Abstract
The ability of marine filter feeders to accumulate metals could help monitor the health of the marine environment. This study examined the concentration of metallic trace elements (MTE) in two marine sponges, Rhabdastrella globostellata and Hyrtios erectus, from three sampling zones of the semi-enclosed Bouraké Lagoon (New Caledonia, South West Pacific). MTE in sponge tissues, seawater, and surrounding sediments was measured using inductively coupled plasma with optical emission spectroscopy. The variability in sponge MTE concentrations between species and sampling zones was visually discriminated using a principal component analysis (PCA). Sponges showed Fe, Mn, Cr, Ni, and Zn concentrations 2 to 10 times higher than in the surrounding sediments and seawater. Hyrtios erectus accumulated 3 to 20 times more MTE than R. globostellata, except for Zn. Average bioconcentration factors in sponge tissues were (in decreasing order) Zn > Ni > Mn > Fe > Cr relate to sediments and Fe > Ni > Mn > Cr > Zn relate to seawater. The PCA confirmed higher MTE concentrations in H. erectus compared to R. globostellata. Our results confirm that marine sponges can accumulate MTE to some extent and could be used as a tool for assessing metals contamination in lagoon ecosystems, particularly in New Caledonia, where 40% of the lagoon is classified as a UNESCO World Heritage Site.
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References
Aljahdali MO, Alhassan AB (2020) Metallic pollution and the use of antioxidant enzymes as biomarkers in Bellamya unicolor (Olivier, 1804) (Gastropoda: Bellamyinae). Water (Switzerland). https://doi.org/10.3390/w12010202
Ambatsian P, Fernex F, Bernat M et al (1997) High metal inputs to closed seas: the New Caledonian lagoon. J Geochem Explor 59:59–74. https://doi.org/10.1016/S0375-6742(96)00020-9
Batista D, Muricy G, Rocha RC, Miekeley NF (2014) Marine sponges with contrasting life histories can be complementary biomonitors of heavy metal pollution in coastal ecosystems. Environ Sci Pollut Res. https://doi.org/10.1007/s11356-014-2530-7
Bauvais C, Zirah S, Piette L et al (2015) Sponging up metals: bacteria associated with the marine sponge Spongia officinalis. Mar Environ Res. https://doi.org/10.1016/j.marenvres.2014.12.005
Bayer K, Jahn MT, Slaby BM et al (2018) Marine sponges as chloroflexi hot spots: genomic insights and high-resolution visualization of an abundant and diverse symbiotic clade. mSystems. https://doi.org/10.1128/msystems.00150-18
Becquer T, Pétard J, Duwig C et al (2001) Mineralogical, chemical and charge properties of Geric Ferralsols from New Caledonia. Geoderma 103:291–306. https://doi.org/10.1016/S0016-7061(01)00045-3
Bell JJ (2008) The functional roles of marine sponges. Estuar Coast Shelf Sci 79:341
Bell JJ, Bennett HM, Rovellini A, Webster NS (2018) Sponges to be winners under near-future climate scenarios. BioScience 68:955
Berthet B, Mouneyrac C, Pérez T, Amiard-Triquet C (2005) Metallothionein concentration in sponges (Spongia officinalis) as a biomarker of metal contamination. Comp Biochem Physiol C Toxicol Pharmacol. https://doi.org/10.1016/j.cca.2005.07.008
Biscéré T, Lorrain A, Rodolfo-Metalpa R et al (2017) Nickel and ocean warming affect scleractinian coral growth. Mar Pollut Bull. https://doi.org/10.1016/j.marpolbul.2017.05.025
Bonanno G, Di Martino V (2017) Trace element compartmentation in the seagrass Posidonia oceanica and biomonitoring applications. Mar Pollut Bull. https://doi.org/10.1016/j.marpolbul.2016.12.081
Bonet B, Corcoll N, Tlili A et al (2014) Antioxidant enzyme activities in biofilms as biomarker of Zn pollution in a natural system: an active bio-monitoring study. Ecotoxicol Environ Saf. https://doi.org/10.1016/j.ecoenv.2013.11.007
Bonvallot J, Gay J-C, Habert É (2012) Atlas de la Nouvelle-Calédonie. Congrès de la Nouvelle-Calédonie. https://doi.org/10.7202/1028943ar
Briand MJ, Bustamante P, Bonnet X et al (2018) Tracking trace elements into complex coral reef trophic networks. Sci Total Environ. https://doi.org/10.1016/j.scitotenv.2017.08.257
Callender E (2003) Heavy metals in the environment-historical trends. Treatise on geochemistry. Elsevier, Amsterdam
Camp EF, Nitschke MR, Rodolfo-Metalpa R et al (2017) Reef-building corals thrive within hot-acidified and deoxygenated waters. Sci Rep. https://doi.org/10.1038/s41598-017-02383-y
Cantillo AY (1998) Comparison of results of mussel watch programs of the United States and France with worldwide mussel watch studies. Mar Pollut Bull. https://doi.org/10.1016/S0025-326X(98)00049-6
Cebrian E, Martí R, Uriz JM, Turon X (2003) Sublethal effects of contamination on the Mediterranean sponge Crambe crambe: metal accumulation and biological responses. Mar Pollut Bull 46:1273–1284. https://doi.org/10.1016/S0025-326X(03)00190-5
Cesar H, Burke L, Pet-soede L (2003) The economics of worldwide coral reef degradation. Cesar Environmental Economics Consulting, Arnhem
Dahms S, van der Bank FH, Greenfield R (2014) A baseline study of metal contamination along the Namibian coastline for Perna perna and Choromytilus meridionalis. Mar Pollut Bull. https://doi.org/10.1016/j.marpolbul.2014.05.037
De Goeij JM, Van Oevelen D, Vermeij MJA et al (2013) Surviving in a marine desert: the sponge loop retains resources within coral reefs. Science. https://doi.org/10.1126/science.1241981
de Mestre C, Maher W, Roberts D et al (2012) Sponges as sentinels: patterns of spatial and intra-individual variation in trace metal concentration. Mar Pollut Bull. https://doi.org/10.1016/j.marpolbul.2011.10.020
Denton GRW, Concepcion LP, Wood HR, Morrison RJ (2006) Trace metals in marine organisms from four harbours in Guam. Mar Pollut Bull. https://doi.org/10.1016/j.marpolbul.2006.09.010
do Marreiro N, Cruz KJC, Morais JBS et al (2017) Zinc and oxidative stress: current mechanisms. Antioxidants. https://doi.org/10.3390/antiox6020024
Dublet G, Juillot F, Morin G et al (2012) Ni speciation in a New Caledonian lateritic regolith: a quantitative X-ray absorption spectroscopy investigation. Geochim Cosmochim Acta. https://doi.org/10.1016/j.gca.2012.07.030
Duke N (2006) Biodiversity of mangrove in New Caledonia—typologies et Biodiversité des mangroves de Nouvelle-Calédonie. ZoNéCo program report
Edward FB, Yap CK, Ismail A, Tan SG (2009) Interspecific variation of heavy metal concentrations in the different parts of tropical intertidal bivalves. Water Air Soil Pollut. https://doi.org/10.1007/s11270-008-9777-x
Fernandez JM, Meunier JD, Ouillon S et al (2017) Dynamics of suspended sediments during a dry season and their consequences on metal transportation in a Coral reef lagoon impacted by mining activities, New Caledonia. Water (Switzerland). https://doi.org/10.3390/w9050338
Fey P, Bustamante P, Bosserelle P et al (2019) Does trophic level drive organic and metallic contamination in coral reef organisms? Sci Total Environ. https://doi.org/10.1016/j.scitotenv.2019.02.311
Fichez R, Adjeroud M, Bozec YM et al (2005) A review of selected indicators of particle, nutrient and metal inputs in coral reef lagoon systems. Aquat Liv Resour 18:125
Furukawa K, Wolanski E, Mueller H (1997) Currents and sediment transport in mangrove forests. Estuar Coast Shelf Sci 44:301–310. https://doi.org/10.1006/ecss.1996.0120
Gabr G, Masood M, Radwan E et al (2020) Potential effects of heavy metals bioaccumulation on oxidative stress enzymes of Mediterranean clam Ruditapes decussatus. Catrina: Int J Environ Sci. https://doi.org/10.21608/cat.2020.24051.1042
Genta-Jouve G, Thomas OP (2012) Sponge chemical diversity. Advances in marine biology. Elsevier, Amsterdam
Gentric C, Rehel K, Dufour A, Sauleau P (2016) Bioaccumulation of metallic trace elements and organic pollutants in marine sponges from the South Brittany Coast, France. J Environ Sci Health. https://doi.org/10.1080/10934529.2015.1094327
Hédouin L, Pringault O, Bustamante P et al (2011) Validation of two tropical marine bivalves as bioindicators of mining contamination in the New Caledonia lagoon: Field transplantation experiments. Water Res. https://doi.org/10.1016/j.watres.2010.09.002
Hooper JNA, Van Soest RWM (2002) Systema Porifera: a guide to the classification of sponges. Systema Porifera. Springer, Boston
Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346
Kassambara A, Mundt F (2020) factoextra: extract and visualize the results of multivariate data analyses. Package Version 1.0.7. R package version
Labrosse P, Fichez R, Farman R, Adams T (2000) New Caledonia. Seas at the millennium—an environmental evaluation. https://doi.org/10.7591/cornell/9781501754746.003.0008
Luo J, Ye Y, Gao Z, Wang W (2014) Essential and nonessential elements in the red-crowned crane Grus Japonensis of Zhalong Wetland, Northeastern China. Toxicol Environ Chem. https://doi.org/10.1080/02772248.2015.1007989
Maggioni F, Pujo-Pay M, Aucan J et al (2021) The Bouraké semi-enclosed lagoon (New Caledonia)—a natural laboratory to study the lifelong adaptation of a coral reef ecosystem to extreme environmental conditions. Biogeosciences 18:5117–5140. https://doi.org/10.5194/bg-18-5117-2021
Maggioni F, Bell JJ, Pujo-Pay M et al (2023a) Sponge organic matter recycling: reduced detritus production under extreme environmental conditions. Mar Pollut Bull 190:114869. https://doi.org/10.1016/J.MARPOLBUL.2023.114869
Maggioni F, Stenger P-L, Jourand P, Majorel C (2023b) The phylum Chloroflexi and their SAR202 clade dominate the microbiome of two marine sponges living in extreme environmental conditions. Mar Ecol. https://doi.org/10.1111/maec.12757
Marchand C, Lallier-Vergès E, Baltzer F et al (2006) Heavy metals distribution in mangrove sediments along the mobile coastline of French Guiana. Mar Chem. https://doi.org/10.1016/j.marchem.2005.06.001
Marchand C, Lallier-Vergès E, Allenbach M (2011) Redox conditions and heavy metals distribution in mangrove forests receiving effluents from shrimp farms (Teremba Bay, New Caledonia). J Soils Sediments. https://doi.org/10.1007/s11368-010-0330-3
Marchand C, Fernandez JM, Moreton B (2016) Trace metal geochemistry in mangrove sediments and their transfer to mangrove plants (New Caledonia). Sci Total Environ 562:216–227. https://doi.org/10.1016/j.scitotenv.2016.03.206
Martias C, Tedetti M, Lantoine F et al (2018) Characterization and sources of colored dissolved organic matter in a coral reef ecosystem subject to ultramafic erosion pressure (New Caledonia, Southwest Pacific). Sci Total Environ 616–617:438–452. https://doi.org/10.1016/j.scitotenv.2017.10.261
Massaro AJ, Weisz JB, Hill MS, Webster NS (2012) Behavioral and morphological changes caused by thermal stress in the Great Barrier Reef sponge Rhopaloeides odorabile. J Exp Mar Biol Ecol. https://doi.org/10.1016/j.jembe.2012.02.008
Mayzel B, Aizenberg J, Ilan M (2014) The elemental composition of demospongiae from the Red Sea, Gulf of Aqaba. PLoS ONE. https://doi.org/10.1371/journal.pone.0095775
Metian M, Bustamante P, Hédouin L, Warnau M (2008) Accumulation of nine metals and one metalloid in the tropical scallop Comptopallium radula from coral reefs in New Caledonia. Environ Pollut. https://doi.org/10.1016/j.envpol.2007.07.009
Moreton BM, Fernandez JM, Dolbecq MBD (2009) Development of a field preconcentration/elution unit for routine determination of dissolved metal concentrations by ICP-OES in marine waters: application for monitoring of the New Caledonia Lagoon. Geostand Geoanal Res. https://doi.org/10.1111/j.1751-908X.2009.00899.x
Morganti T, Coma R, Yahel G, Ribes M (2017) Trophic niche separation that facilitates co-existence of high and low microbial abundance sponges is revealed by in situ study of carbon and nitrogen fluxes. Limnol Oceanogr. https://doi.org/10.1002/lno.10546
Muyssen BTA, Brix KV, DeForest DK, Janssen CR (2004) Nickel essentiality and homeostasis in aquatic organisms. Environ Rev 12:113
Negri A, Burns K, Boyle S et al (2006) Contamination in sediments, bivalves and sponges of McMurdo Sound, Antarctica. Environ Pollut. https://doi.org/10.1016/j.envpol.2005.12.005
Nissenbaum A, Swaine DJ (1976) Organic matter-metal interactions in recent sediments: the role of humic substances. Geochim Cosmochim Acta. https://doi.org/10.1016/0016-7037(76)90033-8
Oksanen J, Blanchet FG, Friendly M et al. (2020) Package “vegan” title community ecology package version 2.5–7. R Package Version 2.6–2
Orani AM, Barats A, Vassileva E, Thomas OP (2018) Marine sponges as a powerful tool for trace elements biomonitoring studies in coastal environment. Mar Pollut Bull. https://doi.org/10.1016/j.marpolbul.2018.04.073
Padovan A, Munksgaard N, Alvarez B et al (2012) Trace metal concentrations in the tropical sponge Spheciospongia vagabunda at a sewage outfall: synchrotron X-ray imaging reveals the micron-scale distribution of accumulated metals. Hydrobiologia. https://doi.org/10.1007/s10750-011-0916-9
Pan K, Lee OO, Qian PY, Wang WX (2011) Sponges and sediments as monitoring tools of metal contamination in the eastern coast of the Red Sea, Saudi Arabia. Mar Pollut Bull. https://doi.org/10.1016/j.marpolbul.2011.02.043
Pao Mendonca K, Angeletti B, Dufour A et al (2023) The sponge Oscarella lobularis (Porifera, Homoscleromorpha) as a suitable biomonitor of metallic contamination in Mediterranean coastal ecosystems. Mar Pollut Bull. https://doi.org/10.1016/j.marpolbul.2023.114665
Patel B, Balani MC, Patel S (1985) Sponge “sentinel” of heavy metals. Sci Total Environ. https://doi.org/10.1016/0048-9697(85)90184-6
Perez T, Vacelet J, Rebouillon P (2004) In situ comparative study of several Mediterranean sponges as potential biomonitors for heavy metals. Boll Mus Ist Biol Univ Genova, Genova
Pillon Y, Munzinger J, Amir H, Lebrun M (2010) Ultramafic soils and species sorting in the flora of New Caledonia. J Ecol. https://doi.org/10.1111/j.1365-2745.2010.01689.x
R Core Team (2019) R. studio Team. R Development Core Team
Rainbow PS (1995) Biomonitoring of heavy metal availability in the marine environment. Mar Pollut Bull. https://doi.org/10.1016/0025-326X(95)00116-5
Rainbow PS, Phillips DJH, Depledge MH (1990) The significance of trace metal concentrations in marine invertebrates. Mar Pollut Bull. https://doi.org/10.1016/0025-326x(90)90791-6
Ribes M, Yahel G, Romera-Castillo C et al (2023) The removal of dissolved organic matter by marine sponges is a function of its composition and concentration: an in situ seasonal study of four Mediterranean species. Sci Total Environ. https://doi.org/10.1016/j.scitotenv.2023.161991
Richir J, Gobert S (2014) A reassessment of the use of Posidonia oceanica and Mytilus galloprovincialis to biomonitor the coastal pollution of trace elements: new tools and tips. Mar Pollut Bull. https://doi.org/10.1016/j.marpolbul.2014.08.030
Richmond RH (1993) Coral reefs: present problems and future concerns resulting from anthropogenic disturbance. Integr Comp Biol. https://doi.org/10.1093/icb/33.6.524
Rosado Rodríguez G, Otero Morales E (2020) Assessment of heavy metal contamination at Tallaboa Bay (Puerto Rico) by marine sponges’ bioaccumulation and fungal community composition. Mar Pollut Bull. https://doi.org/10.1016/j.marpolbul.2020.111803
Roveta C, Annibaldi A, Afghan A et al (2021) Biomonitoring of heavy metals: the unexplored role of marine sessile taxa. Appl Sci (Switzerland). https://doi.org/10.3390/app11020580
Selvin J, Ninawe AS, Seghal Kiran G, Lipton AP (2010) Sponge-microbial interactions: ecological implications and bioprospecting avenues. Crit Rev Microbiol 36:82
Shariati S, Pourbabaee AA, Alikhani HA, Rezaei KA (2019) Investigation of heavy metal contamination in the surface sediments of anzali wetland in north of Iran. Pollution. https://doi.org/10.22059/poll.2018.257276.438
Thomas T, Moitinho-Silva L, Lurgi M et al (2016) Diversity, structure and convergent evolution of the global sponge microbiome. Nat Commun. https://doi.org/10.1038/ncomms11870
Turon M, Cáliz J, Triadó-Margarit X et al (2019) Sponges and their microbiomes show similar community metrics across impacted and well-preserved reefs. Front Microbiol. https://doi.org/10.3389/fmicb.2019.01961
Valavanidis A, Vlahogianni T, Dassenakis M, Scoullos M (2006) Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicol Environ Saf. https://doi.org/10.1016/j.ecoenv.2005.03.013
Webster NS, Thomas T (2016) The sponge hologenome. mBio. https://doi.org/10.1128/mBio.00135-16
Wells PG (1999) Biomonitoring the health of coastal marine ecosystems—the roles and challenges of microscale toxicity tests. Mar Pollut Bull 39:39
Wilkinson CR (1984) Immunological evidence for the Precambrian origin of bacterial symbioses in marine sponges. Proc R Soc London Biol Sci. https://doi.org/10.1098/rspb.1984.0017
Yang Y, Yang X, He M, Christakos G (2020) Beyond mere pollution source identification: determination of land covers emitting soil heavy metals by combining, PCA/APCS GeoDetector and GIS analysis. Catena. https://doi.org/10.1016/j.catena.2019.104297
Zhang C, Yu Z, gang, Zeng G ming, et al (2014) Effects of sediment geochemical properties on heavy metal bioavailability. Environ Int 73:270
Zhang S, Fu K, Gao S et al (2023) Bioaccumulation of heavy metals in the water, sediment, and organisms from the sea ranching areas of Haizhou Bay in China. Water. https://doi.org/10.3390/w15122218
Acknowledgements
We wish to thank the divin,g technical staff of the IRD (Institut de Recherche pour le Développement, Nouméa) for fieldwork assistance. Thanks to Dr. Riccardo Rodolfo-Metalpa for study support and Dr. Barbara Calcinai for helping identify sponges. Federica Maggioni thanks the “Ecole doctorale du Pacifique” for her PhD fellowship (project REEF-ENGINE) from the University of New Caledonia. We thank the “Plateforme du vivant (PFV)” (IRD, Nouméa) and the LAMA laboratory (IRD, Nouméa) for performing analyses and for the use of their instruments and facilities. We also thank the “Province Sud” for sample collection permits (no. 3413-2019).
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Conceptualization: FM, and CM; Formal Analysis, FM, and CM; Data Curation, FM, CM, and PLS; Writing—Original Draft Preparation, FM, CM; Writing—Review & Editing, FM, CM, PLS, PJ, YL; Funding Acquisition, CM, PJ, and YL.
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Maggioni, F., Stenger, PL., Letourneur, Y. et al. Metallic trace elements in marine sponges living in a semi-enclosed tropical lagoon. Biometals 37, 157–169 (2024). https://doi.org/10.1007/s10534-023-00536-3
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DOI: https://doi.org/10.1007/s10534-023-00536-3