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Heavy Metals Assessment in the Medjerda River Basin (Northeastern Algeria): A Preliminary Water Analysis and Toad Skin Biopsy

Heavy Metals Assessment in the Medjerda River Basin (Northeastern Algeria): A Preliminary Water... Proc Zool Soc (Jan-Mar 2021) 74(1):104–113 https://doi.org/10.1007/s12595-020-00342-6 RESEARCH ARTICLE Heavy Metals Assessment in the Medjerda River Basin (Northeastern Algeria): A Preliminary Water Analysis and Toad Skin Biopsy 1,2 2 3 1,2 • • • • Noureddine Guezgouz Costantino Parisi Soumaya Boubsil Gaetano Grieco 1 2,4 Soualah Alila Hana Giulia Guerriero Received: 31 May 2020 / Revised: 21 July 2020 / Accepted: 24 July 2020 / Published online: 21 September 2020 The Author(s) 2020 Abstract Our study attempted to monitor the quality of toad, without euthanizing the specimens and making any water in Medjarda basin (Northeastern Algeria) and to loss to biodiversity of the species. provide baseline information of heavy metals in the water as well as in a potential amphibian biosentinel, the spiny Keywords Heavy metal  Medjarda basin  Spiny toad toad, Bufo spinosus. We measured pH, temperature, dis- Skin biopsy  Non-invasive methods solved oxygen and biological oxygen demand of water and levels of heavy metals in toad skin using an atomic absorption flame spectrophotometer. Lead (Pb) concentra- Introduction tion in water and in toad skin at all sites exceeded respectively 60 and 96 times the standard reference values. The quality of groundwater and surface water in rural and The heavy metal concentrations, in descending order, in urban environments is influenced by natural and anthro- water and in male toad skin were as follows: Pb [ Fe [ pogenic processes (Tang et al. 2014; Fasulo et al. 2015; Cu [ Zn and Fe [ Pb [ Zn [ Cu respectively. This study Lecomte et al. 2017; Vardhan et al. 2019). With anthro- highlights the ecological status of the surrounding areas pogenic human activities, there has been a significant upstream of the Medjarda basin as being a point source of increase in the discharge of industrial waste into the heavy metal pollution. It is further stated that a non-inva- environment, especially in urban areas, which creates an sive skin removal is an ethically sound technique to eval- alarming situation for human life and aquatic biota (Jan uate heavy metal accumulation in aquatic animals like et al. 2015; Lecomte et al. 2017; Guerriero et al. 2019). The anthropogenic factors include discharge of organic pollu- tants such as drugs, personal care products, steroids, hor- mones, endocrine disruptors, surfactants, phosphoric esters, & Noureddine Guezgouz flame retardants, industrial additives and siloxanes into n.guezgouz@univ-soukahras.dz natural freshwater bodies (Jaouadi et al. 2012; Khatri and & Giulia Guerriero Tyagi 2015; Lecomte et al. 2017; Parisi and Guerriero giulia.guerriero@unina.it 2019). Both natural and the anthropogenic processes alter Water and Environmental Science and Technology the heavy metals, coliforms and nutrient load concentra- Laboratory, Department of Biology, Mohamed Cherif tions in these water bodies. As a result of uncontrolled Messaadia University, Souk-Ahras, Algeria agriculture, unplanned urbanization and industrialization Comparative Endocrinology Lab, Department of Biology, rivers have been reported to be polluted with heavy metals University of Naples Federico II, 80126 Naples, Italy in many countries (Adekola and Eletta 2007; Mohiuddin Animal Ecophysiology Laboratory, Department of Biology, et al. 2011; Ali et al. 2016; Pandey and Singh 2017). Faculty of Natural and Life Sciences, Badji Mokhtar Several metals essential for life are naturally found in water University of Annaba, Annaba, Algeria but their levels must be under strict assessment because a Interdepartmental Research Centre for Environment concentration higher than the acceptable range may be (CIRAm), University of Naples Federico II, 80134 Naples, toxic to aquatic organisms (El-Kady and Abdel-Wahhab Italy T Proc Zool Soc (Jan-Mar 2021) 74(1):104–113 105 2018; Diaconu et al. 2020). Such assessment can avoid a polluted river in Europe demonstrated the useful indication serious impact on the global biodiversity (Ficken and provided by the different tissues in these organisms Byrne 2013; Jan et al. 2015; Guerriero et al. 2018a). Many (Trocchia et al. 2015). For all of these reasons, amphibians regions in Algeria have been developed without adequate can be used as sensitive bio-indicators in monitoring planning resulting in soils and water reported as being effects of heavy metals and other anthropogenic activities heavily polluted with various metals including mercury in aquatic environment (Prokic´ et al. 2016; D’Errico et al. (Hg), arsenic (As), lead (Pb), zinc (Zn), manganese (Mn), 2018; Guerriero et al. 2018b). Use of a non-invasive skin lithium (Li), cadmium (Cd ) and chromium (Cr) (Tahar and biopsy is a more relevant bio-monitoring process, because Keltoum 2011; Benhaddya and Hadjel 2014; Larba and it does not require euthanizing of the animal specimens and Soltani 2014; Boudia et al. 2019; Talbi and Kachi 2019). thus avoids ethical issues. The non-invasive procedure can Evidence of different metals also appears in the waters of be applied on large numbers of specimens and also can be Medjarda River, an urban river of Souk-Ahras City in used for repeated assessments without negatively impact- Northeastern Algeria. However, as per current literature ing the population of the selected amphibian species there is no document on heavy metal contamination in the (D’Errico et al. 2018). Medjarda basin. In order to study the state of pollution propagation and Environmental programs in the last decades highlight contamination of heavy metal in the environment, a the importance of organisms for monitoring climate chan- potential biosentinel was chosen as representative of eco- ges and pollutants (Mani and Kumar 2014; De Maio et al. logical damage. The spiny toad Bufo spinosus (Amphibia: 2014; Dixit et al. 2015; Guerriero et al. 2018a,b; Gentilucci Anura) was chosen for this purpose because, it is present in et al. 2020). Aquatic animals such as amphibians can Algeria and in the wettest and most temperate zones in accumulate heavy metals from the environment directly by North Africa (Tlidjane et al. 2019). The choice of an absorption through skin and oral surfaces and indirectly by amphibian was based on their key ecological role in the ingestion of heavy metals contaminated food items. Heavy trophic networks as prey or predators in a wide range of metal toxicity to organisms can damage the function of ecosystems (Niethammer et al. 1985; Ben Hassine and various organs. This is especially true for nonessential Escorzia 2017; Pinelli et al. 2019). In fact, frogs usually elements, such as Pb, which is highly toxic even at low use their own skin as a secondary respiratory surface, concentrations (Niethammer et al. 1985; Jaishankar et al. which is permeable to endogenous and exogenous sub- 2014; Ben Hassine and Escorzia 2017). stances whose potential harmful effects are contrasted by The documented effects of pollutants on biosentinels, keratins. This factor makes them suitable as a biosentinel such as amphibians, range from lethal to sublethal effects (Guerriero et al. 2018b, c) to assess environmental con- and include decreased growth and fertility, increased fre- tamination. In this study, Bufo spinosus underwent a non- quency of developmental abnormalities, increased suscep- invasive skin removal procedure.This procedure, already tibility to disease, behavioral changes, and damage to germ successfully tested on Italian pool frog Pelophylax bergeri, lines (Ortiz et al. 2004; Karraker et al. 2008; Shinn et al. exhibited how adverse impact on the environment could be 2008; Snodgrass et al. 2008; Guerriero et al. 2009; Guer- mitigated by avoiding euthanasia of the biosentinel riero et al. 2011; Guerriero et al. 2019; Parisi and Guerriero organisms (D’Errico et al. 2018). 2019). Furthermore, due to the feeding habits of larval Therefore, our research, as part of a larger project on the microphages of most species, toads frequently ingest sed- pollution affecting the Medjarda basin, was designed with iments through which metals can be accumulated (Hopkins the specific aim of contributing to knowledge regarding the and Rowe 2010; Burlibas¸a and Gavrila 2011; James and distribution of heavy metals (Zn, Cu, Pb and Fe) in the Semlitsch 2011). water and in the skin of the most distributed amphibian. Several researchers have attempted to document the The spiny toad, Bufo spinosus collected along the river impacts of metal buildup in amphibians both in captivity provides baseline information on pollutant distribution as (Herkovits and Helguero 1998; James and Little 2003; well as determining the point source of heavy metals. D’Errico et al. 2018; Guerriero et al. 2018b; Pinelli et al. 2019), and in field conditions (Demichelis et al. 2001; Borkin and Flyaks 2004; Fenoglio et al. 2006; Gavrilovic Materials and Methods et al. 2020). Other studies have reported deformity, delay in metamorphosis, reduced flight response and altered Study Area interactions with predators in amphibians after exposure to metals in water (Chen et al. 2009; James and Semlitsch The study was conducted along the Medjarda River located 2011; Zocche et al. 2013; Chagas et al. 2020). Furthermore, in Souk-Ahras City in northeastern Algeria (Fig. 1). heavy metal assessment using amphibians along the most Covering an area of about 1506 Km , the watershed is 123 106 Proc Zool Soc (Jan-Mar 2021) 74(1):104–113 drained by the Medjerda River and its tributaries. The was located near H’Nancha city. Sampling sites 2 and 3 0 00 0 00 0 00 population is estimated at 340,000 inhabitants, with an (36 15 7.49 N7 47 51.30 E and 36 15 59.59 N7 0 00 estimated growth rate of 1.7%. Located near the eastern 54 44.04 E) were situated upstream and downstream of edge of Algeria, the Medjerda River is a trans-frontal river, Ain Dalia Dam respectively. Site 4 was located close to the with head waters in the Montagnes region before traversing Zaarouria village, south of the city of Souk-Ahras (36 14 00 0 00 0 00 the urban section. Finally, the river drains to Tunisia, 40.84 N7 57 23.36 E) while site 5 (36 16 14.73 N7 0 00 which possibly transports pollutants to different basins 59 50.28 E) was located to the southeast of the same city. downstream. Under the Climate Classification System, the study area has a semi-arid climate characterized by a short dry season. Water Sampling and Analyses Water from each sampling site was collected along Med- Sampling Sites jerda River. Water samples were filtered through a cellu- lose filter (0.45 lm) and kept in the dark at 20 C until A reference control site (Ctrl) and five sampling sites (1–5) analysis. Dissolved phase refers to the fraction of con- along the river (Fig. 2) were selected for collecting speci- taminants passing through the filter, and there are both mens of male toads and water. The sampling sites were dissolved elements and those associated with colloidal chosen according to the variation of anthropogenic activi- organic matter. ties close to each city between up and downstream; the Concentrations of Zn, Cu, Pb and Fe were estimated distances between control and five points were: 2, 7, 15, 27 following the method (Fransion 1981), using an atomic and 33 km respectively. The Ctrl sampling site (36,16 absorption spectrophotometer (Shimadzu AA 6200, Japan). 00 0 00 35.46 N745 44.60 E) was located at the mouth of the Detection limit of Zn, Cu, Pb and Fe in the instrument was main river upstream and away from any anthropogenic 10 - 3 mg/L, 2 9 10 - 3 mg/L, 8 9 10 - 3 mg/L and 0 00 0 00 activities. Sampling site 1 (3615 36.81 N747 5.44 E) 6 9 10 - 3 mg/L, respectively. Appropriate precautions Fig. 1 Geographical location of the Medjerda River basin 123 Proc Zool Soc (Jan-Mar 2021) 74(1):104–113 107 Fig. 2 Sampling sites of water and toads were taken to maintain precision and accuracy of the water to a final volume of 10 ml. Concentrations of Zn, Cu, determinations. Pb and Fe in each sample were estimated using atomic Chemical-physical parameters of water: pH, tempera- absorption spectrophotometry (Fransion 1981). ture, DO (dissolved oxygen) and the BOD (biological oxygen demand) were measured in situ using a multi- Statistical Analysis parametric probe (Ocean Seven mod 401) at each site during the sampling and was done twice a week in the four The experimental data were analyzed using STATISTICA weeks of March 2019. The water samples were collected in software (Version 8.0, StatSoft Ltd, USA). Principle glass sterilized bottles and were stored with 3% (v/v) conc. component analysis (PCA) and cluster analysis (CA) were HNO acid for heavy metal analysis (G03 Committee). used to graphically visualize the hierarchical clustering of the heavy metals in water according to sampling sites. PCA Animal Sampling and Tissue Processing was performed on log-transformed data. CA was per- formed to classify heavy metals from different pollutant Five adult male toads (weight range 150–200 g for each sources on the basis of similarities in their chemical site 2019) identified as Bufo spinosus (Daudin 1803), were properties. In addition, ANOVA was performed on data of randomly captured from water ways in the wild twice a heavy metals of water and toad skin followed by Least week during March 2019 using pitfall traps as standard Significance Difference (LSD) test to compare significance difference between the study sites. The level of significance technique for toad capture (Heyer et al. 1994). After in situ biopsy along the river, the toad samples were released. The was set at p \ 0.05. The results are presented as non-lethal skin biopsy protocol was performed according to mean ± SD. the procedure by D’Errico et al. (2018) by collecting 1 cm skin from each toad. The pool of skin biopsy tissue was dried in an oven at 120 C for 3 h. Weight of the collected Results tissue samples were recorded before and after drying. Aliquots of 0.5 g of tissue were placed in 5 ml of nitric Physicochemical parameters of water showed no signifi- acid (69%) and left at room temperature to allow for cant differences between the five sampling sites where digestion for 5 days to obtain solution of suspended grease. temperature varied approximately from 11 to 25 C, and The samples were then filtered and diluted with deionized pH (6.9 ± 0.4), dissolved oxygen (DO) (9.5 ± 0.2 ppm) 123 108 Proc Zool Soc (Jan-Mar 2021) 74(1):104–113 and biological oxygen demand (BOD) (6.8 ± 0.2 ppm) (PC1) was correlated with Cu and Fe. The second principal showed no marked variations. component (PC2) includes Zn only while Pb was Concentrations of Pb, Fe, Cu and Zn in water of the unequivocally isolated in the third component (PC3) Medjerda river basin are shown in Fig. 3.The metal con- (Fig. 4a). In fact, Pb and Zn both display rather high val- centrations in the five considered sites show two distinct ues, and they are partially represented in (PC1). The result groups in comparison to the control area. A predominant of CA underlines two distinct clusters which can be iden- group consisting of Pb and Fe had levels in the range of tified in cluster I containing Pb and Fe and cluster II con- 0.43–0.72 mg/L and 0.35–0.53 mg/L respectively and an taining Zn and Cu as shown in Fig. 4b. under-represented group consisting of Cu and Zn had levels in the range 0.08–0.12 mg/mL and 0.05–0.11 mg/mL Metals concentration measurements in toad skin biopsy respectively. Specifically Pb, Fe, Cu and Zn concentrations pools (n = 40 males, spiny toad, Bufo spinosus each site) in the five stations didn’t significantly differ between sites were performed to examine Pb, Fe, Zn and Cu (Fig. 5). even though they significantly varied from the control area where Pb, Cu and Zn were undetectable (F value = 0.029; Results show the predominance of Pb and Fe, respec- p value = 0.998). tively, in the range of 0.32 ± 0.09–0.70 ± 0.28 mg/mL and 0.62 ± 0.3–0.89 ± 0.13 mg/mL followed by Cu and Therefore, based on the mean concentration of Pb, Fe, Zn in the range of 0.06 ± 0.007–0.096 ± 0.006 and Cu and Zn (0.60 ± 0.11, 0.43 ± 08, 0.09 ± 0.02 and 0.05 ± 0.02–0.16 ± 0.08 mg/mL. 0.09 ± 0.03 mg/L, respectively) these heavy metals in Thus, based on the mean concentration of heavy metals water were arranged in the following decreasing order of in toad skin biopsy, Pb 0.48 ± 0.15 mg/Kg, Fe concentration: Pb [ Fe [ Cu [ Zn. 0.72 ± 0.11 mg/Kg, Cu 0.08 ± 0.01 mg/Kg and Zn Since the permissible limits of heavy metals for water 0.11 ± 0.05 mg/Kg, they were ranked as follows: quality based on World Health Organization (WHO) Fe [ Pb [ Zn [ Cu. established standards are: Pb 0.01 mg/L; Fe 1–3 mg/L; Cu Based on the Joint FAO/WHO Expert Committee on 2 mg/L and Zn 3 mg/L (WHO 2008), the results of the Food Additives (JECFA), which declare the provisional present study reveal values 60 times higher for Pb while the tolerable weekly intake (PTWI) for Pb equivalent to other metals had concentrations within permissible limits. 0.005 mg/Kg/day, Fe 0.8 mg/kg/day, Cu 2 mg/Kg/day and The results of multivariate statistical analysis, PCA and Zn 1 mg/kg/day (WHO 2008), excessive values detected CA, are shown in Fig. 4. The PCA grouped Pb, Fe, Cu and for Pb which were 96 times higher than the threshold Zn into a three component model which accounted for 80% limits. of all the data variation. The first principal component Fig. 3 Metal concentration of Pb, Fe, Cu and Zn (mg/mL) of water samples in sampled sites. nd = metal concentration not detected; Ctrl = control site; S1–S5 = sampled site 1 to 5 123 Proc Zool Soc (Jan-Mar 2021) 74(1):104–113 109 Fig. 4 a Principal component analysis of heavy metal concentration in water according to factors, factor-plane (1 9 2); b Dendrogram depicting the hierarchical clustering of the heavy metals in water Fig. 5 Metal concentration of Pb, Fe, Cu and Zn (mg/mL) in skin toad Bufo spinosus in sampled sites; Ctrl = control site; S1–S5 = sampled site 1 to on aquatic organism in the literature. As kown, all toxic Discussion and trace metals interfere in the normal functioning of structural proteins, enzymes, and nucleic acids by binding The results presented in this study comprise an attempt to report the heavy metals distributions and their degree of them. But, recently, in amphibian evidence of metabolic and enzyme activities alterations, morphophysiological contamination (Pb, Fe, Cu and Zn) in river water and in the changes were reported after increasing levels of Pb, Fe and/ skin of the male spiny toad Bufo spinosus collected from or Cu and Zn alone or combined (Pinelli et al. 2019; the Medjerda River basin in the northeastern region of Chagas et al. 2020). Algeria. Medjerda river was already explored for natural organic In the present study, five different localities based on human anthropogenic activities and presence of toads were matter (Jouadi et al. 2012) reporting the characterization of the heterogeneous nature and the importance of the various chosen. As shown in the results, even though the concen- trations of Pb, Fe, Cu and Zn in water samples were evenly subcomponents characterization. We focus on the heavy metal, the toxic metal Pb and the essential microminerals distributed among the five sampling stations, they strongly differ from the control area where most of heavy metals as Fe, Cu and Zn for human anthropogenic activities detected in the sites examined and their documented effects were undetectable. 123 110 Proc Zool Soc (Jan-Mar 2021) 74(1):104–113 Further by the dendrogram, the concentrations in the These results in the skin tissue showed higher Pb con- water samples of Cu and Zn result homogenous as cluster centration than the permitted threshold established by as well as the other cluster of Fe and Pb. Since copper is JECFA. In fact, Pb was the only heavy metal with higher susceptible to oxidation, the observed cluster of native levels relative to threshold limits than of the other heavy copper with zinc in water is of interest and deserves our metals detected in the same areas. Several previous studies future attention. on heavy metals, specifically on Pb, have reported a wide The presence of copper mainly comes into the envi- range of biological and neurological effects in different ronment through manufacturing industries such as paint organisms (Assi et al. 2016; Lasley 2018; Rocha and and leaded gasoline, tire wear, lubricating oil, grease, Trujillo 2019), reproductive toxicity (Guerriero 2007; batteries production and ceramics, remains of batteries Huang et al. 2017; Rameshbhai et al. 2019), embryotoxi- whereas the concentration of zinc in the water could be due city (Lee and Ko 2017), teratogenicity (Lee and Ko 2017), to leaching effects from several sources as refineries, brass as well as effects on mutagenicity and carcinogenicity manufacture, metal plating, plumbing. (Thanomsangad et al. 2019). High levels of iron in water sources can been attributed Toads need moist skin, particularly during the devel- to the geology of the area, the main factor controlling opment of embryos and larvae (Unrine et al. 2007; Zhang groundwater hydrology whereas the entry of sewage, et al. 2007). Their semipermeable and highly vascularized caused by the activities of agriculture, industry and skin permits cutaneous gas exchange, resulting in toads domestic sewage as automobile emission, mining, burning being highly susceptible to heavy metal accumulation. In of coal into these ecosystems, can be the reasons for the fact, heavy metals can be absorbed via their skin and the high levels of lead in Medjerda River. intestine and reach to target tissues through circulatory In addition, lead concentration was approximately 60 system (Stolyar et al. 2008; Burlibas¸a and Gavrila˘ 2011; times higher than the permissible limit of the metal in Simon et al. 2011; Thanomsangad et al. 2020). Further- water (WHO 2008). These data indicate that these sites more, heavy metal accumulation in toads strongly depends contain point sources of heavy metal pollution from where not only on the metal concentrations present in the envi- these pollutants are dispersed into the surrounding area. In ronment but also on other factors including the affinities of fact, the sampling site 1 is located near the spillways of metals to different tissues, different rates of uptake and H’Nancha city where, due to a lack of sewage pipelines, deposition, the metal distribution in various organs and the the urban and domestic discharges are injected directly into excretion rate (Putshaka et al. 2015; Guerriero et al. the river. Sampling sites 2 and 3 are situated upstream and 2018b). downstream of Ain Dalia Dam respectively. It is an area At the same time, the high levels of heavy metals in used for washing wool and automobiles as well as where tissue as well as in the water can also be explained by the manufacturing of traditional building materials takes place fact that the typical organisms on which toads prey are and where visible signs of water pollution such as dark insect larvae, crickets, dragonflies, earthworms, grasshop- watercolour and a foul smell is observed. Sampling site 4 pers, and isopods (Burlibas¸a and Gavrila 2011) which in located close to the Zaarouria village, south of the city of turn may contain high concentrations of heavy metals due Souk-Ahras, is characterized by a waste treatment system to contact with the contaminated environment. In fact, which discharges into the river, while the site 5 is located heavy metals in sediment, soil and water may be inadver- in a zone of waste water discharges characterized by tently ingested by toads during their prey capture (James poultry-raising activity at the edge of the river. and Semlitsch 2011). To study the effect of toxic and trace metals examined on biota we chosen amphibian for their key ecological role as bioindicator (Niethammer et al. 1985; Ben Hassine and Conclusions Escorzia 2017; Guerriero et al. 2018b; Pinelli et al. 2019). In particular, for this project we collected skin biopsy from Investigating the chemistry of surface water obtained from male toads because anatomically they are very easy to the Medjerda River basin has given an insight into impact identify and to complete gender detoxification analysis of of land use effect on water quality. Analyses of the various cytochrome aromatase p450 aromatase and glutathione ions has indicated that Pb, Fe, Cu and Zn in water samples S-transferase in Bufo spinosus by Real Time-PCR (studies were found to be evenly distributed among the five sam- in progress). pling stations. These results reveal Pb concentrations Our present results on the concentration of the toxicants, approximately 60 times higher in comparison to permissi- heavy metals in the skin tissue showed high values com- ble limits of heavy metals for water quality (WHO 2008). pared to the control area, which were found within per- Thus, our study provided an opportunity to evaluate the missible limits. spiny toad Bufo spinosus as a potential monitor of heavy 123 Proc Zool Soc (Jan-Mar 2021) 74(1):104–113 111 Assi, M.A., M.N.M. Hezmee, A.W. Haron, M.Y. Sabri, and M.A. metal contamination. This species performs as an appro- Rajion. 2016. 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Heavy Metals Assessment in the Medjerda River Basin (Northeastern Algeria): A Preliminary Water Analysis and Toad Skin Biopsy

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Abstract

Proc Zool Soc (Jan-Mar 2021) 74(1):104–113 https://doi.org/10.1007/s12595-020-00342-6 RESEARCH ARTICLE Heavy Metals Assessment in the Medjerda River Basin (Northeastern Algeria): A Preliminary Water Analysis and Toad Skin Biopsy 1,2 2 3 1,2 • • • • Noureddine Guezgouz Costantino Parisi Soumaya Boubsil Gaetano Grieco 1 2,4 Soualah Alila Hana Giulia Guerriero Received: 31 May 2020 / Revised: 21 July 2020 / Accepted: 24 July 2020 / Published online: 21 September 2020 The Author(s) 2020 Abstract Our study attempted to monitor the quality of toad, without euthanizing the specimens and making any water in Medjarda basin (Northeastern Algeria) and to loss to biodiversity of the species. provide baseline information of heavy metals in the water as well as in a potential amphibian biosentinel, the spiny Keywords Heavy metal  Medjarda basin  Spiny toad toad, Bufo spinosus. We measured pH, temperature, dis- Skin biopsy  Non-invasive methods solved oxygen and biological oxygen demand of water and levels of heavy metals in toad skin using an atomic absorption flame spectrophotometer. Lead (Pb) concentra- Introduction tion in water and in toad skin at all sites exceeded respectively 60 and 96 times the standard reference values. The quality of groundwater and surface water in rural and The heavy metal concentrations, in descending order, in urban environments is influenced by natural and anthro- water and in male toad skin were as follows: Pb [ Fe [ pogenic processes (Tang et al. 2014; Fasulo et al. 2015; Cu [ Zn and Fe [ Pb [ Zn [ Cu respectively. This study Lecomte et al. 2017; Vardhan et al. 2019). With anthro- highlights the ecological status of the surrounding areas pogenic human activities, there has been a significant upstream of the Medjarda basin as being a point source of increase in the discharge of industrial waste into the heavy metal pollution. It is further stated that a non-inva- environment, especially in urban areas, which creates an sive skin removal is an ethically sound technique to eval- alarming situation for human life and aquatic biota (Jan uate heavy metal accumulation in aquatic animals like et al. 2015; Lecomte et al. 2017; Guerriero et al. 2019). The anthropogenic factors include discharge of organic pollu- tants such as drugs, personal care products, steroids, hor- mones, endocrine disruptors, surfactants, phosphoric esters, & Noureddine Guezgouz flame retardants, industrial additives and siloxanes into n.guezgouz@univ-soukahras.dz natural freshwater bodies (Jaouadi et al. 2012; Khatri and & Giulia Guerriero Tyagi 2015; Lecomte et al. 2017; Parisi and Guerriero giulia.guerriero@unina.it 2019). Both natural and the anthropogenic processes alter Water and Environmental Science and Technology the heavy metals, coliforms and nutrient load concentra- Laboratory, Department of Biology, Mohamed Cherif tions in these water bodies. As a result of uncontrolled Messaadia University, Souk-Ahras, Algeria agriculture, unplanned urbanization and industrialization Comparative Endocrinology Lab, Department of Biology, rivers have been reported to be polluted with heavy metals University of Naples Federico II, 80126 Naples, Italy in many countries (Adekola and Eletta 2007; Mohiuddin Animal Ecophysiology Laboratory, Department of Biology, et al. 2011; Ali et al. 2016; Pandey and Singh 2017). Faculty of Natural and Life Sciences, Badji Mokhtar Several metals essential for life are naturally found in water University of Annaba, Annaba, Algeria but their levels must be under strict assessment because a Interdepartmental Research Centre for Environment concentration higher than the acceptable range may be (CIRAm), University of Naples Federico II, 80134 Naples, toxic to aquatic organisms (El-Kady and Abdel-Wahhab Italy T Proc Zool Soc (Jan-Mar 2021) 74(1):104–113 105 2018; Diaconu et al. 2020). Such assessment can avoid a polluted river in Europe demonstrated the useful indication serious impact on the global biodiversity (Ficken and provided by the different tissues in these organisms Byrne 2013; Jan et al. 2015; Guerriero et al. 2018a). Many (Trocchia et al. 2015). For all of these reasons, amphibians regions in Algeria have been developed without adequate can be used as sensitive bio-indicators in monitoring planning resulting in soils and water reported as being effects of heavy metals and other anthropogenic activities heavily polluted with various metals including mercury in aquatic environment (Prokic´ et al. 2016; D’Errico et al. (Hg), arsenic (As), lead (Pb), zinc (Zn), manganese (Mn), 2018; Guerriero et al. 2018b). Use of a non-invasive skin lithium (Li), cadmium (Cd ) and chromium (Cr) (Tahar and biopsy is a more relevant bio-monitoring process, because Keltoum 2011; Benhaddya and Hadjel 2014; Larba and it does not require euthanizing of the animal specimens and Soltani 2014; Boudia et al. 2019; Talbi and Kachi 2019). thus avoids ethical issues. The non-invasive procedure can Evidence of different metals also appears in the waters of be applied on large numbers of specimens and also can be Medjarda River, an urban river of Souk-Ahras City in used for repeated assessments without negatively impact- Northeastern Algeria. However, as per current literature ing the population of the selected amphibian species there is no document on heavy metal contamination in the (D’Errico et al. 2018). Medjarda basin. In order to study the state of pollution propagation and Environmental programs in the last decades highlight contamination of heavy metal in the environment, a the importance of organisms for monitoring climate chan- potential biosentinel was chosen as representative of eco- ges and pollutants (Mani and Kumar 2014; De Maio et al. logical damage. The spiny toad Bufo spinosus (Amphibia: 2014; Dixit et al. 2015; Guerriero et al. 2018a,b; Gentilucci Anura) was chosen for this purpose because, it is present in et al. 2020). Aquatic animals such as amphibians can Algeria and in the wettest and most temperate zones in accumulate heavy metals from the environment directly by North Africa (Tlidjane et al. 2019). The choice of an absorption through skin and oral surfaces and indirectly by amphibian was based on their key ecological role in the ingestion of heavy metals contaminated food items. Heavy trophic networks as prey or predators in a wide range of metal toxicity to organisms can damage the function of ecosystems (Niethammer et al. 1985; Ben Hassine and various organs. This is especially true for nonessential Escorzia 2017; Pinelli et al. 2019). In fact, frogs usually elements, such as Pb, which is highly toxic even at low use their own skin as a secondary respiratory surface, concentrations (Niethammer et al. 1985; Jaishankar et al. which is permeable to endogenous and exogenous sub- 2014; Ben Hassine and Escorzia 2017). stances whose potential harmful effects are contrasted by The documented effects of pollutants on biosentinels, keratins. This factor makes them suitable as a biosentinel such as amphibians, range from lethal to sublethal effects (Guerriero et al. 2018b, c) to assess environmental con- and include decreased growth and fertility, increased fre- tamination. In this study, Bufo spinosus underwent a non- quency of developmental abnormalities, increased suscep- invasive skin removal procedure.This procedure, already tibility to disease, behavioral changes, and damage to germ successfully tested on Italian pool frog Pelophylax bergeri, lines (Ortiz et al. 2004; Karraker et al. 2008; Shinn et al. exhibited how adverse impact on the environment could be 2008; Snodgrass et al. 2008; Guerriero et al. 2009; Guer- mitigated by avoiding euthanasia of the biosentinel riero et al. 2011; Guerriero et al. 2019; Parisi and Guerriero organisms (D’Errico et al. 2018). 2019). Furthermore, due to the feeding habits of larval Therefore, our research, as part of a larger project on the microphages of most species, toads frequently ingest sed- pollution affecting the Medjarda basin, was designed with iments through which metals can be accumulated (Hopkins the specific aim of contributing to knowledge regarding the and Rowe 2010; Burlibas¸a and Gavrila 2011; James and distribution of heavy metals (Zn, Cu, Pb and Fe) in the Semlitsch 2011). water and in the skin of the most distributed amphibian. Several researchers have attempted to document the The spiny toad, Bufo spinosus collected along the river impacts of metal buildup in amphibians both in captivity provides baseline information on pollutant distribution as (Herkovits and Helguero 1998; James and Little 2003; well as determining the point source of heavy metals. D’Errico et al. 2018; Guerriero et al. 2018b; Pinelli et al. 2019), and in field conditions (Demichelis et al. 2001; Borkin and Flyaks 2004; Fenoglio et al. 2006; Gavrilovic Materials and Methods et al. 2020). Other studies have reported deformity, delay in metamorphosis, reduced flight response and altered Study Area interactions with predators in amphibians after exposure to metals in water (Chen et al. 2009; James and Semlitsch The study was conducted along the Medjarda River located 2011; Zocche et al. 2013; Chagas et al. 2020). Furthermore, in Souk-Ahras City in northeastern Algeria (Fig. 1). heavy metal assessment using amphibians along the most Covering an area of about 1506 Km , the watershed is 123 106 Proc Zool Soc (Jan-Mar 2021) 74(1):104–113 drained by the Medjerda River and its tributaries. The was located near H’Nancha city. Sampling sites 2 and 3 0 00 0 00 0 00 population is estimated at 340,000 inhabitants, with an (36 15 7.49 N7 47 51.30 E and 36 15 59.59 N7 0 00 estimated growth rate of 1.7%. Located near the eastern 54 44.04 E) were situated upstream and downstream of edge of Algeria, the Medjerda River is a trans-frontal river, Ain Dalia Dam respectively. Site 4 was located close to the with head waters in the Montagnes region before traversing Zaarouria village, south of the city of Souk-Ahras (36 14 00 0 00 0 00 the urban section. Finally, the river drains to Tunisia, 40.84 N7 57 23.36 E) while site 5 (36 16 14.73 N7 0 00 which possibly transports pollutants to different basins 59 50.28 E) was located to the southeast of the same city. downstream. Under the Climate Classification System, the study area has a semi-arid climate characterized by a short dry season. Water Sampling and Analyses Water from each sampling site was collected along Med- Sampling Sites jerda River. Water samples were filtered through a cellu- lose filter (0.45 lm) and kept in the dark at 20 C until A reference control site (Ctrl) and five sampling sites (1–5) analysis. Dissolved phase refers to the fraction of con- along the river (Fig. 2) were selected for collecting speci- taminants passing through the filter, and there are both mens of male toads and water. The sampling sites were dissolved elements and those associated with colloidal chosen according to the variation of anthropogenic activi- organic matter. ties close to each city between up and downstream; the Concentrations of Zn, Cu, Pb and Fe were estimated distances between control and five points were: 2, 7, 15, 27 following the method (Fransion 1981), using an atomic and 33 km respectively. The Ctrl sampling site (36,16 absorption spectrophotometer (Shimadzu AA 6200, Japan). 00 0 00 35.46 N745 44.60 E) was located at the mouth of the Detection limit of Zn, Cu, Pb and Fe in the instrument was main river upstream and away from any anthropogenic 10 - 3 mg/L, 2 9 10 - 3 mg/L, 8 9 10 - 3 mg/L and 0 00 0 00 activities. Sampling site 1 (3615 36.81 N747 5.44 E) 6 9 10 - 3 mg/L, respectively. Appropriate precautions Fig. 1 Geographical location of the Medjerda River basin 123 Proc Zool Soc (Jan-Mar 2021) 74(1):104–113 107 Fig. 2 Sampling sites of water and toads were taken to maintain precision and accuracy of the water to a final volume of 10 ml. Concentrations of Zn, Cu, determinations. Pb and Fe in each sample were estimated using atomic Chemical-physical parameters of water: pH, tempera- absorption spectrophotometry (Fransion 1981). ture, DO (dissolved oxygen) and the BOD (biological oxygen demand) were measured in situ using a multi- Statistical Analysis parametric probe (Ocean Seven mod 401) at each site during the sampling and was done twice a week in the four The experimental data were analyzed using STATISTICA weeks of March 2019. The water samples were collected in software (Version 8.0, StatSoft Ltd, USA). Principle glass sterilized bottles and were stored with 3% (v/v) conc. component analysis (PCA) and cluster analysis (CA) were HNO acid for heavy metal analysis (G03 Committee). used to graphically visualize the hierarchical clustering of the heavy metals in water according to sampling sites. PCA Animal Sampling and Tissue Processing was performed on log-transformed data. CA was per- formed to classify heavy metals from different pollutant Five adult male toads (weight range 150–200 g for each sources on the basis of similarities in their chemical site 2019) identified as Bufo spinosus (Daudin 1803), were properties. In addition, ANOVA was performed on data of randomly captured from water ways in the wild twice a heavy metals of water and toad skin followed by Least week during March 2019 using pitfall traps as standard Significance Difference (LSD) test to compare significance difference between the study sites. The level of significance technique for toad capture (Heyer et al. 1994). After in situ biopsy along the river, the toad samples were released. The was set at p \ 0.05. The results are presented as non-lethal skin biopsy protocol was performed according to mean ± SD. the procedure by D’Errico et al. (2018) by collecting 1 cm skin from each toad. The pool of skin biopsy tissue was dried in an oven at 120 C for 3 h. Weight of the collected Results tissue samples were recorded before and after drying. Aliquots of 0.5 g of tissue were placed in 5 ml of nitric Physicochemical parameters of water showed no signifi- acid (69%) and left at room temperature to allow for cant differences between the five sampling sites where digestion for 5 days to obtain solution of suspended grease. temperature varied approximately from 11 to 25 C, and The samples were then filtered and diluted with deionized pH (6.9 ± 0.4), dissolved oxygen (DO) (9.5 ± 0.2 ppm) 123 108 Proc Zool Soc (Jan-Mar 2021) 74(1):104–113 and biological oxygen demand (BOD) (6.8 ± 0.2 ppm) (PC1) was correlated with Cu and Fe. The second principal showed no marked variations. component (PC2) includes Zn only while Pb was Concentrations of Pb, Fe, Cu and Zn in water of the unequivocally isolated in the third component (PC3) Medjerda river basin are shown in Fig. 3.The metal con- (Fig. 4a). In fact, Pb and Zn both display rather high val- centrations in the five considered sites show two distinct ues, and they are partially represented in (PC1). The result groups in comparison to the control area. A predominant of CA underlines two distinct clusters which can be iden- group consisting of Pb and Fe had levels in the range of tified in cluster I containing Pb and Fe and cluster II con- 0.43–0.72 mg/L and 0.35–0.53 mg/L respectively and an taining Zn and Cu as shown in Fig. 4b. under-represented group consisting of Cu and Zn had levels in the range 0.08–0.12 mg/mL and 0.05–0.11 mg/mL Metals concentration measurements in toad skin biopsy respectively. Specifically Pb, Fe, Cu and Zn concentrations pools (n = 40 males, spiny toad, Bufo spinosus each site) in the five stations didn’t significantly differ between sites were performed to examine Pb, Fe, Zn and Cu (Fig. 5). even though they significantly varied from the control area where Pb, Cu and Zn were undetectable (F value = 0.029; Results show the predominance of Pb and Fe, respec- p value = 0.998). tively, in the range of 0.32 ± 0.09–0.70 ± 0.28 mg/mL and 0.62 ± 0.3–0.89 ± 0.13 mg/mL followed by Cu and Therefore, based on the mean concentration of Pb, Fe, Zn in the range of 0.06 ± 0.007–0.096 ± 0.006 and Cu and Zn (0.60 ± 0.11, 0.43 ± 08, 0.09 ± 0.02 and 0.05 ± 0.02–0.16 ± 0.08 mg/mL. 0.09 ± 0.03 mg/L, respectively) these heavy metals in Thus, based on the mean concentration of heavy metals water were arranged in the following decreasing order of in toad skin biopsy, Pb 0.48 ± 0.15 mg/Kg, Fe concentration: Pb [ Fe [ Cu [ Zn. 0.72 ± 0.11 mg/Kg, Cu 0.08 ± 0.01 mg/Kg and Zn Since the permissible limits of heavy metals for water 0.11 ± 0.05 mg/Kg, they were ranked as follows: quality based on World Health Organization (WHO) Fe [ Pb [ Zn [ Cu. established standards are: Pb 0.01 mg/L; Fe 1–3 mg/L; Cu Based on the Joint FAO/WHO Expert Committee on 2 mg/L and Zn 3 mg/L (WHO 2008), the results of the Food Additives (JECFA), which declare the provisional present study reveal values 60 times higher for Pb while the tolerable weekly intake (PTWI) for Pb equivalent to other metals had concentrations within permissible limits. 0.005 mg/Kg/day, Fe 0.8 mg/kg/day, Cu 2 mg/Kg/day and The results of multivariate statistical analysis, PCA and Zn 1 mg/kg/day (WHO 2008), excessive values detected CA, are shown in Fig. 4. The PCA grouped Pb, Fe, Cu and for Pb which were 96 times higher than the threshold Zn into a three component model which accounted for 80% limits. of all the data variation. The first principal component Fig. 3 Metal concentration of Pb, Fe, Cu and Zn (mg/mL) of water samples in sampled sites. nd = metal concentration not detected; Ctrl = control site; S1–S5 = sampled site 1 to 5 123 Proc Zool Soc (Jan-Mar 2021) 74(1):104–113 109 Fig. 4 a Principal component analysis of heavy metal concentration in water according to factors, factor-plane (1 9 2); b Dendrogram depicting the hierarchical clustering of the heavy metals in water Fig. 5 Metal concentration of Pb, Fe, Cu and Zn (mg/mL) in skin toad Bufo spinosus in sampled sites; Ctrl = control site; S1–S5 = sampled site 1 to on aquatic organism in the literature. As kown, all toxic Discussion and trace metals interfere in the normal functioning of structural proteins, enzymes, and nucleic acids by binding The results presented in this study comprise an attempt to report the heavy metals distributions and their degree of them. But, recently, in amphibian evidence of metabolic and enzyme activities alterations, morphophysiological contamination (Pb, Fe, Cu and Zn) in river water and in the changes were reported after increasing levels of Pb, Fe and/ skin of the male spiny toad Bufo spinosus collected from or Cu and Zn alone or combined (Pinelli et al. 2019; the Medjerda River basin in the northeastern region of Chagas et al. 2020). Algeria. Medjerda river was already explored for natural organic In the present study, five different localities based on human anthropogenic activities and presence of toads were matter (Jouadi et al. 2012) reporting the characterization of the heterogeneous nature and the importance of the various chosen. As shown in the results, even though the concen- trations of Pb, Fe, Cu and Zn in water samples were evenly subcomponents characterization. We focus on the heavy metal, the toxic metal Pb and the essential microminerals distributed among the five sampling stations, they strongly differ from the control area where most of heavy metals as Fe, Cu and Zn for human anthropogenic activities detected in the sites examined and their documented effects were undetectable. 123 110 Proc Zool Soc (Jan-Mar 2021) 74(1):104–113 Further by the dendrogram, the concentrations in the These results in the skin tissue showed higher Pb con- water samples of Cu and Zn result homogenous as cluster centration than the permitted threshold established by as well as the other cluster of Fe and Pb. Since copper is JECFA. In fact, Pb was the only heavy metal with higher susceptible to oxidation, the observed cluster of native levels relative to threshold limits than of the other heavy copper with zinc in water is of interest and deserves our metals detected in the same areas. Several previous studies future attention. on heavy metals, specifically on Pb, have reported a wide The presence of copper mainly comes into the envi- range of biological and neurological effects in different ronment through manufacturing industries such as paint organisms (Assi et al. 2016; Lasley 2018; Rocha and and leaded gasoline, tire wear, lubricating oil, grease, Trujillo 2019), reproductive toxicity (Guerriero 2007; batteries production and ceramics, remains of batteries Huang et al. 2017; Rameshbhai et al. 2019), embryotoxi- whereas the concentration of zinc in the water could be due city (Lee and Ko 2017), teratogenicity (Lee and Ko 2017), to leaching effects from several sources as refineries, brass as well as effects on mutagenicity and carcinogenicity manufacture, metal plating, plumbing. (Thanomsangad et al. 2019). High levels of iron in water sources can been attributed Toads need moist skin, particularly during the devel- to the geology of the area, the main factor controlling opment of embryos and larvae (Unrine et al. 2007; Zhang groundwater hydrology whereas the entry of sewage, et al. 2007). Their semipermeable and highly vascularized caused by the activities of agriculture, industry and skin permits cutaneous gas exchange, resulting in toads domestic sewage as automobile emission, mining, burning being highly susceptible to heavy metal accumulation. In of coal into these ecosystems, can be the reasons for the fact, heavy metals can be absorbed via their skin and the high levels of lead in Medjerda River. intestine and reach to target tissues through circulatory In addition, lead concentration was approximately 60 system (Stolyar et al. 2008; Burlibas¸a and Gavrila˘ 2011; times higher than the permissible limit of the metal in Simon et al. 2011; Thanomsangad et al. 2020). Further- water (WHO 2008). These data indicate that these sites more, heavy metal accumulation in toads strongly depends contain point sources of heavy metal pollution from where not only on the metal concentrations present in the envi- these pollutants are dispersed into the surrounding area. In ronment but also on other factors including the affinities of fact, the sampling site 1 is located near the spillways of metals to different tissues, different rates of uptake and H’Nancha city where, due to a lack of sewage pipelines, deposition, the metal distribution in various organs and the the urban and domestic discharges are injected directly into excretion rate (Putshaka et al. 2015; Guerriero et al. the river. Sampling sites 2 and 3 are situated upstream and 2018b). downstream of Ain Dalia Dam respectively. It is an area At the same time, the high levels of heavy metals in used for washing wool and automobiles as well as where tissue as well as in the water can also be explained by the manufacturing of traditional building materials takes place fact that the typical organisms on which toads prey are and where visible signs of water pollution such as dark insect larvae, crickets, dragonflies, earthworms, grasshop- watercolour and a foul smell is observed. Sampling site 4 pers, and isopods (Burlibas¸a and Gavrila 2011) which in located close to the Zaarouria village, south of the city of turn may contain high concentrations of heavy metals due Souk-Ahras, is characterized by a waste treatment system to contact with the contaminated environment. In fact, which discharges into the river, while the site 5 is located heavy metals in sediment, soil and water may be inadver- in a zone of waste water discharges characterized by tently ingested by toads during their prey capture (James poultry-raising activity at the edge of the river. and Semlitsch 2011). To study the effect of toxic and trace metals examined on biota we chosen amphibian for their key ecological role as bioindicator (Niethammer et al. 1985; Ben Hassine and Conclusions Escorzia 2017; Guerriero et al. 2018b; Pinelli et al. 2019). In particular, for this project we collected skin biopsy from Investigating the chemistry of surface water obtained from male toads because anatomically they are very easy to the Medjerda River basin has given an insight into impact identify and to complete gender detoxification analysis of of land use effect on water quality. Analyses of the various cytochrome aromatase p450 aromatase and glutathione ions has indicated that Pb, Fe, Cu and Zn in water samples S-transferase in Bufo spinosus by Real Time-PCR (studies were found to be evenly distributed among the five sam- in progress). pling stations. These results reveal Pb concentrations Our present results on the concentration of the toxicants, approximately 60 times higher in comparison to permissi- heavy metals in the skin tissue showed high values com- ble limits of heavy metals for water quality (WHO 2008). pared to the control area, which were found within per- Thus, our study provided an opportunity to evaluate the missible limits. spiny toad Bufo spinosus as a potential monitor of heavy 123 Proc Zool Soc (Jan-Mar 2021) 74(1):104–113 111 Assi, M.A., M.N.M. Hezmee, A.W. Haron, M.Y. Sabri, and M.A. metal contamination. This species performs as an appro- Rajion. 2016. 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Amphibians as model organisms revision received by Emidio Sivieri, Biomedical Engineer at Chil- for study environmental genotoxicity. Applied Ecology and dren’s Hospital Of Philadelphia, Philadelphia (USA). Environmental Research 9: 1–15. Chagas, B.R.C., H.S.M. Utsunomiya, M.N. Fernandes, and C.S. Author Contributions All authors contributed to conception and Carvalho. 2020. Metabolic responses in bullfrog, Lithobates design of the experiments. All the authors have given their approval catesbeianus after exposure to zinc, copper and cadmium. to the final version of the manuscript. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 233: 108768. Funding Open access funding provided by Universita` degli Studi di Chen, T.-H., J.A. Gross, and W.H. Karasov. 2009. Chronic exposure Napoli Federico II within the CRUI-CARE Agreement. to pentavalent arsenic of larval leopard frogs (Rana pipiens): Bioaccumulation and reduced swimming performance. 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