Abstract
Nile crocodiles (Crocodylus niloticus) at Lake St Lucia, South Africa, have some of the highest blood lead (Pb) concentrations ever recorded in wildlife globally. Although exposure to Pb is known to pose major risks to wildlife reproductive success, potential impacts on crocodile reproduction at Lake St Lucia have yet to be examined. In this study, we investigated the accumulation of Pb and other trace metals (Al, V, Cr, Co, Cu, Ni, Zn and Cd) in eggs (n = 20) collected from five wild crocodile nests at Lake St Lucia. All metals analysed in this study were detected in egg contents, although concentrations varied considerably among nests and within clutches. Lead was detected in the contents of all eggs, but only at relatively low concentrations (43 ± 26 ng g−1 dry weight). Although sampling limitations commonly associated with wild population surveys prevent a complete assessment of exposure variability, our findings suggest maternal transfer may not be a significant depuration pathway for Pb and females possibly clear Pb through other mechanisms (e.g. sequestration into claws, bone and osteoderms). Metal concentrations in eggshells and shell membranes were poorly correlated with concentrations measured in egg content and thus do not provide viable non-lethal indicators for monitoring metal exposure in Nile crocodiles. Intra-clutch variability accounted for a considerable proportion of the total variance in egg content metal concentrations, suggesting the “one egg” sampling strategy often applied in reptile studies may not be an effective biomonitoring tool for wild crocodilian populations. Although maternally derived Pb does not appear to present widespread toxicological concern at Lake St Lucia, adverse effects of Pb exposure on other reproductive functions (e.g. spermatogenesis) cannot be discounted and warrant further investigation.
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References
Akearok JA, Hebert CE, Braune BM, Mallory ML (2010) Inter- and intraclutch variation in egg mercury levels in marine bird species from the Canadian Arctic. Sci Total Environ 408:836–840. https://doi.org/10.1016/j.scitotenv.2009.11.039
Alexander GJ, Tolley KA, Maritz B, McKechnie A, Manger P, Thomson RL, et al. (2021) Excessive red tape is strangling biodiversity research in South Africa. South Afr J Sci https://doi.org/10.17159/sajs.2021/10787
Álvarez-Lloret P, Rodríguez-Navarro AB, Romanek CS, Ferrandis P, Martínez- Haro M, Mateo R (2014) Effects of lead shot ingestion on bone mineralization in a population of red-legged partridge (Alectorisrufa). Sci Total Environ 466:34–39. https://doi.org/10.1016/j.scitotenv.2013.06.103
Becker PH (1992) Egg mercury levels decline with the laying sequence in charadriiformes. Bull Environ Contam Toxicol 33:71–75. https://doi.org/10.1007/BF00195999
Berglund ÅMM, Ingvarsson PK, Danielsson H, Nyholm NEI (2010) Lead exposure and biological effects in pied flycatchers (Ficedula hypoleuca) before and after the closure of a lead mine in northern Sweden. Environ Pollut 158:1368–1375. https://doi.org/10.1016/j.envpol.2010.01.005
Buah-Kwofie A, Humphries MS (2021) Organochlorine pesticide accumulation in fish and catchment sediments of Lake St Lucia: risks for Africa’s largest estuary. Chemosphere 274:129712. https://doi.org/10.1016/j.chemosphere.2021.129712
Buah-Kwofie A, Humphries MS, Pillay L (2018) Bioaccumulation and risk assessment of organochlorine pesticides in fish from a global biodiversity hotspot: iSimangaliso Wetland Park, South Africa. Sci Total Environ 621:273–281. https://doi.org/10.1016/j.scitotenv.2017.11.212
Buerger TT, Mirarchi RE, Lisano ME (1986) Effects of lead shot ingestion on captive mourning dove survivability and reproduction. J Wildl Manag 50:1–8. https://doi.org/10.2307/3801479
Burger J, Gibbons JW (1998) Trace elements in egg contents and egg shells of slider turtles (Trachemys scripta) from the Savannah River site. Arch Environ Contam Toxicol 34:382–386. https://doi.org/10.1007/s002449900334
Burger J, Carruth-Hinchey C, Ondroff J, McMahon M, Gibbons JW, Gochfeld M (1998) Effects of lead on behavior, growth, and survival of hatchling slider turtles. J Toxicol Environ Health A 55:495–502. https://doi.org/10.1080/009841098158296
Burger J, Gochfeld M, Rooney AA, Orlando EF, Woodward AR, Guillette LJ Jr (2000) Metals and metalloids in tissues of American alligators in three Florida lakes. Arch Environ Contam Toxicol 38:501–508. https://doi.org/10.1007/s002440010066
Chiasson RB (1962) Laboratory anatomy of the alligator. W.C Brown co, Dubuque
Combrink X, Warner JK, Downs CT (2016) Nest predation and maternal care in the Nile crocodile (Crocodylus niloticus) at Lake St Lucia, South Africa. Behav Proc 133:31–36. https://doi.org/10.1016/j.beproc.2016.10.014
Combrink AS (2014) Spatial and Reproductive Ecology and Population Status of the Nile Crocodile (Crocodylus niloticus) in the Lake St Lucia Estuarine System, South Africa. Unpublished PhD thesis, University of KwaZulu-Natal, Pietermaritzburg, South Africa
Du Preez M, Govender D, Bouwman H (2016) Heavy metals in muscle tissue of healthy crocodiles from the Kruger National Park, South Africa. Afr J Ecol 54:519–523. https://doi.org/10.1111/aje.12308
Eilser R (2000) Handbook of chemical risk assessment: health hazards to humans, plants, and animals. CRC Press, Boca Raton
Gholamhosseini A, Banaee M, Soltanian S, Sakhaie F (2021) Heavy metals in the blood serum and feces of Mugger Crocodile (Crocodylus palustris) in Sistan and Baluchistan Province, Iran. Biol Trace Elem Res https://doi.org/10.1007/s12011-021-02916-7
González F, López I, Suarez L, Moraleda V, Rodríguez C (2017) Levels of blood lead in griffon vultures from a Wildlife Rehabilitation Center in Spain. Ecotoxicol Environ Saf 143:143–150. https://doi.org/10.1016/j.ecoenv.2017.05.010
Grigg GC, Kirshner DS (2015) Biology and evolution of crocodylians. CSIRO and Cornell University Press, New York
Grillitsch B, Schiesari L (2010) The ecotoxicology of metals in reptiles. In: Sparling DW, Linder G, Bishop CA, Krest S (eds) Ecotoxicology of amphibians and reptiles, 2nd edn. CRC Press, Boca Raton, pp 337–448
Heinz GH, Percival HF, Jennings ML (1991) Contaminants in American alligator eggs from Lake Apopka, Lake Griffin, and Lake Okeechobee, Florida. Environ Monit Assess 16:277–285. https://doi.org/10.1007/BF00397615
Hopkins WA, DuRant SE, Staub BP, Rowe CL, Jackson BP (2006) Reproduction, embryonic development, and maternal transfer of contaminants in the amphibian Gastrophryne carolinensis. Environ Health Perspect 114:661–666. https://doi.org/10.1289/ehp.8457
Hopkins WA (2005) Use of tissue residues in reptile ecotoxicology: a call for integration and experimentalism. In: Gardner SC, Oberdörster E (Eds.), Toxicology of reptiles. Taylor & Francis, London
Humphries MS, Green AN, Finch JM (2016) Evidence of El Niño driven desiccation cycles in a shallow estuarine lake: the evolution and fate of Africa’s largest estuarine system, Lake St Lucia. Global Planet Change 147:97–105. https://doi.org/10.1016/j.gloplacha.2016.11.002
Humphries MS, Myburgh JG, Campbell R, Buah-Kwofie A, Combrink X (2021) Organochlorine pesticide bioaccumulation in wild Nile crocodile (Crocodylus niloticus) fat tissues: environmental influences on changing residue levels and contaminant profiles. Sci Total Environ 753:42068. https://doi.org/10.1016/j.scitotenv.2020.142068
Humphries M, Myburgh J, Campbell R, Combrink X (2022) High lead exposure and clinical signs of toxicosis in wild Nile crocodiles (Crocdylus niloticus) from a World Heritage Site: Lake St Lucia estuarine system. South Afr Chemosp. https://doi.org/10.1016/j.chemosphere.2022.134977
Jeffree RA, Markich SJ, Twining JR (2001) Element concentrations in the flesh and osteoderms of estuarine crocodiles (Crocodylus porosus) from the Alligator Rivers Region, northern Australia: biotic and geographic effects. Arch Environ Contam Toxicol 40:236–245. https://doi.org/10.1007/s002440010168
Jose N, Elangovan AV, Awachat VB, Shet D, Ghosh J, David CG (2018) Response of in ovo administration of zinc on egg hatchability and immune response of commercial broiler chicken. J Anim Physiol Anim Nutr 102:591–595. https://doi.org/10.1111/jpn.12777
Keen CL, Taubeneck MW, Zidenberg-Cherr S, Daston GP, Rogers JM (1997) Toxicant exposure and trace element metabolism in pregnancy. Environ Toxicol Pharmacol 4:301–308. https://doi.org/10.1016/S1382-6689(97)10028-X
Kertész V, Fáncsi T (2003) Adverse affects of (surface water pollutants) Cd, Cr and Pb on the embryogenesis of the mallard. Aquat Toxicol 65:425–433. https://doi.org/10.1016/S0166-445X(03)00155-3
Lam SS, McPartland M, Noori B, Garbus S-E, Lierhagen S et al (2020) Lead concentrations in blood from incubating common eiders (Somateria mollissima) in the Baltic Sea. Environ Int 137:105582. https://doi.org/10.1016/j.envint.2020.105582
Lance VA (1989) Reproductive cycle of the American alligator. Am Zool 29:999–1018
Lance VA, Horn TR, Elsey RM, de Peyster A (2006) Chronic incidental lead ingestion in a group of captive-reared alligators (Alligator mississippiensis): possible contribution to reproductive failure. Compar Biochem Physiol Part C 142:30–35. https://doi.org/10.1016/j.cbpc.2005.09.008
Leidens D, Bianchini A, Varela Junior AS et al (2018) Effects of experimental lead exposure on testis of the Chestnut Capped Blackbird Chrysomus ruficapillus. Bull Environ Contam Toxicol 100:324–330. https://doi.org/10.1007/s00128-017-2227-y
Lemaire J, Marquis O, Bustamante P, Mangione R, Brischoux F (2021) I got it from my mother: Inter-nest variation of mercury concentration in neonate Smooth-fronted Caiman (Paleosuchus trigonatus) suggests maternal transfer and possible phenotypical effects. Environ Res 194:110494. https://doi.org/10.1016/j.envres.2020.110494
Leslie AJ (1997) The ecology and physiology of the Nile crocodile, Crocodylus niloticus, in Lake St Lucia, KwaZulu-Natal, South Africa. Unpublished PhD thesis, Drexel University, Drexel
Li C, Zhao K, Zhang H, Liu L, Xiong F, Wang K et al (2018) Lead exposure reduces sperm quality and DNA integrity in mice. Environ Toxicol 33:594–602. https://doi.org/10.1002/tox.22545
Manolis SC, Webb GJ, Britton AR, Jeffree RA, Markich SJ (2002) Trace element concentrations of wild saltwater crocodile eggs. In Markich SJ, Jeffree RA (eds). Australian nuclear science and technology organisation (ANSTO). Report number ANSTO/E—748. pp 58–61
Nagle RD, Rowe CL, Congdon JD (2001) Accumulation and selective maternal transfer of contaminants in the turtle Trachemys scripta associated with coal ash deposition. Arch Environ Contam Toxicol 40:531–536. https://doi.org/10.1007/s002440010206
Nilsen FM, Rainwater TR, Wilkinson PM, Brunelle AM, Lowers RH, Bowden JA, Guillette LJ, Long SE, Schock TB (2020) Examining maternal and environmental transfer of mercury into American alligator eggs. Ecotoxicol Environ Saf 189:110057. https://doi.org/10.1016/j.ecoenv.2019.110057
Palmer BD, Guillette LJ (1992) Alligators provide evidence for an archosaurian mode of oviparity. Biol Reprod 46:39–47. https://doi.org/10.1095/biolreprod46.1.39
Phelps RJ, Focardi S, Fossi C, Leonzio C, Renzoni A (1986) Chlorinated hydrocarbons and heavy metals in crocodile eggs from Zimbabwe. Trans Zimbabwe Sci Assoc 63:8–15
Pooley AC (1969) Preliminary studies on the breeding of the Nile crocodile Crocodylus niloticus in Zululand. Lammergeyer 10:10–44
Pooley AC (1982) The Ecology of the Nile Crocodile (Crocodylus niloticus) in Zululand. Unpublished MSc thesis. University of Natal, Pietermaritzburg, South Africa.
Rest J (1976) The histological effects of copper and zinc on chick embryo skeletal tissues in organ culture. Br J Nutr 36:243–254. https://doi.org/10.1017/S0007114500020237
Russell RE, Franson JC (2014) Causes of mortality in eagles submitted to the National Wildlife Health Center 1975–2013. Wildl Soc Bull 38:697–704. https://doi.org/10.1002/wsb.469
Sakai H, Ichihashi H, Suganuma H, Tatsukawa R (1995) Heavy metal monitoring in sea turtles using eggs. Mar Pollut Bull 30:347–353
Stoneburner D, Kushlan J (1984) Heavy metal burdens in American crocodile eggs from Florida Bay, Florida, USA. J Herpetol 18:192–193. https://doi.org/10.2307/1563748
Storelli MM, Marcotrigiano GO (2003) Heavy metal residues in tissues of marine turtles. Mar Pollut Bull 46:397–400. https://doi.org/10.1016/S0025-326X(02)00230-8
Terrizzi AR et al (2013) Alveolar bone loss associated to periodontal disease in lead intoxicated rats under environmental hypoxia. Arch Oral Biol 58:1407–1414. https://doi.org/10.1016/j.archoralbio.2013.06.010
Tryfonas AE, Tucker JK, Brunkow PE, Johnson KA, Hussein HS, Lin Z-Q (2006) Metal accumulation in eggs of the red-eared slider (Trachemys scripta elegans) in the Lower Illinois River. Chemosphere 63:39–48. https://doi.org/10.1016/j.chemosphere.2005.07.080
Vallverdú-Coll N, Mougeot F, Ortiz-Santaliestra ME, Castaño C, Santiago-Moreno J, Mateo R (2016) Effects of lead exposure on sperm quality and reproductive success in an avian model. Environ Sci Technol 50:12484–12492. https://doi.org/10.1021/acs.est.6b04231
Warner JK, Combrink X, Myburgh JG, Downs CT (2016) Blood lead concentrations in free-ranging Nile crocodiles (Crocodylus niloticus) from South Africa. Ecotoxicology 25:950–958. https://doi.org/10.1007/s10646-016-1652-8
Warner JK (2015) Morphometrics, ecotoxicology and stable isotope ecology of Nile crocodiles (Crocodylus niloticus) in KwaZulu-Natal, South Africa. Ph.D. thesis, University of KwaZulu-Natal, Pietermaritzburg, South Africa.
Williams RJ, Tannenbaum LV, Williams SM, Holladay SD, Tuckfield RC, Sharma A, Humphrey DJ, Gogal RM (2017) Ingestion of a single 2.3 mm lead pellet by laying roller pigeon hens reduces egg size and adversely affects F1 generation hatchlings. Arch Environ Contam Toxicol 73:513–521. https://doi.org/10.1007/s00244-017-0406-9
Wink CS, Elsey RM (1986) Changes in femoral morphology during egg-laying in Alligator mississippiensis. J Morphol 189:183–188. https://doi.org/10.1002/jmor.1051890208
Wink CS, Elsey RM, Hill EM (1987) Changes in femoral robusticity and porosity during the reproductive cycle of the female alligator (Alligator mississippiensis). J Morphol 193:317–321. https://doi.org/10.1002/jmor.1051930309
Wolfe MF, Schwarzbach S, Sulaiman RA (1998) Effects of mercury on wildlife: a comprehensive review. Environ Toxicol Chem 17:146–160. https://doi.org/10.1002/etc.5620170203
Wright I (2002) Aspects of the Cenozoic Evolution of the Northern KwaZulu-Natal Coastal Plain. South Africa. Bulletin No. 132. Council for Geoscience, Pretoria, South Africa.
Wu Q, Fang S, Wang Z, Wang Z (2006) Heavy metal distribution in tissues and eggs of Chinese alligator (Alligator sinensis). Arch Environ Contam Toxicol 50:580–586. https://doi.org/10.1007/s00244-005-1018-3
Yamamoto FY, Neto FF, Freitas PF, Ribeiro CAO, Ortolani-Machado CF (2012) Cadmium effects on early development of chick embryos. Environ Toxicol Pharmacol 34:548–555. https://doi.org/10.1016/j.etap.2012.06.010
Acknowledgements
The iSimangaliso Wetland Park Authority and Ezemvelo KZN Wildlife kindly granted us permission to work at Lake St Lucia and undertake this research. We thank in particular Dirk Rossouw, Caroline Fox and Sifiso Vumasa for facilitating the study. We are grateful to Sibusiso Mfeka, Zacc Larkin, Molly Bright, Fortunate Davhana, Dámaris López Pérez and Jannie Jacobs for assisting with the collection of samples. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
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This research did not receive any specific grant from funding agencies. Chemical analyses were carried out at the University of the Witwatersrand and supported by discretionary funds awarded to MH.
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Humphries, M., Benitez-Nelson, N. & Combrink, X. Trace Metal Accumulation in Eggs of Wild Nile Crocodiles (Crocodylus niloticus) from Lake St Lucia, South Africa: Implications for Biomonitoring in a Global Biodiversity Hotspot. Arch Environ Contam Toxicol 83, 214–225 (2022). https://doi.org/10.1007/s00244-022-00960-5
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DOI: https://doi.org/10.1007/s00244-022-00960-5