Vertical distribution of Pseudo-nitzschia in the Gulf of Naples across the seasons
Published:
Jun 21, 2022
Keywords:
Diatoms HABs LTER-MC diversity Pseudo-nitzschia
Abstract
Pseudo-nitzschia is a widespread genus of marine pennate diatoms comprising 58 species of which 28 can produce the neurotoxin domoic acid, causative of Amnesic Shellfish Poisoning (ASP). Species of the genus are found in both oceanic and coastal waters where they can form large blooms. The timing and magnitude of blooms is generally described based on water samples collected at the surface, while limited information is available on cell distribution within the water column. To address this knowledge gap, we investigated the vertical (0-50 m) distribution of Pseudo-nitzschia species identified in light microscopy using weekly samples collected in the Gulf of Naples (Italy) across an annual cycle (April 2006-April 2007). Physical variables and nutrient concentrations were also monitored. The genus is primarily abundant in surface waters, where spring blooms of P. cf. delicatissima and two morphotypes of P. galaxiae were related to the presence of a water layer with low salinity and high concentration of inorganic nutrients. Blooms of P. cf. pseudodelicatissima, P. allochrona and P. multistriata were recorded at surface during the summer-early autumn, when the water column was stratified and nutrient concentrations were low. Our observations confirmed the marked seasonality of Pseudo-nitzschia species described at our study site with light microscopy and molecular approaches, with species virtually absent from surface waters for long periods of the year. However, the high quantitative resolution applied in this study allowed to reveal low concentrations of Pseudo-nitzschia species/species complexes throughout the water column over the year. Since Pseudo-nitzschia do not produce benthic resting stages, their presence in deeper waters suggests that these species rely on rare overwintering cells that can function as bloom inocula.
Article Details
- How to Cite
-
CIPOLLETTA, F., RUSSO, A., D’ALELIO, D., MARGIOTTA, F., SARNO, . D. ., ZINGONE, A., & MONTRESOR, M. (2022). Vertical distribution of Pseudo-nitzschia in the Gulf of Naples across the seasons. Mediterranean Marine Science, 23(3), 525–535. https://doi.org/10.12681/mms.28147
- Section
- Research Article
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution Non-Commercial License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g. post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are permitted and encouraged to post their work online (preferably in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).
Downloads
Download data is not yet available.
References
Amato, A., Kooistra, W.H.C.F., Levialdi Ghiron, J.H., Mann, D.G., Pröschold, T. et. al., 2007. Reproductive isolation among sympatric cryptic species in marine diatoms. Protist, 158, 193-207.
Amato, A., Montresor, M., 2008. Morphology, phylogeny, and sexual cycle of Pseudo-nitzschia mannii sp. nov. (Bacillariophyceae): a pseudo-cryptic species within the P. pseudodelicatissima complex. Phycologia, 47, 487-497.
Assmy, P., Henjes, J., Smetacek, V., Montresor, M., 2006. Auxospore formation in the silica-sinking oceanic diatom Fragilariopsis kerguelensis (Bacillariophyceae). Journal of Phycology, 42, 1002-1006.
Bates, S.S., Hubbard, K.A., Lundholm, N., Montresor, M., Leaw, C.P., 2018. Pseudo-nitzschia, Nitzschia, and domoic acid: New research since 2011. Harmful Algae, 79, 3-43.
Botte, V., Ribera D’Alcalà, M., Montresor, M., 2013. Hydrodynamic interactions at low Reynolds number: an overlooked mechanism favouring diatom encounters. Journal of Plankton Research, 35, 914-918.
Bresnan, E., Kraberg, A., Fraser, S., Brown, L., Hughes, S. et al., 2015. Diversity and seasonality of Pseudo-nitzschia (Peragallo) at two North Sea time-series monitoring sites. Helgoland Marine Research, 69, 193-204.
Caroppo, C., Congestri, R., Bracchini, L., Albertano, P., 2005. On the presence of Pseudo-nitzschia calliantha Lundholm, Moestrup et Hasle and Pseudo-nitzschia delicatissima (Cleve) Heiden in the Southern Adriatic Sea (Mediterranean Sea, Italy). Journal of Plankton Research, 27, 763-774.
Cerino, F., Orsini, L., Sarno, D., Dell’Aversano, C., Tartaglione et al., 2005. The alternation of different morphotypes in the seasonal cycle of the toxic diatom Pseudo-nitzschia galaxiae. Harmful Algae, 4, 33-48.
Cianelli, D., Falco, P., Iermano, I., Mozzillo, P., Uttieri, M. et al., 2015. Inshore/offshore water exchange in the Gulf of Naples. Journal of Marine Systems, 145, 37-52.
Cianelli, D., D’Alelio, D., Uttieri, M., Sarno, D., Zingone et al., 2017. Disentangling physical and biological drivers of phytoplankton dynamics in a coastal system. Scientific Reports, 7, 15868.
D’Alelio, D., Amato, A., Luedeking, A., Montresor, M., 2009. Sexual and vegetative phases in the planktonic diatom Pseudo-nitzschia multistriata. Harmful Algae, 8, 225-232.
D’Alelio, D., Ribera d’Alcalà, M., Dubroca, L., Sarno, D., Zingone et al., 2010. The time for sex: a biennial life cycle in a marine planktonic diatom. Limnology and Oceanography, 55, 106-114.
D’Alelio, D., Mazzocchi, M.G., Montresor, M., Sarno, D., Zingone et al., 2015. The green-blue swing: plasticity of plankton food-webs in response to coastal oceanographic dynamics. Marine Ecology, 36, 1155–1170.
Davidovich, N.A., Bates, S.S., 1998. Sexual reproduction in the pennate diatoms Pseudo-nitzschia multiseries and P. pseudodelicatissima (Bacillariophyceae). Journal of Phycology, 34, 126-137.
Díaz, P.A., Álvarez, A., Varela, D., Pérez-Santos, I., Díaz et al., 2019. Impacts of harmful algal blooms on the aquaculture industry: Chile as a case study. Perspectives in Phycology, 6, 39-50.
Durham, W.M., Stocker, R., 2012. Thin phytoplankton layers: characteristics, mechanisms, and consequences. Annual Review of Marine Science, 4, 177-207.
Edler, L., Elbrächter, M., 2010. The Utermöhl method for quantitative phytoplankton analysis. p. 13-20. In: Microscopic and Molecular Methods for Quantitative Phytoplankton Analysis. Karlson, B., Cusack, C.K., Bresnan, E. (Eds). UNESCO, Paris.
Fehling, J., Davidson, K., Bolch, C., Tett, P., 2006. Seasonality of Pseudo-nitzschia spp. (Bacillariophyceae) in western Scottish waters. Marine Ecology Progress Series, 323, 91-105.
Fernandes, L.F., Hubbard, K.A., Richlen, M.L., Smith, J., Bates, S.S. et al., 2014. Diversity and toxicity of the diatom Pseudo-nitzschia Peragallo in the Gulf of Maine, Northwestern Atlantic Ocean. Deep-Sea Research Part II-Topical Studies in Oceanography, 103, 139-162.
Font-Muñoz, J.S., Jeanneret, R., Arrieta, J., Anglès, S., Jordi, A. et al., 2019. Collective sinking promotes selective cell pairing in planktonic pennate diatoms. Proceedings of the National Academy of Sciences, 116, 15997-16002.
Forsythe, W.C., Rykiel Jr., E.J., Stahl, R.S., Wu, H., Schoolfield, R.M., 1995. A model comparison for daylength as a function of latitude and day of the year. Ecological Modeling, 80, 87-95.
Guiry, M.D., Guiry, G.M., 2021. AlgaeBase. World-wide electronic publication, http://www.algaebase.org. National University of Ireland, Galway (Accessed 01 October 2021).
Hansen, H.P., Grasshoff, K., 1983. Automated chemical analysis. p. 347-379. In: Methods of Seawater Analysis. Grasshoff, K., Ehrhardt, M., Krernling, K. (Eds). Verlag Chemie, Weinheim.
Holm-Hansen, O., Lorenzen, C.J., Holmes, R.W., Strickland, J.D.H., 1965. Fluorimetric determination of chlorophyll. Journal du Conseil International pour l’Exploration de la Mer, 30, 3-15.
Holtermann, K.E., Bates, S.S., Trainer, V.L., Odell, A., Armbrust, E.V., 2010. Mass sexual reproduction in the toxigenic diatoms Pseudo-nitzschia australis and P. pungens (Bacillariophyceae) on the Washington coast. Journal of Phycology, 46, 41-52.
Iermano, I., Liguori, G., Iudicone, D., Buongiorno Nardelli, B. et al., 2012. Filament formation and evolution in buoyant coastal waters: observation and modelling. Progress in Oceanography, 106, 118-137.
Jeffery, B., Barlow, T., Moizer, K., Paul, S., Boyle, C., 2004. Amnesic shellfish poison. Food and Chemical Toxicology, 42, 545-557.
Lelong, A., Hégaret, H., Soudant, P., Bates, S.S., 2012. Pseudo- nitzschia (Bacillariophyceae) species, domoic acid and amnesic shellfish poisoning: revisiting previous paradigms. Phycologia, 51, 168-216.
Lim, H.C., Tan, S.N., Teng, S.T., Lundholm, N., Orive, E. et al., 2018. Phylogeny and species delineation in the marine diatom Pseudo-nitzchia (Bacillariophyta) using cox1, LSU and ITS2 rRNA genes: A perspective in character evolution. Journal of Phycology, 54, 234-248.
Lundholm, N., Moestrup, Ø., Hasle, G.R., Hoef-Emden, K., 2003. A study of the Pseudo-nitzschia pseudodelicatissima/ cuspidata complex (Bacillariophyceae): what is P. pseudodelicatissima? Journal of Phycology, 39, 797-813.
Lundholm, N., Moestrup, Ø., Kotaki, Y., Hoef-Emden, K., Scholin, C. et al., 2006. Inter- and intraspecific variation of the Pseudo-nitzschia delicatissima complex (Bacillariophyceae) illustrated by rRNA probes, morphological data and phylogenetic analyses. Journal of Phycology, 42, 464-481.
Lundholm, N., 2021. Bacillariophyceae. In: IOC-UNESCO Taxonomic Reference List of Harmful Micro Algae. Moestrup, Ø., Akselmann-Cardella, R., Churro, C., Fraga, S., Hoppenrath, M. et al., (Eds). http://www.marinespecies. org/hab (Accessed 24 September 2021).
Marcus, N.H., Boero, F., 1998. The importance of benthic-pelagic coupling and the forgotten role of life cycles in coastal aquatic systems. Limnology and Oceanography, 43, 763-768.
Marić, D., Ljubešić, Z., Godrijan, J., Viličić, D., Ujević, I. et al., 2011. Blooms of the potentially toxic diatom Pseudo-nitzschia calliantha Lundholm, Moestrup & Hasle in coastal waters of the northern Adriatic Sea (Croatia). Estuarine and Coastal Shelf Science, 92, 323-331.
McDonald, S.M., Sarno, D., Zingone, A., 2007. Identifying Pseudo-nitzschia species in natural samples using genus- specific PCR primers and clone libraries. Harmful Algae, 6, 849-860.
McManus, M.A., Kudela, R.M., Silver, M.W., Steward, G.F., Donaghay, P.L. et al., 2008. Cryptic blooms: Are thin layers the missing connection? Estuaries and Coasts. 31, 396-401.
McQuoid, M.R., Hobson, L.A., 1996. Diatom resting stages. Journal of Phycology, 32, 889-902. McQuoid, M.R., Godhe, A., 2004. Recruitment of coastal planktonic diatoms from benthic versus pelagic cells: variations in bloom development and species composition. Limnology and Oceanography, 49, 1123-1133.
Montresor, M., Di Prisco, C., Sarno, D., Margiotta, F., Zingone, A., 2013. Diversity and germination patterns of diatom resting stages at a coastal Mediterranean site. Marine Ecology Progress Series, 484, 79-95.
Montresor, M., Vitale, L., D’Alelio, D., Ferrante, M.I., 2016. Sex in marine planktonic diatoms: insights and challenges. Perspectives in Phycology, 3, 61-75.
Oksanen, J., Blanchet, F.G., Friendly, M., Kindt, R., Legendre, P. et al., 2019. vegan: Community Ecology Package. R package, version 2.5-6. https://CRAN.R-project.org/package= vegan (Accessed 23 July 2021).
Percopo, I., Ruggiero, M.V., Sarno, D., Longobardi, L., Rossi, R. et al., 2021. Phenological segregation suggests speciation by time in the planktonic diatom Pseudo-nitzschia allochrona sp. nov. BioRxiv.
Piredda, R., Sarno, D., Lange, C.B., Tomasino, M.P., Zingone, A. et al., 2017. Diatom resting stages in surface sediments: a pilot study comparing Next Generation Sequencing and Serial Dilution Cultures. Cryptogamie Algologie, 38, 31-46.
Quijano-Scheggia, S., Garces, E., Sampedro, N., van Lenning, K., Flo, E. et al., 2008. Identification and characterisation of the dominant Pseudo-nitzschia species (Bacillariophyceae) along the NE Spanish coast (Catalonia, NW Mediterranean). Scientia Marina, 72, 343-359.
R Core Team, 2021. R: A language and environment for statistical computing R Foundation for Statistical Computing, Vienna, Austria https://www.R-project.org/ (Accessed 23 July 2021).
Ribera d’Alcalà, M., Conversano, F., Corato, F., Licandro, P., Mangoni, O. et al., 2004. Seasonal patterns in plankton communities in a pluriannual time series at a coastal Mediterranean site (Gulf of Naples): an attempt to discern recurrences and trends. Scientia Marina, 68, 65-83.
Rines, J.E.B., Donaghay, P.L., Dekshenieks, M.M., Sullivan, J.M., Twardowski, M.S., 2002. Thin layers and camouflage: hidden Pseudo-nitzschia spp. (Bacillariophyceae) populations in a fjord in the San Juan Islands, Washington, USA. Marine Ecology Progress Series, 225, 123-137.
Ruggiero, M.V., Sarno, D., Barra, L., Kooistra, W.H.C.F., Montresor, M. et al., 2015. Diversity and temporal pattern of Pseudo-nitzschia species (Bacillariophyceae) through the molecular lens. Harmful Algae, 42, 15-24.
Sabia, L., Costanzo, A., d’Alcalà, M. R., Saggiomo, V., Zingone, A. et al., 2019. Assessing the quality of biogeochemical coastal data: a step-wise procedure. Mediterranean Marine Science, 20 (1), 56-73.
Sarno, D., Zingone, A., Montresor, M., 2010. A massive and simultaneous sex event of two Pseudo-nitzschia species. Deep-Sea Research Part II, 57, 248-255.
Schlitzer, R., 2018. Ocean Data View, https://odv.awi.de. Scholin, C.A., Gulland, F., Doucette, G.J., Benson, S., Busman, M. et al., 2000. Mortality of sea lions along the central California coast linked to a toxic diatom bloom. Nature, 403, 80-84.
Smith, J., Connell, P., Evans, R.H., Gellene, A.G., Howard, M.D.A. et al., 2018. A decade and a half of Pseudo-nitzschia spp. and domoic acid along the coast of southern California. Harmful Algae, 79, 87-104.
Soliño, L., Ferrer-Obiol, J., Navarro-Herrero, L., González-Solís, J., Costa, P.R., 2019. Are pelagic seabirds exposed to amnesic shellfish poisoning toxins? Harmful Algae, 84, 172-180.
Trainer, V.L., Bates, S.S., Lundholm, N., Thessen, A.E., Cochlan, W.P. et al., 2012. Pseudo-nitzschia physiological ecology, phylogeny, toxicity, monitoring and impacts on ecosystem health. Harmful Algae, 14, 271-300.
Trainer, V.L., Kudela, R.M., Hunter, M.V., Adams, N.G., Mc- Cabe, R.M., 2020. Climate Extreme Seeds a New Domoic Acid Hotspot on the US west coast. Frontiers in Climate, 23.
Velo-Suarez, L., González-Gil, S., Gentien, P., Lunven, M., Bechemin, C. et al., 2008. Thin layers of Pseudo-nitzschia spp. and the fate of Dinophysis acuminata during an upwelling- downwelling cycle in a Galician Ría. Limnology and Oceanography, 53, 1816-1834.
Work, T.M., Barr, B., Beale, A.M., Fritz, L., Quillam, M.A. et al., 1993. Epidemiology of domoic acid poisoning in brown pelicans (Pelecanus occidentalis) and brandt cormarants (Phalacrocorax. penicillatus) in California. Journal of Zoo and Wildlife Medicine, 24, 54-62.
Zingone, A., Montresor, M., Marino, D. 1990. Summer phytoplankton physiognomy in coastal water of the Gulf of Naples. PSZNI: Marine Ecology, 11, 157-172.
Zingone, A., Casotti, R., Ribera d’Alcalà, M., Scardi, M., Marino, D., 1995. ‘St Martin’s Summer’: the case of an autumn phytoplankton bloom in the Gulf of Naples (Mediterranean Sea). Journal of Plankton Research 17, 575-593.
Zingone, A., Licandro, P., Sarno, D., 2003. Revising paradigms and myths of phytoplankton ecology using biological time series. p. 109-114. In: Mediterranean Biological Time Series. Briand, F. (Eds). CIESM Workshop Monographs n° 22, Monaco.
Zingone, A., Siano, R., D’Alelio, D., Sarno, D., 2006. Potentially toxic and harmful microalgae from coastal waters of the Campania region (Tyrrhenian Sea, Mediterranean Sea). Harmful Algae. 5, 321-337.
Zingone, A., Escalera, L., Aligizaki, K., Fernández-Tejedor, M., Ismael, A., et al., 2020. Toxic marine microalgae and noxious blooms in the Mediterranean Sea: A contribution to the Global HAB Status Report. Harmful Algae, 101843.
