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CITATION Kudela, R.M., E. Berdalet, H. Enevoldsen, G. Pitcher, R. Raine, and E. Urban. 2017. GEOHAB–The Global Ecology and Oceanography of Harmful Algal Blooms Program: Motivation, goals, and legacy. Oceanography 30(1):12–21, https://doi.org/10.5670/ oceanog.2017.106.

DOI https://doi.org/10.5670/oceanog.2017.106

COPYRIGHT This article has been published in Oceanography, Volume 30, Number 1, a quarterly journal of The Oceanography Society. Copyright 2017 by The Oceanography Society. All rights reserved.

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DOWNLOADED FROM HTTP://TOS.ORG/OCEANOGRAPHY SPECIAL ISSUE ON INTERNATIONAL COOPERATION IN HARMFUL SCIENCE

GEOHAB The Global Ecology and Oceanography of Harmful Algal Blooms Program MOTIVATION, GOALS, AND LEGACY

By Raphael M. Kudela, Elisa Berdalet, Henrik Enevoldsen, Grant Pitcher, Robin Raine, and Ed Urban

ABSTRACT. In 2001, the first international research program focusing exclusively on harmful marine , GEOHAB (Global Ecology and Oceanography of Harmful Algal Blooms), was established by the HAB research community, under the sponsorship of the Intergovernmental Oceanographic Commission of UNESCO and the Scientific Committee on Oceanic Research. Its mission was to foster international cooperation to advance understanding of HAB dynamics and to improve our ability to predict them. The main efforts were focused on (1) the physiological, behavioral, and genetic characteristics of harmful microalgal species, and (2) the interactions between physical and other environmental conditions that promote the success of one group of species over another. GEOHAB was designed to study HABs with a view to integrating global data from comparable ecosystems. With an international, multidisciplinary, and comparative approach, GEOHAB advanced our understanding of the mechanisms underlying population dynamics of HABs within an ecological and oceanographic context and from an ecosystem perspective at the regional scale. GEOHAB encouraged combined Image credits: M. Chinain, experimental, observational, and modeling tools, using both existing and innovative Defra Crown ©, technologies in a multidisciplinary approach, consistent with the multiple scales and M. Kahru, K. Matsuoka oceanographic complexity of HAB phenomena. GEOHAB established the basis for continued international efforts now and into the future in order to better understand and predict the global complex phenomena of harmful algal blooms.

12 Oceanography | Vol.30, No.1 INTRODUCTION HISTORY OF GEOHAB their causes, predict their occurrences Photosynthetic algae, which include Coordinated research on HABs began in and mitigate their effects.” At the fourth single-​celled organisms (phytoplank- earnest in 1974 with the First International IPHAB meeting, IOC and SCOR jointly ton), (sometimes referred Conference on Toxic agreed to develop an international pro- to as blue-green algae), and macroalgae, Blooms. This later developed into a series gram for the advancement of scientific support healthy aquatic ecosystems by of international conferences on harmful research on HABs, which led to a work- forming the base of the , fixing marine , and at the fourth shop and subsequent formation, in 1998, carbon, and producing oxygen. Under meeting of this group in 1989, it was rec- of the Global Ecology and Oceanography certain circumstances, some species can ommended “that international research of Harmful Algal Blooms Programme form high-biomass and/or toxic prolifer- efforts be undertaken to evaluate the pos- (GEOHAB), cosponsored by IOC and ations of cells (known as “blooms”) that sibility of global expansion of algal blooms SCOR, with wide support from the inter- can cause harm to aquatic ecosystems, and man’s involvement in this phenom- national community through the Member including plants and animals, and to enon” (Granéli et al., 1990). This recom- States of IOC/IPHAB, and with sup- humans via direct exposure to water- mendation ultimately led to the request by port and guidance, particularly regarding borne or by consumption of toxic Member States of the Intergovernmental data management, from the Joint Global seafood. Ecosystem damage by high-​ Oceanographic Commission (IOC) to Ocean Flux Study (JGOFS). biomass blooms may include, for instance, form an international program on HABs. GEOHAB acknowledged from its disruption of food webs, fish killing by The the Scientific Committee on Oceanic inception that the HAB problem is global gill damage, or the development of low-​ Research (SCOR)/IOC WG 97 on the in nature, and that from a scientific per- oxygen “dead zones” after bloom degra- Physiological Ecology of Harmful Algal spective, there was incomplete informa- dation. Some species produce potent nat- Blooms also played an important role in tion about the biological, chemical, and ural chemicals (toxins) that can persist in focusing and starting to develop consen- physical factors regulating HAB dynam- the water or enter the food web, leading sus in the HAB research community. At ics and impacts (GEOHAB, 2001). Thus, to illness or death of aquatic animals and/ a 1991 workshop sponsored by the IOC the mission of GEOHAB was estab- or human seafood consumers. and SCOR, the IOC Harmful Algal Bloom lished, which was to “foster interna- Algal assemblages, visible or not, toxic Programme was first initiated, followed tional co-operative research on HABs in or not, and irrespective of cell concentra- shortly thereafter in 1992 by the estab- ecosystem types sharing common fea- tion, can have harmful impacts and are lishment of the Intergovernmental Panel tures, comparing the key species involved often generically referred to as “red tides” on Harmful Algal Blooms (IOC/IPHAB), and the oceanographic processes that (Figure 1). Collectively, all of these organ- with a goal “to foster the effective manage- influence their population dynam- isms and events are referred to as “harm- ment of, and scientific research on, harm- ics.” GEOHAB then adopted the goal ful algal blooms,” or HABs. The definition ful algal blooms in order to understand of “Improv(ing) prediction of HABs by of a HAB is a societal concept rather than a scientific definition, and these organ- isms and events are considered to be HABs if they negatively impact human health or socioeconomic interests or are detrimental to aquatic systems. HABs occur in all aquatic systems, including marine, brackish, and fresh- water, but they most dramatically affect human activities when they occur in coastal and inland waters. They are pres- ent from the to the Antarctic, even in sparsely settled coastal regions and in offshore areas. They are emerging as seri- ous threats in freshwater systems such as the US , in drinking water , and in coastal watersheds that FIGURE 1. Some algal blooms result in discoloration of the water, known as “red tides,” but harm- can deliver freshwater HAB cells and tox- ful algal blooms can include highly toxic algae that result in no discoloration, while some dramatic ins to the coastal ocean. events, such as this bloom caused by the dinoflagellate Noctiluca (inset), can be essentially harmless.

Oceanography | March 2017 13 determining the ecological and ocean- naturally occurring temporal and spatial of relevant instrumentation and models, ographic mechanisms underlying their variations in existing conditions and phe- are encouraged to contribute to this pro- population dynamics, integrating bio- nomena substitute for controlled experi- gramme. Active participation by the widest logical, chemical, and physical studies mental treatments. international representation of the research supported by enhanced observation and A key requirement for an international, community will be essential to ensure the modelling systems.” comparative approach to scientific under- success of GEOHAB. A core concept of the GEOHAB standing of HABs was the definition of program has been the comparative the systems and phenomena to be com- This invitation served to set the basis approach—indeed, this approach is pared. This was laid out by the GEOHAB for GEOHAB, with the explicit empha- embedded within both the mission and Scientific Steering Committee (SSC), sis on open, community participation goal espoused by GEOHAB. Mayr (1982) chaired by Patrick Gentien, and published and consensus-building by international identified experimental approachesas the GEOHAB Science Plan in 2001, scientists focused on HAB research. One and comparative approaches as “the the first of many GEOHAB reports. To significant difference from other similar two great methods of science” (see also define the boundary of GEOHAB activ- international programs, such as Global Anderson et al., 2005), and the organiz- ities, the Science Plan outlined five pro- Ocean Ecosystem Dynamics (GLOBEC; ers of GEOHAB quickly recognized that gram elements to serve as a framework to Turner et al., 2013), was that GEOHAB a global perspective of HAB phenom- guide priorities and research (Figure 2): never established an international pro- ena was best addressed with a compar- Biodiversity and Biogeography; gram office, which led to more empha- ative approach, from the cellular to the Nutrients and ; Adaptive sis on support and coordination from the ecosystem level. This approach is based Strategies; Comparative Ecosystems; and IOC and SCOR, and more reliance on the on the view that the ecology and ocean- Observation, Modelling, and Prediction. SSC and Core Research Projects (CRPs). ography of HABs can best be understood It was envisioned that these elements, CRPs were developed within GEOHAB through the study of causative organisms when combined, would lead to the sci- as the primary mechanism for coordinat- and affected systems in relation to compa- entific basis for improved management ing international research, with Targeted rable species and systems. The compara- and mitigation, and that GEOHAB would Research and Regional/National Projects tive approach directly addresses the fun- interact and coordinate with related pro- providing complementary efforts. damental issue that marine systems are grams at the regional, national, and inter- The CRPs directly addressed Program generally not amenable to experimental national levels. This Science Plan was Element 4 of the Science Plan (compar- control, and lend themselves to a coor- both ambitious and forward looking, ative research) and comprised oceano- dinated, international program where and served to steer the GEOHAB pro- graphic field studies conducted in, and gram from publication, in application of models to, comparable eco- 2001, through transition to the systems, supported by identification of GlobalHAB program, in 2016. relevant organisms, and measurements Biodiversity & Adaptive A major challenge for of the physical, chemical, and biologi- Biogeography Strategies any international coordinat- cal processes that control their popula- ing effort is to implement tion dynamics (GEOHAB, 2003). A major the high-level vision, mis- objective of core research was the integra- Observation, sion, and goals of the pro- tion achieved by the application of coupled Modeling, & Prediction gram. GEOHAB adopted an biological/chemical/physical models to Implementation Plan in 2003 HAB dynamics in geographically distinct (GEOHAB, 2003), and issued ecosystems sharing common features. Nutrients & Comparative the following call to scientists: Four CRPs spanned the lifetime of Eutrophication Ecosystems GEOHAB: “HABs in Upwelling Systems,” This plan for implementation “HABs in Eutrophic Systems,” “HABs in of the programme serves as an Stratified Systems,” and “HABs in Fjords invitation to the broad scien- and Coastal Embayments.” It was evi- tific community to participate. dent midway through the GEOHAB Management & Mitigation Scientists working in physical, program that a new CRP on “HABs in chemical and/or biological dis- Benthic Systems” should be established, FIGURE 2. The goals of the Global Ecology and ciplines, or other fields related and in 2010 this CRP was added as a Oceanography of Harmful Algal Blooms (GEOHAB) pro- gram were advanced through the linkages among the to harmful algal research, fifth element. Inclusion of benthic HABs program elements. including the development (BHABs) arose because, first, BHABs

14 Oceanography | Vol.30, No.1 appear to be increasing in area and Science Meeting (OSM) held in 2004 primarily on comparison of systems using impact within the coastal ocean. Second, (GEOHAB, 2005), identified eight core existing data and field efforts. This led to better attention to the BHAB phenom- questions related to upwelling systems: numerous publications, including a spe- enon highlighted the disparity in our • Are there definable adaptive strate- cial issue of Progress in Oceanography knowledge of the ecology of the species gies that characterize HAB species in (Pitcher and Pillar, 2010) that highlighted associated with benthic com- upwelling systems? progress and still-needed effort related to pared to phytoplanktonic species. A third • What seeding strategies persist within the eight core objectives of this CRP. driver was the opportunity to share the upwelling regions and are they consis- System-based studies have been use- collective experience and expertise accu- tent among regions? ful in advancing our knowledge of the mulated over the years in other systems • How do small-scale physical processes ecology and oceanography of HABs, and and organisms on tropical and subtropi- affect HAB growth and dispersion in the comparative approach, as endorsed cal benthic HABs. upwelling systems? by GEOHAB, is considered to have These five CRPs each had unique sci- • How do nutrient supply, type, and added value to regional or national sci- entific questions, participants, and out- ratios determine HAB population ence plans. GEOHAB has provided use- comes, but a common feature to all was dynamics in upwelling systems? ful direction to HAB research in upwell- their development with full and open • What is the role of genetic predispo- ing systems over the past decade through involvement from the international scien- sition versus environmental condi- formulation of common research objec- tific community, and with an emphasis on tions in production in differ- tives and the development of common the comparative approach as defined in the ent upwelling systems within a given research approaches that have contrib- Science Plan (GEOHAB, 2001; Figure 3). genus or species? uted significantly to improving the avail- These CRPs are briefly described below • How does coastal morphology and ability of comparable data. The strong with major goals and accomplishments. bathymetry affect HAB dynamics in influence of physical forcing in upwell- upwelling systems? ing systems has allowed a great deal of HABS IN UPWELLING SYSTEMS • What is the relative importance of understanding to be gained from physi- The CRP “HABs in Upwelling Systems” cross-shelf and alongshore advec- cal models with passive tracers represent- recognized that assessment of the extent tion in different upwelling systems ing HABs. Physical transport models have to which HAB species respond in a sim- for HABs? provided a very useful first step in pre- ilar way within these systems will allow • Are climate indicators predictive of dicting the movement of blooms through the oceanographic processes that influ- HAB events in upwelling systems? advection. Successful prediction of HABs ence HAB population dynamics and as a possible outcome of the integration community interactions to be estab- Given the difficulty of launching a truly of real-time data into model systems as a lished. Equally important was identifica- comparative field program across multiple component of operational forecasting of tion of upwelling systems that have dis- ecosystems without a concerted national/ the ocean is most likely to be achieved in similar HAB species or groupings. The international effort such as JGOFS (Karl upwelling systems, thus taking a critical CRP science plan developed at an Open et al., 2001), the Upwelling CRP focused step toward fulfillment of GEOHAB goals.

HABs in Eutrophic Systems GEOHAB CORE RESEARCH PROJECT: HABs IN BENTHIC SYSTEMS

GEOHAB CORE RESEARCH PROJECT: HABs IN UPWELLING SYSTEMS GEOHAB CORE RESEARCH PROJECT: HABs IN STRATIFIED SYSTEMS

1



FIGURE 3. Five Core Research Projects provided the backbone for GEOHAB scientific efforts.

Oceanography | March 2017 15 HABS IN EUTROPHIC SYSTEMS and the US Harmful Algal Research • What are the relative contributions of The science plan of the CRP “HABs in and Response National Environmental biological and physical processes to Eutrophic Systems” (GEOHAB, 2006) Strategy (HARRNESS, 2005). Over the the initial formation of thin layers in was developed at an OSM held in 2005. lifetime of GEOHAB, this CRP con- stratified systems? This meeting identified that an important ducted two OSMs (Baltimore, USA, and • What are the key processes defining consequence of eutrophication, or nutri- Beijing, China), produced two special the different strategies that maintain ent pollution, is the increased prevalence issues on HABs and eutrophication (in phytoplankton in thin layers? of HABs primarily through the formation Harmful Algae and the Chinese Journal of • What are the biological and chemi- of high-biomass events. These events lead Oceanology; Glibert et al., 2008b, 2011), cal outcomes of the physical concen- to fish kills, trophic transfer of algal tox- and published a position paper iden- tration of plankton into high-density ins, oxygen depletion, and altered trophic tifying the negative consequences of thin layers? interactions through direct stimulation fertilization for enhanced carbon • What causes a high-density population of HABs by nutrients, but also through sequestration and fisheries production in a thin layer to collapse? more subtle alterations of ecosystem (Glibert et al., 2008a). function. This CRP laid out a roadmap Historically, the conceptual under- The unique nature of the habitat asso- for international research, focusing on standing of the links between nutrients ciated with these events, typically involv- the following questions: and HABs was based upon the simplis- ing subsurface layers, led to a strong • Are there clusters or specific types tic notion that more nutrients directly emphasis on development of technology of HAB species that are indicative of lead to higher algal biomass. Results and methods for sampling and modeling global nutrient increases? from this GEOHAB CRP led to the rec- HAB organisms in stratified systems, cul- • To what extent do residence time and ognition that HAB species can be directly minating in a 2012 workshop in Monterey other physical processes impact the and/or indirectly stimulated by nutrient Bay, (GEOHAB, 2013; Berdalet relationship between nutrient loading over-enrichment, and that chronic, subtle et al., 2014) and the publication of a spe- and HAB proliferation? effects related to nutrient forms, ratios, cial issue of Deep Sea Research Part II • How do feedbacks and interactions and loads can be equally or even more (Raine et al., 2014). A main outcome of between nutrients and the planktonic, important than the obvious, acute effects the CRP was the recognition that thin microbial food webs impact HABs and (Glibert et al., 2011). layers are important in the initiation and their detrimental effects? development of HABs, as populations • Do anthropogenic alterations of the HABS IN STRATIFIED SYSTEMS develop inside retentive physical struc- food web, including overfishing and The CRP on “HABs in Stratified Systems” tures that are then transported toward the aquaculture activities, synergistically held an OSM in 2005. The resulting coast where impacts occur. interact with nutrients to favor HABs? CRP science plan (GEOHAB, 2008) • How do anthropogenic changes in focused on understanding the small-scale HABS IN FJORDS AND COASTAL land use, agricultural use of , hydrographic features that are encoun- EMBAYMENTS NOx emissions from vehicles, and tered in any environmental system, Coastal regions represent a small frac- global changes in land cover affect the including the systems the other CRPs tion of the world ocean, but are of con- delivery of nutrients to coastal waters focused on (upwelling, fjords, and semi-​ siderable importance because of the ever- and the resulting incidence of HABs? enclosed coastal areas, and both eutrophic increasing human population that lives How do the stoichiometry and quality and non-eutrophic systems). Particular there, as well as the generally high pro- of these nutrient sources regulate the emphasis was placed on thin layers where ductivity of these regions. Harmful algal biological responses favoring HABs? many harmful phytoplankton organisms blooms frequently occur in this environ- • Do and climate vari- can thrive, on rheology dynamics, and on ment, with negative outcomes on human ability have impacts on ecosystems technological and modeling challenges to health, tourism, aquaculture, and com- that augment the impacts of eutrophi- resolve the biological and physical inter- mercial fisheries. The CRP “HABs in cation in the formation of HABs? actions operating at small physical scales. Fjords and Coastal Embayments” resulted The overall objective was to determine from an OSM held in 2004. The CRP sci- Members of the CRP focused on estab- the factors underlying the development ence plan (GEOHAB, 2010) focused on lishing collaborative international com- of communities related to HABs in sub- the need to better understand the ecol- parative projects, with eutrophication surface microlayers and the real-time dis- ogy and oceanography of harmful algal being a core component of regional and persion of these microlayers as a func- species in these regions, which are char- national programs such as CEOHAB tion of turbulent and advective regimes. acterized by shallow depths and prox- in China, the GEOHAB Asia program, Four key questions were identified: imity to land. Seven key questions were

16 Oceanography | Vol.30, No.1 defined in the science plan: of cysts to the recurrence of blooms in species from similar habitat types and • Are there definable adaptive strategies certain retentive areas (e.g., Onda et al., identification of functional groups that characterize HAB species in con- 2014), but not in others (e.g., Estrada • Identify the important physical and fined and semi-confined systems? et al., 2010). chemical factors that control abun- • What is the importance of life history A physical/biological numerical dance and distribution over appropri- transitions and cyst distribution in model of the population dynamics of ate temporal and spatial scales bloom initiation and maintenance— A. fundyense in the Gulf of Maine has • Inform conceptual and numerical endogenous seed beds versus exoge- been run routinely each year since 2015. models that help to predict BHAB nous introduction? Continued fieldwork provided clear evi- events • How do physical dispersion and dence of the interannual variability of • Develop and validate technologies aggregation processes within a semi-​ cyst beds in the region, and also showed for detailed and extensive monitoring confined basin affect HAB growth and links between cyst distribution patterns and establish real-time observation distribution? and the intensity and extension of blooms platforms • What is the relative contribution of nutrient flux and supply ratios to HAB dynamics in eutrophic versus non- eutrophic coastal embayments? • What is the importance of spatial scale With an international, multidisciplinary, and and retention time in the expression comparative approach, GEOHAB advanced our and effects of allelochemicals/toxins in semi-confined systems? understanding of the mechanisms underlying • How do embayment morphology, population“ dynamics of HABs within an ecological bathymetry, and hydrodynamic flux affect HAB dynamics? and oceanographic context and from an ecosystem • Are the effects of anthropogenic activ- perspective at the regional scale. . ities (e.g., aquaculture) and global cli- mate change on HAB dynamics mag- nified in enclosed and semi-enclosed embayments? in the years immediately before and after Discoveries over the last five to” seven Following the first OSM, this group cyst mapping surveys (McGillicuddy years have brought new researchers into held a second one (Victoria, Canada) in et al., 2011). It is now possible to empir- the field, with a considerable increase in 2012 entitled “Progress in Interpreting ically forecast the geographic extent of a related publications. The establishment Life History and Growth Dynamics of forthcoming bloom based on cyst abun- of an international program that can Harmful Algal Blooms in Fjords and dances (Anderson et al., 2014). coordinate information and data shar- Coastal Environments.” This meet- ing of different science communities, ing focused on four themes: (1) life his- HABS IN BENTHIC SYSTEMS many of which are geographically sepa- tory of HAB species, (2) allelochemi- The newest CRP, “HABs in Benthic rated, was the objective of the BHAB cal interactions, (3) genetic diversity, Systems,” developed out of the recogni- CRP, and this activity continues under and (4) transport and mixing of blooms tion that BHABs are becoming increas- the GlobalHAB program. in small-scale, mesoscale, and semi-​ ingly significant globally, and that inter- Although GEOHAB made prog- confined systems. Progress in this CRP national coordination would benefit this ress on many of the research questions related primarily to the life histories of research community. Following from an listed above, many still remain to be fully HAB species, including resistance and OSM in 2010 (GEOHAB, 2012), this CRP explored through future research, as the sexual reproduction phases, thanks developed an approach to facilitate this BHAB group is one of the most diffi- to advances in culturing, microscopy coordination: cult types of HABs to mitigate, and the (e.g., nuclei staining and visualization), • Determine the primary physiological, demand for improved approaches and and molecular tools (e.g., Bravo et al., genetic, environmental, or behavioral methods is widespread, given that ben- 2014). Species-specific strategies for cyst processes that regulate cellular growth thic HABs are associated with both high- germination and encystment coupled and toxicity value tourism (e.g., coral reef systems) to particular water circulation patterns • Define common characteristics,and high-impact consequences (such as explain in some cases the importance including the groupings of harmful ciguatera fish poisoning).

Oceanography | March 2017 17 GEOHAB TARGETED, REGIONAL, Harmful Algal Blooms in the HAB problems, and provided a frame- AND NATIONAL RESEARCH (PhilHABs) and Chinese Ecology and work for guiding priorities for research The GEOHAB SSC was well aware that Oceanography of Harmful Algal Blooms based on the five GEOHAB program ele- the CRPs focused on specific objec- (CEOHAB). The mission and goals of ments. The need to develop a compar- tives within the larger Science Plan, and GEOHAB were also articulated and ative, international program on HABs that coordination with related and com- implemented at a regional level through in Asia was particularly compelling for plementary programs was critical to development of the EU-US Scientific several reasons. Asia is characterized the successful development of a coordi- Initiative on Harmful Algal Blooms by (1) the highest production of aqua- nated international program. Targeted (European Commission, 2013), which culture fish and globally, and research included numerous projects that developed a coordinated research effort thus the greatest impacts from HABs on requested endorsement by GEOHAB or between the US and the EU EUROHAB these resources; (2) a diversity of harm- were aligned with the goals of the CRPs. programs. A total of eight regional/ ful syndromes and causative organisms Regional and national research activ- national programs were endorsed by occur in Asia; (3) an apparent trend of ities were identified as relevant to the GEOHAB (Figure 4). increasing HABs throughout the region GEOHAB Science Plan, but were coor- Another significant accomplishment has been observed; and (4) an increasing dinated by regional or national organiza- facilitated by GEOHAB was the establish- trend toward regional eutrophication has tions independent of the GEOHAB SSC. ment of a regional plan for HAB research been linked to HABs. The ecological and These projects and programs ranged from in Asia. This plan developed out of two economic impacts of HABs in Asia are narrowly focused efforts, such as a pro- regional meetings (Tokyo, Japan, in 2007 thus profound and apparently increas- gram entitled “Dynamics of Alexandrium and Nha Trang, Vietnam, in 2008). These ing. GEOHAB Asia provided, and still fundyense distributions in the Gulf of meetings were held in coordination with provides, a template for regional coordi- Maine: An observational and modeling IOC/WESTPAC and the IOC HABViet nation on HAB research, leading to fur- study of nearshore and offshore shell- program, culminating in the GEOHAB ther partnerships under both GEOHAB fish toxicity, vertical toxin flux, and “Harmful Algal Blooms in Asia: A and now GlobalHAB, as well as through bloom dynamics in a complex shelf sea,” Regional Comparative Programme” ongoing efforts by IOC/WESTPAC and (GOMTOX) to large, national programs (GEOHAB, 2010; Furuya et al., 2010). The other regional organizations. including Ecology and Oceanography of report developed an overview of Asian CROSSCUTTING AND FRAMEWORK ACTIVITIES

Development of In addition to the research efforts sup- GEOSS/GOOS Other Tools and Models ported by GEOHAB, the Implementation International Plan also called for Framework activ- Observational Programs Development ities focusing on data management, protocols, and quality control; capac- Geo/Blue GEOHAB Planet ity building; modeling; and coordina- tion with other international programs. Monitoring An early and highly successful exam- SCOR IOC IPHAB IOCCG ple of GEOHAB activity within this cat- egory was the “Workshop on Real- Time Coastal Observing Systems for

Future Ecosystem Dynamics and Harmful Management ICES GEOHAB Earth Algal Blooms,” or HABWatch, held in Asia US HAB 2003 at the Observatoire Océanologique CEO HAB and Citadelle of Villefranche-sur-Mer, PICES IMBER France (e.g., Figure 5). The idea for the workshop initially emerged from the Working Group on Harmful Algal FIGURE 4. GEOHAB cooperated and coordinated with relevant national, regional, and international programs. GEOSS/GOOS = Global Earth Observation System of Systems/Global Ocean Observing Blooms Dynamics of ICES (International System. SCOR = Scientific Committee on Oceanic Research. IOC IPHAB = Intergovernmental Council for the Exploration of the Sea), Oceanographic Commission Intergovernmental Panel on Harmful Algal Blooms. ICES = International and was supported by GEOHAB and the Council for the Exploration of the Sea. PICES = North Pacific Marine Science Organization. IOCCG = International Ocean-Colour Coordinating Group. IMBER = Integrated Marine Biogeochemistry and Coastal Ocean Observing Panel (COOP) Ecosystem Research. of the Global Ocean Observing System

18 Oceanography | Vol.30, No.1 (GOOS), and initiated with major sup- has been the development of a series of to HAB events and organisms. port from the European Commission. workshops on the relationship between Moving forward, GlobalHAB is also This workshop, attended by an interna- HABs and climate change (Wells expected to interact with the IOC- tional audience, provided participants et al., 2015). The general topic of cli- UNESCO working group GO2NE (Global with both the theory relevant to under- mate change was acknowledged in the Ocean Oxygen Network), recently formed standing the basic principles of real-time GEOHAB science and implementation in response to a need for a global analysis observation and modelling tools and plans but was not a primary focus of the of ocean deoxygenation and its impacts. tutorials to allow the use of these tools. various CRPs in large part because it was This international network of ocean oxy- The lectures and tutorials are still avail- felt that there was insufficient informa- gen scientists will benefit investigation of able at http://HABWatch.obs-vlfr.fr, and tion about the link(s) and causative rela- ocean deoxygenation in response to cli- the workshop culminated in the publi- tionships between HABs and climate mate change and eutrophication. Formal cation of a manual within the UNESCO change while the CRPs were active. The collaboration between GlobalHAB and

Oceanographic Methodology Series, first workshop was jointly sponsored by GO2NE will serve investigation of the Real-Time Coastal Observing Systems for GEOHAB, ICES, and the North Pacific likely global increase in episodic oxy- Marine Ecosystem Dynamics and Harmful Marine Sciences Organization (PICES), gen depletion associated with increasing Algal Blooms: Theory, Instrumentation, under the auspices of the “Workshop on HABs in the coastal environment. and Modeling (Babin et al., 2008). Harmful Algae Blooms in a Changing Following on from HABWatch, World” (ICES, 2013). Outcomes from GEOHAB LEGACIES GEOHAB ran another very successful this workshop included assessment of There are many potential ways to gauge workshop and training activity in 2009 the current state of knowledge (Wells the successes and impacts of interna- in Galway, Ireland, focused on mod- et al., 2015), description of two types tional research programs; one of the most eling: “GEOHAB Modeling: Linking of “sentinel” sites for observing change tangible is to document the outcomes of Observations to Predictions” (GEOHAB, based on long-term observations, and these activities within the scientific lit- 2011). Similar to HABWatch, it empha- planning for a larger OSM. erature. In addition to the GEOHAB sized training young investigators, facil- The follow-on OSM took place in report series, multiple special issues itating international coordination, devel- Gothenburg, Sweden, in 2015, again were produced during the lifetime of oping strategies for using observations cosponsored by GEOHAB, ICES, and the GEOHAB program. GEOHAB also and models to address GEOHAB CRP sci- PICES. Workshop participants devel- directly coordinated research activities, ence questions, and furthering the goals oped several urgent recommendations on cosponsored other activities, and pro- of the GEOHAB Science Plan. The work- research priorities related to HABs and vided endorsement for targeted, national, shop focused specifically on the science climate change. These include focusing and regional programs aligned with pro- questions articulated by the Eutrophic, more intensive research on key organ- gram objectives. There was no require- Stratified, and Upwelling Systems CRPs, isms; continuing to develop ecological ment for acknowledgment of GEOHAB with a significant outcome being the pub- and forecast models; strengthening link- in publications, but many authors iden- lication of a special issue of the Journal of ages among global, national, and regional tified GEOHAB as a contributor to these Marine Systems (McGillicuddy, 2011). observation programs to establish the research efforts. The SSC tracked the One of the most recent crosscutting recommend HAB sentinel sites; and GEOHAB documents, acknowledgments activities supported by GEOHAB, con- development of a “best practices” manual in other peer-reviewed manuscripts, and tinuing under the GlobalHAB program, for assessment of climate change linkages publications from key endorsed projects

FIGURE 5. GEOHAB workshops, including HABWatch and Stratified Systems, focused on the use of advanced technology to detect HABs, such as (left) the Environmental Sample Processor, (middle) buoyancy gliders, and (right) the wave-powered WireWalker.

Oceanography | March 2017 19 and special journal issues sponsored by to the mission and goals identified by Colour Coordinating Group (IOCCG), GEOHAB. At the end of 2016, there were the GEOHAB program. As importantly, with the anticipated production of a 330 publications in 75 journals, while the GEOHAB has continued to raise aware- monograph on satellite remote sensing of GEOHAB science and implementation ness of the general scientific consensus HABs in 2017. Finally, while GEOHAB plans were cited 220 times. Expanding that public health, recreational and tour- has ended, a result of the final OSM, held this to include all publications that refer- ism, fishery, aquaculture, and ecosystem in Paris in 2013, was that the interna- ence GEOHAB in the title or text, there impacts from HABs have all increased tional scientific community requested were more than 1,000 publications as of over the past few decades and need to that a program like GEOHAB continue 2016 (Figure 6). be addressed with a coordinated, inter- into the future. As one participant sum- GEOHAB also had a positive influ- national effort. GEOHAB recently pub- marized, “we all came to Paris because ence on other international programs. lished Harmful Algal Blooms: A Scientific we recognize a fundamental problem Beginning with HABWatch, GEOHAB Summary for Policy Makers (Kudela (HABs), and cannot solve this problem in has partnered with GOOS; the increased et al., 2015) and has contributed to the our individual laboratories. This requires visibility of HABs provided by GEOHAB “Oceans and Society: Blue Planet” initia- an international approach.” From this and other efforts has led to the inclu- tive coordinated by the Group on Earth recognition came the formal adoption sion of phytoplankton generally, and Observations (Bernard et al., 2014). of the GlobalHAB program, adopted by HAB organisms specifically, as pro- These efforts, while more intangible than IOC (through IPHAB) and SCOR, and posed Biological Core Variables within a list of publications, continue to inform endorsed by the International Atomic the US Integrated Ocean Observing and guide research activities on harmful Energy Agency. The GlobalHAB Science System (National Ocean Council, 2016), algal blooms well beyond the formal end and Implementation plan builds on the while the GOOS Biology and Ecosystems of the GEOHAB program. GEOHAB Science Plan, and incorpo- Panel has identified phytoplankton spe- The GEOHAB legacy also continues rates suggestions from members of the cies, and HABs as a specific subset, as an beyond 2016 through ongoing activities international HAB community who par- Essential Ocean Variable. OSMs such as initiated by GEOHAB and now main- ticipated in the GEOHAB OSM in Paris. the “HABs in a Changing World” sympo- tained by GEOHAB partners. For exam- It is also enriched by many other contri- sium, cohosted by GEOHAB, ICES, and ple, the ICES, PICES, and GEOHAB butions during the first year of the pro- PICES, continue to define research pri- efforts on HABs and climate change gram and by subsequent inputs at the orities for the next decade by these pro- are expected to produce a “best prac- International Conference on Harmful grams, while the regional planning and tices” manual in the near future. Another Algae in Florianópolis, Brazil (October implementation activities established partnership was established between 2016), where the first draft of the plan was both nationally and regionally contribute GEOHAB and the International Ocean presented. GlobalHAB builds on the sci- entific framework provided by GEOHAB 350 and also expands into new disciplines and addresses emerging issues. GlobalHAB will address the scientific and societal 300 challenges of HABs through the appli- cation of advanced technologies, train- 250 ing, and capacity building, with a multi- disciplinary approach. It will also build 200 linkages with broader science domains (climate, toxicology, economy, medicine, 150 public health), emphasize social science communications, and address manage- 100 ment priorities. We are proud of what the GEOHAB 50 program accomplished, and we look for-

Number of Publications Referencing GEOHAB Referencing Number of Publications ward to future research programs such 0 as GlobalHAB that both benefit from 2000 2002 2004 2006 2008 2010 2012 2014 2016 and build upon this legacy of informed Year GEOHAB CORE RESEARCH PROJECT: science and international coordination FIGURE 6. GEOHAB is directly acknowledged in or central to 330 publicationsHABs IN BENTHIC SYSTEMS in 75 journals. Expanding this to include all publications that reference GEOHAB, there were more than 1,000 pub- to continue improving the prediction of lications as of 2016. HABs by determining the ecological and

20 Oceanography | Vol.30, No.1 oceanographic mechanisms underlying GEOHAB. 2003. Global Ecology and Oceanography Kudela, R.M., E. Berdalet, S. Bernard, M. Burford, of Harmful Algal Blooms: Implementation Plan. L. Fernand, S. Lu, S. Roy, P. Tester, G. Usup, their population dynamics, integrating P. Gentien, G. Pitcher, A. Cembella, and P. Glibert, R. Magnien, and others. 2015. Harmful Algal biological, chemical, and physical stud- eds, SCOR and IOC, Baltimore and Paris, 36 pp. Blooms: A Scientific Summary for Policy Makers. GEOHAB. 2005. Global Ecology and Oceanography IOC/UNESCO, Paris (IOC/INF-1320), 19 pp. ies supported by enhanced observation of Harmful Algal Blooms, GEOHAB Core Research Mayr, E. 1982. The Growth of Biological Thought. and modeling systems, and also incor- Project: HABs in Upwelling Systems. G. Pitcher, Harvard University Press, Cambridge, MA, USA, T. Moita, V. Trainer, R. Kudela, F. Figuieras, and 974 pp. porating new challenges and a wider T. Probyn, eds, IOC and SCOR, Paris and Baltimore, McGillicuddy, D.J. Jr. 2011. Models of harm- 88 pp. ful algal blooms: Conceptual, empirical, and scope in order to translate this knowledge GEOHAB. 2006. Global Ecology and Oceanography numerical approaches. Journal of Marine into sound policy- and decision-making of Harmful Algal Blooms: Eutrophication and HABs. Systems 83:105–107, https://doi.org/10.1016/​ SCOR and IOC, Paris and Baltimore, 74 pp. j.jmarsys.2010.06.008. based on sound science. GEOHAB. 2008. Global Ecology and Oceanography Onda, D.F.L., A O. Lluisma, and R.V. Azanza. 2014. The following papers in this special of Harmful Algal Blooms, GEOHAB Core Research Development, morphological characteristics and Project: HABs in Stratified Systems.SCOR and IOC, viability of temporary cysts of Pyrodinium baha- issue of Oceanography will provide more Paris, France, and Newark, Delaware, USA, 59 pp. mense var. compressum (Dinophyceae) in vitro. GEOHAB. 2010. Global Ecology and Oceanography European Journal of Phycology 49:265–275, detail on the specific accomplishments in of Harmful Algal Blooms, GEOHAB Core Research https://doi.org/10.1080/09670262.2014.915062. each area of GEOHAB. Project: HABs in Fjords and Coastal Embayments. Pitcher, G.C., and S. Pillar, eds. 2010. Special Issue A. Cembella, L. Guzman, S. Roy, J. Diogene, on Harmful Algal Blooms in Upwelling Systems. eds, IOC and SCOR, Paris, France, and Newark, Progress in Oceanography 85(1–2):1–136. REFERENCES Delaware, 57 pp. Raine, R., E. Berdalet, M.A. McManus, and Anderson, D.M., G.C. Pitcher, and M. Estrada. GEOHAB. 2011. GEOHAB Modelling: A Workshop H. Yamazaki, eds. 2014. Harmful algae in stratified 2005. The comparative “systems” approach to Report. D.J. McGillicuddy Jr., P.M. Glibert, systems. Deep Sea Research Part II 101:1–254. HAB research. Oceanography 18(2):148–157, E. Berdalet, C. Edwards, P. Franks, and O. Ross, Turner, E., D.B. Haidvogel, E.E. Hofmann, https://doi.org/10.5670/oceanog.2005.50. eds, IOC and SCOR, Paris and Newark, Delaware, H.P. Batchelder, M.J. Fogarty, and T. Powell. Anderson, D.M., B.A. Keafer, J.L. Kleindinst, 85 pp. 2013. US GLOBEC: Program goals, approaches, D.J. McGillicuddy, J.L. Martin, K. Norton, GEOHAB. 2012. Global Ecology and Oceanography and advances. Oceanography 26(4):12–21, C.H. Pilskaln, J.L. Smith, C.R. Sherwood, and of Harmful Algal Blooms, Core Research Project: https://doi.org/10.5670/oceanog.2013.72. B. Butman. 2014. Alexandrium fundyense cysts in Harmful Algal Blooms in Benthic Systems. Wells, M.L., V.L. Trainer, T.J. Smayda, B.S. Karlson, the Gulf of Maine: Long-term time series of abun- E. Berdalet, P. Tester, and A. Zingone, eds, IOC and C.G. Trick, R.M. Kudela, A. Ishikawa, S. Bernard, dance and distribution, and linkages to past and SCOR, Paris and Newark, 64 pp. A. Wulff, D.M. Anderson, and W.P. Cochlan. 2015. future blooms. Deep Sea Research Part II 103:6–26, GEOHAB. 2013. Global Ecology and Oceanography Harmful algal blooms and climate change: Learning https://doi.org/10.1016/​j.dsr2.2013.10.002. of Harmful Algal Blooms, GEOHAB Core Research from the past and present to forecast the future. Babin, M., C.S. Roesler, and J.J. Cullen, eds. 2008. Project: HABs in Stratified Systems. Workshop on Harmful Algae 49:68–93, https://doi.org/10.1016/​ Real-Time Coastal Observing Systems for “Advances and Challenges for Understanding j.hal.2015.07.009. Marine Ecosystem Dynamics and Harmful Algal Physical-Biological Interactions in HABs in Stratified Blooms: Theory, Instrumentation and Modelling. Environments.” M.A. McManus, E. Berdalet, J. Ryan, Oceanographic Methodology series, UNESCO, H. Yamazaki, J.S. Jaffe, O.N. Ross, H. Burchard, and ACKNOWLEDGMENTS Paris, 830 pp. F.P. Chavez, eds, IOC and SCOR, Paris and Newark, We thank the many participants who have contrib- Berdalet, E., M.A. McManus, O.N. Ross, H. Burchard, Delaware, USA, 88 pp. uted to GEOHAB over the lifetime of the program, F.P. Chavez, J.S. Jaffe, I.R. Jenkinson, R. Kudela, Glibert, P.M., R. Azanza, M. Burford, K. Furuya, and in particular the 36 Science Steering Committee I. Lips, U. Lips, and A. Lucas. 2014. Understanding E. Abal, A. Al-Azri, F. Al-Yamani, P. Andersen, members who provided their time, ideas, and enthu- harmful algae in stratified systems: Review D.M. Anderson, J. Beardall, and others. 2008. siasm to make GEOHAB a success. Funding, pro- of progress and future directions. Deep Sea Ocean urea fertilization for carbon credits grammatic support, and guidance were provided by Research Part II 101:4–20, https://doi.org/10.1016/​ poses high ecological risks. SCOR, IOC, and IPHAB with significant support from j.dsr2.2013.09.042. Bulletin 56(6):1,049–1,056, https://doi.org/10.1016/​ the US National Science Foundation, the US National Bernard, S., R. Kudela, and L. Velo-Suárez. 2014. j.marpolbul.2008.03.010. Oceanic and Atmospheric Administration, and the Developing global capabilities for the observation Glibert, P.M., J.M. Burkholder, E. Granéli, and European Commission. and prediction of harmful algal blooms. Pp. 46–52 D.M. Anderson. 2008. Advances and insights in Oceans and Society: Blue Planet. S. Djavidnia, in the complex relationships between eutrophi- V. Cheung, M. Ott, and S. Seeyave, eds, Cambridge AUTHORS cation and HABs: Preface to the special issue. Raphael M. Kudela ([email protected]) is Professor, Scholars Publishing. Harmful Algae 8:1–2, https://doi.org/10.1016/​ Ocean Sciences Department, University of California Bravo, I., R.I. Figueroa, and S. Fraga. 2014. Cellular j.hal.2008.08.020. Santa Cruz, Santa Cruz, CA, USA. Elisa Berdalet is and nuclear morphological variability within a sin- Glibert, P.M., M. Zhou, M. Zhu, and M.A. Burford. 2011. Tenured Scientist, Institute of Marine Sciences (CSIC), gle species of the toxigenic dinoflagellate genus Preface to the special issue on eutrophication and Barcelona, Catalonia, Spain. Henrik Enevoldsen Gambierdiscus: Relationship to life-cycle pro- HABs: The GEOHAB approach. Chinese Journal is Intergovernmental Oceanographic Commission cesses. Harmful Algae 40:1–8, https://doi.org/​ of Oceanology and Limnology 29(4):719–723, (IOC) UNESCO Programme Coordinator, IOC of 10.1016/j.hal.2014.09.009. https://doi.org/10.1007/s00343-011-0501-0. UNESCO, IOC Science and Communication Centre Estrada, M., J. Solé, S., Anglès, and E. Garcés. 2010. Granéli, E., B. Sundström, L. Edler, and D. Anderson, on Harmful Algae, University of Copenhagen, The role of resting cysts in Alexandrium minu- eds. 1990. Toxic Marine Phytoplankton: Copenhagen, Denmark. Grant Pitcher is a researcher tum population dynamics. Deep-Sea Research Proceedings of the Fourth International in the Fisheries Research and Development Branch, Part II 57:308–321, https://doi.org/10.1016/​ Conference on Toxic Marine Phytoplankton, Held Department of Agriculture, Forestry and Fisheries, j.dsr2.2009.09.007. June 26–30, 1989, in Lund, Sweden. Elsevier, Cape Town, . Robin Raine is Professor, European Commission. 2013. The EU-US Scientific , 576 pp. Earth and Ocean Sciences, National University of Initiative on Harmful Algal Blooms: A Report from HARRNESS. 2005. Harmful Algal Research and Ireland, Galway, Ireland. Ed Urban is Executive a Workshop Jointly Funded by the European Response: A National Environmental Science Director, Scientific Committee on Oceanic Research, Commission – Environment and Sustainable Strategy 2005–2015. J.S. Ramsdell, D.M. Anderson, University of Delaware, Newark, DE, USA. Development Programme and the US National and P.M. Glibert, eds, Ecological Society of Science Foundation. EUR 20578, https://cordis. America, DC, 96 pp. europa.eu/pub/sustdev/docs/environment/ ICES. 2013. Report of the ICES/PICES/IOC-GEOHAB ARTICLE CITATION ki-na-20578-en-c_eu-us_algal_blooms.pdf. Workshop on Harmful Algae Blooms in a Changing Kudela, R.M., E. Berdalet, H. Enevoldsen, G. Pitcher, Furuya, K., P.M. Glibert, M. Zhou, and R. Raine. 2010. World (WKHABCW), March 18–22, 2013, Friday R. Raine, and E. Urban. 2017. GEOHAB–The Global GEOHAB Asia. Global Ecology and Oceanography Harbor Laboratories, USA. ICES CM 2013/ Ecology and Oceanography of Harmful Algal of Harmful Algal Blooms in Asia: A Regional SSGHIE:01, 13 pp. Blooms Program: Motivation, goals, and legacy. Comparative Programme. IOC and SCOR, Karl, D.M., J.E. Dore, R. Lukas, A.F. Michaels, Oceanography 30(1):12–21, https://doi.org/10.5670/ Baltimore and Paris, 68 pp. N.R. Bates, and A. Knap. 2001. Building the long- oceanog.2017.106. GEOHAB. 2001. Global Ecology and Oceanography term picture: The US JGOFS time-series programs. of Harmful Algal Blooms: Science Plan. P. Glibert Oceanography 14(4):6–17, https://doi.org/10.5670/ and G. Pitcher, eds, SCOR and IOC, Baltimore and oceanog.2001.02. Paris, 86 pp.

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