Marine Biology

, 166:9 | Cite as

Re-shaping marine plankton communities: effects of diatom oxylipins on copepods and beyond

  • Ennio Russo
  • Adrianna Ianora
  • Ylenia CarotenutoEmail author
Review, concept, and synthesis


Diatoms, ubiquitous primary producers in marine systems, synthesize oxylipins, which impair copepod fitness through a maternal effect. While oxylipins do not directly affect the adults, these chemicals alter basic cellular and developmental processes of copepod embryos, thereby negatively affecting egg hatching and naupliar survival. Inspecting the effects of oxylipins on copepod reproductive success is extremely challenging, because wide variations in their synthesis potentials among diatom genera, species, populations and strains have been detected. In parallel, distinct copepod species and populations can be differently sensitive to oxylipin-producing diatoms. Lately, application of chemical and molecular methods allowed to finely characterize the oxylipin profiles of single diatom strains and to highlight detoxification responses of copepods through the relative expression of selected genes of interest. Thus far, integrative experimental approaches encompassing physiological, chemical and molecular data were mostly applied to laboratory setups, whereas few in situ experiments were presented in this perspective. Moreover, only a restricted number of papers tested the effects of oxylipins on the plankton community as a whole. This review synthesizes latest advances in conceptual and methodological approaches in diatom–copepod interactions and aims at discussing possible re-shaping of the plankton community in response to oxylipin-producing diatom occurrence.



Ennio Russo was supported by a Ph. D. fellowship funded by Stazione Zoologica Anton Dohrn. We thank Jefferson Turner for reviewing the early version of the manuscript and Gayantonia Franzè for constructive review comments. We thank Flora Palumbo for graphical support.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.


  1. Adolph S, Bach S, Blondel M et al (2004) Cytotoxicity of diatom-derived oxylipins in organisms belonging to different phyla. J Exp Biol 207:2935–2946. CrossRefPubMedGoogle Scholar
  2. Amato A, Carotenuto Y (2018) Planktonic calanoids embark into the “Omics Era”. In: Uttieri M (ed) Trends in copepod studies: distribution, biology and ecology. Nova Science Publisher, Hauppauge, pp 287–314Google Scholar
  3. Armbrust EV (2009) The life of diatoms in the world’s oceans. Nature 459:185–192. CrossRefPubMedGoogle Scholar
  4. Armengol L, Franchy G, Ojeda A, Santana-del Pino Á, Hernández-León S (2017) Effects of copepods on natural microplankton communities: do they exert top–down control? Mar Biol. CrossRefGoogle Scholar
  5. Asai S, Ianora A, Lauritano C, Lindeque PK, Carotenuto Y (2015) High-quality RNA extraction from copepods for next generation sequencing: a comparative study. Mar Genomics 24:115–118. CrossRefPubMedGoogle Scholar
  6. Ask J, Reinikainen M, Båmstedt U (2006) Variation in hatching success and egg production of Eurytemora affinis (Calanoida, Copepoda) from the Gulf of Bothnia, Baltic Sea, in relation to abundance and clonal differences of diatoms. J Plankton Res 28:683–694CrossRefGoogle Scholar
  7. Barreiro A, Carotenuto Y, Lamari N et al (2011) Diatom induction of reproductive failure in copepods: the effect of PUAs versus non volatile oxylipins. J Exp Mar Biol Ecol 401:13–19. CrossRefGoogle Scholar
  8. Benedetti F, Gasparini S, Ayata S-D (2016) Identifying copepod functional groups from species functional traits. J Plankton Res 38:159–166. CrossRefPubMedGoogle Scholar
  9. Boxshall GA, Defaye D (2007) Global diversity of copepods (Crustacea: Copepoda) in freshwater. Hydrobiologia 595:195–207CrossRefGoogle Scholar
  10. Bron JE, Frisch D, Goetze E, Johnson SC, Lee CE, Wyngaard GA (2011) Observing copepods through a genomic lens. Front Zool 8:22. CrossRefPubMedPubMedCentralGoogle Scholar
  11. Brugnano C, Granata A, Guglielmo L, Minutoli R, Zagami G, Ianora A (2016) The deleterious effect of diatoms on the biomass and growth of early stages of their copepod grazers. J Exp Mar Biol Ecol 476:41–49CrossRefGoogle Scholar
  12. Buttino I, De Rosa G, Carotenuto Y et al (2008) Aldehyde-encapsulating liposomes impair marine grazer survivorship. J Exp Biol 211:1426–1433. CrossRefPubMedGoogle Scholar
  13. Calbet A (2008) The trophic roles of microzooplankton in marine systems. ICES J Mar Sci 65:325–331. CrossRefGoogle Scholar
  14. Calbet A, Saiz E (2005) The ciliate-copepod link in marine ecosystems. Aquat Microb Ecol 38:157–167CrossRefGoogle Scholar
  15. Caldwell GS (2009) The influence of bioactive oxylipins from marine diatoms on invertebrate reproduction and development. Mar Drugs 7:367–400CrossRefGoogle Scholar
  16. Carotenuto Y, Ianora A, Buttino I, Romano G, Miralto A (2002) Is postembryonic development in the copepod Temora stylifera negatively affected by diatom diets? J Exp Mar Biol Ecol 276:49–66CrossRefGoogle Scholar
  17. Carotenuto Y, Ianora A, Miralto A (2011) Maternal and neonate diatom diets impair development and sex differentiation in the copepod Temora stylifera. J Exp Mar Biol Ecol 396:99–107. CrossRefGoogle Scholar
  18. Carotenuto Y, Esposito F, Pisano F, Lauritano C, Perna M, Miralto A, Ianora A (2012) Multi-generation cultivation of the copepod Calanus helgolandicus in a re-circulating system. J Exp Mar Biol Ecol 418–419:46–58. CrossRefGoogle Scholar
  19. Carotenuto Y, Dattolo E, Lauritano C et al (2014) Insights into the transcriptome of the marine copepod Calanus helgolandicus feeding on the oxylipin-producing diatom Skeletonema marinoi. Harmful Algae 31:153–162. CrossRefPubMedGoogle Scholar
  20. Cózar A, Morillo-García S, Ortega MJ, Li QP, Bartual A (2018) Macroecological patterns of the phytoplankton production of polyunsaturated aldehydes. Sci Rep 8:12282. CrossRefPubMedPubMedCentralGoogle Scholar
  21. Cutignano A, Lamari N, d’ippolito G, Manzo E, Cimino G, Fontana A (2011) Lipoxygenase products in marine diatoms: a concise analytical method to explore the functional potential of oxylipins. J Phycol 47:233–243. CrossRefPubMedGoogle Scholar
  22. d’Ippolito G, Romano G, Iadicicco O, Miralto A, Ianora A, Cimino G, Fontana A (2002) New birth-control aldehydes from the marine diatom Skeletonema costatum: characterization and biogenesis. Tetrahedron Lett 43:6133–6136. CrossRefGoogle Scholar
  23. d’Ippolito G, Tucci S, Cutignano A, Romano G, Cimino G, Miralto A, Fontana A (2004) The role of complex lipids in the synthesis of bioactive aldehydes of the marine diatom Skeletonema costatum. Biochim Biophys Acta 1686:100–107. CrossRefPubMedGoogle Scholar
  24. d’Ippolito G, Cutignano A, Briante R, Febbraio F, Cimino G, Fontana A (2005) New C16 fatty-acid-based oxylipin pathway in the marine diatom Thalassiosira rotula. Org Biomol Chem 3:4065–4070. CrossRefPubMedGoogle Scholar
  25. d’Ippolito G, Lamari N, Montresor M, Romano G, Cutignano A, Gerecht A et al (2009) 15S-lipoxygenase metabolism in the marine diatom Pseudo-nitzschia delicatissima. New Phytol 183:1064–1071CrossRefGoogle Scholar
  26. d’Ippolito G, Nuzzo G, Sardo A, Manzo E, Gallo C, Fontana A (2018) Chapter four—lipoxygenases and lipoxygenase products in marine diatoms. In: Moore BS (ed) Methods in enzymology, vol 605. Academic Press, New York, pp 69–100. CrossRefGoogle Scholar
  27. Elser JJ, Urabe J (1999) The stoichiometry of consumer-driven nutrient recycling: Theory, observations, and consequences. Ecology 80:735–751CrossRefGoogle Scholar
  28. Flynn KJ, Irigoien X (2009) Aldehyde-induced insidious effects cannot be considered as a diatom defence mechanism against copepods. Mar Ecol Prog Ser 377:79–89CrossRefGoogle Scholar
  29. Fontana A, d’Ippolito G, Cutignano A, Miralto A, Ianora A, Romano G et al (2007a) Chemistry of oxylipin pathways in marine diatoms. Pure Appl Chem 79(4):481–490CrossRefGoogle Scholar
  30. Fontana A, d’Ippolito G, Cutignano A et al (2007b) LOX-induced lipid peroxidation mechanism responsible for the detrimental effect of marine diatoms on zooplankton grazers. ChemBioChem 8:1810–1818. CrossRefPubMedGoogle Scholar
  31. Franzè G, Pierson JJ, Stoecker DK, Lavrentyev PJ (2017) Diatom-produced allelochemicals trigger trophic cascades in the planktonic food web. Limnol Oceanogr 63:1093–1108. CrossRefGoogle Scholar
  32. Gerecht A, Romano G, Ianora A, d’Ippolito G, Cutignano A, Fontana A (2011) Plasticity of oxylipin metabolism among clones of the marine diatom Skeletonema marinoi (Bacillariophyceae). J Phycol 47:1050–1056. CrossRefPubMedGoogle Scholar
  33. Gerecht A, Carotenuto Y, Ianora A et al (2013) Oxylipin production during a mesocosm bloom of Skeletonema marinoi. J Exp Mar Biol Ecol 446:159–165. CrossRefGoogle Scholar
  34. Glud RN, Grossart H-P, Larsen M, Tang KW, Arendt KE, Rysgaard S et al (2015) Copepod carcasses as microbial hot spots for pelagic denitrification. Limnol Oceanogr 60:2026–2036CrossRefGoogle Scholar
  35. Granéli E, Turner JT (2002) Top-down regulation in ctenophore-copepod-ciliate-diatom-phytoflagenate communities in coastal waters: a mesocosm study. Mar Ecol Progr Ser 239:57–68CrossRefGoogle Scholar
  36. Halsband-Lenk C (2005) Metridia pacifica in Dabob Bay, Washington: The diatom effect and the discrepancy between high abundance and low egg production rates. Progr Oceanogr 67:422–441. CrossRefGoogle Scholar
  37. Halsband-Lenk C, Pierson JJ, Leising AW (2005) Reproduction of Pseudocalanus newmani (Copepoda: Calanoida) is deleteriously affected by diatom blooms—a field study. Progr Oceanogr 67:332–348. CrossRefGoogle Scholar
  38. Ianora A, Miralto A (2010) Toxigenic effects of diatoms on grazers, phytoplankton and other microbes: a review. Ecotoxicol 19:493–511. CrossRefGoogle Scholar
  39. Ianora A, Miralto A, Poulet SA et al (2004) Aldehyde suppression of copepod recruitment in blooms of a ubiquitous planktonic diatom. Nature 429:403–407. CrossRefPubMedGoogle Scholar
  40. Ianora A, Casotti R, Bastianini M et al (2008) Low reproductive success for copepods during a bloom of the non-aldehyde-producing diatom Cerataulina pelagica in the North Adriatic Sea. Mar Ecol 29:399–410. CrossRefGoogle Scholar
  41. Ianora A, Romano G, Carotenuto Y, Esposito F, Roncalli V, Buttino I et al (2011a) Impact of the diatom oxylipin 15S-HEPE on the reproductive success of the copepod Temora stylifera. Hydrobiologia 666:265–275CrossRefGoogle Scholar
  42. Ianora A, Bentley MG, Caldwell GS et al (2011b) The relevance of marine chemical ecology to plankton and ecosystem function: an emerging field. Mar Drugs 9:1625–1648. CrossRefPubMedPubMedCentralGoogle Scholar
  43. Ianora A, Miralto A, Romano G (2012) Antipredatory defensive role of planktonic marine natural products. In: Fattorusso E, Gerwick WH, Taglialatela-Scafati O (eds) Handbook of marine natural products. Springer, Dordrecht, pp 711–748CrossRefGoogle Scholar
  44. Ianora A, Bastianini M, Carotenuto Y et al (2015) Non-volatile oxylipins can render some diatom blooms more toxic for copepod reproduction. Harmful Algae 44:1–7. CrossRefGoogle Scholar
  45. Irigoien X (2005) Phytoplankton blooms: a ‘loophole’ in microzooplankton grazing impact? J Plankton Res 27:313–321CrossRefGoogle Scholar
  46. Katechakis A, Stibor H, Sommer U, Hansen T (2002) Changes in the phytoplankton community and microbial food web of Blanes Bay (Catalan Sea, NW Mediterranean) under prolonged grazing pressure by doliolids (Tunicata), cladocerans or copepods (Crustacea). Mar Ecol Progr Ser 234:55–69. CrossRefGoogle Scholar
  47. Kiørboe T (2011) How zooplankton feed: mechanisms, traits and trade-offs. Biol Rev 86:311–339CrossRefGoogle Scholar
  48. Koski M (2007) High reproduction of Calanus finmarchicus during a diatom-dominated spring bloom. Mar Biol 151:1785–1798CrossRefGoogle Scholar
  49. Kuhlisch C, Deicke M, Ueberschaar N, Wichard T, Pohnert G (2017) A fast and direct liquid chromatography-mass spectrometry method to detect and quantify polyunsaturated aldehydes and polar oxylipins in diatoms. Limnol Oceanogr Meth 15:70–79. CrossRefGoogle Scholar
  50. Lamari N, Ruggiero MV, d’Ippolito G, Kooistra WH, Fontana A, Montresor M (2013) Specificity of lipoxygenase pathways supports species delineation in the marine diatom genus Pseudo-nitzschia. PLoS One 8:e73281. CrossRefPubMedPubMedCentralGoogle Scholar
  51. Lauritano C, Borra M, Carotenuto Y, Biffali E, Miralto A, Procaccini G, Ianora A (2011a) First molecular evidence of diatom effects diets in the copepod Calanus helgolandicus. J Exp Mar Biol Ecol 404:79–86. CrossRefGoogle Scholar
  52. Lauritano C, Borra M, Carotenuto Y, Biffali E, Miralto A, Procaccini G, Ianora A (2011b) Molecular evidence of the toxic effects of diatom diets on gene expression patterns in copepods. PLoS One 6:e26850. CrossRefPubMedPubMedCentralGoogle Scholar
  53. Lauritano C, Carotenuto Y, Miralto A, Procaccini G, Ianora A (2012) Copepod population-specific response to a toxic diatom diet. PLoS One 7:e47262. CrossRefPubMedPubMedCentralGoogle Scholar
  54. Lauritano C, Carotenuto Y, Vitiello V, Buttino I, Romano G, Hwang JS, Ianora A (2015) Effects of the oxylipin-producing diatom Skeletonema marinoi on gene expression levels of the calanoid copepod Calanus sinicus. Mar Genomics 24:89–94. CrossRefPubMedGoogle Scholar
  55. Lauritano C, Romano G, Roncalli V et al (2016) New oxylipins produced at the end of a diatom bloom and their effects on copepod reproductive success and gene expression levels. Harmful Algae 55:221–229. CrossRefPubMedGoogle Scholar
  56. Lavrentyev PJ, Franze G, Pierson JJ, Stoecker DK (2015) The effect of dissolved polyunsaturated aldehydes on microzooplankton growth rates in the Chesapeake Bay and Atlantic coastal waters. Mar Drugs 13:2834–2856. CrossRefPubMedPubMedCentralGoogle Scholar
  57. Malviya S, Scalco E, Audic S et al (2016) Insights into global diatom distribution and diversity in the world’s ocean. Proc Natl Acad Sci USA 113:E1516–E1525. CrossRefPubMedGoogle Scholar
  58. Md Amin R, Koski M, Bamstedt U, Vidoudez C (2011) Strain-related physiological and behavioral effects of Skeletonema marinoi on three common planktonic copepods. Mar Biol 158:1965–1980. CrossRefPubMedPubMedCentralGoogle Scholar
  59. Meunier CL, Boersma M, Wiltshire KH, Malzahn AM (2016) Zooplankton eat what they need: copepod selective feeding and potential consequences for marine systems. Oikos 125:50–58CrossRefGoogle Scholar
  60. Miralto A, Barone G, Romano G et al (1999) The insidious effect of diatoms on copepod reproduction. Nature 402:173–176. CrossRefGoogle Scholar
  61. Morello E, Arneri E (2009) Anchovy and sardine in the Adriatic sea—an ecological review. In: Gibson RN, Atkinson RJA, Gordon JDM (eds) Oceanography and marine biology: an annual review. Taylor & Francis Group, Milton Park, pp 209–256Google Scholar
  62. Moriceau B, Iversen MH, Gallinari M et al (2018) Copepods boost the production but reduce the carbon export efficiency by diatoms. Front Mar Sci 5:82. CrossRefGoogle Scholar
  63. Nanjappa D, d’Ippolito G, Gallo C, Zingone A, Fontana A (2014) Oxylipin diversity in the diatom family Leptocylindraceae reveals DHA derivatives in marine diatoms. Mar Drugs 12:368–384. CrossRefPubMedPubMedCentralGoogle Scholar
  64. Paffenhöfer GA, Köster M (2011) From one to many: on the life cycle of Dolioletta gegenbauri Uljanin (Tunicata, Thaliacea). J Plankton Res 33:1139–1145. CrossRefGoogle Scholar
  65. Paffenhöfer GA, Ianora A, Miralto A, Turner JT, Kleppel GS, d’Alcalà MR et al (2005) Colloquium on diatom-copepod interactions. Mar Ecol Prog Ser 286:293–305CrossRefGoogle Scholar
  66. Palomera I, Olivar MP, Salat J, Sabatés A, Coll M, García A et al (2007) Small pelagic fish in the NW Mediterranean sea: an ecological review. Prog Oceanogr 74:377–396CrossRefGoogle Scholar
  67. Pancic M, Kiørboe T (2018) Phytoplankton defence mechanisms: traits and trade-offs. Biol Rev Camb Philos Soc 93:1269–1303. CrossRefPubMedGoogle Scholar
  68. Pierson JJ, Halsband-Lenk C, Leising AW (2005) Reproductive success of Calanus pacificus during diatom blooms in Dabob Bay, Washington. Progr Oceanogr 67:314–331. CrossRefGoogle Scholar
  69. Pohnert G (2002) Phospholipase A2 activity triggers the wound-activated chemical defense in the diatom Thalassiosira rotula. Plant Physiol 129:103–111. CrossRefPubMedPubMedCentralGoogle Scholar
  70. Poulet SA, Wichard T, Ledoux JB, Lebreton B, Marchetti J, Dancie C et al (2006) Influence of diatoms on copepod reproduction. I. Field and laboratory observations related to Calanus helgolandicus egg production. Mar Ecol Prog Ser 308:129–142CrossRefGoogle Scholar
  71. Poulet SA, Cueff A, Wichard T, Marchetti J, Dancie C, Pohnert G (2007a) Influence of diatoms on copepod reproduction. III. Consequences of abnormal oocyte maturation on reproductive factors in Calanus helgolandicus. Mar Biol 152:415–428CrossRefGoogle Scholar
  72. Poulet SA, Escribano R, Hidalgo P, Cueff A, Wichard T, Aguilera V et al (2007b) Collapse of Calanus chilensis reproduction in a marine environment with high diatom concentration. J Exp Mar Biol Ecol 352:187–199CrossRefGoogle Scholar
  73. Rombouts I, Beaugrand G, Ibanez F, Gasparini S, Chiba S, Legendre L (2009) Global latitudinal variations in marine copepod diversity and environmental factors. Proc Biol Sci 276:3053–3062. CrossRefPubMedPubMedCentralGoogle Scholar
  74. Rombouts I, Beaugrand G, Ibañez F, Gasparini S, Chiba S, Legendre L (2010) A multivariate approach to large-scale variation in marine planktonic copepod diversity and its environmental correlates. Limnol Oceanogr 55:2219–2229. CrossRefGoogle Scholar
  75. Selander E, Thor P, Toth G, Pavia H (2006) Copepods induce paralytic shellfish toxin production in marine dinoflagellates. Proc Biol Sci 273:1673–1680. CrossRefPubMedPubMedCentralGoogle Scholar
  76. Sherr EB, Sherr BF (2007) Heterotrophic dinoflagellates: a significant component of microzooplankton biomass and major grazers of diatoms in the sea. Mar Ecol Prog Ser 352:187–197. CrossRefGoogle Scholar
  77. Sommer U, Sommer F (2006) Cladocerans versus copepods: the cause of contrasting top-down controls on freshwater and marine phytoplankton. Oecologia 147:183–194. CrossRefPubMedGoogle Scholar
  78. Sommer U, Adrian R, De Senerpont Domis L et al (2012) Beyond the plankton ecology group (PEG) model: mechanisms driving plankton succession. Annu Rev Ecol Evol Syst 43:429–448. CrossRefGoogle Scholar
  79. Steinberg DK, Landry MR (2017) Zooplankton and the ocean carbon cycle. Ann Rev Mar Sci 9:413–444CrossRefGoogle Scholar
  80. Stibor H, Vadstein O, Lippert B, Roederer W, Olsen Y (2004a) Calanoid copepods and nutrient enrichment determine population dynamics of the appendicularian Oikopleura dioica: a mesocosm experiment. Mar Ecol Prog Ser 270:209–215CrossRefGoogle Scholar
  81. Stibor H, Vadstein O, Diehl S et al (2004b) Copepods act as a switch between alternative trophic cascades in marine pelagic food webs. Ecol Lett 7:321–328. CrossRefGoogle Scholar
  82. Tréguer P, Bowler C, Moriceau B et al (2017) Influence of diatom diversity on the ocean biological carbon pump. Nat Geosci 11:27–37. CrossRefGoogle Scholar
  83. Turner JT (2015) Zooplankton fecal pellets, marine snow, phytodetritus and the ocean’s biological pump. Prog Oceanogr 130:205–248CrossRefGoogle Scholar
  84. Van Donk E, Ianora A, Vos M (2010) Induced defences in marine and freshwater phytoplankton: a review. Hydrobiologia 668:3–19CrossRefGoogle Scholar
  85. Vargas CA, Escribano R, Poulet S (2006) Phytoplankton food quality determines time windows for successful zooplankton reproductive pulses. Ecology 87:2992–2999CrossRefGoogle Scholar
  86. Vehmaa A, Larsson P, Vidoudez C, Pohnert G, Reinikainen M, Engström-Öst J (2011) How will increased dinoflagellate:diatom ratios affect copepod egg production? A case study from the Baltic Sea. J Exp Mar Biol Ecol 401:134–140CrossRefGoogle Scholar
  87. Verity PG, Smetacek V (1996) Organism life cycles, predation, and the structure of marine pelagic ecosystems. Mar Ecol Progr Ser 130:277–293CrossRefGoogle Scholar
  88. Vidoudez C, Pohnert G (2012) Comparative metabolomics of the diatom Skeletonema marinoi in different growth phases. Metabolomics 8:654–669. CrossRefGoogle Scholar
  89. Wichard T, Poulet SA, Halsband-Lenk C, Albaina A, Harris R, Liu D et al (2005) Survey of the chemical defence potential of diatoms: screening of fifty species for α, β, γ, δ-unsaturated aldehydes. J Chem Ecol 31:949–958CrossRefGoogle Scholar
  90. Wichard T, Gerecht A, Boersma M, Poulet SA, Wiltshire K, Pohnert G (2007) Lipid and fatty acid composition of diatoms revisited: rapid wound-activated change of food quality parameters influences herbivorous copepod reproductive success. ChemBioChem 8:1146–1153. CrossRefPubMedGoogle Scholar
  91. Wichard T, Poulet SA, Boulesteix A-L, Ledoux JB, Lebreton B, Marchetti J, Pohnert G (2008) Influence of diatoms on copepod reproduction. II. Uncorrelated effects of diatom-derived α, β, γ, δ-unsaturated aldehydes and polyunsaturated fatty acids on Calanus helgolandicus in the field. Progr Oceanogr 77:30–44. CrossRefGoogle Scholar
  92. Zhou C, Carotenuto Y, Vitiello V, Wu C, Zhang J, Buttino I (2018) De novo transcriptome assembly and differential gene expression analysis of the calanoid copepod Acartia tonsa exposed to nickel nanoparticles. Chemosphere 209:163–172. CrossRefPubMedGoogle Scholar

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© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Integrative Marine EcologyStazione Zoologica Anton DohrnNaplesItaly

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