Abstract
Despite the general lack of studies that use reptiles as bioindicators, the value of freshwater turtles and crocodilians in ecotoxicology has been proven, due to their importance as sentinel species. The aim of this study was to compile information on the use of freshwater turtles and crocodilians as environmental biomonitors of inorganic element contamination. We searched for articles in databases using specific keywords. A total of 104 studies published between the years 1970 and 2020 were collected. We noted a general increase in the number of studies involving turtles and crocodilians during the study time period. The Order Testudines were the subjects of 46% of the analysed publications, and the Order Crocodylia accounted for 54%. Within these studies, we counted 39 species (turtles n = 29 and crocodilians n = 10). Forty chemical elements were evaluated in the analysed articles, of which the majority represented non-essential elements (Hg, Cd, Pb). Although internal organs constituted the main biological matrix chosen for each group (37%), we observed an increase in the use of non-destructive matrices in both groups (scale, blood, tail muscle, carapace). The majority of analysed studies used HNO3 for the sample decomposition, with the majority of analyses being performed using atomic absorption spectroscopy (53%). Mainly blank controls (19%), analyte recovery (18%) and replicates (18%) were used as methods of validating analytical procedures. Furthermore, the studies used certified reference materials, which measure the accuracy of the methods used. We conclude that the increase in the use of aquatic reptiles in environmental monitoring research is mainly due to their ability to reveal integrated changes in ecosystems, aiding in environmental public policy decision-making and effective management plans.
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Appendices
Appendix 1 Description of species, elements, equipment and respective authors, separated by Order (Testudines and Crocodylia) from 1976 to 2020. List of abbreviations are at footnote
Species | Elements | Equipment | Author(s) | Year | |
|---|---|---|---|---|---|
Testudines | |||||
Trachemys scripta | Not reported | Not reported | Schwartz and Flamenbaum | ||
Trachemys scripta | Cd, Cr, Cu, Ni, Pb, Zn, Hg | AAS | Albers, Sileo and Mulhern | ||
Trachemys scripta | Pb, Hg, Cd, Se, Cr, Mn | SS-GF ASS and CV-AAS | Burger and Gibbons | ||
Trachemys scripta | Al, Cd, Cr, Cu, Mn, Ni, Pb, Va, Zn | ICP-AES | Tryfonas, et al., | ||
Trachemys scripta | Pb | SS-GF AAS | Bisho,p et al., | ||
Trachemys scripta | Cd, Cr, Cu, Pb, Hg | CV-AAS and SS-GF AAS | Yu, et al., | ||
Trachemys scripta | Cd | ICP-MS | Guirlet, et al., | ||
Trachemys scripta | Hg | SS-GF AAS and CV-AAS | Yu, et al., | ||
Trachemys scripta | As, Se, Zn, Hg, Sr | ICP-MS | Van Dyke, et al., | ||
Trachemys scripta | Se | ICP-MS | Dyc, et al., | ||
Trachemys scripta | As, Ba, Cd, Cr, Cu, Fe, Mn, Hg, Se, Zn, Sr, Tl, Va | IDA | Van Dyke, et al.,, | ||
Chelydra serpentina | Hg, Cd | not reported | Helwig & Hora, | ||
Chelydra serpentina | Cd, Cr, Cu, Ni, Pb, Zn, Hg | AAS | Albers, Sileo & Mulhern, | ||
Chelydra serpentina | Sr, Co and Hg | CV-AAS | Linda Meyers-Schone, et al., | ||
Chelydra serpentina | Cd, Cr, Cu, Fe, Pb, Mg, Mn and Zn | ICP-AES | Smith, et al., | ||
Chelydra serpentina | As, Ba, Cd, Cr, Cu, Fe, Mn, Hg, Se, Zn, Sr, Tl, Va | IDA | Van Dyke, et al., | ||
Apalone spinifera | As, Ba, Cd, Cr, Cu, Fe, Mn, Hg, Se, Zn, Sr, Tl, Va | IDA | Van Dyke, et al., | ||
Aspideretes gangeticus | Cd, Co, Cr,Cu, Fe, Mn, Ni, Pb, Zn | AAS | Malik, et al., | ||
Chelus fimbriatus | Hg | CV-AAS | Schneider, et al., | ||
Chelus fimbriatus | As, Cd, Cr, Pb, Hg and Se | not reported | Burger, et al., | ||
Chelus fimbriatus | Hg | CV-AAS | Schneider, et al., | ||
Chrysemys picta | Cd | ICP-MS | Rie, Lendas & Callard, | ||
Chrysemys picta | Cd | not reported | Kitana & Callard, | ||
Chrysemys picta | Cd, Cr, Cu, Fe, Pb, Mg, Mn and Zn | ICP-AES | Smith, et al., | ||
Cuora amboinensis | Hg | DMA 80 | Green, et al., | ||
Emys orbicularis | Zn, Pb, Cu, Cd | ASS and ICP-MS | Namroodi,, et al., | ||
Emys orbicularis | Zn, Ag, Cd, Hg, Pb, As, Co, Cr, Cu, Fe, Mn, Ni, Se, Va | ICP-MS, SS-GF-AAS and HG-AAS | Guillot, et al., | ||
Heosemys spinosa | Hg | DMA 80 | Green, et al., | ||
Kachuga smithi | Cu, Zn, Ni, Cd, Co, Pb, Cr | AAS | Nisa, et al., | ||
Kachuga smithi | Cu, Zn, Ni, Cd, Cr, Co, Pb | FAAS | Nisa, et al., | ||
Kachuga tecta | Cu, Zn, Ni, Cd, Co, Pb, Cr | ASS | Nisa, et al., | ||
Kachuga tecta | Cu, Zn, Ni, Cd, Cr, Co, Pb | FAAS | Nisa, et al., | ||
Lissemys punctata | Cu, Zn, Ni, Cd, Co, Pb, Cr | FAAS | Nisa, et al., | ||
Lissemys punctata | Cu, Zn, Ni, Cd, Cr, Co, Pb | ASS | Nisa, et al., | ||
Macroclemys temminckii | Cr, Cd and Pb | ICP-AES | Dupre, et al., | ||
Macroclemys temminckii | Pb, Zn and Hg | SS-GF-AAS and CV-AAS | DiGeronimo, | ||
Malaclemys terrapin | Hg | CV-AAS | Sherwood, et al., | ||
Malaclemys terrapin | Zn, Hg and Pb | SS-GF AAS and CV-AAS | DiGeronimo, | ||
Mauremys reevesii | Cd | not reported | Huo, et al., | ||
Mauremys caspica | Zn, Pb, Cu, Cd | AAS | Yadollahvand, et al., | ||
Mauremys caspica | Hg, Pb and Cd | SS-GF AAS and CV-AAS | Adel, et al., | ||
Mauremys leprosa | Hg, Pb, Cu, Zn and Cd | CV AAS and ASV | Martínez-López, et al., | ||
Mauremys leprosa | Pb and Hg | FAAS | Ortiz-Santaliestra, et al., | ||
Podocnemis dumerilianus | Hg | CV-AAS | Schneider, et al., | ||
Podocnemis dumerilianus | As, Cd, Cr, Pb, Hg and Se | not reported | Burger, et al., | ||
Podocnemis dumerilianus | Hg | CV-AAS | Schneider, et al., | ||
Podocnemis erythrocephala | Hg | CV-AAS | Schneider, et al., | ||
Podocnemis erythrocephala | As, Cd, Cr, Pb, Hg and Se | not reported | Burger, et al., | ||
Podocnemis erythrocephala | Hg | CV-AAS | Schneider, et al., | ||
Podocnemis expansa | Hg | CV-AAS | Schneider, et al., | ||
Podocnemis expansa | As, Cd, Cr, Pb, Hg and Se | not reported | Burger, et al., | ||
Podocnemis expansa | Hg | CV-AAS | Schneider, et al., | ||
Podocnemis expansa | Hg [CH3Hg]+ | ICP-MS | Eggins, et al., | ||
Podocnemis expansa | Hg | CV-AAS | Souza-Araujo, Giarrizzo & Lima, | ||
Podocnemis sextuberculata | Hg | CV-AAS | Schneider, et al., | ||
Podocnemis sextuberculata | As, Cd, Cr, Pb, Hg and Se | not reported | Burger, et al., | ||
Podocnemis sextuberculata | Hg | CV-AAS | Schneider, et al., | ||
Podocnemis unifilis | Hg | CV-AAS | Schneider, et al., | ||
Podocnemis unifilis | As, Cd, Cr, Pb, Hg and Se | not reported | Burger, et al., | ||
Podocnemis unifilis | Hg | CV-AAS | Schneider, et al., | ||
Podocnemis unifilis | Hg [CH3Hg]+ | ICP-MS | Eggins, et al., | ||
Podocnemis unifilis | Hg | CV-AAS | Souza-Araujo, Giarrizzo & Lima, | ||
Pseudemys rubriventri | Pb | SS-GF-AAS | Bishop, et al., | ||
Siebenrockiella crassicollis | Hg | DMA 80 | Green, et al., | ||
Sternotherus odoratus | Hg | SS-GF-AAS and CV-AAS | Yu, et al., | ||
Sternotherus odoratus | As, Se, Zn, Hg, Sr | ICP-MS | Vand Dyke, et al., | ||
Sternotherus odoratus | As, Ba, Cd, Cr, Cu, Fe, Mn, Hg, Se, Zn, Sr, Tl, Va | IDA | Vand Dyke, et al., | ||
Terrapene carolina carolina | Pb, As, Zn, Cr, Se, Cu, Cd and Ag | ICP-MS | Allender,, et al., | ||
Trachemys callirostris | Hg | CV-AAS | Rendón-Valencia, et al., | ||
Trachemys callirostris | Hg | DMA 80 | Meza-Martínez, et al., | ||
Trionyx triunguis | Cr, Cd, Cu, Fe, Ni and Pb | FAAS | Gidis & Kaska, | ||
Crocodylia | |||||
Alligator mississipiensis | Cu, Zn, Fe, Cr, Hg, Pb, As and Pt | AAS and SS-GF-AAS | Delany, Bell & Sundlof, | ||
Alligator mississipiensis | Al, As, Be, Cd, Cr, Cu, Fe, Pb, Mn, Hg, Mo, Ni Se, Ta and Va | ICP | Heinz, Percival & Jennings, | ||
Alligator mississipiensis | Hg | CV-AAS | Ruckel, | ||
Alligator mississipiensis | Hg | CV-AAS | Heaton-Jones, et al., | ||
Alligator mississipiensis | Hg | CV-AAS and gold leaf amalgam with conductivity detection | Yanochko, Jagoe & Brisbin, | ||
Alligator mississipiensis | Hg | CV-AAS | Jago, et al., | ||
Alligator mississipiensis | Pb | SS-GF-AAS | Camus, et al., | ||
Alligator mississipiensis | As, Cd, Cr, Pb, Mn, Hg and Se | CV-AAS | Burger, et al., | ||
Alligator mississipiensis | Hg | not reported | Khan & Tansel, | ||
Alligator mississipiensis | Hg | AAS | Rumbold, et al., | ||
Alligator mississipiensis | Se | ICP-MS | Roe, et al., | ||
Alligator mississipiensis | Pb, Cd and Se | SS-GF-AAS | Lance, et al., | ||
Alligator mississipiensis | Pb | ICP-AES | Seltzer, et al., | ||
Alligator mississipiensis | Cd, Co, Cr, Ni, Pb, As, Hg and Se | ICP and PSA | Campbell, et al., | ||
Alligator mississipiensis | Cd, Cu, Fe, Pb and Zn | ICP-AES | Guillory, et al., | ||
Alligator mississipiensis | Li, Mg, Al, Va, Cr, Mn, Fe, Co, Ni, Cu, Zn, GaAs, Se, S, Sr, Mo, Ag, In, Sn, Sb, Cs, Tl, Hg, Pb and Bi | ICP and CV-AAS | Horai, et al., | ||
Alligator mississipiensis | As, Cd, Cu, Fe, Pb, Se and Zn | ICP-AES | Tellez et al., | ||
Alligator mississipiensis | Hg, Al, Va, Cr, Mn, Co, Ni, Cu, Zn, As, Se, Rb, Sr, Mo, Cd, Pb, Sn | ICP-MS | Nilsen, et al., | ||
Alligator mississipiensis | As, Cd, Cr, Cu and Se | ICP-MS | Tuberville, et al., | ||
Alligator mississipiensis | Al, Va, Cr, Mn, Co, Ni, Zn, As, Se, Rb, Sr, Mo, Cd, Sn, Cd and Pb | ICP-MS | Nilsen, et al., | ||
Alligator mississipiensis | Hg | DMA | Nilsen, et al., | ||
Alligator mississipiensis | Hg | DMA | Lawson, et al., | ||
Alligator mississipiensis | Al, Cu, Zn, Mo, Se, As, Cd, Pb and Hg | ICP-MS | Nilsen, et al., | ||
Alligator mississipiensis | Hg | DMA | Nilsen, et al., | ||
Alligator sinensis | As, Fe, Mn, Cu, Pb, Cd, Cr, Zn and Hg | CV-AAS | Xu, et al., | ||
Caiman crocodilus | Hg | CV-AAS | Schneider, et al., | ||
Caiman crocodilus | Hg | ICP-MS | Schneider, et al., | ||
Caiman crocodilus | Hg | DMA | Marrugo-Negrete, et al., | ||
Crocodylus acutus | Al, Cd, Co, Cu, Pb, Mo and Sr | ICP | Stoneburner & Kushlan, | ||
Crocodylus acutus | Cd, Cu, Pb, Hg, Zn and As | ICP-AES | Rainwater, et al., | ||
Crocodylus moreletii | Hg | CV-AAS | Rainwate, et al., | ||
Crocodylus moreletii | Cd, Cu, Pb, Hg, Zn and As | ICP-AES | Rainwater, et al., | ||
Crocodylus moreletii | As, Hg, Pb, Ni, Cd, Cr | FAAS and HG-AAS | Trillanes et al | ||
Crocodylus moreletii | Hg and Cd | SS-GF-AAS | Buenfil-Rojas, et al., | ||
Crocodylus moreletii | Hg | AAS | Buenfil-Rojas, et al., | ||
Crocodylus moreletii | Cd, Cr and Pb | FAAS | Cedillo-Leal, et al., | ||
Crocodylus moreletii | Hg, Cd, Cu and Zn | VEQ and HG-AAS | Buenfil-Rojas, et al., | ||
Crocodylus niloticus | Cd, Co, Mn, Mo, Pb, As, Hg, Se, Co and Zn | FAAS and SS-GF-AAS | Almli,, et al., | ||
Crocodylus niloticus | Cr, Cd, Zn, Ti, Hg, Pt, Au, Ag, Pb, Ni, Mn and U | ICP-AES | Du Preez, et al., | ||
Crocodylus niloticus | Pb | SS-GF-AAS | Warner, et al., | ||
Crocodylus niloticus | Al, Cu, Hg, Cr, Ni, Co, Cd, Zn, Se, As, Mn, Fe, Ba, Va, Pt, Au, Ag and Ti | not reported | Du Preez, et al., | ||
Crocodylus porosus | Na, K, Ca, Mg, Sr, Fe, Al, Mn, Zn, Pb, Cu, Ni, Cr, Co, Se, U and Tl | ICP | Jeffree, Markich & Twining, | ||
Crocodylus porosus | Ba, Al, Ca, Cd, Cr, Fe, H, K, Mg, Mn, Na, Ni, P, Pb, S, Se, Sr, Zn and Sn | ICP-MS | Manolis, et al., | ||
Crocodylus porosus | Pb | ICP-MS | Hammerton, Jayasinghe & Lim, | ||
Crocodylus porosus | Ba, Cd, Co, Cu, Mn, Ni, Pb, U, Zn, As, Cr, Hg, Mo, Sb, Se, Ta and Sn | ICP | Jeffree, et al., | ||
Melanosuchus niger | Hg | CV-AAS | Schneider, et al., | ||
Melanosuchus niger | Hg | not reported | Correia, et al., | ||
Melanosuchus niger | Hg [CH3Hg] + | ICP-MS | Eggins,, et al., | ||
Melanosuchus niger | Hg | ICP-MS | Schneider, et al.., | ||
Caiman latirostris | As and Pb | AAS | Quintela, et al., | ||
Appendix 2 Part of the studies that analysed concentrations of cadmium, lead and mercury in blood, keratin, muscle and/or liver samples analysed by the articles in this review. The concentrations presented may not represent all samples from the selected articles, due to the large amount of information and elements analysed by the authors (median ± SD) (ww/dw) (ND not detected)
Year | Author (s) | Element(s) | Specie | Element | Sample | Unit | |||||
|---|---|---|---|---|---|---|---|---|---|---|---|
Cadmium | Wet weight | mg g-1 | |||||||||
Albers, Sileo & Mulhern | Cd, Cr, Cu, Ni, Pb, Zn, Hg | Trachemys scripta | Lead | ||||||||
Mercury | |||||||||||
Cadmium | Wet weight | ng g-1 | |||||||||
Burger, et al., | As, Cd, Cr, Pb, Hg and Se | Chelus fimbriatus | Lead | ||||||||
Mercury | |||||||||||
Guillot, et al., | Zn, Ag, Cd, Hg, Pb, As, Co, Cr, Cu, Fe, Mn, Ni, Se, Va | Emys orbicularis | Cadmium | Dry weight | µg g-1 | ||||||
Lead | |||||||||||
Mercury | |||||||||||
Cadmium | Dry weight | mg kg-1 | |||||||||
Adel, et al., | Hg, Pb and Cd | Mauremys caspica | Lead | ||||||||
Mercury | |||||||||||
Cadmium | Wet weight | µg dL-1 | |||||||||
Martínez-López, et al., | Hg, Pb, Cu, Zn and Cd | Mauremys leprosa | Lead | ||||||||
Mercury | |||||||||||
As, Cd, Cr, Pb, Mn, Hg and Se | Cadmium | Wet weight | ppb | ||||||||
Burger, et al., | Alligator mississipiensis | Lead | |||||||||
Mercury | |||||||||||
Cd, Co, Cr, Ni, Pb, As, Hg and Se | Cadmium | µg g-1 | |||||||||
Campbell, et al., | Alligator mississipiensis | Lead | Not reported | ||||||||
Mercury | |||||||||||
Alligator mississipiensis | Cadmium | Wet weight | ng g-1 | ||||||||
Nilsen, et al., | Al, Cu, Zn, Mo, Se, As, Cd, Pb and Hg | Lead | |||||||||
Mercury | |||||||||||
As, Fe, Mn, Cu, Pb, Cd, Cr, Zn and Hg | Cadmium | Dry weight | µg g-1 | ||||||||
Xu, et al., | Alligator sinensis | Lead | |||||||||
Mercury | |||||||||||
Cadmium | Dry weight | ng g-1 | |||||||||
Trillanes, et al., | As, Hg, Pb, Ni, Cd, Cr | Crocodylus moreletii | Lead | ||||||||
Mercury | |||||||||||
Cd, Co, Mn, Mo, Pb, As, Hg, Se, Co and Zn | Cadmium | Wet weight | µg g-1 | ||||||||
Almli, et al., | Crocodylus niloticus | Lead | |||||||||
Mercury | |||||||||||
Cr, Cd, Zn, Ti, Hg, Pt, Au, Ag, Pb, Ni, Mn and U | Cadmium | Dry weight | mg kg-1 | ||||||||
Preez ,et al., | Crocodylus niloticus | Lead | |||||||||
Mercury | |||||||||||
Concentration (s) | |||||||||||
Males | Female | Gender not defined | |||||||||
Blood | Muscle | keratin | Live | Blood | Muscle | Keratin | Liver | Blood | Muscl | Keratin | Liver |
– | – | – | 0.10 ± 0.06 | – | – | – | 0.08 ± 0.05 | – | – | – | – |
– | – | – | ND | – | – | – | ND | – | – | – | – |
1.28 ± 0.79 | 1.27 ± 0.34 | – | – | – | – | ||||||
0.05 ± 0.04 | – | – | – | 0.01 ± 0 | – | – | – | – | – | – | – |
25.7 ± 4.24 | – | – | – | 26.6 ± 4.87 | – | – | – | – | – | – | – |
1.47 ± 0.35 | – | – | – | 1.81 ± 0.35 | – | – | – | – | – | – | – |
– | – | – | – | – | – | – | – | – | 0.015 ± 0.012 | – | – |
– | – | – | – | – | – | – | – | – | 0.21 ± 0.19 | – | 0.74 ± 2.51 |
– | – | – | – | – | – | – | – | – | 0.662 ± 0.375 | – | 1.128 ± 1.077 |
– | 2.10 ± 0.10 | – | 4.29 ± 0.19 | – | 2.29 ± 0.19 | – | 4.82 ± 2.82 | – | – | – | – |
– | 23.82 ± 1.12 | – | 35.46 ± 1.90 | – | 22.12 ± 1.57 | – | 35.34 ± 2.05 | – | – | – | – |
– | 1.63 ± 0.11 | – | 2.70 ± 0.13 | – | 1.66 ± 0.14 | – | 2.78 ± 0.18 | – | – | – | – |
0.23 ± 0.30 | – | – | – | 0.05 ± 0.08 | – | – | – | – | – | – | – |
10.53 ± 6.59 | – | – | – | 7.33 ± 7.82 | – | – | – | – | – | – | – |
1.00 ± 0.50 | – | – | – | 0.44 ± 0.38 | – | – | – | – | – | – | – |
– | – | – | – | – | – | – | – | – | 62.8 ± 618.6 | – | 123 ± 19.2 |
– | – | – | – | – | – | – | – | – | 40.8 ± 9.3 | – | 27.7 ± 4.76 |
– | – | – | – | – | – | – | – | – | 403 ± 80.1 | – | 62.5 ± 16.5 |
– | – | – | 0.562 ± 0.20 | – | – | – | 0.389 ± 0.12 | – | – | – | – |
– | – | – | 5.52 ± 2.2 | – | – | – | 11.7 ± 7.8 | – | – | – | – |
– | – | – | 7.32 ± 2.4 | – | – | – | 3.44 ± 0.82 | – | – | – | – |
– | – | – | – | – | – | – | – | 1.1 ± 0.4 | – | – | – |
– | – | – | – | – | – | – | – | 464 ± 1308 | – | – | – |
– | – | – | – | – | – | – | – | 1364 ± 673 | – | – | – |
– | – | 0.201 | 0.53 | – | 0.109 | - | 0.275 | – | – | – | – |
– | – | 0.71 | 0.85 | – | 0.75 | - | 0.54 | – | – | – | – |
– | – | 0.105 | 0.492 | – | 0.281 | - | 0.626 | – | – | – | – |
– | – | – | – | – | – | – | – | – | – | ND | – |
– | – | – | – | – | – | – | – | – | – | 64.8 ± 57.8b | – |
– | – | – | – | – | – | – | – | – | – | 4.3 ± 2.7 | – |
– | – | – | – | – | – | – | – | – | – | – | 0.04 |
– | – | – | – | – | – | – | – | – | – | – | 3.3 |
– | – | – | – | – | – | – | – | – | – | – | 3.7 |
– | – | – | – | – | – | – | – | – | 0.0079 | – | – |
– | – | – | – | – | – | – | – | – | 0.1 | – | – |
– | – | – | – | – | – | – | – | – | 2.8 | – | – |
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dos Santos, R.L., de Sousa Correia, J.M. & dos Santos, E.M. Freshwater aquatic reptiles (Testudines and Crocodylia) as biomonitor models in assessing environmental contamination by inorganic elements and the main analytical techniques used: a review. Environ Monit Assess 193, 498 (2021). https://doi.org/10.1007/s10661-021-09212-w
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DOI: https://doi.org/10.1007/s10661-021-09212-w