Abstract
This study aims to characterize the microbial community and its relationship with heavy metal pollution in the beaches of Sugözü, an important nesting site for the green turtle. Heavy metal concentrations of sand samples from subregions of Sugözü were determined using ICP-MS. The microbial community was analyzed using the Biolog® EcoPlate. The relationship between microbial catalytic activity and heavy metal levels were analyzed using canonical correspondence analysis. Levels of 27Al, 57Fe, 55Mn, and 52Cr were quite high (4332.34, 13,764.77, 590.98, and 48.21 mg/kg, respectively). The microbial community in subregions with high levels of metals was found to use carboxylic acid as a carbon source. Bioactivity, substrate utilization, diversity, and evenness values indicated negative correlations concentrations of 27Al, 56Fe, and 52Cr (−0.820, −0.508, and −0.560, respectively). It was also found that microbial diversity decreased in the subregions where heavy metal concentration increased. Embryonic deaths were found highest at early stage (0.1 to 0.2 eggs) and lowest at middle stage for whole study sites by inspecting a total 6408 eggs of 63 green turtle nests. The Biolog EcoPlate was firstly applied to determine pollution, and our findings clearly demonstrate the applicability and effectiveness of this method in assessing nesting beaches.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Not applicable
References
Al-Bahry S, Mahmoud I, Elshafie A, Al-Harthy A, Al-Ghafri S, Al-Amri I, Alkindi A (2009) Bacterial flora and antibiotic resistance from eggs of green turtles Chelonia mydas: an indication of polluted effluents. Mar Pollut Bull 58(5):720–725. https://doi.org/10.1016/j.marpolbul.2008.12.018
Al-Musharafi SK, Mahmoud IY, Al-Bahry SN (2015) Heavy metals and antibiotic resistant bacteria in green turtles are indicators of environmental pollution. Int J Environ Ecol Eng 9(4):409–412. https://doi.org/10.5281/zenodo.1100569
Al-Rawahy SH, AlKindi AY, Elshafie A, Ibrahim M, Al Bahry SN, Al Siyabi SS, Mansour MH, Al Kiyumi AA (2007) Accumulation of metals in the egg yolk and liver of hatchling of green turtles Chelonia mydas at Ras Al Hadd, Sultante of Oman. J Biol Sci 7(6):925–930. https://doi.org/10.3923/jbs.2007.925.930
Anan Y, Kunito T, Sakai H, Tanabe S (2002) Subcellular distribution of trace elements in the liver of sea turtles. Mar Pollut Bull 45(1-12):224–229. https://doi.org/10.1016/S0025-326X(02)00106-6
Andreani G, Santoro M, Cottignoli S, Fabbri M, Carpenè E, Isani G (2008) Metal distribution and metallothionein in loggerhead (Caretta caretta) and green (Chelonia mydas) sea turtles. Sci Total Environ 390(1):287–294. https://doi.org/10.1016/j.scitotenv.2007.09.014
Canbolat AF, Atatunç K, Candan O, Barcak D (2005) A new green turtle (Chelonia mydas) nesting site in the Mediterranean: Sugözü beaches, Adana (Turkey). In Proceedings of the Second Mediterranean Conference on Sea Turtles, Kemer, Turkey
Candan ED (2018a) Molecular identification of fungal isolates and hatching success of green turtle (Chelonia mydas) nests. Arch Microbiol 200(6):911–919. https://doi.org/10.1007/s00203-018-1496-0
Candan O (2018b) Impact of nest relocation on the reproductive success of Loggerhead Turtles, Caretta caretta, in the Göksu Delta, Turkey (Reptilia: Cheloniidae). Zool Middle East 64(1):38–46. https://doi.org/10.1080/09397140.2017.1414978
Candan O, Candan ED (2020) Bacterial diversity of the green turtle (Chelonia mydas) nest environment. Sci Total Environ:137717. https://doi.org/10.1016/j.scitotenv.2020.137717
Casale P, Broderick AC, Camiñas JA, Cardona L, Carreras C, Demetropoulos A, Fuller WJ, Godley BJ, Hochscheid S, Kaska Y, Lazar B, Margaritoulis D, Panagopoulou A, Rees AF, Tomás J, Türkozan O (2018) Mediterranean sea turtles: current knowledge and priorities for conservation and research. Endanger Species Res 36:229–267. https://doi.org/10.3354/esr00901
Caurant F, Bustamante P, Bordes M, Miramand P (1999) Bioaccumulation of cadmium, copper and zinc in some tissues of three species of marine turtles stranded along the French Atlantic Coasts. Mar Pollut Bull 38:1085–1091. https://doi.org/10.1016/S0025-326X(99)00109-5
Çelik A, Kaska Y, Bağ H, Aureggi M, Semiz G, Kartal AA, Elçi L (2006) Heavy metal monitoring around the nesting environment of green sea turtles in Turkey. Water Air Soil Pollut 169(1-4):67–79. https://doi.org/10.1007/s11270-006-1562-0
Cevik U, Koz B, Makarovska Y (2010) Heavy metal analysis around Iskenderun Bay in Turkey. X-Ray Spectrom 39(3):202–207. https://doi.org/10.1002/xrs.1250
Degens BP, Schipper LA, Sparling GP, Duncan LC (2001) Is the microbial community in a soil with reduced catabolic diversity less resistant to stress or disturbance? Soil Biol Biochem 33(9):1143–1153. https://doi.org/10.1016/S0038-0717(01)00018-9
Dennis MM, Poppenga R, Conan A, Hill K, Hargrave S, Maroun V, Stewart KM (2020) Leatherback sea turtle (Dermochelys coriacea) hatch success and essential and nonessential metals in eggs and embryos from nests in St. Kitts (2015). Mar Pollut Bull 161:111726. https://doi.org/10.1016/j.marpolbul.2020.111726
Dong XUE, Huai-Ying YAO, De-Yong GE, Huang CY (2008) Soil microbial community structure in diverse land use systems: a comparative study using Biolog, DGGE, and PLFA Analyses Project supported by the National Natural Science Foundation of China (Nos. 30671207 and 40371063). Pedosphere 18(5):653–663. https://doi.org/10.1016/S1002-0160(08)60060-0
Doygun H, Alphan H (2006) Monitoring urbanization of Iskenderun, Turkey, and its negative implications. Environ Monit Assess 114(1-3):145–155. https://doi.org/10.1007/s10661-006-2524-0
Fairbrother A, Wenstel R, Sappington K, Wood W (2007) Framework for metals risk assessment. Ecotoxicol Environ Saf 68(2):145–227. https://doi.org/10.1016/j.ecoenv.2007.03.015
Foti M, Giacopello C, Bottari T, Fisichella V, Rinaldo D, Mammina C (2009) Antibiotic resistance of gram negatives isolates from loggerhead sea turtles (Caretta caretta) in the central Mediterranean Sea. Mar Pollut Bull 58(9):1363–1366. https://doi.org/10.1016/j.marpolbul.2009.04.020
Garland JL (1996) Analytical approaches to the characterization of samples of microbial communities using patterns of potential C source utilization. Soil Biol Biochem 28(2):213–221. https://doi.org/10.1016/0038-0717(95)00112-3
Garland JL (1997) Analysis and interpretation of community-level physiological profiles in microbial ecology. FEMS Microbiol Ecol 24(4):289–300. https://doi.org/10.1016/S0168-6496(97)00061-5
Giller KE, Witter E, Mcgrath SP (1998) Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review. Soil Biol Biochem 30(10-11):1389–1414. https://doi.org/10.1016/S0038-0717(97)00270-8
Godley BJ, Thompson DR, Furness RW (1999) Do heavy metal concentrations pose a threat to marine turtles from the Mediterranean Sea? Mar Pollut Bull 38(6):497–502. https://doi.org/10.1016/S0025-326X(98)00184-2
Gryta A, Frąc M, Oszust K (2014) The application of the Biolog EcoPlate approach in ecotoxicological evaluation of dairy sewage sludge. Appl Biochem Biotechnol 174(4):1434–1443. https://doi.org/10.1007/s12010-014-1131-8
Guedon E, Desvaux M, Petitdemange H (2000) Kinetic analysis of Clostridium cellulolyticum carbohydrate metabolism: importance of glucose 1-phosphate and glucose 6-phosphate branch points for distribution of carbon fluxes inside and outside cells as revealed by steady- state continuous culture. J Bacteriol 182(7):2010–2017. https://doi.org/10.1128/JB.182.7.2010-2017.2000
Hamann M, Godfrey MH, Seminoff JA, Arthur K, Barata PCR, Bjorndal KA, Bolten AB, Broderick AC, Campbell LM, Carreras C, Casale P, Chaloupka M, Chan SKF, Coyne MS, Crowder LB, Diez CE, Dutton PH, Epperly SP, FitzSimmons NN, Formia A, Girondot M, Hays GC, Cheng IJ, Kaska Y, Lewison R, Mortimer JA, Nichols WJ, Reina RD, Shanker K, Spotila JR, Tomás J, Wallace BP, Work TM, Zbinden J, Godley BJ (2010) Global research priorities for sea turtles: informing management and conservation in the 21st century. Endanger Species Res 11(3):245–269. https://doi.org/10.3354/esr00279
Honarvar S, Spotila JR, O’Connor MP (2011) Microbial community structure in sand on two olive ridley arribada nesting beaches, Playa La Flor, Nicaragua and Playa Nancite, Costa Rica. J Exp Mar Biol Ecol 409(1-2):339–344. https://doi.org/10.1016/j.jembe.2011.09.015
Huang N, Wang W, Yao Y, Zhu F, Wang W, Chang X (2017) The influence of different concentrations of bio-organic fertilizer on cucumber Fusarium wilt and soil microflora alterations. PLoS One 12(2):e0171490. https://doi.org/10.1371/journal.pone.0171490
Jiang W, Wang J, Tang J, Hou F, Lu Y (2010) Soil bacterial functional diversity as influenced by cadmium, phenanthrene and degrade bacteria application. Environ Earth Sci 59(8):1717–1722. https://doi.org/10.1007/s12665-009-0153-y
Jickells T, Baker A (2015) Heavy Metals. In: North G, Pyle J, Zhang F (eds) Encyclopedia of atmospheric sciences, 2nd edn. Elsevier, Cambridge, pp 201–204
Kapanen A, Vikman M, Rajasärkkä J, Virta M, Itävaara M (2013) Biotests for environmental quality assessment of composted sewage sludge. Waste Manag 33(6):1451–1460. https://doi.org/10.1016/j.wasman.2013.02.022
Kaska Y, Celik A, Bag H, Aureggi M, Özel K, Elçi A, Kaska A, Elçi L (2004) Heavy metal monitoring in stranded sea turtles along the Mediterranean coast of Turkey. Fresenius Environ Bull 13(8):769–776
Kılıç Ç, Candan O (2014) Hatchling sex ratio, body weight and nest parameters for chelonia mydas nesting on Sugözü beaches (Turkey). Anim Biodivers Conserv 37(2):177–182
Klimek B, Sitarz A, Choczyński M, Niklińska M (2016) The effects of heavy metals and total petroleum hydrocarbons on soil bacterial activity and functional diversity in the Upper Silesia Industrial Region (Poland). Water Air Soil Pollut 227(8):265. https://doi.org/10.1007/s11270-016-2966-0
Lewis DE, White JR, Wafula D, Athar R, Dickerson T, Williams HN, Chauhan A (2010) Soil functional diversity analysis of a bauxite-mined restoration chronosequence. Microb Ecol 59(4):710–723. https://doi.org/10.1007/s00248-009-9621-x
Mahrous NN, Columbus MP, Southam G, Macfie SM (2019) Changes in microbial community structure and increased metal bioavailability in a metal-contaminated soil and in the rhizosphere of corn (Zea mays). Rhizosphere 11:100169. https://doi.org/10.1016/j.rhisph.2019.100169
Nagaoka S, Martins A, Santos R (2012) Diet of juvenile green turtles (Chelonia mydas) associating with artisanal fishing traps in a subtropical estuary in Brazil. Mar Biol 159:573–589. https://doi.org/10.1007/s00227-011-1836-y
Owens DW, Day RD, Blanvillain GJ, Schwenter JA, Christopher SJ, Roumillat WA (2006) Turtles as physiological models for environmental stress: can they be “used” and is it ethical. In: Proceedings of the 26th Annual Symposium on Sea Turtle Biology and Conservation, Island of Crete, Greece
Pająk M, Błońska E, Frąc M, Oszust K (2016) Functional diversity and microbial activity of forest soils that are heavily contaminated by lead and zinc. Water Air Soil Pollut 227(9):348. https://doi.org/10.1007/s11270-016-3051-4
Pérez-de-Mora A, Burgos P, Madejón E, Cabrera F, Jaeckel P, Schloter M (2006) Microbial community structure and function in a soil contaminated by heavy metals: effects of plant growth and different amendments. Soil Biol Biochem 38(2):327–341. https://doi.org/10.1016/j.soilbio.2005.05.010
Ribeiro F, O’Brien JW, Galloway T, Thomas KV (2019) Accumulation and fate of nano- and micro-plastics and associated contaminants in organisms. TrAC Trends Anal Chem 111:139–147. https://doi.org/10.1016/j.trac.2018.12.010
Sahoo G, Sahoo RK, Mohanty-Hejmadi P (1996) Distribution of heavy metals in the eggs and hatchlings of olive ridley sea turtle, Lepidochelys olivacea, from Gahirmatha, Orissa. Indian J Mar Sci 25:371–372
Sakai H, Saeki K, Ichihashi H, Kamezaki N, Tanabe S, Tatsukawa R (2000) Growth-Related Changes in Heavy Metal Accumulation in Green Turtle (Chelonia mydas) from Yaeyama Islands, Okinawa, Japan. Arch Environ Contam Toxicol 39:378–385. https://doi.org/10.1007/s002440010118
Seminoff JA (2004) Chelonia mydas. The IUCN Red List of Threatened Species 2004: e. T4615A11037468
Seminoff JA, Shanker K (2008) Marine turtles and IUCN Red Listing: a review of the process, the pitfalls, and novel assessment approaches. J Exp Mar Biol Ecol 356(1-2):52–68. https://doi.org/10.1016/j.jembe.2007.12.007
Sinaei M, Bolouki M (2017) Metals in blood and eggs of green sea turtles (Chelonia mydas) from nesting colonies of the northern coast of the Sea of Oman. Arch Environ Contam Toxicol 73(4):552–561. https://doi.org/10.1007/s00244-017-0421-x
Souza NLN, Carneiro MTWD, Pimentel EF, Frossard A, Freire JB, Endringer DC, Júnior PDF (2018) Trace elements influence the hatching success and emergence of Caretta caretta and Chelonia mydas. J Trace Elem Med Biol 50:117–122. https://doi.org/10.1016/j.jtemb.2018.06.007
State of the environment report for Republic of Turkey (2016) Republic of Turkey Ministry of Environment and Urbanisation, Ankara. Available at: https://webdosya.csb.gov.tr/db/ced/editordosya/tcdr_ing_2015.pdf. Accessed 10 Oct 2020
Storelli MM, Barone G, Storelli A, Marcotrigiano GO (2008) Total and subcellular distribution of trace elements (Cd, Cu and Zn) in the liver and kidney of green turtles (Chelonia mydas) from the Mediterranean Sea. Chemosphere. 70(5):908–913. https://doi.org/10.1016/j.chemosphere.2007.06.069
US Environmental Protection Agency (2007) Framework for metals risk assessment. US Environmental Protection Agency, Office of the Science Advisor: Washington, DC. EPA 120/R-07/001
Wang X, Gao P, Li D, Liu J, Yang N, Gu W, He X, Tang W (2019) Risk assessment for and microbial community changes in Farmland soil contaminated with heavy metals and metalloids. Ecotoxicol Environ Saf 185:109685. https://doi.org/10.1016/j.ecoenv.2019.109685
Weber KP, Legge RL (2009) One-dimensional metric for tracking bacterial community divergence using sole carbon source utilization patterns. J Microbiol Methods 79(1):55–61. https://doi.org/10.1016/j.mimet.2009.07.020
Whitmore CP, Dutton PH (1985) Infertility, embryonic mortality and nest-site selection in leatherback and green sea turtles in Suriname. Biol Conserv 34:251–272. https://doi.org/10.1016/0006-3207(85)90095-3
Xie Y, Fan J, Zhu W, Amombo E, Lou Y, Chen L, Fu J (2016) Effect of heavy metals pollution on soil microbial diversity and bermudagrass genetic variation. Front Plant Sci 7:755. https://doi.org/10.3389/fpls.2016.00755
Yalçın-Özdilek Ş, Özdilek H, Sanguen M (2006) The effects of some elements (Ca, Mg and Cr) on the nesting activity of green turtles on the Samandag Beach, Turkey. Fresenius Environ Bull 15(12b):1607–1615
Yao H, Xu J, Huang C (2003) Substrate utilization pattern, biomass and activity of microbial communities in a sequence of heavy metal-polluted paddy soils. Geoderma 115(1-2):139–148. https://doi.org/10.1016/S0016-7061(03)00083-1
Yilmaz AB (2003) Levels of heavy metals (Fe, Cu, Ni, Cr, Pb, and Zn) in tissue of Mugil cephalus and Trachurus mediterraneus from Iskenderun Bay, Turkey. Environ Res 92(3):277–281. https://doi.org/10.1016/S0013-9351(02)00082-8
Yilmaz AB, Sangün MK, Yaǧlioǧlu D, Turan C (2010) Metals (major, essential to non-essential) composition of the different tissues of three demersal fish species from İskenderun Bay, Turkey. Food Chem 123(2):410–415. https://doi.org/10.1016/j.foodchem.2010.04.057
Yu G, Ma J, Jiang P, Li J, Gao J, Qiao S, Zhao Z (2019) The mechanism of plant resistance to heavy metal. In: IOP Conf Series Earth Environ Sci 310(5):052004. IOP Publishing
Zak JC, Willig MR, Moorhead DL, Wildman HG (1994) Functional diversity of microbial communities: a quantitative approach. Soil Biol Biochem 26(9):1101–1108. https://doi.org/10.1016/0038-0717(94)90131-7
Zhang C, Nie S, Liang J, Zeng G, Wu H, Hua S, Liu J, Yuan Y, Xiao H, Deng L, Xiang H (2016) Effects of heavy metals and soil physicochemical properties on wetland soil microbial biomass and bacterial community structure. Sci Total Environ 557:785–790. https://doi.org/10.1016/j.scitotenv.2016.01.170
Acknowledgements
We thank Fatih Fazlıoğlu, PhD., and Matthew Haworth, PhD., for linguistic advice and criticism and Sevda Türkiş, PhD., and Davut Canlı, PhD., for statistical suggestions and volunteers of Sea Turtle Conservation Project supported by BIL (BOTAŞ International Limited Co., Turkey). We also thank Seaturtle.org team for MapTool. The authors also would like to thank anonymous reviewers for their contribution to the manuscript.
Funding
This research was partially funded by Giresun University Scientific Researches Project Coordination Department (FEN-BAP-A-150219-11).
Author information
Authors and Affiliations
Contributions
EDC, NI, and OC conceived the study. OC provided the framework for sample collections and provided in situ documentation. EDC and NI analyzed the samples, and EDC, NI, and OC wrote the manuscript.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
Not applicable. None of the experiments involved here sacrifice animals, and therefore, an approval from an institutional animal research ethics committee is not required.
Consent to publish
Not applicable. This manuscript does not contain any individual person’s data in any form.
Competing interest
The authors declare no competing interests.
Additional information
Responsible Editor: V. V.S.S. Sarma
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Candan, E.D., İdil, N. & Candan, O. The microbial community in a green turtle nesting beach in the Mediterranean: application of the Biolog EcoPlate approach for beach pollution. Environ Sci Pollut Res 28, 49685–49696 (2021). https://doi.org/10.1007/s11356-021-14196-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-021-14196-8