Phytoplankton Dynamics and Bio-Optical Variables Associated with Harmful Algal Blooms in Aquaculture Zones

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Phytoplankton Dynamics and Bio-Optical Variables Associated with Harmful Algal Blooms in Aquaculture Zones Phytoplankton dynamics and bio-optical variables associated with Harmful Algal Blooms in aquaculture zones Dissertation Zur Erlangung des Akademischen Grades eines Doktors der Naturwissenschaften -Dr. rer. nat. - im Fachbereich 2 (Biologie/Chemie) der Universität Bremen vorgelegt von Julia A. Busch Bremen, Oktober 2013 1. Gutachter: Prof. Dr. Allan D. Cembella Alfred Wegener Institute Helmholtz Centre for Polar and Marine Research University Bremen 2. Gutachter: Prof. Dr. Oliver Zielinski Institute for Chemistry and Biology of the Marine Environment (ICBM) Carl von Ossietzky University Oldenburg 1. Gutachter: Prof. Dr. Allan D. Cembella 2. Gutachter: Prof. Dr. Oliver Zielinski 3. Prüfer: Dr. Marcel Wernand 4. Prüfer: Prof. Dr. Kai Bischof Tag des Promotionskolloquiums: 09.12.2013 ABSTRACT ABSTRACT The surveillance of Harmful Algal Blooms (HABs) in aquaculture zones is a crucial component in monitoring and mitigation of adverse effects caused by accumulation of high biomass of algal cells and/or associated toxins. The high diversity among HAB species, their harmful impact and spatio-temporal distributional patterns necessitates regionally adopted observational approaches that cover a broad spectrum of temporal and spatial scales. General objectives of this thesis were firstly, to outline how bio-optical techniques support the coverage of adequate spatio-temporal dimensions for HAB surveillance, in particular in the aquaculture zones of the Ebro Delta embayments of Alfacs and Fangar, and secondly, to gain insights into distribution, adaptive strategies and habitat preferences of harmful taxa that would eventually lead to prediction of algal growth and proliferation patterns. In addition to data generated continuously from a hyperspectral radiometric sensor system, extensive field samples on inherent optical properties, environmental variables, phytoplankton taxa and associated phycotoxins completed the picture on bio-optical characteristics and phytoplankton dynamics in the area during seasonal study periods over two years. The findings of this study established a sound basis for the operational enhancement of spatio-temporal scales for the surveillance of selected HAB taxa by means of a bio-optical sensor system. In particular, the installation of an environmental observatory in the aquaculture area, and the capability of a radiometric sensor system as key component are highly motivated by study results. One crucial factor is the high variability of phytoplankton, and in particular of HAB dynamics during the study period, which profoundly changed within weeks and formed small sized patches in the water column. In the temporal aspect, phytoplankton dynamics thereby clearly exceeded the limits of conventional weekly sampling, whereas the temporal resolution of bio-optical measurements was sufficiently resolved to detect and locate changes in proliferation patterns, such as the initiation of algal blooms. The second convincing result of this study is the establishment of regionally adapted techniques that allow a rapid automated processing of long-term remote sensing data-sets. These include the correction or elimination of remote sensing spectra which were compromised by boat traffic and specular sun reflection, and the subsequent retrieval of the algal biomass proxy chlorophyll a (Chl a) by a parameterised algorithm. In the Ebro Delta, these techniques permit the operational detection of algal biomass anomalies of a defined group of HAB taxa. Their applicability was demonstrated for the study period, but may require adjustment due to expected seasonal changes in bio-optical characteristics. Enhancement of areal scales was not effectively achieved by the single bio-optical test unit, but would be solved by additional components of an environmental observatory at key locations of the embayments. i ABSTRACT In the Ebro Delta embayments the biomass proxy Chl a is applicable to detect harmful blooms of several taxa that often dominate algal biomass at critical cell abundances, such as that of the ichthyotoxic dinoflagellate Karlodinium. Yet it was clearly shown that for the interpretation of bio-optical data, detailed knowledge on bloom characteristics is crucial. For instance, based on findings of this study Chl a is not likely to be a regional indicator for toxic blooms of the diatom Pseudo-nitzschia spp., as high abundances of this genus were not coinciding with the presence of the associated toxin domoic acid, and were therefore not classified as HAB. Hence the general limitation of bio-optical approaches to determine whether or not an observed bloom is harmful, or to delineate taxa, implies the use of complementary methods. One exception outlined in this study is the case for high abundances of K. veneficum and K. armiger, as their rare pigment gyroxanthin-diester is likely to be a regional indicator for this genus as outlined in this study. Bloom dynamics observed during the study period were typical for the season. Notable is the first observed development of high Karlodinium spp. abundances in Fangar Bay, which could be identified as K. veneficum in this study. Furthermore, a potentially new toxigenic species of the genus Azadinium was identified by means of light microscopy. Comparative findings of this thesis work indicate that Karlodinium spp. and Dinophysis spp. constitute alternative species types with different preferable habitats during the study period in spring/summer. Such understanding of bloom dynamics may be transferable to other embayments in a comparative approach and eventually lead to the delineation of habitat preferences of harmful taxa. Integrated findings of this thesis strongly stress the significance of synoptic bio-optical and conventional measures for efficient surveillance of HABs and environmental triggers. By the effective coverage of bloom dynamics, combined with insights on environmental scenarios that promote the proliferation of certain taxa, public and private responses can be optimised. By following such regional approaches, mitigation actions may be anticipated by preventive measures for certain HAB taxa in the future. ii ZUSAMMENFASSUNG ZUSAMMENFASSUNG Die Überwachung Schädlicher Algenblüten (HABs) in Aquakulturgebieten ist eine entscheidende Komponente um negativen Auswirkungen hoher Biomassen und/oder Toxine begrenzen zu können. Die Überwachung von HABs und Schadensbegrenzung ihrer negativen Auswirkungen setzt regional angepaßte Strategien voraus, die sowohl die Diversität der verantwortlichen Algen-Arten mit den von ihnen produzierten Phycotoxinen, als auch ihre räumlich-zeitlichen Verteilungsmuster einbeziehen. Zur Einschätzung der Gefährdung ist also die genaue Bestimmung der Arten und ihrer Toxine ebenso entscheidend wie die Erfassung der von der Phytoplankton-Dynamik diktierten räumlichen-zeitlichen Ebenen. Zielsetzung dieser Arbeit war es, durch den Einsatz bio-optischer Techniken die räumlich- zeitlichen Dimensionen für die Überwachung von HABs zu erweitern. Konkret wurde diese Fragestellung auf die Aquakulturzonen innerhalb der vom Mittelmeer halb isolierten Buchten Alfacs und Fangar im Ebro Delta angewandt. Zudem sollten Verteilungsmuster, adaptive Strategien und räumliche Nischen schädlicher Taxa charakterisiert werden mit dem Ziel, diese letztendlich zur Vorhersage von Blütenbildung heranziehen zu können. Innerhalb zweier Feldkampagnen in zwei aufeinanderfolgenden Jahren wurden neben einer Dauermessung mit einem hyperspektralen radiometrischen Sensorsystem auch umfangreiche Daten von inhärenten optischen Eigenschaften, Umweltparametern, Phytoplankon Taxa und Phycotoxinen gesammelt. Die Ergebnisse dieser Studie sind von grundlegender Relevanz für die bio-optische operationelle Überwachung von HAB Arten über erweiterten Raum-Zeit Skalen. Sie weisen insbesondere sowohl die Installation eines synoptischen Überwachungssystems innerhalb der Aquakulturzone als wichtigen Faktor aus, als auch ein radiometrisches Sensorsystem als dessen zentrale Komponente. Dies liegt vor allem auch in der hohen Variabilität der Phytoplankton-Verteilung während der Feldphase begründet, insbesondere in derer von HAB- Arten, die sich in zeitlichen Skalen von unter einer Woche grundlegend veränderten und sich in räumlich klar definierten Bereichen der Wassersäule abgrenzten. Während konventionelle Beprobungsansätze diese zeitliche Heterogenität der Phytoplankton-Dynamik nicht abdecken konnten, waren die bio-optischen Messungen ausreichend aufgelöst, um auch kleine Veränderungen im Verbreitungsbild von Algen zu detektieren und zu datieren. Sie können somit auch die Entstehungsphase von Algenblüten erfassen. Des weiteren wurden im Rahmen dieser Studie regional angepaßte Methoden zur schnellen und automatisierten Prozessierung von Langzeitdaten aus radiometrischen Messungen entwickelt. Diese bestehen aus der Korrektur oder ggf. dem Ausschluss von Radiometerspektren, die durch Bootsverkehr oder starke Sonnenreflexion beeinträchtigt wurden. Zudem wurde ein parametrisierter Algorithmus zur Berechnung des iii ZUSAMMENFASSUNG Biomasseindikators Chlorophyll a (Chl a) unter Berücksichtigung der lokalen inhärenten optischen Eigenschaften erstellt. Durch diese Techniken können Anomalien in der Entwicklung oder Verteilung einer begrenzten Gruppe von HAB-Taxa anhand ihrer Biomasse operationell erfaßt werden. Während die Methoden innerhalb des Untersuchungszeitraums erfolgreich eingesetzt werden konnten, ist aufgrund von saisonalen Veränderungen der inhärenten bio-optischen Eigenschaften eine Anpassung an diese
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