Abstract
Recurrent blooms of the toxic dinoflagellate Ostreopsis cf. ovata are frequently reported in the Northwestern Mediterranean Sea. The impact of these proliferations on other microalgal species inhabiting the same habitats is of interest from an ecological prospective. In vitro experiments were carried out to investigate the influence of O. cf. ovata on the growth of the co-occurring benthic diatoms Licmophora paradoxa, Navicula arenaria and the benthic dinoflagellates Prorocentrum lima and Coolia monotis. Overall, O. cf. ovata exhibited weak allelopathic effects towards these microalgal species, with a reduction in the cell abundance for L. paradoxa and P. lima only. Interestingly, dead cells of L. paradoxa and N. arenaria were observed embedded in the thick mucus surrounding O. cf. ovata cells, suggesting that the mucous layer could act as a toxic phycosphere, especially for non-motile cells. All competitors were further exposed for 24 h to ovatoxins, the major toxins produced by O. cf. ovata, and the maximum quantum yield efficiency of L. paradoxa, N. arenaria and P. lima was affected at a minimum concentration of 10 µg mL−1. We then hypothesized that the diffusion of solubilized ovatoxins in the culture medium affects only moderately the competitors’ growth, whereas their accumulation in the mucus would yield deleterious effects. More precisely, the competitors’ sensitivity to ovatoxins was enhanced in their stationary phase of growth and resulted from a rapid inhibition of an uncharacterized photosynthetic step downstream photosystem II. Altogether, these results emphasize the predominant role of the O. cf. ovata’s mucus in driving ecological interactions and suggest that it can affect the growth of several benthic microalgae by accumulating the potent ovatoxins.
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References
Accoroni S, Romagnoli T, Pichierri S, Totti C (2016) Effects of the bloom of harmful benthic dinoflagellate Ostreopsis Cf. ovata on the microphytobenthos community in the northern adriatic sea. Harmful Algae 55:179–190. https://doi.org/10.1016/j.hal.2016.03.003
Bailleul B, Cardol P, Breyton C, Finazzi G (2010) Electrochromism: a useful probe to study algal photosynthesis. Photosynth Res 106(1–2):179–189. https://doi.org/10.1007/s11120-010-9579-z
Bendschneider K, Robinson RJ (1952) A new spectrophotometric method for the determination of nitrite in sea water, Technical report 8, Oceanographic laboratories: University of Washington
Bigalke A, Pohnert G (2019) Algicidal bacteria trigger contrasting responses in model diatom communities of different composition. MicrobiologyOpen 8(8):e00818. https://doi.org/10.1002/mbo3.818
Bondoc KGV, Lembke C, Lang SN, Germerodt S, Schuster S, Vyverman W, Pohnert G (2019) Decision-making of the benthic diatom seminavis robusta searching for inorganic nutrients and pheromones. ISME J 13(2):537–546. https://doi.org/10.1038/s41396-018-0299-2
Botana LM (2014) Seafood and freshwater toxins: pharmacology, physiology and detection, 3rd edn. CRC Press
Brissard C, Herrenknecht C, Sechet V, Herve F, Pisapia F, Harcouet J, Lemee R, Chomerat N, Hess P, Amzil Z (2014) Complex toxin profile of French Mediterranean Ostreopsis Cf. ovata strains, seafood accumulation and ovatoxins prepurification. Mar Drugs 12(5):2851–2876. https://doi.org/10.3390/md12052851
Brissard C, Herve F, Sibat M, Sechet V, Hess P, Amzil Z, Herrenknecht C (2015) Characterization of ovatoxin-h, a new ovatoxin analog, and evaluation of chromatographic columns for ovatoxin analysis and purification. J Chromatogr A 1388:87–101. https://doi.org/10.1016/j.chroma.2015.02.015
Brown ER, Cepeda MR, Mascuch SJ, Poulson-Ellestad KL, Kubanek J (2019) Chemical ecology of the marine plankton. Nat Prod Rep 36(8):1093–1116. https://doi.org/10.1039/C8NP00085A
Ciminiello P, Dell’Aversano C, Fattorusso E, Forino M, Tartaglione L, Grillo C, Melchiorre N (2008) Putative palytoxin and its new analogue, ovatoxin-a, in Ostreopsis ovata collected along the ligurian coasts during the 2006 toxic outbreak. J Am Soc Mass Spectrom 19(1):111–120. https://doi.org/10.1016/j.jasms.2007.11.001
Consalvey M, Paterson DM, Underwood GJC (2004) The ups and downs of life in a benthic biofilm: migration of benthic diatoms. Diatom Res 19(2):181–202. https://doi.org/10.1080/0269249X.2004.9705870
Faimali M, Giussani V, Piazza V, Garaventa F, Corrà C, Asnaghi V, Privitera D, Gallus L, Cattaneo-Vietti R, Mangialajo L, Chiantore M (2012) Toxic effects of harmful benthic dinoflagellate Ostreopsis Ovata on invertebrate and vertebrate marine organisms. Mar Environ Res 76:97–107. https://doi.org/10.1016/j.marenvres.2011.09.010
Fernández-Herrera LJ, Band-Schmidt CJ, López-Cortés DJ, Hernández-Guerrero CJ, Bustillos-Guzmán JJ, Núñez-Vázquez E (2016) Allelopathic effect of chattonella marina var. marina (raphidophyceae) on gymnodinium catenatum (dinophycea). Harmful Algae 51:1–9. https://doi.org/10.1016/j.hal.2015.10.009
Gallo C, d’Ippolito G, Nuzzo G, Sardo A, Fontana A (2017) Autoinhibitory sterol sulfates mediate programmed cell death in a bloom-forming marine diatom. Nat Commun 8(1):1292. https://doi.org/10.1038/s41467-017-01300-1
García-Portela M, Riobó P, Franco JM, Bañuelos RM, Rodríguez F (2016) Genetic and toxinological characterization of north atlantic strains of the dinoflagellate ostreopsis and allelopathic interactions with toxic and non-toxic species from the genera prorocentrum. Coolia and Gambierdiscus Harmful Algae 60:57–69. https://doi.org/10.1016/j.hal.2016.10.007
Gémin M, Réveillon D, Hervé F, Pavaux A, Tharaud M, Séchet V, Bertrand S, Lemée R, Amzil Z (2020) Toxin content of Ostreopsis Cf. ovata depends on bloom phases, depth and macroalgal substrate in the NW Mediterranean sea. Harmful Algae 92:101727. https://doi.org/10.1016/j.hal.2019.101727
Gillard J, Frenkel J, Devos V, Sabbe K, Paul C, Rempt M, Inzé D, Pohnert G, Vuylsteke M, Vyverman W (2013) Metabolomics enables the structure elucidation of a diatom sex pheromone. Angew Chem Int Ed 52(3):854–857. https://doi.org/10.1002/anie.201208175
Giussani V, Sbrana F, Asnaghi V, Vassalli M, Faimali M, Casabianca S, Penna A, Ciminiello P, Dell’Aversano C, Tartaglione L, Mazzeo A, Chiantore M (2015) Active role of the mucilage in the toxicity mechanism of the harmful benthic dinoflagellate Ostreopsis Cf. ovata. Harmful Algae 44:46–53. https://doi.org/10.1016/j.hal.2015.02.006
Granéli E, Hansen PJ (2006) Allelopathy in harmful algae: A mechanism to compete for resources? In: Granéli E, Turner JT (eds) Ecology of harmful algae. Springer, Berlin, pp 189–201. https://doi.org/10.1007/978-3-540-32210-8_15
Grover JP, Wang F-B (2013) Competition for one nutrient with internal storage and toxin mortality. Math Biosci 244(2):82–90. https://doi.org/10.1016/j.mbs.2013.04.009
Guidi F, Pezzolesi L, Vanucci S (2018) Microbial dynamics during harmful dinoflagellate Ostreopsis Cf. ovata growth: bacterial succession and viral abundance pattern. MicrobiologyOpen 7(4):e00584. https://doi.org/10.1002/mbo3.584
Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms; I cyclotella nana hustedt, and detonula confervacea (cleve) gran. Can J Microbiol 8(2):229–239. https://doi.org/10.1139/m62-029
Hakanen P, Suikkanen S, Kremp A (2014) Allelopathic activity of the toxic dinoflagellate alexandrium ostenfeldii: intra-population variability and response of co-occurring dinoflagellates. Harmful Algae 39:287–294. https://doi.org/10.1016/j.hal.2014.08.005
Hattenrath-Lehmann TK, Gobler CJ (2017) Identification of unique microbiomes associated with harmful algal blooms caused by alexandrium fundyense and dinophysis acuminata. Harmful Algae 68:17–30. https://doi.org/10.1016/j.hal.2017.07.003
Holman JD, Tabb DL, Mallick P (2014) Employing proteowizard to convert raw mass spectrometry data. Curr Protoc Bioinforma 46(1):13.24.1-13.24.9. https://doi.org/10.1002/0471250953.bi1324s46
Ianora A, Miralto A, Poulet SA, Carotenuto Y, Buttino I, Romano G, Casotti R, Pohnert G, Wichard T, Colucci-D’Amato L, Terrazzano G, Smetacek V (2004) Aldehyde suppression of copepod recruitment in blooms of a ubiquitous planktonic diatom. Nature 429(6990):403–407. https://doi.org/10.1038/nature02526
Jauzein C, Couet D, Blasco T, Lemée R (2017) Uptake of dissolved inorganic and organic nitrogen by the benthic toxic dinoflagellate Ostreopsis Cf. ovata. Harmful Algae 65:9–18. https://doi.org/10.1016/j.hal.2017.04.005
Jonsson PR, Pavia H, Toth G (2009) Formation of harmful algal blooms cannot be explained by allelopathic interactions. Proc Natl Acad Sci 106(27):11177–11182
Kubanek J, Hicks MK, Naar J, Villareal TA (2005) Does the red tide dinoflagellate karenia brevis use allelopathy to outcompete other phytoplankton? Limnol Oceanogr 50(3):883–895. https://doi.org/10.4319/lo.2005.50.3.0883
Kubanek J, Snell TW, Pirkle C (2007) Chemical Defense of the red tide dinoflagellate karenia brevis against rotifer grazing. Limnol Oceanogr 52(3):1026–1035. https://doi.org/10.4319/lo.2007.52.3.1026
Lim AS, Jeong HJ, Jang TY, Jang SH, Franks PJS (2014) Inhibition of growth rate and swimming speed of the harmful dinoflagellate Cochlodinium polykrikoides by diatoms: implications for red tide formation. Harmful Algae 37:53–61. https://doi.org/10.1016/j.hal.2014.05.003
Long M, Tallec K, Soudant P, Le Grand F, Donval A, Lambert C, Sarthou G, Jolley DF, Hégaret H (2018a) Allelochemicals from alexandrium minutum induce rapid inhibition of metabolism and modify the membranes from chaetoceros muelleri. Algal Res 35:508–518. https://doi.org/10.1016/j.algal.2018.09.023
Long M, Tallec K, Soudant P, Lambert C, Le Grand F, Sarthou G, Jolley D, Hégaret H (2018b) A rapid quantitative fluorescence-based bioassay to study allelochemical interactions from alexandrium minutum. Environ Pollut 242:1598–1605. https://doi.org/10.1016/j.envpol.2018.07.119
Long M, Peltekis A, González-Fernández C, Hégaret H, Bailleul B (2021) Allelochemicals of alexandrium minutum: kinetics of membrane disruption and photosynthesis inhibition in a co-occurring diatom. Harmful Algae 103:101997. https://doi.org/10.1016/j.hal.2021.101997
Lyczkowski ER, Karp-Boss L (2014) Allelopathic effects of alexandrium fundyense (dinophyceae) on thalassiosira cf gravida (bacillariophyceae): a matter of size. J Phycol 50(2):376–387. https://doi.org/10.1111/jpy.12172
Ma H, Krock B, Tillmann U, Muck A, Wielsch N, Svatoš A, Cembella A (2011) Isolation of activity and partial characterization of large non-proteinaceous lytic allelochemicals produced by the marine dinoflagellate alexandrium tamarense. Harmful Algae 11:65–72. https://doi.org/10.1016/j.hal.2011.07.004
Mangialajo L, Ganzin N, Accoroni S, Asnaghi V, Blanfune A, Cabrini M, Cattaneo-Vietti R, Chavanon F, Chiantore M, Cohu S, Costa E, Fornasaro D, Grossel H, Marco-Miralles F, Maso M, Rene A, Rossi AM, Sala MM, Thibaut T, Totti C, Vila M, Lemee R (2011) Trends in ostreopsis proliferation along the northern mediterranean coasts. Toxicon off J Int Soc Toxinology 57(3):408–420. https://doi.org/10.1016/j.toxicon.2010.11.019
Marro S, Pavaux A-S, Drouet K, Lemée R (2019) Diversity of benthic microphytoplankton associated to Ostreopsis Cf. ovata bloom in the NW Mediterranean sea. In: Poster at French national conference on HAB, PHYCOTOX Group, Brest, pp 1
Meyer N, Pohnert G (2019) Isolate-specific resistance to the algicidal bacterium kordia algicida in the diatom chaetoceros genus. Bot Mar. https://doi.org/10.1515/bot-2019-0007
Monti M, Cecchin E (2012) Comparative growth of three strains of ostreopsis ovata at different light intensities with focus on inter-specific allelopathic interactions. Cryptogam Algol 33(2):113–119. https://doi.org/10.7872/crya.v33.iss2.2011.113
Ninčević Gladan Ž, Arapov J, Casabianca S, Penna A, Honsell G, Brovedani V, Pelin M, Tartaglione L, Sosa S, Dell’Aversano C, Tubaro A, Žuljević A, Grbec B, Čavar M, Bužančić M, Bakrač A, Skejić S (2019) Massive occurrence of the harmful benthic dinoflagellate Ostreopsis Cf. ovata in the eastern adriatic sea. Toxins 11(5):300
Pavaux A-S, Rostan J, Guidi-Guilvard L, Marro S, Ternon E, Thomas OP, Lemée R, Gasparini S (2019) Effects of the toxic dinoflagellate Ostreopsis Cf. Ovata on survival, feeding and reproduction of a phytal harpacticoid copepod. J Exp Mar Biol Ecol 516:103–113. https://doi.org/10.1016/j.jembe.2019.05.004
Pavaux A-S, Ternon E, Dufour L, Marro S, Gémin M-P, Thomas OP, Lemée R (2020) Efficient, fast and inexpensive bioassay to monitor benthic microalgae toxicity: application to Ostreopsis species. Aquat Toxicol 223:105485. https://doi.org/10.1016/j.aquatox.2020.105485
Place AR, Bowers HA, Bachvaroff TR, Adolf JE, Deeds JR, Sheng J (2012) Karlodinium veneficum—the little dinoflagellate with a big bite. Harmful Algae-Requir Species-Specif Inf 14:179–195. https://doi.org/10.1016/j.hal.2011.10.021
Pohnert G (2005) Diatom/copepod interactions in plankton: the indirect chemical defense of unicellular algae. ChemBioChem 6(6):946–959. https://doi.org/10.1002/cbic.200400348
Poulin RX, Hogan S, Poulson-Ellestad KL, Brown E, Fernández FM, Kubanek J (2018) Karenia brevis allelopathy compromises the lipidome, membrane integrity and photosynthesis of competitors. Sci Rep 8(1):9572. https://doi.org/10.1038/s41598-018-27845-9
Poulson-Ellestad K, McMillan E, Montoya JP, Kubanek J (2014) Are offshore phytoplankton susceptible to karenia brevis allelopathy? J Plankton Res 36(5):1344–1356. https://doi.org/10.1093/plankt/fbu064
Poulson-Ellestad KL, Jones CM, Roy J, Viant MR, Fernandez FM, Kubanek J, Nunn BL (2014) Metabolomics and proteomics reveal impacts of chemically mediated competition on marine phytoplankton. PNAS 111(24):9009–9014. https://doi.org/10.1073/pnas.1413432111
Prince EK, Myers TL, Kubanek J (2008) Effects of harmful algal blooms on competitors: allelopathic mechanisms of the red tide dinoflagellate karenia brevis. Limnol Oceanogr 53(2):531–541. https://doi.org/10.4319/lo.2008.53.2.0531
Prince EK, Poulson KL, Myers TL, Sieg RD, Kubanek J (2010) Characterization of allelopathic compounds from the red tide dinoflagellate karenia brevis. Harmful Algae 10(1):39–48. https://doi.org/10.1016/j.hal.2010.06.003
Sala-Pérez M, Alpermann TJ, Krock B, Tillmann U (2016) Growth and bioactive secondary metabolites of arctic protoceratium reticulatum (dinophyceae). Harmful Algae 55:85–96. https://doi.org/10.1016/j.hal.2016.02.004
Schwartz ER, Poulin RX, Mojib N, Kubanek J (2016) Chemical ecology of marine plankton. Nat Prod Rep 33(7):843–860. https://doi.org/10.1039/C6NP00015K
Selander E, Kubanek J, Hamberg M, Andersson MX, Cervin G, Pavia H (2015) Predator lipids induce paralytic shellfish toxins in bloom-forming algae. Proc Natl Acad Sci 112(20):6395–6400. https://doi.org/10.1073/pnas.1420154112
Shimizu Y (1993) Dinoflagellates as Sources of Bioactive Molecules. In: Zaborsky OR (ed) Pharmaceutical and bioactive natural products; attaway DH. Springer, Boston, pp 391–410. https://doi.org/10.1007/978-1-4899-2391-2_10
Simon N, Cras AL, Foulon E, Lemée R (2009) Diversity and evolution of marine phytoplankton. Numéro Spéc Evol 332(2–3):159–170
Simonini R, Orlandi M, Abbate M (2011) Is the toxic dinoflagellate Ostreopsis Cf. Ovata harmful to Mediterranean benthic invertebrates? evidences from ecotoxicological tests with the polychaete dinophilus gyrociliatus. Mar Environ Res 72(4):230–233. https://doi.org/10.1016/j.marenvres.2011.08.009
Smith EA, Mackintosh FH, Grant F, Gallacher S (2002) Sodium channel blocking (SCB) Activity and transformation of paralytic shellfish toxins (PST) by dinoflagellate-associated bacteria. Aquat Microb Ecol 29(1):1–9
Ternon E, Pavaux A-S, Marro S, Thomas OP, Lemée R (2018) Allelopathic interactions between the benthic toxic dinoflagellate Ostreopsis Cf. Ovata and a co-occurring diatom. Harmful Algae 75:35–44
Tichadou L, Glaizal M, Armengaud A, Grossel H, Lemée R, Kantin R, Lasalle J-L, Drouet G, Rambaud L, Malfait P, de Haro L (2010) Health impact of unicellular algae of the Ostreopsis genus blooms in the Mediterranean sea: experience of the French Mediterranean coast surveillance network from 2006 to 2009. Clin Toxicol 48(8):839–844. https://doi.org/10.3109/15563650.2010.513687
Tillmann U, Hansen P (2009) Allelopathic effects of alexandrium tamarense on other algae: evidence from mixed growth experiments. Aquat Microb Ecol 57:101–112
Tillmann U, John U, Cembella A (2007) On the allelochemical potency of the marine dinoflagellate alexandrium ostenfeldii against heterotrophic and autotrophic protists. J Plankton Res 29(6):527–543. https://doi.org/10.1093/plankt/fbm034
Tillmann U, John U (2002) toxic effects of alexandrium spp. on heterotrophic dinoflagellates: an allelochemical defence mechanism independent of psp-toxin content. Mar Ecol Prog Ser 47(58)
Tilney CL, Pokrzywinski KL, Coyne KJ, Warner ME (2014) Growth, death, and photobiology of dinoflagellates (dinophyceae) under bacterial-algicide control. J Appl Phycol 26(5):2117–2127. https://doi.org/10.1007/s10811-014-0248-z
Vila M, Garcés E, Maso M (2001) potentially toxic epiphytic dinoflagellate assemblages on macroalgae in the NW Mediterranean. Aquat Microb Ecol 26:51–60
Vila M, Abós-Herràndiz R, Isern-Fontanet J, Àlvarez J, Berdalet E (2016) Establishing the link between Ostreopsis cf. ovata blooms and human health impacts using ecology and epidemiology. Sci Mar 80(S1):107–115. https://doi.org/10.3989/scimar.04395.08A
Wang M, Carver JJ, Phelan VV, Sanchez LM, Garg N, Peng Y, Nguyen DD, Watrous J, Kapono CA, Luzzatto-Knaan T, Porto C, Bouslimani A, Melnik AV, Meehan MJ, Liu W-T, Crüsemann M, Boudreau PD, Esquenazi E, Sandoval-Calderón M, Kersten RD, Pace LA, Quinn RA, Duncan KR, Hsu C-C, Floros DJ, Gavilan RG, Kleigrewe K, Northen T, Dutton RJ, Parrot D, Carlson EE, Aigle B, Michelsen CF, Jelsbak L, Sohlenkamp C, Pevzner P, Edlund A, McLean J, Piel J, Murphy BT, Gerwick L, Liaw C-C, Yang Y-L, Humpf H-U, Maansson M, Keyzers RA, Sims AC, Johnson AR, Sidebottom AM, Sedio BE, Klitgaard A, Larson CB, Boya CA, Torres-Mendoza D, Gonzalez DJ, Silva DB, Marques LM, Demarque DP, Pociute E, O’Neill EC, Briand E, Helfrich EJN, Granatosky EA, Glukhov E, Ryffel F, Houson H, Mohimani H, Kharbush JJ, Zeng Y, Vorholt JA, Kurita KL, Charusanti P, McPhail KL, Nielsen KF, Vuong L, Elfeki M, Traxler MF, Engene N, Koyama N, Vining OB, Baric R, Silva RR, Mascuch SJ, Tomasi S, Jenkins S, Macherla V, Hoffman T, Agarwal V, Williams PG, Dai J, Neupane R, Gurr J, Rodríguez AMC, Lamsa A, Zhang C, Dorrestein K, Duggan BM, Almaliti J, Allard P-M, Phapale P, Nothias L-F, Alexandrov T, Litaudon M, Wolfender J-L, Kyle JE, Metz TO, Peryea T, Nguyen D-T, VanLeer D, Shinn P, Jadhav A, Müller R, Waters KM, Shi W, Liu X, Zhang L, Knight R, Jensen PR, Palsson BØ, Pogliano K, Linington RG, Gutiérrez M, Lopes NP, Gerwick WH, Moore BS, Dorrestein PC, Bandeira N (2016) Sharing and community curation of mass spectrometry data with global natural products social molecular networking. Nat Biotechnol 34(8):828–837. https://doi.org/10.1038/nbt.3597
Wang R, Wang J, Xue Q, Sha X, Tan L, Guo X (2017a) Allelopathic Interactions between skeletonema costatum and alexandrium minutum. Chem Ecol 33(6):485–498. https://doi.org/10.1080/02757540.2017.1332187
Wang R, Xue Q, Wang J, Tan L, Zhang Q, Zhao Y, Anderson DM (2017b) Effects of an allelochemical in phaeodactylum tricornutum filtrate on heterosigma akashiwo: morphological physiological and growth effects. Chemosphere 186:527–534. https://doi.org/10.1016/j.chemosphere.2017.08.024
Xia J, Wishart DS (2016) Using metaboanalyst 3.0 for comprehensive metabolomics data analysis. Curr Protoc Bioinforma 55(1):14.10.1-14.10.91. https://doi.org/10.1002/cpbi.11
Xu N, Tang Y, Qin J, Duan S, Gobler C (2015) Ability of the marine diatoms pseudo-nitzschia multiseries and P. pungens to inhibit the growth of co-occurring phytoplankton via allelopathy. Aquat Microb Ecol 74:29–41
Xu W, Wang J, Tan L, Guo X, Xue Q (2019) Variation in allelopathy of extracellular compounds produced by cylindrotheca closterium against the harmful-algal-bloom dinoflagellate prorocentrum donghaiense. Mar Environ Res 148:19–25. https://doi.org/10.1016/j.marenvres.2019.05.005
Acknowledgements
This work benefited from the support of the project OCEAN-15 (ANR-15-CE35-0002-01) of the French National Research Agency (ANR) and the European MSCA project CHEMICROS (#841051). The authors are grateful to Julien Lopez and Lola Miro-Solé for their help with maintaining the co-cultures and cell counting. The authors declare no conflict of interest.
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Ternon, E., Pavaux, AS., Peltekis, A. et al. Assessment of the allelochemical activity of Ostreopsis cf. ovata and the ovatoxins towards competitive benthic microalgae. Aquat Ecol 56, 475–491 (2022). https://doi.org/10.1007/s10452-022-09953-x
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DOI: https://doi.org/10.1007/s10452-022-09953-x