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CITATION Berdalet, E., M. Montresor, B. Reguera, S. Roy, H. Yamazaki, A. Cembella, and R. Raine. 2017. Harmful algal blooms in fjords, coastal embayments, and stratified systems: Recent progress and future research. Oceanography 30(1):46–57, https://doi.org/​ 10.5670/oceanog.2017.109.

DOI https://doi.org/10.5670/oceanog.2017.109

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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Harmful Algal Blooms in Fjords, Coastal Embayments, and Stratified Systems Recent Progress and Future Research

By Elisa Berdalet, ABSTRACT. Harmful algal blooms (HABs) are natural phenomena that result from the Marina Montresor, interplay of biological, chemical, physical, and sedimentary processes occurring at different Beatriz Reguera, temporal and spatial scales. This paper provides an integrated description of HAB dynamics Suzanne Roy, occurring at the mesoscale (10–100 km, sensu Haury et al., 1978) in confined and semi-confined Hidekatsu Yamazaki, coastal environments and under stratified water column conditions in a diversity of habitats where HAB events occur. It also focuses on relevant aspects occurring at the fine scale and even Allan Cembella, smaller cellular scales that are critical to species interactions with their environments. Examples and Robin Raine include the key role of life-history stages in the recurrence of HABs in certain embayments; the physical-biological interactions driving the formation, maintenance, and decline of thin layers of , including harmful ; the fascinating, but poorly understood, domain of small-scale chemical interactions between HAB species and components of the ; and the potential link between human activities and and the trends in HAB occurrence. Development of new observing and sampling technologies and of new modeling approaches has resulted in greater understanding of these phenomena. We summarize the scientific achievements of two Core Research Projects initiated under the GEOHAB Implementation Strategy, “HABs in Fjords and Coastal Embayments” and “HABs in Stratified Systems,” and outline the priorities for future research toward improving the management and mitigation of HAB impacts.

Aquaculture activities are often located in enclosed and semi-enclosed embayments, such as shown here in Killary Harbor, Ireland. HAB outbreaks can cause sub- stantial economic loss and problems for human health. Photo credit: Caroline Cusack, Marine Institute

46 Oceanography | Vol.30, No.1 Complex hydrodynamic processes (estuarine circulation, wind mixing, tidal dynamics, salinity, and thermal stratification) and pelagic-benthic coupling “ can play a major role in the dynamics of HABs in [confined or semi-confined coastal] systems. .

INTRODUCTION often heavily occupied by human pop- www.globalhab.info; Berdalet et al.,” 2017, A major goal of the research conducted ulations whose activities not only foster in this issue). This paper is also a trib- worldwide over the past two decades HABs but are then negatively affected by ute to our colleague and friend Patrick within the framework of the Global their consequences. Gentien, who passed away in 2010. Ecology and Oceanography of Harmful The Strat-HAB CRP (Gentien et al., Patrick inspired and fostered research Algal Blooms (GEOHAB) program 2005; GEOHAB, 2008) was a cross- on the fine- and small-scale processes has been to achieve a deeper under- cutting theme focused on understanding involved in HAB dynamics. standing of HAB dynamics and bio- small-scale hydrographic features that geography. This objective was addressed are encountered in virtually all aquatic LIFE-HISTORY STRATEGIES by linking the strategies implemented systems, including upwelling areas, OF HARMFUL SPECIES IN within various Core Research Projects fjords, and coastal regions and bays, CONFINED AND SEMI-CONFINED (CRPs). Among the CRPs, the projects whether or not they are affected by eutro- ENVIRONMENTS on “Harmful Algal Blooms in Fjords phication. A particular emphasis was on Although HAB species thriving in fjords and Coastal Embayments” (F&CE-HAB) thin layers (TLs), where many harm- and coastal embayments are not gener- and “Harmful Algal Blooms in Stratified ful organisms can thrive, ally specific to these environments, an Systems” (Strat-HAB) provided an ideal and on rheological properties. In addi- exception could be the harmful brown template for data integration and created tion, technological and modeling chal- tides of the pelagophytes Aureococcus novel syntheses based on observations in lenges to resolve biological and physi- anophagefferens and Aureoumbra lagun- comparative systems that were stratified cal interactions at fine and small scales ensis. Blooms of these species reported and hydrographically constrained. were tackled (GEOHAB 2011, 2013; from enclosed systems are character- The F&CE-HAB CRP (Cembella et al., Berdalet et al., 2014). ized as thriving in high organic nutri- 2005; GEOHAB 2010, 2013) focused on Based on the state of knowledge of ent concentrations (Gobler and Sunda, coastal systems that are partially sur- their themes, the two CRPs addressed 2012). The fish-killingAureococcus can rounded by land and thus affected by specific key questions (GEOHAB, 2008, attain high biomass levels when inor- land-sea interactions (runoff, sediment 2010) identified by the participants at ganic nutrient concentrations are low dynamics) operating at spatial scales Open Science Meetings held prior to the because it can utilize organic forms of much smaller than those in open coastal launch of each CRP. Details presented carbon, nitrogen, and , and or upwelling systems. Complex hydro- in the GEOHAB CRP reports, includ- produce allelochemicals (biologically dynamic processes (estuarine circulation, ing mid-term and final program reviews, active compounds that elicit specific wind mixing, tidal dynamics, salinity, are openly available (http://www.geohab. responses in target organisms) that harm and thermal stratification) and pelagic- info). Processes occurring at submeso­ its potential predators. benthic coupling can play a major role scale as well as fine and small physi- In confined and semi-confined areas, in the dynamics of HABs in these sys- cal scales (Figure 1) are common fea- recurrent or chronic infestations of HAB tems. Fjords and coastal bays often act tures of both CRPs. For this reason, the species can develop as a consequence as “seed beds” for benthic cysts or rel- achievements of both CRPs are presented of the life-history strategy to produce ict populations of HAB species when together in this article, along with some benthic resting stages. During the past there is limited water exchange with open future research priorities to be addressed decade, there has been a major effort to coastal waters. Such coastal habitats are by the new GlobalHAB program (http:// understand the life histories of the main

Oceanography | March 2017 47 HAB species that rely on resting stages. As de Souza et al., 2015). They allow the such as resuspension, encystment, and a result of major technological advances, organisms to occupy different ecological germination rates and oxygen levels in we now have better insights into different niches in the water column (holoplank- the sediment (reviewed in Azanza et al., life forms, not always clearly associated tonic species), and also in the benthos in press). Díaz et al. (2014a) observed a with different morphologies, and their (meroplanktonic species). Benthic rest- very rapid depletion of cysts from the functionality (e.g., Brosnahan et al., 2015; ing cysts can be a safety mechanism for a sediments (<3 months), suggesting that see section below). Complex life cycles planktonic cell population driven to vir- resting cyst deposits play a minor role in involving vegetative cells, a sexual phase, tual extinction at the end of the bloom- the recurrence of blooms of PSP-causing and temporal and resting cysts have ing period (Estrada et al., 2010). In addi- Alexandrium catenella along the southern been described for many tion, cyst beds are known to play key Chilean coast. (Figures 1 and 2; Kremp, 2013; Bravo and roles in the recurrence of the blooms Furthermore, the intensity of some Figueroa, 2014). Although resting stage in certain cases. For instance, in open Alexandrium spp. blooms in inshore formation has not been reported in spe- coastal waters and at a wide spatial scale, bays apparently does not depend on cyst cies of the potentially toxigenic cyst distribution patterns of the dinofla- distribution or abundance (Cosgrove Pseudo-nitzschia (Montresor et al., 2013), gellate Alexandrium fundyense, which et al., 2014; Ralston et al., 2014). These sexual events required for the formation is the source of paralytic poi- blooms are determined by a combination of large-sized cells occur during blooms soning (PSP), have been linked to inter- of retention of vegetative cells behind (Figure 3). In this genus, laboratory stud- annual variability in the intensity and bathymetric barriers (shallow sills), daily ies indicate that sex is a cell density- extension of the blooms of this species vertical migration, and temperature that dependent mechanism (as reviewed by (McGillicuddy et al., 2011). Anderson controls cell division rates (Crespo et al., Montresor et al., 2016). et al. (2014) developed a model for empir- 2011). In the case of the tropical and sub- The different life forms provide alter- ical forecast of the geographic extent of a tropical dinoflagellatePyrodinium baha- native adaptive strategies in response to forthcoming bloom based on cyst abun- mense, the most common cause of PSP nutrient availability, dispersion avoid- dances. However, this link varies among in the and in Southeast Asia, ance, and protection against grazers species and habitats, and interpretation blooms are inoculated by cyst germi- and parasites (Fistarol et al., 2004; Alves is complicated by many natural factors, nation in small tropical bays but not in open coastal waters. Vegetative cells and cyst densities of P. bahamense seem to be governed primarily by the monsoons that may disperse them (Azanza, 2013). In shallow systems, P. bahamense often undergoes several cycles of transforma- tion between pellicle cysts and vegetative cells during a single bloom period (Onda et al., 2014). A major challenge is to char- acterize the transition between the par- ticular life-history phases in natural hab- itats (e.g., Ní Rathaille and Raine, 2011). This requires a sound understanding of the biological and environmental fac- tors that control the life-history phases and their transitions. For instance, in the case of cysts, physical and sedimen- tary processes, such as resuspension from the bottom layer by bottom cur- rents or sediment dredging, may play a greater role than previously suspected. The initiation of A. fundyense blooms along the eastern US coast seems to be FIGURE 1. Submesoscale to small-scale processes relevant to understanding of HAB dynamics in linked to the resuspension of cysts from confined and semiconfined environments. (A) Physical forcings important to the confinement or dis- persion of the cells. Redrawn from Reguera et al. (2012). (B) Thin layer formation. (C) Life history of a benthic nepheloid layers (reviewed in .Redrawn from Bravo and Figueroa (2014). The diatom life cycle is shown in Figure 3. Azanza et al., in press).

48 Oceanography | Vol.30, No.1 Life-history strategies can also display intraspecific genetic diversity, as recently revealed using molecular tools. This diversity could reflect unique life-cycle properties that are responding to environmental variability or ecological pres- sures, and/or different germination timing of the cyst pool in the sediments. For example, genetically distinct populations within the species A. fundyense coexist in the same coastal ponds but bloom at different times (e.g., Richlen et al., 2012). Analysis of rRNA transcripts allowed reconstruction of the demographic history of two genetically different A. minutum populations, where an ancestral divergence was followed by FIGURE 2. Resting cysts of two dinoflagellates,Alexandrium mediterraneum (left) and Gymnodinium nolleri (right). Photo credits: M. Montresor, SNZ a secondary contact of the two populations, resulting in gene flow (Le Gac et al., 2016). Moreover, functional differences between the two groups were identified, linked to calcium A C and potassium fluxes across membranes, the calcium trans- duction signal, and production. These studies are examples of how population genetics coupled with genomic approaches can shed light on the mechanisms that lead to population differentiation and structure in space and time (reviewed in Rengefors et al., 2017).

PHYSICAL FACTORS IN HAB DYNAMICS WITHIN 50 µm ENCLOSED AND SEMI-CONFINED BASINS Many HAB events are caused by the bulk transport of cells B from nearshore waters into semi-confined basins. Wind- driven water exchange occurs in many northwestern European bays because they are axially aligned to the pre- vailing southwestern wind direction (Raine et al., 2010). In combination with water column stratification, potentially harmful phytoplankton populations are advected into the bays either with the influx of cool bottom water, as has been observed with mikimotoi (a fish-killing dinoflagel- 20 µm late at high cell densities), or with the subsequent influx of FIGURE 3. (A) Early-stage Pseudo-nitzschia auxospores (arrows; i.e., the dip- warm surface water, a situation more typical of blooms of loid stage produced by gamete conjugation) in a natural phytoplankton lipophilic, -producing Dinophysis species that cause sample. (B) One auxospore still connected to the frustule of the gametan- diarrhetic shellfish poisoning (DSP; Raine, 2014). gium. (C) Schematic drawing of the life cycle of a Pseudo-nitzschia. The sexual phase can be induced when cells of opposite mating types con- Once inside confined and semi-confined environments, tact one another. It includes gametogenesis, syngamy, and forma- cells can be retained or dispersed by different physical fac- tion of a specialized zygote, the auxospore, where the large initial cell tors. For instance, in the microtidal of Alfacs Bay is produced. (A) and (B) photo credits: M. Montresor. (C) Redrawn from Montresor et al. (2016) (northwest ), an active aquaculture site threatened by HAB events (Fernández-Tejedor et al., 2008), phytoplankton accumulation occurs preferentially in the often stratified environments that can act as plankton “incubators” northeastern part of the estuary throughout the year (Artigas (including HAB species) are the “upwelling shadows” developed et al., 2014). Cell retention is determined by the interplay adjacent to the landward side of promontories and within bays, between freshwater input from land (irrigation of the sur- where surface wind forcing is relatively weak and retentive oceanic rounding rice fields and submarine groundwater discharge) circulation develops (e.g., Ryan et al., 2010). and wind-induced turbulence that controls the strength of In addition to hydrodynamics, bay morphology in association the estuarine circulation and vertical stratification. Weak with freshwater inputs of nutrients and humic acids (see section stratification facilitates cell retention, whereas flushing rates below on nutrients) modulates phytoplankton biomass, produc- are higher during increased stratification and stronger estu- tivity, and community structure in semi-confined systems (Raine arine flow periods. These mechanisms apply to harmful spe- et al., 2010). The aquaculture sites in Alfacs and Fangar Bays of cies as well as other planktonic organisms. Other retentive, the Ebro Delta in the northwest Mediterranean provide a case

Oceanography | March 2017 49 study related to morphology. Llebot et al. brown tides caused by the pelagophyte introduction of cyst-forming alien species (2011) characterized the seasonal pat- Aureococcus anophagefferens in are among the features linked to aqua- terns of phytoplankton community vari- and bays of the eastern United States and culture that can alter the marine environ- ability in both bays and their coupling (Gobler and Sunda, 2012), ment and favor HAB blooms, especially with environmental forcing based upon and the local blooms of the Alexandrium in confined environments. Determining a 13-year time series. Plankton dynamics catenella/tamarense species complex in the possible links between marine aqua- in the two bays was subjected to the typi- Thau lagoon, southern France (Collos culture and HAB occurrence, and find- cal climatology of the Mediterranean Sea et al., 2014). Nutrients can reach coastal ing efficient methods to protect farmed and local meteorological forcing. Alfacs embayments through both direct runoff seafood products from HABs impacts, is Bay receives lower nutrient inputs than and submarine groundwater discharges. one of the objectives included in the new Fangar Bay. However, Alfacs Bay is about In Alfacs Bay, this process could deliver program on HAB research, GlobalHAB 10 times larger and thus has a longer res- a nutrient supply from the surrounding (http://www.globalhab.info). idence time than Fangar Bay, which has rice fields in periods when direct run- Ship ballast water discharge near or higher flushing rates. The resulting cir- off from irrigation channels is artificially within harbors and in other coastal envi- culation patterns, turbulence inten- restricted (Rodellas et al., 2017). ronments also contributes to harm- sity, and stratification in each bay deter- Nutrient availability can play an ful microalgal transfer worldwide (Roy mine the typically higher phytoplankton important role in determining the nature et al., 2012). Efforts have been invested biomass levels in Alfacs Bay compared and degree of harmful effects. For exam- in the last decade to prevent such inva- to Fangar Bay. ple, the toxicity of Pseudo-nitzschia sive species introductions (e.g., see blooms was heightened during the late International Convention for the Control NUTRIENT SUPPLY FROM LAND, phases of blooms under certain nutrient-​ and Management of Ships’ Ballast Water HUMAN ACTIVITIES, AND HABS limited conditions (e.g., phosphorus and Sediments; IMO, 2017). However, IN COASTAL EMBAYMENTS limitation; Timmerman et al., 2014). predicted increases in global shipping Land-sea interactions directly affect Furthermore, uncoupling between cell highlight the need to continue efforts to coastal ecosystems, which are often under division and toxin production rates decrease the risk of aquatic species inva- disruptive pressure from human activi- resulted in maximal cell-toxin quota sions, including those of HAB taxa, into ties that varies with the degree and type during the stationary growth phase of new habitats. of land and water uses. Increased nutrient Dinophysis populations (Pizarro et al., supply has been linked with high phyto- 2009). Still, the link between nutri- INTERPLAY BETWEEN PHYSICAL plankton biomass and eutrophic con- ent availability and toxicity shows AND BIOLOGICAL PROCESSES IN ditions in many bays (e.g., GEOHAB, unclear trends and requires further THE DYNAMICS OF THIN LAYERS 2010). This is illustrated, for instance, by intensive research. AND AT SMALL SCALES the positive correlation between nitro- Fish farms and other aquaculture Thin layers are discontinuities in the ver- gen loads and the relative abundance of activities that represent important food tical structure of the wind-mixed surface Pseudo-nitzschia pungens in the 100-year sources for the increasing human pop- layer of a stratified water column that record of from sediment cores in ulation, especially in developing coun- exhibit physical, chemical, and biological a Danish fjord (Lundholm et al., 2010). tries, are often located in enclosed and signatures distinct from the surrounding However, establishing a definitive causal semi-enclosed embayments. HAB out- water. Lasker (1978) was the first to pro- link between an increase in HABs and a breaks can dramatically affect these pose that TLs play a major trophic role in change in either nitrogen or phosphorus activities, causing substantial economic aquatic ecosystems because they favor an as the limiting nutrient is not usually pos- losses and problems for human health. abundance of planktonic organisms and sible (Davidson et al., 2012). Considerable research has addressed the thus satisfy the growth requirements of Traditionally, research on nutrient implementation of effective monitor- fish larvae. Plankton TLs can persist for concentrations and fluxes has mainly ing programs for HAB species and their days or longer (McManus et al., 2003), focused on the inorganic nutrient forms . However, limited information is with horizontal length scales on the order (i.e., , , and silicate). available on the potential effects of aqua- of kilometers and vertical extents from However, recent studies show the impor- culture activities on the geographic distri- several meters to millimeters. tance of organic nutrient sources, includ- bution, frequency, and intensity of HABs The understanding of HAB dynamics ing (coming from agricultural fertil- (e.g., Bouwman et al., 2013). Increased changed when advances in sampling and izers) and humic acids (e.g., GEOHAB, inorganic and organic nutrient load- observational methods revealed that TL 2010). For instance, HAB associations ing, application of pharmaceuticals and structures are important to HAB ecology with high organic nutrients include the pesticides to the local environment, and (Figures 1B and 4; Gentien et al., 2005).

50 Oceanography | Vol.30, No.1 Some harmful microalgae can concen- conditions and the vertical structure of generation of TLs. Regions of enhanced trate into TLs; examples include the dino- the water column, including depth and shear could disrupt vertical migrations flagellatesKarenia mikimotoi (also known gradient definition of the pycnocline. of plankton cells and promote sharp- as Gyrodinium aureolum), Akashiwo san- Several niches could also exist across peaked cell accumulations. Besides, guinea (high biomass bloom-forming the pycnocline in which different phyto- pycnoclines may act as retention areas for species, also known as Gymnodinium plankton may be found (i.e., resulting in non-​swimming phytoplankton, such as sanguineum), and Dinophysis spp., as “a thin layer within a thin layer”; Raine, Pseudo-nitzschia and other diatoms. The well as diatoms in the genus Pseudo- 2014, and references there in). In coastal respective TLs of these Pseudo-nitzschia nitzschia (revised in Gentien et al., 2005; waters around Ireland, fine-scale sam- blooms have been observed in associa- Berdalet et al., 2014). pling led to the observation of mixed tion with steep density gradients in the TL dynamics involves interactions populations of D. acuminata and D. ovum Northeast Pacific Ocean and in Monterey between fine-scale physical, chemical, in a high-density layer (40,000 cells L–1) Bay (Rines et al., 2002) and in pycnoclines and biological processes, as illustrated of thickness ca. 30 cm within a 3 m thick established after upwelling pulses in the in the conceptual model presented in subsurface layer of D. acuta, at a density Galician Rias (Velo-Suárez et al., 2008). Figure 5. Biological processes that pro- of ca. 104 cells L–1. Eddies can also facilitate formation mote the accumulation of phytoplank- Gradients in turbulence and verti- and persistence of TLs by minimizing lat- ton in TLs include enhanced growth rate, cal shear are important physical con- eral dispersion of plankton populations. active aggregation by swimming and/or trols in the formation and persistence of In this way, the Juan de Fuca Eddy acted buoyancy control, and grazer avoidance TLs (Dekshenieks et al., 2001; Ryan et al., as an incubator for Pseudo-nitzschia pop- within the layer. 2008; Durham et al., 2009). Vertical shear ulations that were then transported to the For instance, swimming seems to tends to tilt and stretch an existing phyto- coast (Trainer et al., 2002). have played a major role in the accu- plankton patch, as one part moves hor- The high abundances of these diatoms mulation of Akashiwo sanguinea in a TL izontally relative to a deeper part of the caused a quick rise to above regulatory observed in Monterey Bay (Steinbuck water column. Furthermore, gyrotactic levels in the content of the et al., 2009). High cell densities of this trapping (Durham et al., 2009) couples in shellfish from the area. dinoflagellate were located in the thermo- biological processes (active swimming Persistent eddies in the Bay of Biscay have cline of a 20.5 m water column between of cells) and hydrodynamic shear in the been involved in the local accumulation a strongly turbulent surface mixed layer and a weakly turbulent stratified inte- (A) Fluorescence rior. Swimming balanced the diffusion 0 by turbulent mixing on both sides of 100 the layer, while sinking or growth pro- 80 cesses were not major drivers. The study 5 combined high-resolution sampling, an 60 Eulerian advection-diffusion model, and Depth (m) 40 a Lagrangian particle-tracking model. A 10 combination of vertical migration and 1 km 20 phototaxis may also create a TL, as shown 0 by a numerical model that produces real- (B) Salinity istic mixing and turbulent conditions 0 30 (Yamazaki et al., 2014). In the systems described, TL formation would occur at 25 –1 wind speeds below 5 m s . 5 Although TL formation can be facili- 20 tated by vertical migration (due to photo- Depth (m) taxis, nutrient availability, or other trig- 10 1 km 15 gers such as reproduction, sexual and asexual encystment rhythms, and water- 10 35.58 35.59 35.60 35.61 35.62 35.63 borne chemical cues), this behavior seems Latitude to be species- and location-specific.​ The FIGURE 4. Representative profiles of salinity and fluorescence in a stratified system with a well- vertical distribution of the same species developed thin layer. (A) Fluorescence and (B) salinity observed on May 19, 2011, in Tokyo Bay. From likely varies according to physiological Masunaga and Yamazaki (2014)

Oceanography | March 2017 51 Organism Growth Grazing Dispersion Current identification of the chemical struc- Abundance Rate Organics Mortality Losses Velocity tures of one class of these waterborne A B C D E F cues known as copepodamides (Selander et al., 2015), supports a defensive func- tion for these . Depth Chemically mediated species inter- actions within the plankton are com- Density plex, but we do know how they can be Immigration Resources Rate n1 & n2 regulated at the gene level. For instance, Alexandrium populations comprise mul- FIGURE 5. General conceptual model of mechanisms controlling thin layers. Credit: P.L. Donaghay tiple genotypes that display phenotypic variation for traits such as the ability to of Dinophysis acuminata and K. mikimo- the night. Physical dispersion is, doubt- lyse co-occurring competitors and poten- toi in the pycnocline (Patrick Gentien, less, a key factor contributing to the col- tial grazers. In laboratory experiments, data unpublished before his death; Xie lapse of TLs, but the natural life processes exposure of two A. fundyense strains et al., 2007). These structures protect the of plankton must be involved as well. For to the presence of Polykrikos kofoidii integrity of the HAB species patch until instance, processes inducing cell encyst- (a dinoflagellate grazer) induced differ- the eddy disperses at the coast and the ment could cause the decay of dinofla- ential transcriptomic changes in gene HAB organisms within it are released and gellate populations within the TLs. These expression (Wohlrab et al., 2016). The thereby cause harm. processes are still speculative. More stud- affected genes are involved in endocytotic Local reduction in horizontal and ies are required to improve understand- processes, cell cycle control, and outer vertical dispersal can facilitate the for- ing of the formation, maintenance, and membrane properties, and the observed mation of small (7 km in diameter and decay of harmful phytoplankton TLs. trends suggest different competitive about 3 m thickness at 20 m depth) but capacities at the strain level. high-density patches of Dinophysis acuta BIOLOGICAL AND Allelochemistry and chemically medi- cells (104–105 cells L–1) in open waters off CHEMICAL INTERACTIONS ated species interactions may play an southern Ireland (Farrell et al., 2012). AT SMALL SCALES important role in the dynamics of HABs In some cases, TLs seem to be quite Chemical cues mediate interactions within spatially constrained fjords and dynamic structures that can be formed between marine micro- and metazoan embayments, notably at small scales, par- and eroded rapidly. After moderate grazers and their prey, and allelochem- ticularly within TLs occurring at sharp upwelling pulses in the Galician Rias, a ical (and/or toxic) substances pro- density discontinuities (e.g., pycnocline Pseudo-nitzschia TL was formed by shear, duced by various HAB taxa could con- interfaces). Trophic interactions between which favored passive aggregation of cells stitute defenses against predators and different components of plankton food in the pycnocline. The TL was eroded competitors and regulate other species webs are likely to be particularly active during the next downwelling period and interactions (reviewed by Ianora et al., in TLs. For example, feed- formed again in the subsequent upwell- 2011). Such “top-down” interactions ing could be higher in high phytoplank- ing pulse (Díaz et al., 2014b). Likewise, could modulate the equilibrium among ton density TLs compared to most parts a downwelling event eroded a TL of a species and hence affect both species- of the water column where there are senescent diatom community where specific population dynamics and com- lower food concentrations. Given the P. australis was dominant (Velo-Suárez munity structure. Known responses of high cell density of particular species et al., 2008). Yamazaki et al. (2010) char- toxic dinoflagellates exposed to meta- within a TL, sexual recombination rates acterized the layered structures of small- zoan predators (i.e., copepods) or their would be facilitated due to an increased scale biophysical signals within a 24-hour waterborne chemical cues include ini- gamete encounter rate (Wyatt and period at a station in Lake Biwa (Japan). tiation of life-history transitions, col- Jenkinson, 1997; Persson et al., 2013), Using an LED fluorescence probe ony size changes, and alterations in and interactions between harmful micro­ mounted on TurboMAP-L, the study swimming behavior to escape preda- and bacteria, parasites, or showed the dynamic formation and dis- tion. The induction and increase of PSP may also exhibit particular dynamics. sipation of chlorophyll TLs in the water toxin (saxitoxin analogs) production by Unfortunately, these interactions have column, within the surface mixed layer. A. minutum and A. tamarense/fundyense been mainly described in the laboratory While the study was being conducted, the exposed to copepods and/or to their over the last 20 years (e.g., Kiørboe, 2010) turbulent kinetic energy dissipation rate chemical signals (Wohlrab et al., 2010; and are only rarely documented in the (ε) reached almost 10–6 W kg–1 during Selander et al., 2015), and the recent field (Alldredge et al., 2002; Timmerman

52 Oceanography | Vol.30, No.1 et al., 2014). There is a need to incentiv- blooms. Microalgae may have mecha- Advances in sampling and observa- ize progress and utilization of technolo- nisms to make the water more viscous by tion methods have been fundamental to gies to directly observe plankton behav- generating loose or sticky EPS, to engi- understanding TL structure and dynam- ior in situ within and around the edges of neer ambient fluidics to protect them- ics. Traditional bottle sampling at fixed TLs in stratified systems. Semi-confined selves from predators, and to favor nutri- depths is inefficient and often completely systems, given the relative physical con- ent diffusion (Jenkinson et al., 2015). misses TLs (Escalera et al., 2012). Satellite straints on advection and dispersion of Furthermore, EPS production can con- remote-sensing detection of subsurface blooms, offer suitable conditions for this stitute another harmful effect of some structures is restricted to waters with spe- challenging investigation in the future. high-biomass blooms. A surfactant-like cific properties. In the last 15 years, tech- Other understudied processes oper- protein in the organic matter released nologies have progressed to allow fine- ating at micro- and nanoscales may also by a dense, senescent-phase bloom of scale vertical resolution monitoring of play roles in HAB dynamics. During Akashiwo sanguinea occurring along the essential phytoplankton properties (chlo- recent decades, studies have been west coast of the United States (Jessup rophyll fluorescence, absorption, or bio- devoted to investigating the direct impact et al., 2009) coated birds that encoun- luminescence) and direct sampling of of small-scale turbulence on harmful tered the bloom-generated foam. This cells and certain key physical parame- phytoplankton cells. Observed effects caused loss of the insulating capacity of ters (GEOHAB, 2008, 2013, and refer- include facilitation of nutrient uptake, the birds’ feathers and led to mortality by ences therein). Examples of such tech- and in certain dinoflagellates, physio- hypothermia. nologies include the fine-scale sampler logical responses include inhibition of (FSS; Lunven et al., 2005; Figure 6) capa- cell division, decrease of cell toxin con- ADVANCES IN TECHNOLOGY ble of taking 15 samples, 20 cm apart, centration, increase in dimethylsulfonio- AND MODELING over a vertical distance of 3 m, and the propionate (DMSP) content, or alteration Major advances in knowledge of the life high-​resolution Ifremer Particle Size of swimming patterns (e.g., Berdalet history of HAB species dwelling in con- Analyzer Profiler (IPSAP; Lunven et al., et al., 2011, and references therein). fined and semi-confined environments 2005; Figure 6) that combines par- Reduced turbulence (within a TL or and stratified systems have been achieved ticle size analysis with microphoto- not) may promote some life-cycle transi- in recent years thanks to sophisticated graphic video. Tow-body systems such tions (pellicle cyst formation; e.g., Smith moored instruments. For example, the as the SCANFISH (undulating CTD) and Persson, 2005; Gentien et al., 2007) original Flowcytobot, capable of fixed- and Acrobat (SeaSciences), and autono- that are otherwise inhibited under high-​ depth, high-resolution imaging of dif- mous underwater vehicles (AUVs) like agitation conditions. ferent life-cycle stages during blooms of the Monterey Bay Aquarium Research Important research efforts have been Alexandrium and Dinophysis has now Institute Dorado, have been used to designed to understand how viscosity been developed into a yo-yo system that quantify the horizontal extent of thin and other rheological properties influ- records the whole water column in shal- phytoplankton layers on scales of 1 km ence, and are influenced by, several low embayments (Campbell et al., 2010; to 100 km. New modeling tools have aspects of plankton dynamics, including Brosnahan et al., 2015). been fundamental to understanding of HABs (e.g., Jenkinson and Sun, 2010). Dense phytoplankton patches are often associated with increased viscosity as well as elasticity of the sea­water or fresh- water medium. Based on the knowl- edge gained, including the few available measurements of rheological properties of some algal cultures and phytoplank- ton blooms, models have been proposed to describe how organic exopolymeric substances (EPS) could change pyc- nocline thickness. The studies empha- size the need for new measurements under natural oceanic concentrations as well as future experimental and in situ FIGURE 6. (left) Fine Scale Sampler (Ifremer). (right) Patrick Gentien sets up the Ifremer Particle Size investigations into the modulation of Analyzer Profiler during the HABIT 2005 cruise on board pycnocline dynamics by phytoplankton R/V Mytilus (CSIC, Spain). Photo credit: B. Reguera

Oceanography | March 2017 53 TL dynamics (GEOHAB, 2011, 2013). sufficient exposure time. The result sup- interactions (Hallegraeff, 2010). This Among the instruments that allow esti- ports the idea that D. acuta and D. acum- complexity, associated with limited mates of the turbulent kinetic energy dis- inata have distinctly different ecological knowledge of physiological acclimation sipation rate and shear within TLs, there niches. Furthermore, using the FSS and and adaptive responses of unicellular are free-fall microstructure turbulence IPSAP, Velo-Suárez et al. (2008) showed microalgae and genetic strain diversity, profilers (Figure 7), the free-gliding, very heterogeneous vertical distribution calls for further studies. quasi-horizontal profiler TurboMAP-G of D. acuminata at fine scale (decimeter Fjords provide a good testing ground (Foloni-Neto et al., 2014; see GEOHAB, resolution) in the Ría de Pontevedra for climate change and HAB studies. 2013, cover photo), and various ship- (northwest Spain). Higher temperatures will coincide with board autonomous profilers. Characterizing the temporal devel- the additive effect of increased snowmelt The IPSAP profiler combined with opment of TLs is a major challenge. In a and stratification. In particular, recent the FSS have proven to be useful tools unique study, Ryan et al. (2010) estimated attention to HAB biodiversity and bio- for studying TL characteristics. In 2007, that phytoplankton cell density in a TL geography has begun to focus on frontier these instruments were deployed off dominated by A. sanguinea in Monterey locations within and adjacent to fjords the south coast of Ireland to sample a Bay, , doubled during a four- in the and sub-Arctic, where the high-density, 3 m thick, subsurface layer day period. The process was concurrent effects of climate change are anticipated of Dinophysis acuta with density peaks of with increased stratification and internal to be most rapid and dramatic and may 8,000 cells L–1. At one location, repeated tide-driven nutrient supply. The inves- yield evidence of regime shifts in these IPSAP casts, followed by the FSS, identi- tigation acquired nearly 7,000 profiles habitats. Application of metagenomic fied a high cell density TL of D. acuminata with an AUV in a set of sections repeated and metatranscriptomic approaches <40 cm thick in the middle of the layer of almost continuously for a week. by parallel amplicon sequencing of D. acuta (Raine, 2014). Such an observa- Few studies have documented the role 28S rRNA in comparative Arctic fjords tion of interleaving of fine layers would of nutrients in HAB formation and sus- reveals differential patterns of molecular not be possible with conventional tech- tenance in TLs. Fine-scale chemical gra- diversity in plankton size fractions and nologies. Furthermore, both species were dients and chemically distinct TLs may identifies links between the occurrence present in densities >105 cells L–1, while exist in stratified coastal environments of particular HAB taxa and their toxins as few as 200 cells L–1 can make shellfish (Lunven et al., 2005; Ryan et al., 2010). (Elferink et al., 2016). unfit for human consumption, provided Formation of such TLs may provide There is evidence that climate-related advantages in all kinds of nutritional con- regime shifts may have led to changes in ditions. There may be concurrent favor- HAB biogeography in the fjord regions able light and nutrient conditions if TLs of the Chilean coast. In 2016, blooms are located in the upper part of the nutri- of Pseudochattonella caused mortali- cline. Such high-prey density layers can ties of 20% of the total Chilean salmon be favorable for mixotrophic species production: about 30 million fish were (e.g., Dinophysis spp.; Velo-Suárez et al., killed in a few days (Clement et al., 2016). 2008), and breakdown products from These events were followed by excep- senescent cells could accumulate in the tional blooms of Alexandrium catenella density gradient (pycnocline). These fac- (in terms of their northward expansion), tors favor nutrient recycling and phyto- which devastated shellfish production plankton productivity. and led to social upheaval (Hernández et al., 2016). These phenomena were CLIMATE CHANGE AND HABS IN clearly associated with climate anoma- CONFINED AND SEMI-CONFINED lies and were linked to one of the stron- ENVIRONMENTS gest El Niño signals in the southeastern Recent studies have examined how cli- Pacific Ocean in recent decades. mate change might influence HABs in Wells et al. (2015) present a broad the global ocean. The response of plank- overview of the knowledge and gaps in FIGURE 7. This free-fall microstructure turbu- lence profiler on board R/V Ramón Margalef tonic communities to changes in the knowledge about the environmental con- (IEO, Spain) was used to investigate the role of physical environment (e.g., higher tem- ditions that favor initiation and main- mixing in phytoplankton community structure in perature, increased stratification, heavy tenance of HABs in order to forecast the Galician Rias (northwest Iberian Peninsula). Photo credit: B. Mouriño-Carballido, University precipitation) is expected to be the result changes in near-future scenarios. These of Vigo, Spain of many factors, including complex authors highlight the lack of uniform

54 Oceanography | Vol.30, No.1 experimental protocols, which limits the HAB-threatened environments. Artigas, M.L., C. Llebot, O.N. Ross, N.Z. Neszi, V. Rodellas, J. Garcia-Orellana, P. Masqué, J. Piera, quantitative cross-investigation compar- 2. Improve knowledge of submesoscale M. Estrada, and E. Berdalet. 2014. Understanding isons essential to improving our knowl- processes (<10 km) of importance to the spatio-temporal variability of phytoplank- ton biomass distribution in a microtidal estu- edge. GlobalHAB program objectives HABs in coastal environments, inte- ary. Deep Sea Research Part II 101:180–192, include advancing understanding of grating biology, chemical ecology, bio- https://doi.org/10.1016/j.dsr2.2014.01.006. Azanza, R.V. 2013. Harmful Algal Blooms in tropical global patterns in HAB responses to cli- geochemistry, physical oceanography, embayments affected by monsoons. Pp. 20–23 in GEOHAB Core Research Project: HABs in Fjords mate change, in terms of magnitude, fre- and sedimentary studies. and Coastal Embayments Second Open Science quency, and distributional shifts, through 3. Investigate the influence of coastal Meeting: Progress in Interpreting Life History and Growth Dynamics of Harmful Algal Blooms comprehensive region-specific studies aquaculture (shellfish and fish farm- in Fjords and Coastal Environments. S. Roy, that integrate biological processes with ing) on the development of HABs; this V. Pospelova, M. Montresor, and A.D. Cembella, eds, IOC and SCOR, Paris, France, and Newark, downscaled climate projections (http:// will contribute to the sustainable use of Delaware, USA. Azanza, R.V., M.L. Brosnahan, D.M. Anderson, www.globalhab.info; Berdalet et al., 2017, renewable resources. I. Hense, M. Montresor. In press. The role of life in this issue). 4. Investigate the role of toxins and other cycle characteristics on harmful algal bloom dynamics. In Global Ecology and Oceanography allelochemical substances in structur- of Harmful Algal Blooms (GEOHAB). P.M. Glibert, CONCLUSIONS AND NEXT STEPS ing food webs, in cell defense, and in E. Berdalet, M. Burfot, G. Pitcher, and M. Zhou, Ecological Studies Series, Springer. The GEOHAB program provided a solid nutrient acquisition. Further research Berdalet, E., R. Kudela, E. Urban, H. Enevoldsen, N.S. Banas, E. Bresnan, M. Burford, K. Davidson, foundation for coordinated research on on the modulation of toxin production C.J. Gobler, B. Karlson, and others. 2017. HABs worldwide. The objectives iden- by nutrients or the presence of pred- GlobalHAB: A new program to promote inter- national research, observations, and model- tified in the two CRPs presented in this ators, which is especially challeng- ing of harmful algal blooms in aquatic systems. paper were complementary and allowed ing to study in the field, is required. Oceanography 30(1):70–81, https://doi.org/10.5670/ oceanog.2017.111. synergies to advance the understanding Due to their dimensions and hydro- Berdalet, E., G. Llaveria, and R. Simó. 2011. Modulation of HAB dynamics. Here, we summarized dynamic features, fjords and coastal of dimethylsulfoniopropionate (DMSP) concentra- tion in an Alexandrium minutum (Dinophyceae) improved knowledge of processes at sub- embayments and associated TL struc- culture by small-scale turbulence: A link to toxin production? Harmful Algae 10:88–95, mesoscale and fine and small scales that tures offer suitable scenarios for in situ https://doi.org/10.1016/j.hal.2011.08.003. also apply to upwelling (Pitcher et al., research. Berdalet, E., M.A. McManus, O.N. Ross, H. Burchard, F.P. Chavez, J.S. Jaffe, I.R. Jenkinson, R. Kudela, 2017) and eutrophic (Glibert and Burfort, 5. Improve knowledge of physical- I. Lips, U. Lips, and others. 2014. Understanding 2017) systems also described in this spe- biological processes at small scales, harmful algae in stratified systems: Review of progress and future directions. Deep Sea cial issue of Oceanography. including rheological properties Research Part II 101:4–20, https://doi.org/10.1016/​ j.dsr2.2013.09.042. At the end of GEOHAB, we identi- related to cell aggregations. Bouwman, L., A. Beusen, P.M. Glibert, C. Overbeek, fied some priorities to be addressed by 6. Investigate the ongoing trends of HAB M. Pawlowski, J. Herrera, S. Mulsow, R. Yu, and M. Zhou. 2013. 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Interacting physical, chemical and bio- Research (SCOR) for financial and logistical support to Development, morphological characteristics and logical forcing of phytoplankton thin-layer vari- launch and implement the GEOHAB CRPs “HABs in viability of temporary cysts of Pyrodinium baha- ability in Monterey Bay, California. Continental Stratified Systems” and “HABs in Fjords and Coastal mense var. compressum (Dinophyceae) in vitro. Shelf Research 30:7–16, https://doi.org/10.1016/​ Embayments.” The authors acknowledge support European Journal of Phycology 49:265–275, j.csr.2009.10.017. from the US National Science Foundation to GEOHAB https://doi.org/10.1080/09670262.2014.915062. Selander, S., J. Kubanek, M. Hamberg, through the following grants to SCOR: OCE-0003700, Persson, A., B.C. Smith, G.H. Wikfors, and M.X. Andersson, G. Cervin, and H. Pavia. 2015. OCE-0326301, OCE-0608600, OCE-0938349, and J.H. Alix. 2013. Differences in swimming pat- Predator lipids induce paralytic shellfish tox- OCE-1243377. The work summarized here bene- terns between life cycle stages of the toxic dino- ins in bloom-forming algae. Proceedings of the fited from the various projects endorsed by GEOHAB flagellates Alexandrium fundyense. Harmful Natural Academy of Sciences of the United States along its lifetime (see http://www.geohab.info), as well Algae 21–22:36–43, https://doi.org/10.1016/​ of America 112(20):6,395–6,400, https://doi.org/​ as the RITMARE (Ricerca ITaliana per il MARE) pro- j.hal.2012.11.005. 10.1073/pnas.1420154112. gram and the ASIMUTH (FP7-SPACE 261860) and Pitcher, G.C., A.B. Jiménez, R.M. Kudela, and Smith, B.C., and A. Persson. 2005. Synchronization of JEDI System (JST CREST) projects. B. Reguera. 2017. Harmful algal blooms in east- encystment of Scrippsiella lachrymosa (Dinophyta). ern boundary upwelling systems: A GEOHAB Core Journal of Applied Phycology 17:317–321, Research Project. Oceanography 30(1):22–35, https://doi.org/10.1007/s10811-005-4944-6. AUTHORS https://doi.org/10.5670/oceanog.2017.107. Steinbuck, J.V., M.T. Stacey, M.A. McManus, Elisa Berdalet ([email protected]) is Tenured Pizarro, G., B. Paz, S. González-Gil, J.M. Franco, and O.M. Cheriton, and J.P. Ryan. 2009. Observations Scientist, Institute of Marine Sciences (CSIC), B. Reguera. 2009. Seasonal variability of lipophilic of turbulent mixing in a phytoplankton thin Barcelona, Catalonia, Spain. Marina Montresor is toxins during a Dinophysis acuta bloom in west- layer: Implications for formation, mainte- Senior Scientist, Stazione Zoologica Anton Dohrn ern Iberia: Differences between picked cells and nance, and breakdown. Limnology and (SZN), Naples, Italy. Beatriz Reguera is Research plankton concentrates. Harmful Algae 8:926–937, Oceanography 544:1,353–1,368, https://doi.org/​ Professor, Spanish Institute of Oceanography https://doi.org/10.1016/j.hal.2009.05.004. 10.4319/lo.2009.54.4.1353. (IEO), Vigo, Spain. Suzanne Roy is Research Raine, R. 2014. A review of the biophysical inter- Timmerman, A.H.V., M.A. McManus, O.M. Cheriton, Professor (retired), Institut des Sciences de la actions relevant to the promotion of HABs in strati- R.K. Cowen, A.T. Greer, R.M. Kudela, K. Ruttenberg, Mer, Université du Québec à Rimouski, Rimouski, fied systems: The case study of Ireland. Deep Sea and J. Sevadjian. 2014. Hidden thin layers of toxic Canada. Hidekatsu Yamazaki is Head, Laboratory Research Part II 101:21–31, https://doi.org/10.1016/​ diatoms in a coastal bay. Deep Sea Research of Ocean Ecosystem Dynamics, School of Marine j.dsr2.2013.06.021. Part II 101:129–140, https://doi.org/10.1016/​ Resources and Environment, Tokyo University of Raine, R., G. McDermott, J. Silke, K. Lyons, G. Nolan, j.dsr2.2013.05.030. Marine Science and Technology, Tokyo, Japan. and C. Cusack. 2010. A simple short range model Trainer, V.L., B.M. Hickey, and R. Homer. 2002. Allan Cembella is Professor and Head, Department for the prediction of harmful algal events in the Biological and physical dynamics of domoic of Ecological Chemistry, Alfred-Wegener-Institut, bays of southwestern Ireland. Journal of Marine acid production off the Washington coast. Helmholtz-Zentrum für Polar- und Meeresforschung, Systems 83:150–157, https://doi.org/10.1016/​ Limnology and Oceanography 47:1,438–1,446, Bremerhaven, Germany. Robin Raine is Adjunct j.jmarsys.2010.05.001. https://doi.org/10.4319/lo.2002.47.5.1438. Lecturer, Earth and Ocean Sciences, National Ralston, D.K., B.A. Keafer, M.L. Brosnahan, and Velo-Suárez, L., S. González-Gil, P. Gentien, University of Ireland, Galway, Ireland. D.M. Anderson. 2014. Temperature depen- M. Lunven, C. Bechemin, L. Fernand, R. Raine and dence of an estuarine harmful algal bloom: B. Reguera. 2008. 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