Why Was There a Harmful Algal Bloom in 2015: The Relative Growth of Toxic and Non-toxic Diatoms as a Function of Temperature

A coastwide bloom of the toxigenic diatom Pseudo-nitzschia in 2015 resulted in the largest recorded outbreak and unprecedented levels of the neurotoxin, domoic acid (DA), along the North American west coast. The scientific community has suggested that warmer ocean temperatures were the main cause of this harmful algal bloom (HAB), but little scientific evidence to support the relationship between temperature, and the growth and toxicity of Pseudo-nitzschia has been provided for local isolates of these diatoms. To gain insight into bloom dynamics, a laboratory study was conducted to examine the growth of toxic and non-toxic phytoplankton species at a range of temperatures. Non- (or low) toxic diatoms Pseudo-nitzschia fraudulenta, Skeletonema costatum, and Chaetoceros decipiens were isolated from the 2015 bloom, and cultured at eight temperature conditions (5.6, 6.8, 8.7, 10.8, 13.3, 15.2, 17.2, 19.0°C). A total of 48 cultures (6 tubes per condition), with duplicates at each temperature, were grown in a temperature gradient incubator and monitored for 31 days over three complete growth cycles (runs) of exponential and stationary growth. Specific growth rates, determined from daily measures of in vivo fluorescence, indicate that by Run 3, there was no growth at 5.6°C for Chaetoceros decipiens, and a large decline in the growth rate for Skeletonema costatum at 17.2 and 19.0°C. Pseudo-nitzschia fraudulenta demonstrated the greatest growth rates of all species from 10.8 to 19.0°C, and exhibited the broadest range of elevated growth rates. These temperature results indicate that Skeletonema costatum does not thrive in ocean temperatures above 15°C, and is outcompeted by other algae, including both species of Pseudo-nitzschia. Results of this study will greatly aid oceanographers in determining the dominant species in a coastal region as a function of ambient ocean temperature conditions

The Effects of Iron Complexing Ligands on the Long Term Ecosystem Response to Iron Enrichment of HNLC waters

The central hypothesis of this project is that natural iron-complexing organic ligands in seawater differentially regulate iron availability to large (microplankton) and small (nano and picoplankton) class of phytoplankton and thereby strongly influence the potential carbon sequestration in High Nitrate Low Chlorophyll (HNLC) regions of the ocean. The primary project goals are to: 1) determine how different natural and synthetic Fe chelators affect Fe availability to phytoplankton species that are representative of offshore HNLC waters, 2) elucidate how the changes in absolute concentrations of these chelators affect the longer-term ecosystem response to alleviation of Fe limitation, and 3) ascertain how changes in the ligand composition affect rates of cell sinking and aggregation - representative measures of the efficiency of carbon sequestration to the deep

Marine Microalgae: Climate, Energy, and Food Security From the Sea

Climate, energy, and food security are three of the greatest challenges society faces this century. Solutions for mitigating the effects of climate change often conflict with solutions for ensuring society’s future energy and food requirements. For example, BioEnergy with Carbon Capture and Storage (BECCS) has been proposed as an important method for achieving negative CO2 emissions later this century while simultaneously producing renewable energy on a global scale. However, BECCS has many negative environmental consequences for land, nutrient, and water use as well as biodiversity and food production. In contrast, large-scale industrial cultivation of marine microalgae can provide society with a more environmentally favorable approach for meeting the climate goals agreed to at the 2015 Paris Climate Conference, producing the liquid hydrocarbon fuels required by the global transportation sector, and supplying much of the protein necessary to feed a global population approaching 10 billion people

Pseudo-nitzschia physiological ecology, phylogeny, toxicity, monitoring and impacts on ecosystem health

This paper is not subject to U.S. copyright. The definitive version was published in Harmful Algae 14 (2012): 271-300, doi:10.1016/j.hal.2011.10.025.Over the last decade, our understanding of the environmental controls on Pseudo-nitzschia blooms and domoic acid (DA) production has matured. Pseudo-nitzschia have been found along most of the world's coastlines, while the impacts of its toxin, DA, are most persistent and detrimental in upwelling systems. However, Pseudo-nitzschia and DA have recently been detected in the open ocean's high-nitrate, low-chlorophyll regions, in addition to fjords, gulfs and bays, showing their presence in diverse environments. The toxin has been measured in zooplankton, shellfish, crustaceans, echinoderms, worms, marine mammals and birds, as well as in sediments, demonstrating its stable transfer through the marine food web and abiotically to the benthos. The linkage of DA production to nitrogenous nutrient physiology, trace metal acquisition, and even salinity, suggests that the control of toxin production is complex and likely influenced by a suite of environmental factors that may be unique to a particular region. Advances in our knowledge of Pseudo-nitzschia sexual reproduction, also in field populations, illustrate its importance in bloom dynamics and toxicity. The combination of careful taxonomy and powerful new molecular methods now allow for the complete characterization of Pseudo-nitzschia populations and how they respond to environmental changes. Here we summarize research that represents our increased knowledge over the last decade of Pseudo-nitzschia and its production of DA, including changes in worldwide range, phylogeny, physiology, ecology, monitoring and public health impacts

Harmful algal blooms and eutrophication : examining linkages from selected coastal regions of the United States

Author Posting. © Elsevier B.V., 2008. This is the author's version of the work. It is posted here by permission of Elsevier B.V. for personal use, not for redistribution. The definitive version was published in Harmful Algae 8 (2008): 39-53, doi:10.1016/j.hal.2008.08.017.Coastal waters of the United States (U.S.) are subject to many of the major harmful algal bloom (HAB) poisoning syndromes and impacts. These include paralytic shellfish poisoning (PSP), neurotoxic shellfish poisoning (NSP), amnesic shellfish poisoning (ASP), ciguatera fish poisoning (CFP) and various other HAB phenomena such as fish kills, loss of submerged vegetation, shellfish mortalities, and widespread marine mammal mortalities. Here, the occurrences of selected HABs in a selected set of regions are described in terms of their relationship to eutrophication, illustrating a range of responses. Evidence suggestive of changes in the frequency, extent or magnitude of HABs in these areas is explored in the context of the nutrient sources underlying those blooms, both natural and anthropogenic. In some regions of the U.S., the linkages between HABs and eutrophication are clear and well documented, whereas in others, information is limited, thereby highlighting important areas for further research.Support was provided through the Woods Hole Center for Oceans and Human Health (to DMA), National Science Foundation (NSF) grants OCE-9808173 and OCE-0430724 (to DMA), OCE-0234587 (to WPC), OCE04-32479 (to MLP), OCE-0138544 (to RMK), OCE-9981617 (to PMG); National Institute of Environmental Health Sciences (NIEHS) grants P50ES012742-01 (to DMA) and P50ES012740 (to MLP); NOAA Grants NA96OP0099 (to DMA), NA16OP1450 (to VLT), NA96P00084 (to GAV and CAH), NA160C2936 and NA108H-C (to RMK), NA860P0493 and NA04NOS4780241 (to PMG), NA04NOS4780239-02 (to RMK), NA06NOS4780245 (to DWT). Support was also provided from the West Coast Center for Oceans and Human Health (to VLT and WPC), USEPA Grant CR826792-01-0 (to GAV and CAH), and the State of Florida Grant S7701617826 (to GAV and CAH)

Final Technical Report: The Effects of Iron Complexing Ligands on the Long Term Ecosystem Response to Iron Enrichment of HNLC waters

Substantial increases in the concentrations of the stronger of two Fe(III) complexing organic ligand classes measured during the mesoscale Fe enrichment studies IronEx II and SOIREE appeared to sharply curtailed Fe availability to diatoms and thus limited the efficiency of carbon sequestration to the deep. Detailed observations during IronEx II (equatorial Pacific Ocean) and SOIREE (Southern Ocean –Pacific sector) indicate that the diatoms began re-experiencing Fe stress even though dissolved Fe concentrations remained elevated in the patch. This surprising outcome likely is related to the observed increased concentrations of strong Fe(III)-complexing ligands in seawater. Preliminary findings from other studies indicate that diatoms may not readily obtain Fe from these chemical species whereas Fe bound by strong ligands appears to support growth of cyanobacteria and nanoflagellates. The difficulty in assessing the likelihood of these changes with in-situ mesoscale experiments is the extended monitoring period needed to capture the long-term trajectory of the carbon cycle. A more detailed understanding of Fe complexing ligand effects on long-term ecosystem structure and carbon cycling is essential to ascertain not only the effect of Fe enrichment on short-term carbon sequestration in the oceans, but also the potential effect of Fe enrichment in modifying ecosystem structure and trajectory

Primary productivity, bacterial productivity and nitrogen uptake in response to iron enrichment during the SEEDS II

Primary productivity (PP), bacterial productivity (BP) and the uptake rates of nitrate and ammonium were measured using isotopic methods (13C, 3H, 15N) during a mesoscale iron (Fe)-enrichment experiment conducted in the western subarctic Pacific Ocean in 2004 (SEEDS II). PP increased following Fe enrichment, reached maximal rates 12 days after the enrichment, and then declined to the initial level on day 17. During the 23-d observation period, we observed the development and decline of the Fe-induced bloom. The surface mixed layer (SML) integrated PP increased by 3-fold, but was smaller than the 5-fold increase observed in the previous Fe-enrichment experiment conducted at almost the same location and season during 2001 (SEEDS). Nitrate uptake rates were enhanced by Fe-enrichment but decreased after day 5, and became lower than ammonium uptake rates after day 17. The total nitrogenous nutrient uptake rate declined after the peak of the bloom, and accumulation of ammonium was obvious in the euphotic layer. Nitrate utilization accounted for all the requirements of N for the massive bloom development during SEEDS, whereas during SEEDS II, nitrate accounted for >90% of total N utilization on day 5, declining to 40% by the end of the observation period. The SML integrated BP increased after day 2 and peaked twice on days 8 and 21. Ammonium accumulation and the delayed heterotrophic activity suggested active regeneration occurred after the peak of the bloom. The SML integrated PP between days 0 and day 23 was 19.0g Cm^[-2]. The SML integrated BP during the same period was 2.6 g C m^[-2], which was 14% of the SML integrated PP. Carbon budget calculation for the whole experimental period indicated that 33% of the whole (particulate plus dissolved) PP (21.5 gCm^[-2]) was exported below the SML and 18% was transferred to the meso-zooplankton (growth). The bacterial carbon consumption (43% of the whole PP) was supported by DOC or POC release from phytoplankton, zooplankton, protozoa and viruses. More than a half (56%) of the whole PP in the Fe patch was consumed within the SML by respiration of heterotrophic organisms and returned to CO2

Carbon and nitrogen uptake response to light by phytoplankton during an upwelling event

even

Climate Change and the Growth and Ichthyotoxicity of Heterosigma akashiwo in the Salish Sea: Effects of Salinity, Temperature and Acidity

Three critically important alterations of Salish Sea waters − reduced salinity, increased temperature and elevated CO2 levels, were examined in controlled laboratory studies of an impactful harmful algal bloom species on sustainable aquaculture efforts in British Columbia and Washington. Our results demonstrate the capability of the raphidophyte Heterosigma akashiwo (Y. Hada) Y. Hada ex Y. Hara et M. Chihara, to grow at varying levels of salinity, temperature and CO2-induced acidity (pH), and provide evidence of the potential ichthyotoxicity of this raphidophyte estimated from a gill cell assay approach that quantifies cytotoxicity. A non-axenic strain of H. akashiwo isolated from Puget Sound, WA was exposed to a combination of three salinity (32, 20 and 10) and five temperature (14.7, 18.4, 21.4, 24.4 and 27.8°C) conditions, as well as two pH levels (8.1 and 7.4). Laboratory findings demonstrate that cell permeability and cytotoxicity are strongly correlated in unialgal cultures of H. akashiwo, which both increase as salinity decreases from 32 to 10. Specific growth rates were found to increase with increasing temperature (14.7-24.4°C) for cultures grown at salinities of 10 (0.7-1.1 d-1), 20 (1.0-1.5 d-1) and 32 (0.7-1.2 d-1), with the fastest growth rates occurring at the salinity of 20. Furthermore, over a range of environmentally realistic lower salinities (10 and 20), neither temperature nor specific growth rate were correlated with cytotoxicity. However, the 400% increase in acidity experienced by cultures grown at salinity of 32 and pH 7.4, results in faster exponential growth rates, and 2-3 fold increases in cytotoxicity as these flagellated raphidophytes enter their N-limited stationary phase of growth. These laboratory results reveal the capacity of H. akashiwo to increase its growth potential and become more toxic not only at reduced salinities, but also in more acidic waters − environmental conditions expected in the Salish Sea due to CO2-induced ocean acidification and greenhouse warming

Effect of ocean acidification on the nutritional quality of marine phytoplankton for copepod reproduction.

Phytoplankton are the oceans' principal source of polyunsaturated fatty acids that support the growth and reproduction of consumers such as copepods. Previous studies have demonstrated ocean acidification (OA) can change the availability of polyunsaturated fatty acids to consumer diets which may affect consumer reproduction. Two laboratory experiments were conducted to examine the effects of feeding high-pCO2-reared phytoplankton on copepod egg production, hatching success, and naupliar survival. Marine phytoplankton Rhodomonas salina, Skeletonema marinoi, Prorocentrum micans, and Isochrysis galbana were exponentially grown in semi-continuous cultures at present (control) (400 ppm CO2, pH~8.1) and future (1,000 ppm CO2, pH~7.8) conditions and provided to Acartia tonsa copepods over 4 consecutive days as either nitrogen-limited (Exp. I) or nitrogen-depleted (Exp. II) mixed assemblage of phytoplankton. The composition of FAs in the phytoplankton diet was affected by pCO2 concentration and nitrogen deficiency; the ratio of essential fatty acids to total polyunsaturated fatty acids decreased in phytoplankton grown under high pCO2 and the mass of total fatty acids increased under nitrogen depletion. Additionally, total concentrations of essential fatty acids and polyunsaturated fatty acids in the diet mixtures were less under the high-pCO2 compared to the control-pCO2 treatments. Median egg production, hatching success, and naupliar survival were 48-52%, 4-87%, and 9-100% lower, respectively, in females fed high-pCO2 than females fed low-pCO2 phytoplankton, but this decrease in reproductive success was less severe when fed N-depleted, but fatty acid-rich cells. This study demonstrates that the effects of OA on the nutritional quality of phytoplankton (i.e., their cellular fatty acid composition and quota) were modified by the level of nitrogen deficiency and the resulting negative reproductive response of marine primary consumers