Environ Monit Assess (2020) 192:454 https://doi.org/10.1007/s10661-020-08435-7 Lizards as model organisms to evaluate environmental contamination and biomonitoring Jadna Maria Silva & Júlio Alejandro Navoni & Eliza Maria Xavier Freire Received: 25 March 2020 /Accepted: 18 June 2020 # Springer Nature Switzerland AG 2020 Abstract Environmental contamination is reaching ev- most investigated was Lacertidae. The studies were er higher levels and affecting several animal popula- classified into two categories: organic contaminants tions, including humans. In this context, studies are (pesticides, petroleum by-products, and explosives) being developed to monitor and evaluate this environ- and inorganic contaminants (metals such as zinc, lead mental problem using bioindicators organisms, in addi- and aluminum, and radionuclides). Contaminants di- tion to testing the toxicity of contaminants in the labo- rectly contributed to DNA damage and to increasing ratory. In this perspective, reptiles are ideal animals for the frequency of micronuclei in exposed animals, histo- these types of studies, considering that they are ecto- pathological effects, and oxidative stress. The per- thermic and have a slower metabolism directly influenc- formed analysis highlights the usefulness of lizards as ing their recovery power, and therefore, they are more environmental biomonitors. However, the response pro- sensitive to xenobiotic effects. Among reptiles, lizards file is dependent on the exposure level and route, in are animals that adapt to various environmental condi- addition to the environmental scenario analyzed. There- tions, even being found in areas with arid characteristics. fore, future studies aimed at evaluating environmental Therefore, a literature review was conducted in this contaminants are required under exposure conditions study regarding the use of lizards as models for ecotox- more related to the environmental reality to be studied. icological studies, including biomonitoring, carried out in the last 10 years, with the aim of evaluating them as Keywords Bioindicators . Environmental monitoring . bioindicators in Brazilian semi-arid region. Studies were Organic contaminants . Pesticides . Inorganic found involving ten lizard families, among which the contaminants : J. M. Silva E. M. X. Freire Introduction Departamento de Botânica e Zoologia, Laboratório de Herpetologia, Universidade Federal do Rio Grande do Norte, Natal, Rio Grande do Norte, Brazil Environmental contamination at a global level has reached worrying levels, and therefore, studies have : : * J. M. Silva J. A. Navoni E. M. X. Freire ( ) been developed in order to monitor and evaluate this Programa Regional de Pós-graduação em Desenvolvimento e Meio Ambiente - PRODEMA, Natal, Rio Grande do Norte, Brazil problem (Poletta et al. 2008;Márquez-Ferrandoetal. e-mail: [email protected] 2009;Marconetal.2010;Al-Hashem2011;Cabarcas- Montalvo et al. 2012; Zocche et al. 2013; Schaumburg J. A. Navoni et al. 2016; Nasri et al. 2017). A wide variety of terres- Programa de Pós-Graduação em Uso Sustentável de Recursos Naturais, Instituto Federal de Educação, Ciência e Tecnologia do trial and aquatic organisms have been used as tools to Rio Grande do Norte, Natal, Rio Grande do Norte, Brazil assess the environmental impacts linked to pollution in 454 Page 2 of 13 Environ Monit Assess (2020) 192:454 the different environmental compartments to understand The investigation level of ecotoxicological studies the effects of chemical agents on biota (Zapata et al. using lizards has been deepened to better assess and 2016). Among these organisms, reptiles and especially demonstrate the consequences of environmental con- lizards stand out, since environmental pollution together tamination (Campbell and Campbell 2002). These au- with global climate changes and the unsustainable use of thors introduced a synthesis showing the scarcity of natural resources constitute the most significant threats studies, which used reptiles of the Squamata group to to the populations of these animal species (Gibbons assess environmental contamination. Based on this prin- et al. 2000). ciple, reptiles have been considered good biomonitors to Organisms that are reactive to environmental con- assess environmental contamination given that they tamination, with the exception of humans, can be have reduced mobility, they do not normally live in considered apt to be evaluation models, as long as large areas, and it is possible to assess the effective they are found in abundance in the area, have a low exposure in a given area (Burger et al. 2004); however, migration rate and a reduced displacement area, with it is argued that there is a lack of studies with these this being the case for most lizards (Zocche et al. animals when it comes to biomonitoring studies, mainly 2013). In addition, these animals are ectothermic in relation to the effects generated by environmental and present a slower metabolism; therefore, they are contaminants in this group (Mitchelmore et al. 2005; more sensitive to toxic and xenobiotic agents, which Zapata et al. 2016;Sargsyanetal.2018). This is because directly influence their recovery power (Schaumburg lizards have great potential as bioindicator organisms to et al. 2012). Animals in general are exposed to vari- assess the environmental risk of several areas, as well as ous types of pollution daily, many of them of an- being shown to be excellent examples with their appli- thropic origin, but there are also those of natural cation in ecotoxicological studies (Simonyan et al. origin, and they constantly need to adapt to survive 2018). Lizards are usually associated with a specific in the environment (Hopkins 2000). Reptiles are spe- habitat, thus being more vulnerable to environmental cifically sensitive to environmental pollutants, being degradation than other vertebrates such as birds and exposed by several routes from the possibility of mammals (Hopkins 2000). Therefore, this review article ingesting part of contaminated soil, water, or food, aims to qualitatively and quantitatively assess current as well as dermal contact on contaminated substrates knowledge worldwide about the relevance of using and gas inhalation (Burger et al. 2004; Márquez- lizards as biomonitors and model organisms in environ- Ferrando et al. 2009; Simonyan et al. 2018). The mental contamination studies. ingestion of contaminated soil particles is a situation that has been causing serious risks to animals, since studies have already shown that lizards living in Material and methods radioactive areas or contaminated with hydrocarbons presented damage to their DNA by ingesting soil Articles were searched about environmental biomoni- particles during feeding, a situation which can cause toring and experimental models using lizards for ana- further damage later (Marsili et al. 2009;Al-Hashem lyzing environmental contaminants carried out in the 2011). Contaminated foods are one of the most rele- period 2009 to 2019, thus contemplating the studies vant sources of exposure to toxic agents, considering published on environmental contaminants in lizards in that there may be bioaccumulation of chemical ele- the last 10 years. It is worth mentioning that studies, ments of metallic origin or even organic contami- which did not indicate that they are inserted in this nants such as agrochemicals via the food chain, there- required group and which were not related to any spe- by generating an accumulation cycle within the or- cific contaminant, were not included. The searches were ganisms (Nasri et al. 2017). Finally, dermal contam- carried out in the following databases: PubMed, Web of ination is an important entry point for pesticides and Science, Scielo, and Google Scholar in the mentioned airborne pollutants, as well as contaminants in the period, using the following combinations of keywords: substrate itself (Zocche et al. 2013). Therefore, all biomonitoring + lizards + contaminants, biomonitoring of these factors can be considered as means of mon- + lizards + heavy metals, lizards + contamination, liz- itoring and evaluating various chemical substances ards + pollution, lizards + pesticides, and lizards + foundintheenvironment. persistent organic contaminants + pollution. The Environ Monit Assess (2020) 192:454 Page 3 of 13 454 obtained results were divided into two categories ac- other areas it can be found in other countries such cording to their origin: organic contaminants and inor- as Portugal, Spain, France, Montenegro, Croatia, ganic contaminants. The performed review shows Turkey, Libya, and Tunisia, all being geographically where we are in relation to ecotoxicological research close to Italy (Verderame and Scudiero 2019a). using lizard species, presenting a view of the deficien- The results obtained through this survey were divid- cies and gaps which still need to be filled. ed into two categories: contaminants of organic origin (pesticides, petroleum products, coal, and explosives) and contaminants of inorganic origin (heavy metals and radionuclides; Table 1). Results and discussion A total of 30 studies using lizards as biomonitors Organic contaminants and/or model organisms for assessing environmental contaminants have been found for the past 10 years Lizards are an important target group of vertebrate (2009–2019), which represent samples from five animals exposed to various pesticides (fungicides, continents (Tabela 1). The lizard family most stud- insecticides, and herbicides) of varying combinations