD also serve as models for studying temperature effects on the development of other traits that display continuous variation. Temperature directly influences metabolic and developmental rate of embryos and can have permanent effects on phenotype that last beyond the embryonic period. For instance, incubation temperature programs post-hatching hormone production and growth physiology, which can profoundly influence fitness. Here, we review current knowledge of temperature effects on phenotypic and developmental plasticity in reptiles. First, we examine the direct effect of temperature on biophysical processes, the concept of thermal performance curves, and the process of thermal acclimation. After discussing these reversible temperature effects, we focus the bulk of the review on developmental programming of phenotype by temperature during embryogenesis (i.e., permanent developmental effects). We focus on oviparous species because eggs are especially susceptible to changes in ambient temperature. We then discuss recent work probing the role of epigenetic mechanisms in mediating temperature effects on phenotype. Based on phenotypic effects of temperature, we return to the potential impact of global warming on reptiles. Finally, we highlight key areas for future research, including the identification of temperature sensors and assessment of genetic variation for thermosensitivity.
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Effects of perchlorate and exogenous T4 on growth, development and tail resorption of Rana chensinensis
Article
  • Aug 2023
Endocrine disruptors have been demonstrated to exert adverse effects on growth and development of amphibians by disrupting hormone levels. Tail resorption, which is one of the most remarkable events during amphibian metamorphosis, is closely associated with thyroid hormones levels. However, limited research has been conducted on the effects of endocrine disruptors on tail resorption in amphibians. This study explored the effects of NaClO4 and T4 on the growth, development and tail resorption during the metamorphosis of Rana Chensinensis. The results demonstrated that exposure to NaClO4 led to an increase in body size and a delay in metamorphosis of R. Chensinensis tadpoles. Histological analysis revealed that both NaClO4 and exogenous T4 exposure resulted in thyroid gland injury, and NaClO4 treatment delayed the degradation of notochord and muscles, thereby delaying tail resorption. Moreover, transcriptome sequencing results showed that apoptosis-related genes (APAF1, BAX and CASP6) and cell component degradation-related genes (MMP9 and MMP13) were highly expressed in the T4 exposure group, and the expression of oxidative stress-related genes (SOD and CAT) was higher in the NaClO4 exposure group. Taken together, both NaClO4 and exogenous T4 affect tail resorption in R. Chensinensis, thereby affecting their adaptation to terrestrial life. The present study will not only provide a reference for future experimental research on the effects of other endocrine disruptors on the growth, development and tail resorption of amphibians but will also provide insights into environmental protection and ecological risk assessment.
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Effects of perchlorate and exogenous T4 exposures on development, metamorphosis and endochondral ossification in Bufo gargarizans larvae
Article
  • Nov 2021
  • AQUAT TOXICOL
Several endocrine-disrupting chemicals (EDCs) have been proven to interfere with the physiological function of thyroid hormone (TH), which affected growth and development. However, few studies have investigated the effects of EDCs on TH axis with consequence for skeletal development in amphibians. This study thus examined the potential role of perchlorate and T4 in growth, development and endochondral ossification during metamorphosis of Bufo gargarizans. Our studies showed that NaClO₄ treatment caused weight gain and delayed the developmental stage in B. gargarizans tadpoles, while T4 decreased body size and survival rate, accelerated metamorphic duration and increased the risk of early death. Histological sections suggested that NaClO₄ and T4 treatments caused damages to thyroid tissue, such as decreased thyroid gland size, follicle size, colloid area, the height of follicular epithelial cells and the number of follicles. In addition, the double skeletal staining and RT-qPCR showed that NaClO₄ and T4 treatments inhibited the endochondral ossification by regulating TH synthesis (TRs, Dios) and endochondral ossification-related genes (MMPs, Runxs, VEGFs and VEGFRs) expression levels, which might affect terrestrial locomotion and terrestrial life. Altogether, these thyroid injury and gene expression changes as caused by NaClO₄ and T4 may have an influence on development and endochondral ossification during the metamorphosis of amphibians.
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Is maternal thyroid hormone deposition subject to a trade-off between self and egg because of iodine? An experimental study in rock pigeon
Article
Full-text available
  • Oct 2021
Maternal hormones constitute a key signalling pathway for mothers to shape offspring phenotype and fitness. Thyroid hormones (THs; triiodothyronine, T3 and thyroxine, T4) are metabolic hormones known to play crucial roles in embryonic development and survival in all vertebrates. During early developmental stages, embryos exclusively rely on the exposure to maternal THs, and maternal hypothyroidism can cause severe embryonic maldevelopment. The TH molecule includes iodine, an element that cannot be synthesised by the organism. Therefore, TH production may become costly when environmental iodine availability is low. This may yield a trade-off for breeding females between allocating the hormones to self or to their eggs, potentially to the extent that it even influences the number of laid eggs. In this study, we investigated whether low dietary iodine may limit TH production and transfer to the eggs in a captive population of Rock pigeons (Columba livia). We provided breeding females with an iodine-restricted (I- diet) or iodine-supplemented diet (I+ diet) and measured the resulting circulating and yolk iodine and TH concentrations and the number of eggs laid. Our iodine-restricted diet successfully decreased both circulating and yolk iodine concentrations compared to the supplemented diet, but not circulating or yolk THs. This indicates that mothers may not be able to independently regulate hormone exposure for self and their embryos. However, egg production was clearly reduced in the I- group, with fewer females laying eggs. This result shows that restricted availability of iodine does induce a cost in terms of egg production. Whether females reduced egg production to preserve THs for themselves or to prevent embryos from exposure to low iodine and/or THs is as yet unclear.
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Is maternal thyroid hormone deposition subject to a trade-off between self and egg because of iodine? An experimental study in rock pigeon
Preprint
Full-text available
  • Jan 2021
Maternal hormones constitute a key signalling pathway for mothers to shape offspring phenotype and fitness. Thyroid hormones (THs; triiodothyronine, T3 and thyroxine, T4) are metabolic hormones known to play crucial roles in embryonic development and survival in all vertebrates. During early developmental stages, embryos exclusively rely on the exposure to maternal THs, and maternal hypothyroidism can cause severe embryonic maldevelopment. The TH molecule includes iodine, an element that cannot be synthesised by the organism. Therefore, TH production may become costly when environmental iodine availability is low. This may yield a trade-off for breeding females between allocating the hormones to self or to their eggs, potentially to the extent that it even influences the number of laid eggs. In this study, we investigated whether low dietary iodine may limit TH production and transfer to the eggs in a captive population of Rock pigeons (Columba livia). We provided breeding females with an iodine-restricted (I- diet) or iodine-supplemented diet (I+ diet) and measured the resulting circulating and yolk iodine and TH concentrations and the number of eggs laid. Our iodine-restricted diet successfully decreased both circulating and yolk iodine concentrations compared to the supplemented diet, but not circulating or yolk THs. This indicates that mothers may not be able to independently regulate hormone exposure for self and their embryos. However, egg production was clearly reduced in the I- group, with fewer females laying eggs. This result shows that restricted availability of iodine does induce a cost in terms of egg production. Whether females reduced egg production to preserve THs for themselves or to prevent embryos from exposure to low iodine and/or THs is as yet unclear.
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Growth Rates of Crocodylus Porosus (Reptilia: Crocodilia) From Arnhem Land, Northern Australia
Article
Full-text available
  • Jan 1978
In C. porosus < 80 cm SVL (snout-vent length), growth rate decreases as body size increases; males grow faster than females, and both sexes grow faster in the wet season than in the dry season. If the exponential growth curve for specimens < 80cm SVL is extrapolated, it underestimates the maximum size of C. porosus. A second growth curve for specimens > 80cm SVL has been derived separately, and the two curves intersect in the vicinity of 70 cm SVL. The size at which C. porosus cease growing seems quite variable and some data indicate a range of 3.9-6.0 m total length for males. The twocurve growth model is thought to reflect an energetic advantage in feeding on large rather than small prey.
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Lingual salt glands inCrocodylus acutus andC. johnstoni and their absence fromAlligator mississipiensis andCaiman crocodilus
Article
Full-text available
  • Mar 1982
1. Lingual salt glands, secreting hyperosmotic Na/K solutions in response to methacholine, are present inCrocodylus acutus andC. johnstoni but apparently absent from the alligatorids,Alligator mississipiensis andCaiman crocodilus. 2. Both secretory rates (6–20 mol/100 gh) and concentrations (450–600 mM Na) of glandular secretions are essentially identical in the marine/estuarineC. acutus andC. porosus and significantly higher than in the freshwaterC. johnstoni (1–2 mol/100 gh; 320–420 mM Na). 3. Lingual glands inAlligator secrete isosmotic Na/K at low rates (1–2 mol/100 gh) while those ofCaiman show no response to methacholine. 4. The physiological contrast between alligatorids and crocodylids is reflected in distinct differences in the superficial appearance of the tongue and lingual pores. 5. It is postulated that the alligatorid condition of low secretory capacity and isosmotic secretion reflects the primitive salivary function of lingual glands from which the salt-secreting capability in crocodylids was derived.
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Modeling the effect of toxicants on the parameters of dynamic energy budget models
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  • Jan 1997
Toxicants negatively affect the rates of growth and reproduction of organisms. Dynamic energy budget models offer a convenient mathematical framework to describe growth and reproduction by individuals. Since these models take into account the lipid content of an animal, the accumulation of toxicants is easily incorporated. This paper deals with the subsequent effects of toxicants on growth and reproduction. We argue that the concept of non-competitive inhibition is applicable for toxicants that increase maintenance demands and reduce assimilation. In this way, energy investment in growth and reproduction are indirectly reduced.
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Contaminants in American alligator eggs from Lake Apopka, Lake Griffin, and Lake Okeechobee, Florida
Article
  • Mar 1991
Residues of organochlorine pesticides, polychlorinated biphenyls (PCBs), and 16 elements were measured in American alligator (Alligator mississippiensis) eggs collected in 1984 from Lakes Apopka, Griffin, and Okeechobee in central and south Florida. Organochlorine pesticides were highest in eggs from Lake Apopka. None of the elements appeared to be present at harmful concentrations in eggs from any of the lakes. A larger sample of eggs was collected in 1985, but only from Lakes Griffin, a lake where eggs were relatively clean, and Apopka, where eggs were most contaminated. In 1985, hatching success of artificially incubated eggs was lower for Lake Apopka, and several organochlorine pesticides were higher than in eggs from Lake Griffin. However, within Lake Apopka, higher levels of pesticides in chemically analyzed eggs were not associated with reduced hatching success of the remaining eggs in the clutch. Therefore, it did not appear that any of the pesticides we measured were responsible for the reduced hatching success of Lake Apopka eggs.
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Developmental Plasticity, Epigenetics and Human Health
Article
  • Dec 2012
The unrelenting rise in global rates of non-communicable disease has necessitated a thorough re-evaluation of the current use of adult- and lifestyle-based strategies to curb the growing epidemic. There is a rapidly emerging set of epidemiological, experimental and clinical data suggesting that developmental factors play a considerable role in determining individual disease risk later in life. This phenomenon is known as the Developmental Origins of Health and Disease (DOHaD). Developmental factors, such as maternal and paternal nutrition, gestational diabetes mellitus, and even the normative range of developmental experiences, may evoke the processes of developmental plasticity which enable an organism to change its developmental trajectory in response to environmental cues. However in the event of a mismatch between the early and mature environment, such anticipatory responses may become maladaptive and lead to elevated risk of disease. The evo-devo and eco-evo-devo framework for DOHaD has more recently been supported by mechanistic insights enabled by rapid advances in epigenetic research. Increasing evidence suggests that developmental plasticity may be effected by epigenetically mediated modulation of the expression of specific genes. These mechanisms include DNA methylation, histone modifications and noncoding RNA activity. A growing number of animal studies also point towards the transgenerational inheritance of epigenetic marks, which may have implications for the perpetuation of ill-health. However early-life epigenotyping may find utility as a prognostic marker of metabolic dysfunction for identification and treatment of at-risk individuals.
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Contaminant-induced endocrine and reproductive alterations in reptiles
Article
Many chemicals introduced into the environment by humans adversely affect embryonic development and the functioning of the vertebrate reproductive system. It has been hypothesized that many developmental alterations are due to the endocrine-disruptive effects of various environmental contaminants. The endocrine system exhibits an organizational effect on the developing embryo, altering gene expression and dosing. Thus, a disruption of the normal hormonal signals can permanently modify the organization and future functioning of the reproductive and endocrine system. We have worked extensively with contaminant-exposed and reference populations of the American alligator ( Alligator mississippiensis ) as well as performed a number of experimental studies exposing developing embryos to various persistent and nonpersistent pesticides. Using this species, we have described altered steroidogenesis, circulating hormone levels, and hepatic transformation of androgen and endocrine organ (gonad, thyroid) morphology in juvenile alligators living in polluted environments. Given the adverse observations reported to date, we recommend several important future needs: Further development of "receptor zoos" and other molecular tools that include key reptiles from various major ecosystems, in addition to freshwater ecosystems. Global studies extending the current knowledge base on crocodilians and freshwater turtles to comparable ecosystems on other continents, such as linked studies examining and extending current molecular to population level studies in Florida (USA) to tropical and temporate regions of Africa, Australia, and South America. Further studies of actual exposure, assimilation and excretion of contaminants by ectothermic vertebrates, especially reptiles that occupy high levels of the food chain.
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Sex‐steroid and thyroid hormone concentrations in juvenile alligators (Alligator mississippiensis) from contaminated and reference lakes in Florida, USA
Article
  • Mar 1998
  • ENVIRON TOXICOL CHEM
Sex-steroid and thyroid hormones are critical regulators of growth and reproduction in all vertebrates, and several recent studies suggest that environmental chemicals can alter circulating concentrations of these hormones. This study examines plasma concentrations of estradiol-17β (E2), testosterone (T), triiodothyronine (T3), and thyroxine (T4) in juvenile alligators (60–140 cm total length) from two contaminated lakes and one reference lake in Florida. First, the data were analyzed by comparing hormone concentrations among males and females from the different lakes. Whereas there were no differences in plasma E2 concentrations among animals of the three lakes, male alligators from the contaminated lakes (Lake Apopka and Lake Okeechobee) had significantly lower plasma T concentrations compared to males from the reference lake (Lake Woodruff). Concentrations of thyroid hormones also differed in animals of the three lakes, with T4 concentrations being elevated in Lake Okeechobee males compared to Lake Woodruff males. Second, the relationship between body size and hormone concentration was examined using regression analysis. Most notably for steroid hormones, no clear relationship was detected between E2 and total length in Apopka females (r2 = 0.09, p = 0.54) or between T and total length in Apopka males (r2 = 0.007, p = 0.75). Females from Apopka (r2 = 0.318, p = 0.09) and Okeechobee (r2 = 0.222, p = 0.09) exhibited weak correlations between T3 and total length. Males from Apopka (r2 = 0.015, p = 0.66) and Okeechobee (r2 = 0.128, p = 0.19) showed no correlation between T4 and total length. These results indicate: some of the previously reported abnormalities in steroid hormones of hatchling alligators persist, at least, through the juvenile years; steroid and thyroid hormones are related to body size in juvenile alligators from the reference lake, whereas alligators living in lakes Apopka and Okeechobee experience alterations in circulating thyroid and steroid hormones in relationship to body size; and a number of the hormone abnormalities reported previously for Lake Apopka alligators are observed in alligators from Lake Okeechobee—a lake associated with numerous contaminant sources but no major chemical spill. The endocrine alterations reported in this study are hypothesized to be a response to embryonic exposure to endocrine-disrupting contaminants.
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