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Abstract

Many threats exist to reptile populations, environmental pollutants being one of them. Lizards and other reptiles are usually not taken into consideration in environmental risk assessments, with the use of surrogate species for their estimates. Unfortunately, not all pesticides have the same effects in the reptile species and on these surrogates, birds and mammals, some being more toxic in lizards. This difference brings the need to evaluate their toxicity in lizards to safeguard its protection. Studies in the last decades involving contaminants’ toxicity in lizard species have increased, thus we proposed to gather these information in this comprehensive review. Through searches in databases about the toxicity of pesticides in lizards, 16 scientific articles were found. Most studies investigated locomotor performance, histopathology, oxidative stress, neurotoxicology, and genetic damage from diverse pesticides with different modes of action. Progress has been made to acquire data on lizard ecotoxicology and more research is needed to cover more variables, such as studies in the embryologic stage and different pesticides.

Keywords

Reptile histopathology oxidative stress neurotoxicity locomotor performance

Introduction

Reptile populations are declining and their main threats are environmental pollutants, global climate changes, habitat loss and degradation, invasive species, and disease/parasitism. Despite its significance, very little is understood from pollutant effects in reptiles, and the group has been highly overlooked in ecotoxicological investigations. A paucity of data regarding exposure and effects of environmental contaminants on reptiles present a challenge for assessing ecological risks to these species.^1
–3

Reptiles are usually not considered in environmental risk assessments under the assumption that birds and mammals estimates would be good and safe surrogates for them. Nevertheless, some pesticides are more toxic to lizards than birds and mammals. Due to unique physiological and biological features of reptiles, predicting the effects of environmental contaminants on reptiles with toxicity parameters established to other vertebrates may likely to be ineffective. More toxicological data are needed to determine which pesticides provide a reasonable surrogate for reptiles.^3,4
–6

Lizards must be included in any realistic study on environmental toxicants, as they comprise a large percentage of reptiles and are an important component in many terrestrial and aquatic ecosystems, from which one in five lizard species is threatened with extinction.^4,7 Lizards are easily exposed to pesticides in several ways, including ingestion of contaminated food, dermal exposure, inhalation, maternal transfer to eggs/young, and absorption by eggs of contaminants from surrounding environments. Thus, many species are vulnerable to the adverse effects of pollutants, even though they are not the target species, and these threats to their diversity need more attention from the scientific community.⁸

Fortunately, in the last decades, there has been an increase in ecotoxicological studies involving lizards. We aimed to assess data concerning the toxicology of diverse pesticides on lizard species, gathering here the main effects reported.

To this purpose, subjects and titles/abstracts containing the keywords “pesticide” and “reptile” or “lizard” were searched. Two scientific databases were used, PubMed and Periódicos CAPES. Inclusion factors were studies evaluating the toxicity of pesticides in lizard species. Exclusion factors were scientific articles that did not evaluate pesticides effects, studies without lizards as the animal model, and studies that did not involve a laboratory-controlled experiment.

Literature review

We found 48 articles (excluding redundant titles) and 16 of them fit the inclusion criteria, half of which were published in the last 5 years. Most works (16–81.25%) studied the effects of insecticides, from which one also studied a fungicide and three (18.75%) evaluated the effects of herbicides. Oral gavage was the preferred method of administration of the pesticides (9–56.25%), followed by direct or indirect dermal exposition (4–25%), the remaining studies (18.75%) each had different methods. One study injected it and another administered through the diet. Only one work used embryos to test the pesticide, and it was applied directly in the eggs. Information about the species, route and period of exposure, doses, and parameters evaluated are listed in Table 1.

Table 1.

Data from the articles analyzed in the review.

Reference	Type of pesticide	Pesticide	Species	Number (n) of lizards	Route of exposure	Period of exposure	Doses	Parameters evaluated
Carpenter et al.⁹	Herbicide	Glyphosate	Oligosoma polychrome	58	Sprayed in subject (covered with a 4-cm layer of loose straw)	Once	144 mg/L water	Mass (once a week for 8 weeks); thermoregulatory behavior (across 21 days)
Schaumburg et al.¹⁰	Herbicide	Glyphosate	Salvator merianae	96 eggs	Topical on egg	Once	50, 100, 200, 400, 800, and 1600 μg/egg	Micronucleus test; nuclear abnormalities assay; comet assay (after 6 and 12 months of life)
Zhang et al.¹¹	Herbicide	GLA; l-GLA	Eremias argus	90	Contaminated soil	60 days	20 mg/kg soil weight	Locomotor perfomance (after 14 days); brain accumulation of the herbicide; biochemical analysis (GS, AChE, CAT, SOD enzyme, and MDA)
Holem et al.¹²	Insecticide	Malathion	Sceloporus occidentalis	50	Oral gavage	Once	0.2, 2, 20, and 200 mg/kg body weight	Locomotor performance (24 h before dosing, 4, 24, 120, and 312 h post-dose)
Khan¹³	Insecticide	Cypermethrin; malathion	Calotes versicolor	No data	Injected	Once	1 µL	Cholinesterase activity (after 24 h)
Holem et al.¹⁴	Insecticide	Malathion	Sceloporus occidentalis	52	Oral gavage	81 days—every 27 days	2.0, 20, and 100 mg/kg body weight	Terrestrial and arboreal locomotor performance (24 h before dosing, 24, 288, and 576 h post-dose); growth and food consumption (before each feeding)
DuRant et al.¹⁵	Insecticide	Carbaryl	Sceloporus occidentalis	121	Oral gavage	Once	2.5, 25, and 250 mg/kg	Terrestrial and arboreal locomotor performance (24 h before dosing, 4, 24, and 96 h post-dose)
Cakici and Akat¹⁶	Insecticide	Carbaryl	Ophisops elegans	64	Oral gavage	Once	2.5, 25, and 250 mg/kg	Histopathology of the digestive system (after 96 h)
Cakici and Akat¹⁷	Insecticide	Carbaryl	Ophisops elegans	No data	Oral gavage	Once	2.5, 25, and 250 mg/kg	Histopathology of testis (after 96 h)
Alexander et al.¹⁸	Insecticide	Deltamethrin	Meroles suborbitalis; Pedioplanis namaquensis	24; 28	Sprayed on subjects; sprayed on soil	Once	17.5 and 25 g	Poisoning symptoms (every 15 min after treatment for a day, then every 4 h for 2 days)
Talent¹⁹	Insecticide	Pyrethrin	Anolis carolinensis	140	Subjects were dipped in the solution	Once	300 mg/L	Temperature (15°C, 20°C, 25°C, 30°C, 35°C, and 38°C) influence on sensibility to pesticide (for 48 h)
Chen et al.²⁰	Insecticide	Beta-cypermethrin	Eremias argus	12	Oral gavage	Once	20 mg/kg body weight	Biochemical analyses (SOD, CAT, LDH, AChE enzyme, and MDA; after 96 h)
Chen et al.²¹	Insecticide	ACP	Eremias argus	144	Dietary (contaminate mealworms)	8 weeks	2 and 20 mg/kg wet weight of mealworms	Bioaccumulation of insecticide; biochemical analyses (SOD, CAT, GST enzyme, and MDA); hormone levels; histopathology; reproductive output
Chang et al.²²	Insecticide	LCT	Eremias argus	81	Oral gavage	21 days—once a week	10 mg/kg body weight	Bioaccumulation; thyroid gland lesions; thyroid hormone levels; HPT axis related gene expression
Wang et al.²³	Insecticide	Dinotefuran; TMX; IMI	Eremias argus	48	Oral gavage	35 days—twice a week	20 mg/kg body weight	Distribution, hormone concentrations (GH, GHRH, and SST); histopathology
Chang et al.²⁴	Insecticide	Flufenoxuron	Eremias argus	18	Oral gavage	21 days—once a week	50 mg/kg	Thyroid hormone levels; thyroid gland lesions; expression of HPT axis related genes
Chen et al.²¹	Fungicide	Myclobutanil	Eremias argus	12	Oral gavage	Once	20 mg/kg body weight	Biochemical analyses (SOD, CAT, LDH, AChE enzyme, and MDA; after 96 h

GLA: glufosinate-ammonium; l-GLA: l-glufosinate-ammonium; GS: glutamine synthetase; AChE: acetylcholinesterase; CAT: catalase; SOD: superoxide dismutase; MDA: malondialdehyde; LDH: lactate dehydrogenase; GST: glutathione-S-transferase; HPT: hypothalamus–pituitary–thyroid; ACP: alpha-cypermethrin; LCT: lambda-cyhalothrin; TMX: thiamethoxam; IMI: imidacloprid; GH: growth hormone; GHRH: growth hormone-releasing hormone; SST: somatostatin.

Herbicides

Herbicides are synthetic or natural compounds used to eliminate unwanted plants. Nonselective herbicides kill all plants on contact, while selective herbicides control specific weeds. Current herbicides have several modes of action, including inhibition of specific enzymes that cause the stop of a metabolic via, leading to the organisms’ death.^25,26 Glyphosate is a widely used herbicide, and it inhibits the activity of the enzyme enolpyruvylshikimate-3-phosphate synthase from the shikimic acid pathway, which converts simple carbohydrate into aromatic amino acids.^26,27 Glufosinate ammonium inhibits glutamine synthetase (GS), an enzyme responsible for the production of glutamine, leading to the buildup of ammonia and impairment of photorespiration and photosynthesis.^11,28

Additives in commercial formulations of pesticides may be more toxic than the active ingredient.^9,29 Aronzon et al.²⁹ suggest that the toxicity of commercial products is relevant to risk assessments regarding environmental protection and human health because only the data of active ingredients are considered for regulatory purposes and the effect on nontarget species may be undervalued.

Two glyphosate formulations, Agpro Glyphosate 360 and Yates Roundup Weedkiller, were tested in adult Oligosoma polychroma (New Zealand common skink) for changes in mass and temperature. The animals were sprayed with a 4-cm layer of loose straw above the lizard to simulate vegetation cover. Neither of the glyphosate formulations impacted the mass significantly. Specimens could choose a cold or hot spot in the terrarium and those treated with Yates Roundup Weedkiller selected significantly higher temperatures across 3 weeks after exposure, which was not observed in the Agpro Glyphosate 360 group. This pesticide difference could be due to the different adjuvants used in the formulations.⁹

Genotoxic effects of the herbicide glyphosate Roundup® has been evaluated in neonates of Salvator merianae (Tegu lizard) after a single embryonic application at the beginning of incubation using doses of 50, 100, 200, 400, 800, and 1600 μg/egg. The size and growth of lizards at birth and after 6 months were not influenced by the herbicide. Through the micronucleus test, nuclear abnormalities assay and comet assay, which are biomarkers for genotoxic effects induced in erythrocytes, it was not observed any teratogenic effects. The comet assay indicates early DNA damage which can later be removed by DNA repair systems, while the other tests indicate harmful events. Only the comet assay presented statistically significant differences between the groups, the effect being worse in the 800 and 1600 μg/egg groups than in the 200 and 400 μg/egg groups.¹⁰

Glufosinate-ammonium (GLA) has a chiral center and a pair of chiral isomers. Its herbicidal activity was ascribed to the l-Glufosinate-ammonium (l-GLA).¹¹ Zhang et al.¹¹ hypothesized that both isomers would have different effects due to their different biological activity and bioaccumulation. Therefore, both enantiomers were tested in male and female specimens of Eremias argus (Mongolian racerunners). A dose of 20 mg/kg soil weight was mixed in the soil in which the experimental animals were kept for 60 days. GLA concentration in the brain was significantly higher, supporting the authors’ hypothesis that the isomers have different effects due to their difference in bioaccumulation.

Neurotoxic effects were a possibility for GLA and l-GLA, since glutamate is also a neurotransmitter and timidity and anxiety were observed in the lizards. Total number of turning back, mean sprint velocity, body weight, brain weight, and brain index were reduced in all groups, especially males. However, no changes in length were observed. A score to different neurotoxicity-related enzymes (GS, acetylcholinesterase (AChE), and Na⁺/K⁺-ATPase), antioxidant system (catalase (CAT) and superoxide dismutase (SOD)), and malondialdehyde (MDA) levels indicated that GLA mainly acted on GS, AChE, and CAT, while l-GLA pointed at AChE, Na⁺/K⁺-ATPase, SOD, and MDA levels. This study showed that both GLA and l-GLA could be neurotoxic and cause oxidative stress, although the isomers have different toxic effects, possibly due to different accumulation of the isomers in the lizard brain. It also reinforced the idea that males may be more sensitive and vulnerable to exogenous contaminants.¹¹

Insecticides

Organophosphates and carbamates

Organophosphates and carbamates are pesticides that act via cholinesterase inhibition. Cholinestarases are enzymes that cause the hydrolysis of acetylcholine, an excitatory neurotransmitter that is abundant in the nervous system and present in neuromuscular junctions. AChE inhibitors are either reversible or irreversible. Killing action of carbamates is based on reversible AChE inactivation and is considered safer than organophosphates insecticides, which irreversibly inhibit AChE causing more severe cholinergic poisoning.³⁰

Exposure to AChE inhibitory pesticides may result in a buildup of acetylcholine in neuromuscular junctions and disruption of neural function, possibly affecting locomotor performance and other activities such as food consumption, which could influence growth. The typical symptoms of AChE inhibitory pesticides acute poisoning are agitation, muscle weakness, muscle fasciculation, body/limb tremors, twitching, miosis, hypersalivation, and sweating. Severe poisoning may cause respiratory failure, unconsciousness, confusion, convulsions, and/or death.^12,30

Malathion is an organophosphate insecticide that has been studied in the lizard species Calotes versicolor (Oriental garden lizard) and Sceloporus occidentalis (Western fence lizard).^12
–14 Khan¹³ measured the cholinesterase activity in the liver and kidney of adult specimens of C. versicolor injected with 0.1% and 1% malathion and detected a decrease up to 30% and 65.09%, respectively, in its activity.

The terrestrial and arboreal locomotor performances of juvenile S. occidentalis were evaluated after exposure to malathion. Doses of 0.2, 2, 20, 100, and 200 mg/kg body weight were applied, and the doses of 0.2 and 200 mg/kg were administered once while the others were applied three times, weekly. Mass, length, growth, and food consumption were not significantly different from control. Mortality was similar among all groups, though the higher doses seemed to have more deaths, but it was not statistically significant.^12,14

Clinical symptoms of poisoning were exhibited by 70% of lizards that received a dose of 200 mg/kg malathion and 85% in the lizards that received three doses of 100 mg/kg (the effects subsided within 24 h). Terrestrial sprint velocity was increased in both groups, although not significantly. The mean maximum arboreal velocity was reduced in the high-dose group after the second dose was administered and half of the lizards refused to transverse in the arboreal setting, suggesting the lizards were less likely to engage in coordination-dependent activities.^12,14

Similar methods were used to study the terrestrial and arboreal sprint velocity of S. occidentalis after administration of the carbamate carbaryl. Single doses of 2.5, 25, or 250 mg/g were used in adult specimens. No deaths were observed; however, 58% the lizards of the high-dose group exhibited clinical signs of its exposure, which persisted up to 48 h after exposure. Carbaryl was found to have a stimulatory effect in lower doses (2.5 and 25 mg/g), but at the highest dose, the sprint speed was impaired. Endurance was also found to be reduced, as the speed diminished over time, especially in the highest dose group. The medium and high-dose groups also exhibited symptoms of impairment in arboreal tests, as it was more challenging and these data can be more relevant to the species, as it uses trees to capture preys and evade predators.¹⁵

Another species, Ophisops elegans (Snake-eyed lizard), was used to evaluate the histopathological effects of carbaryl on the digestive system and testes. Adult specimens were administered 2.5, 25, or 250 mg/kg in a single oral dose. No deaths were observed, though in the high-dose groups, the animals had slower movements.^16,17 Carbaryl potentially affect germ cell development and possibly have adverse effects on spermatogenesis and male fertility. It induced seminiferous tubule degeneration, increase of diameters of tubules, the disarrangement of spermatogenic cell lines, disrupted germ cell association, vacuolization, sloughing, and hemorrhage in a dose-related trend.¹⁶

The most important histological defects in the digestive system were observed in the stomach. Hemorrhage in the esophagus and vacuolization of gastric gland cells were the alterations observed in the low-dose group. Hemorrhage intensified in the esophagus and appeared in the large intestine; degeneration in the epithelial layer was observed in the stomach and small intestine in the medium dose. At high dose, epithelial cells were scattered and gastric glands disappeared in the stomach; in the small intestine, collapse of villi and hemorrhage were prominent, and in the large intestine, scattered secretory granules of goblet cells were observed.¹⁷ Thus, carbaryl has the potential to disrupt both male fertility and the digestive system of lizards.^16,17

Pyrethroids

Pyrethroids are synthetic insecticides derived from natural pyrethrins that target voltage-dependent sodium channels, which are present in axons of neurons leading nerve impulses through the organism. Closure of such channels is prevented by pyrethroids, keeping the axonal membrane depolarized, which leads to repetitive movement, paralysis, and ultimately death.^31,32

Alexander et al.¹⁸ tested the effect of deltamethrin diluted at 17.5 g (the recommended dose at the time) and 25 g in two lizard species, Meroles suborbitalis (spotted sand lizard) and Pedioplanis namaquensis (Namaqua sand lizard). Specimens were contaminated either directly via spray or indirectly via sprayed soil. Within an hour of treatment symptoms of poisoning were observed a loss of coordination, loss of righting response, sensitivity to bright light, and muscle spasms and panic. Animals with indirect contact took twice as long to manifest symptoms. Although the lizards appeared to recover by the next day, they all died within 2 months of treatments. The authors recommend cautions when spraying the pesticide to try and diminish the effects it has on nontarget lizard species.¹⁸

The toxicity of a natural pyrethrin insecticide was tested in adult Anolis carolinensis (Green anole lizards) through percutaneous exposition (18.7, 37.5, 75, 150, and 300 mg/L) in different temperatures (15°C, 20°C, 25°C, 30°C, 35°C, and 38°C). The animals were dipped in the solution, except the head, for 2 s. Mortality of lizards maintained at 15°C and 20°C and pyrethrin concentration levels of 75, 150, and 300 mg/L were significantly higher than of lizards maintained at 35°C and 38°C and exposed to lower doses. At 35°C, no mortality occurred when lizards were exposed to the 75 mg/L of pyrethrin mixture; however, at this same concentration, 70% of the lizards maintained at 20°C died. These results suggest that temperature is a factor to be considered when evaluating the toxicity of pesticides.¹⁹

Cholinesterase activity in the liver and kidney of C. versicolor was evaluated under the effect of 0.1% and 1% cypermethrin, administered by injection. Cypermethrin caused up to 35% and 54% decrease in the cholinesterase activity.¹³

Beta-cypermethrin was tested in E. argus to check oxidative stress and test whether saliva is a good diagnostic tool for oxidative stress in lizards. A single dose of 20 mg/kg body weight was administered through oral gavage. Antioxidant enzymes (SOD and CAT), lactate dehydrogenase (LDH), AChE, and MDA were measured from serum, saliva, brain, liver, kidney, and testes. The tested biomarkers increased or decreased in different manners in different tissues. Saliva was more correlated with kidney and gonad and LDH was more relevant to predict oxidative stress and could be a testing manner for toxicity that did not evolve the death of the animal.²⁰

Reproductive toxicity was tested in E. argus after treated food ingestion of alpha-cypermethrin (ACP). Mealworms were treated with 2 and 20 mg/kg of its wet weight and fed to the lizards for 8 weeks. Antioxidant enzyme levels, SOD, CAT, and glutathione-S-transferase (GST), MDA levels, hormone levels from serum, gonads, histopathology, and reproductive output were evaluated in adult male and female. Food consumption in both groups was decreased and decreases in body mass index and mortality were observed in a dose-dependent trend, having a stronger effect in females. Significant variations in GST and CAT activities and MDA levels in gonads suggest that lizards were under oxidative stress.²¹

No histopathological changes were observed in ovaries, although testis presented seminiferous tubule damage, germ cells sloughing and degeneration, and giant cells. ACP exposure also increased testosterone levels in males and reduced egg production of females. Females were in the breeding phase and may have been more susceptive to the pesticide. These negative effects highlight that ACP dietary exposure is a potential threat to lizards’ reproduction.¹³

Bioaccumulation, thyroid gland lesions, thyroid hormone levels, and gene expression related to the hypothalamus–pituitary–thyroid (HPT) axis was evaluated after administration of two lambda-cyhalothrin (LCT) enantiomers in juvenile male E. argus at three oral doses of 10 mg/kg body weight, for 3 weeks. Samples from plasma, feces, thyroid, liver, and brain were analyzed. The body and liver weight and were lower in the (+)-LCT enantiomer, and it was more concentrated in the feces than the (−)-LCT. The expression of HPT axis-related genes was altered in both enantiomers.²²

The thyroid gland treated with the (+)-LCT enantiomer showed an irregular shape of the follicles and there were clear signs of reabsorption in the follicle lumen. In the (−)-LCT enantiomer exposure group, the follicular area was enlarged and the number of follicles was decreased and the colloids were also decreased and no reabsorbing vacuoles were observed. Enantiomer (−)-LCT appeared to accumulate higher levels in the liver, however, its toxic effects on lizard growth, T3 level, and thyroid activity were relatively lower than those of (+)-LCT. Suggesting that (−) enantiomer caused less disruption on lizard thyroid than (+) enantiomer.²²

Neonicotinoids

Neonicotinoids are systemic pesticides with selective toxicity for insects that are agonists with irreversible binding at nicotinic acetylcholine receptors (nAChRs), which are present in the nervous system and are activated by acetylcholine. Contrary to acetylcholine, AChE does not act on neonicotinoids, leading to their prolonged action on the nAChRs which may cause paralysis and death.^33
–35

Distribution, metabolism, and hepatotoxicity of neonicotinoids dinotefuran (DIN), thiamethoxam (TMX), and imidacloprid (IMI) in E. argus were assessed at a dose of 20 mg/kg body weight through oral gavage, twice a week for 35 days. The accumulation of neonicotinoids increases the risk to lizards. The residual concentration of DIN was the highest among the three neonicotinoids selected, followed by TMX. IMI was most easily metabolized in lizards, and its terminal metabolite CPA was the main form of existence in lizards. Results indicated that all three neonicotinoids are easily excreted by excretion, and the order of accumulation in lizards was DIN > TMX > IMI. Bodyweight decrease during the experiment, being significantly different only in the DIN group by the end of the experiment. A significant decrease in the number of nuclei was observed in the liver tissues of all groups. The number of hepatocytes in the DIN, TMX, and IMI exposure groups decreased by 42 ± 11%, 30 ± 5%, and 56 ± 8%, respectively. Mild fibrosis occurred in all exposure groups, which was a precursor to cirrhosis. Accumulation of cells occurred in the DIN and IMI exposure groups.²³

In the continuous exposure of 35 days, exposure to DIN caused a decrease in plasma growth hormone (GH) concentration, downregulation of ghr, igf1, and igfbp2 gene expression, accompanied by oxidative stress damage in the liver, showing significant growth inhibition. Although IMI caused severe liver oxidative stress damage, the effect of IMI on the growth hormone/insulin-like growth factor (GH/IGF) pathway was not obvious. Compared to DIN and IMI, TMX was the least toxic to lizards. In general, neonicotinoids can significantly damage the liver of lizards and cause growth inhibition, being worthy of attention in the conservation of farmland lizards. Although concentrations of neonicotinoids in environmental soils usually do not reach the laboratory exposure concentration, lizards are exposed to a high concentration of pesticides during the pesticide application season.²³

Benzoylureas

The HTP axis is important to the development of lizards and the toxic effect of the insecticide flufenoxuron was evaluated on this axis through plasma thyroid hormone levels, thyroid gland histopathology, and expression profiles of thyroid hormone receptors, deiodinases, and transthyretin. Eremias argus was tested in the two phases of skin shedding, resting phase and proliferating phase, adult males and females were used for tests. Three doses of 50 mg/kg were used, administered once a week via oral gavage.²⁴

The results indicated that the sensibility of the specimens of E. argus to the pesticide varied according to the stages. The proliferation phase suggested downregulation on the T4 levels, whereas the T4 level was significantly increased at the resting phase after exposure. There was more serious damage to the thyroid gland in the proliferation phase. The expression of HPT axis-related genes correlates with the gender and tissue. It was tested in the liver, gonad, brain, kidney, skin, and thyroid gland, but there was a high expression only in the kidney, brain, and liver. In the female liver, the expression of tra, trb, dio1, dio2, and ttr genes was more seriously affected at the proliferation phase than that at the resting stage after treatment and in the brain, it was similar between both phases. In summary, flufenoxuron affects the thyroid endocrine system of lizards, having different effects on females and males.²⁴

Fungicides

Myclobutanil, a triazole fungicide, was evaluated in adult E. argus. A single dose of 20 mg/kg body weight through oral gavage was used and SOD, CAT, LDH, and AChE enzymes, as well as MDA, were measured from serum, saliva, brain, liver, kidney, and testes for oxidative stress. SOD activities were failed to be evaluated in serum and saliva. Myclobutanil did not affect SOD activities. CAT activities increased in kidney and decreased in brain and gonad. MDA levels decreased in gonad, serum, and saliva, which indicate an alteration in cell metabolism. LDH activity was increased in the brain and kidney, indicating cellular damage and anaerobic metabolism, while in the gonads, serum, and saliva, it decreased, suggesting reduced metabolism. The activity of AChE in the kidney and gonad decreased, while the activity in saliva increased, indicating different metabolism between different tissues and organs. Oxidative stress was less severe than beta-cypermethrin, tested in the same experiment.²⁰

Conclusion

Lizards can be contaminated with pesticides through several routes, mainly oral or dermal exposure, however, most works preferred oral administration, thus lacking data about dermal exposure. Younger animals are more sensitive to external pollutants and should get more attention in research, as eggs can be easily contaminated, and this review showed that only one report has been published which investigates neonates exposed in ovo.

Some pesticides are neurotoxic, targeting enzymes or receptors of the nervous system, which reflects in the behavior. It has been shown that locomotor velocity and even impairment of more coordinated movements may be a result of pesticide contamination. Oxidative stress assessment is also a common tool being used to assess toxicology of pesticides, as gene expression and bioaccumulation.

Pesticide effects cannot be generalized from a single group, and therefore, lizard data need to be considered in toxicology assessments, meaning more research needs to be done to acquire these data, as only 13 pesticides have been studied in lizards so far.

Footnotes

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was supported by the Fundação de Amparo à Pesquisa do Estado de Goiás (FAPEG) [scholarship number 201810267000852].

ORCID iD

LM Freitas

References

Gibbons

Scott

Ryan

, et al. The global decline of reptiles, Déjà Vu Amphibians. BioScience 2000; 50(8): 653–666.

Hopkins

. Reptile toxicology: challenges and opportunities on the last frontier in vertebrate ecotoxicology. Environ Toxicol Chem 2000; 19(10): 2391–2393.

Weir

Suski

Salice

. Ecological risk of anthropogenic pollutants to reptiles: evaluating assumptions of sensitivity and exposure. Environ Pollut 2010; 158(12): 3596–3606.

Campbell

. A logical starting point for developing priorities for lizard and snake ecotoxicology: a review of available data. Environ Toxicol Chem 2002; 21(5): 894–898.

Weir

Talent

, et al. Improving reptile ecological risk assessment: oral and dermal toxicity of pesticides to a common lizard species (Sceloporus occidentalis). Environ Toxicol Chem 2015; 34(8): 1778–1786.

Ortiz-Santaliestra

Maia

Egea-Serrano

, et al. Validity of fish, birds and mammals as surrogates for amphibians and reptiles in pesticide toxicity assessment. Ecotoxicology 2018; 27(7): 819–833.

Böhm

Collen

Baillie

JEM

, et al. The conservation status of the world’s reptiles. Biol Conserv 2013; 157: 372–385.

Amaral

Carretero

Bicho

, et al. The use of a lacertid lizard as a model for reptile ecotoxicology studies – part 1: field demographics and morphology. Chemosphere 2012; 87(7): 757–764.

Carpenter

Monks

Nelson

. The effect of two glyphosate formulations on a small, diurnal lizard (Oligosoma polychroma). Ecotoxicology 2016; 25(3): 548–554.

10.

Schaumburg

Siroski

Poletta

, et al. Genotoxicity induced by Roundup® (glyphosate) in tegu lizard (Salvator merianae) embryos. Pest Biochem Physiol 2016; 130: 71–78.

11.

Zhang

Chen

Meng

, et al. Bioaccumulation, behavior changes and physiological disruptions with gender-dependent in lizards (Eremias argus) after exposure to glufosinate-ammonium and L-glufosinate-ammonium. Chemosphere 2019; 226: 817–824.

12.

Holem

Hopkins

Talent

. Effect of acute exposure to malathion and lead on sprint performance of the western fence lizard (Sceloporus occidentalis). Arch Environ Contam Toxicol 2006; 51(1): 111–116.

13.

Khan

. Effects of agro pesticides cypermethrin and malathion on cholinesterase activity in liver and kidney of Calotes versicolor Daudin (Agamidae: Reptilia). Turk J Zool 2005; 29(1): 77–81.

14.

Holem

Hopkins

Talent

. Effects of repeated exposure to malathion on growth, food consumption, and locomotor performance of the western fence lizard (Sceloporus occidentalis). Environ Pollut 2008; 152(1): 92–98.

15.

DuRant

Hopkins

Talent

. Impaired terrestrial and arboreal locomotor performance in the western fence lizard (Sceloporus occidentalis) after exposure to an AChE-inhibiting pesticide. Environ Pollut 2007; 149(1): 18–24.

16.

Cakici

Akat

. Histopathological effects of carbaryl on digestive system of snake-eyed lizard, Ophisops elegans. Bull Environ Contam Toxicol 2012; 88(5): 685–690.

17.

Cakici

Akat

. Histopathological effects of carbaryl on testes of snake-eyed lizard, Ophisops elegans. Environ Sci Pollut Res Int 2012; 19(1): 64–71.

18.

Alexander

Horne

Hanrahan

. An evaluation of the effects of deltamethrin on two non-target lizard species in the Karoo, South Africa. J Arid Environ 2002; 50(1): 121–133.

19.

Talent

. Effect of temperature on toxicity of a natural pyrethrin pesticide to green anole lizards (Anolis carolinensis). Environ Toxicol Chem 2005; 24(12): 3113–3116.

20.

Chen

Diao

Zhang

, et al. Effects of beta-cypermethrin and myclobutanil on some enzymes and changes of biomarkers between internal tissues and saliva in reptiles (Eremias argus). Chemosphere 2019; 216: 69–74.

21.

Chen

Wang

Zhang

, et al. Ecological risk assessment of alpha-cypermethrin-treated food ingestion and reproductive toxicity in reptiles. Ecotoxicol Environ Safe 2019; 171: 657–664.

22.

Chang

Hao

, et al. Stereoselective degradation and thyroid endocrine disruption of lambda-cyhalothrin in lizards (Eremias argus) following oral exposure. Environ Pollut 2018; 232: 300–309.

23.

Wang

Zhang

, et al. Distribution, metabolism and hepatotoxicity of neonicotinoids in small farmland lizard and their effects on GH/IGF axis. Sci Total Environ 2019; 662: 834–841.

24.

Chang

Guo

, et al. Unraveling the different toxic effect of flufenoxuron on the thyroid endocrine system of the Mongolia racerunner (Eremias argus) at different stages. Chemosphere 2017; 172: 210–216.

25.

Zimdahl

. A history of weed science in the United States. London: Elsevier, 2010, p. 206.

26.

Duke

. Why have no new herbicide modes of action appeared in recent years? Pest Manag Sci 2012; 68(4): 505–512.

27.

Amrhein

Schab

Steinrücken

. The mode of action of the herbicide glyphosate. Naturwissenschaften 1980; 67(7): 356–357.

28.

Hack

Ebert

Ehling

, et al. Glufosinate ammonium—some aspects of its mode of action in mammals. Food Chem Toxicol 1994; 32(5): 461–470.

29.

Aronzon

Sandoval

Herkovits

, et al. Stage-dependent toxicity of 2,4-dichlorophenoxyacetic on the embryonic development of a South American toad, Rhinella arenarum. Environ Toxicol 2011; 26(4): 373–381.

30.

Colovic

Krstić

Lazarević-Pašti

, et al. Acetylcholinesterase inhibitors: pharmacology and toxicology. Curr Neuropharmacol 2013; 11(3): 315–335.

31.

Casida

Gammon

Glickman

, et al. Mechanisms of selective action of pyrethroid insecticides. Annu Rev Pharmacol Toxicol 1983; 23: 413–438.

32.

Vijverberg

vanden Bercken

. Neurotoxicological effects and the mode of action of pyrethroid insecticides. Crit Rev Toxicol 1990; 21(2): 105–126.

33.

Matsuda

Buckingham

Kleier

, et al. Neonicotinoids: insecticides acting on insect nicotinic acetylcholine receptors. Trends Pharmacol Sci 2001; 22(11): 573–580.

34.

Tomizawa

Casida

. Neonicotinoid insecticide toxicology: mechanisms of selective action. Annu Rev Pharmacol Toxicol 2005; 45: 247–268.

35.

Simon-Delso

Amaral-Rogers

Belzunces

, et al. Systemic insecticides (neonicotinoids and fipronil): trends, uses, mode of action and metabolites. Environ Sci Pollut Res Int 2015; 22(1): 5–34.

Toxicity of pesticides in lizards

Abstract

Keywords

Introduction

Literature review

Herbicides

Insecticides

Organophosphates and carbamates

Pyrethroids

Neonicotinoids

Benzoylureas

Fungicides

Conclusion

Footnotes

Declaration of conflicting interests

Funding

ORCID iD

References