Raphael M. Kudela

Marine phytoplankton temperature versus growth responses from polar to tropical waters – outcome of a scientific community-wide study

“It takes a village to finish (marine) science these days” Paraphrased from Curtis Huttenhower (the Human Microbiome project) The rapidity and complexity of climate change and its potential effects on ocean biota are challenging how ocean scientists conduct research. One way in which we can begin to better tackle these challenges is to conduct community-wide scientific studies. This study provides physiological datasets fundamental to understanding functional responses of phytoplankton growth rates to temperature. While physiological experiments are not new, our experiments were conducted in many laboratories using agreed upon protocols and 25 strains of eukaryotic and prokaryotic phytoplankton isolated across a wide range of marine environments from polar to tropical, and from nearshore waters to the open ocean. This community-wide approach provides both comprehensive and internally consistent datasets produced over considerably shorter time scales than conventional individual and often uncoordinated lab efforts. Such datasets can be used to parameterise global ocean model projections of environmental change and to provide initial insights into the magnitude of regional biogeographic change in ocean biota in the coming decades. Here, we compare our datasets with a compilation of literature data on phytoplankton growth responses to temperature. A comparison with prior published data suggests that the optimal temperatures of individual species and, to a lesser degree, thermal niches were similar across studies. However, a comparison of the maximum growth rate across studies revealed significant departures between this and previously collected datasets, which may be due to differences in the cultured isolates, temporal changes in the clonal isolates in cultures, and/or differences in culture conditions. Such methodological differences mean that using particular trait measurements from the prior literature might introduce unknown errors and bias into modelling projections. Using our community-wide approach we can reduce such protocol-driven variability in culture studies, and can begin to address more complex issues such as the effect of multiple environmental drivers on ocean biota.

Evidence for a Novel Marine Harmful Algal Bloom: Cyanotoxin (Microcystin) Transfer from Land to Sea Otters

“Super-blooms” of cyanobacteria that produce potent and environmentally persistent biotoxins (microcystins) are an emerging global health issue in freshwater habitats. Monitoring of the marine environment for secondary impacts has been minimal, although microcystin-contaminated freshwater is known to be entering marine ecosystems. Here we confirm deaths of marine mammals from microcystin intoxication and provide evidence implicating land-sea flow with trophic transfer through marine invertebrates as the most likely route of exposure. This hypothesis was evaluated through environmental detection of potential freshwater and marine microcystin sources, sea otter necropsy with biochemical analysis of tissues and evaluation of bioaccumulation of freshwater microcystins by marine invertebrates. Ocean discharge of freshwater microcystins was confirmed for three nutrient-impaired rivers flowing into the Monterey Bay National Marine Sanctuary, and microcystin concentrations up to 2,900 ppm (2.9 million ppb) were detected in a freshwater lake and downstream tributaries to within 1 km of the ocean. Deaths of 21 southern sea otters, a federally listed threatened species, were linked to microcystin intoxication. Finally, farmed and free-living marine clams, mussels and oysters of species that are often consumed by sea otters and humans exhibited significant biomagnification (to 107 times ambient water levels) and slow depuration of freshwater cyanotoxins, suggesting a potentially serious environmental and public health threat that extends from the lowest trophic levels of nutrient-impaired freshwater habitat to apex marine predators. Microcystin-poisoned sea otters were commonly recovered near river mouths and harbors and contaminated marine bivalves were implicated as the most likely source of this potent hepatotoxin for wild otters. This is the first report of deaths of marine mammals due to cyanotoxins and confirms the existence of a novel class of marine “harmful algal bloom” in the Pacific coastal environment; that of hepatotoxic shellfish poisoning (HSP), suggesting that animals and humans are at risk from microcystin poisoning when consuming shellfish harvested at the land-sea interface.

River Influences on Shelf Ecosystems: Introduction and synthesis

[1] River Influences on Shelf Ecosystems (RISE) is the first comprehensive interdisciplinary study of the rates and dynamics governing the mixing of river and coastal waters in an eastern boundary current system, as well as the effects of the resultant plume on phytoplankton standing stocks, growth and grazing rates, and community structure. The RISE Special Volume presents results deduced from four field studies and two different numerical model applications, including an ecosystem model, on the buoyant plume originating from the Columbia River. This introductory paper provides background information on variability during RISE field efforts as well as a synthesis of results, with particular attention to the questions and hypotheses that motivated this research. RISE studies have shown that the maximum mixing of Columbia River and ocean water occurs primarily near plume liftoff inside the estuary and in the near field of the plume. Most plume nitrate originates from upwelled shelf water, and plume phytoplankton species are typically the same as those found in the adjacent coastal ocean. River-supplied nitrate can help maintain the ecosystem during periods of delayed upwelling. The plume inhibits iron limitation, but nitrate limitation is observed in aging plumes. The plume also has significant effects on rates of primary productivity and growth (higher in new plume water) and microzooplankton grazing (lower in the plume near field and north of the river mouth); macrozooplankton concentration (enhanced at plume fronts); offshelf chlorophyll export; as well as the development of a chlorophyll ‘‘shadow zone’’ off northern Oregon.

Mass Stranding of Marine Birds Caused by a Surfactant-Producing Red Tide

In November-December 2007 a widespread seabird mortality event occurred in Monterey Bay, California, USA, coincident with a massive red tide caused by the dinoflagellate Akashiwo sanguinea. Affected birds had a slimy yellow-green material on their feathers, which were saturated with water, and they were severely hypothermic. We determined that foam containing surfactant-like proteins, derived from organic matter of the red tide, coated their feathers and neutralized natural water repellency and insulation. No evidence of exposure to petroleum or other oils or biotoxins were found. This is the first documented case of its kind, but previous similar events may have gone undetected. The frequency and amplitude of red tides have increased in Monterey Bay since 2004, suggesting that impacts on wintering marine birds may continue or increase.

Movement and diving behavior of male California sea lion (Zalophus californianus) during anomalous oceanographic conditions of 2005 compared to those of 2004

[1] During the highly anomalous conditions in early 2005, characterized by increased water temperatures and decreased productivity, male California sea lions adopted previously undocumented foraging behaviors. We investigated the movement and spatially explicit foraging behavior of males using satellite-linked data loggers and compared foraging behavior and effort between 2003-2004 and 2004-2005. Males foraged almost exclusively over the continental shelf during short trips in 2003-2004, while during anomalous conditions in 2004-2005 they altered their foraging effort by spending more time at sea and venturing up to 450 km offshore. Foraging trips in 2004-2005 were more than twice the distance and three times the duration of trips during 2003-2004. Our data indicated that the effects of climatic shifts during 2005 extended beyond the physical oceanography and lower trophic levels, to an apex predator; providing insight into the plasticity of foraging behavior and movement patterns of sea lions as they respond to environmental perturbations.

An unprecedented coastwide toxic algal bloom linked to anomalous ocean conditions

Abstract A coastwide bloom of the toxigenic diatom Pseudo‐nitzschia in spring 2015 resulted in the largest recorded outbreak of the neurotoxin, domoic acid, along the North American west coast. Elevated toxins were measured in numerous stranded marine mammals and resulted in geographically extensive and prolonged closures of razor clam, rock crab, and Dungeness crab fisheries. We demonstrate that this outbreak was initiated by anomalously warm ocean conditions. Pseudo‐nitzschia australis thrived north of its typical range in the warm, nutrient‐poor water that spanned the northeast Pacific in early 2015. The seasonal transition to upwelling provided the nutrients necessary for a large‐scale bloom; a series of spring storms delivered the bloom to the coast. Laboratory and field experiments confirming maximum growth rates with elevated temperatures and enhanced toxin production with nutrient enrichment, together with a retrospective analysis of toxic events, demonstrate the potential for similarly devastating ecological and economic disruptions in the future.

Ocean urea fertilization for carbon credits poses high ecological risks

The proposed plan for enrichment of the Sulu Sea, Philippines, a region of rich marine biodiversity, with thousands of tonnes of urea in order to stimulate algal blooms and sequester carbon is flawed for multiple reasons. Urea is preferentially used as a nitrogen source by some cyanobacteria and dinoflagellates, many of which are neutrally or positively buoyant. Biological pumps to the deep sea are classically leaky, and the inefficient burial of new biomass makes the estimation of a net loss of carbon from the atmosphere questionable at best. The potential for growth of toxic dinoflagellates is also high, as many grow well on urea and some even increase their toxicity when grown on urea. Many toxic dinoflagellates form cysts which can settle to the sediment and germinate in subsequent years, forming new blooms even without further fertilization. If large-scale blooms do occur, it is likely that they will contribute to hypoxia in the bottom waters upon decomposition. Lastly, urea production requires fossil fuel usage, further limiting the potential for net carbon sequestration. The environmental and economic impacts are potentially great and need to be rigorously assessed.

Modeling the impact of the 1992 El Niño on new production in Monterey Bay, California

Abstract New primary production is estimated using a physiologically driven model of phytoplankton utilization of nitrate for the Monterey Bay, California region. Primary inputs for the model come from temperature and phytoplankton biomass (chlorophyll) from 3 moorings, allowing daily estimation of surface new production. The model successfully reproduces the seasonal pattern of nitrate utilization determined from shipboard experiments using traditional stable-isotope techniques, with a spring peak corresponding to upwelling favorable conditions, a more oceanic fall period, and low values during winter. Comparison of the climatological model output to discrete bottle measurements from 1989–1995 provided an r 2 value of 0.74 for surface waters. This correlation decreased to 0.52 when bottle depths from the 50% light level were included, suggesting that the model does not perform well in subsurface waters due to the lack of an irradiance-response in the modeled N uptake. We use the model to explore the effects of the 1992 El Nino event. There was a small decrease in primary production during the 1992 even with no discernible change in vertical export of organic material ( Chavez, 1996 ; Pilskaln et al., 1996 ). In contrast, this model demonstrates a substantial decrease in new production (about four fold) during 1992, while during this same period, new production was greatly reduced (more than four-fold) farther from shore and presumably downstream during the spring upwelling season. These results are consistent with the hypothesis that moderate upwelling during 1992 provided sufficient nutrients near the coast to maintain “normal” levels of primary productivity, but that productivity downstream and offshore from the upwelling centers was impacted due to the suppression of the themocline and nitracline associated with the ENSO event.

Host-specific adaptation governs the interaction of the marine diatom, Pseudo-nitzschia and their microbiota

The association of phytoplankton with bacteria is ubiquitous in nature and the bacteria that associate with different phytoplankton species are very diverse. The influence of these bacteria in the physiology and ecology of the host and the evolutionary forces that shape the relationship are still not understood. In this study, we used the Pseudo-nitzschia–microbiota association to determine (1) if algal species with distinct domoic acid (DA) production are selection factors that structures the bacterial community, (2) if host-specificity and co-adaptation govern the association, (3) the functional roles of isolated member of microbiota on diatom–hosts fitness and (4) the influence of microbiota in changing the phenotype of the diatom hosts with regards to toxin production. Analysis of the pyrosequencing-derived 16S rDNA data suggests that the three tested species of Pseudo-nitzschia, which vary in toxin production, have phylogenetically distinct bacterial communities, and toxic Pseudo-nitzschia have lower microbial diversity than non-toxic Pseudo-nitzschia. Transplant experiments showed that isolated members of the microbiota are mutualistic to their native hosts but some are commensal or parasitic to foreign hosts, hinting at co-evolution between partners. Moreover, Pseudo-nitzschia host can gain protection from algalytic bacteria by maintaining association with its microbiota. Pseudo-nitzschia also exhibit different phenotypic expression with regards to DA production, and this depends on the bacterial species with which the host associates. Hence, the influences of the microbiota on diatom host physiology should be considered when studying the biology and ecology of marine diatoms.

Application of the hyperspectral imager for the coastal ocean to phytoplankton ecology studies in Monterey Bay, CA, USA

As a demonstrator for technologies for the next generation of ocean color sensors, the Hyperspectral Imager for the Coastal Ocean (HICO) provides enhanced spatial and spectral resolution that is required to understand optically complex aquatic environments. In this study we apply HICO, along with satellite remote sensing and in situ observations, to studies of phytoplankton ecology in a dynamic coastal upwelling environment—Monterey Bay, CA, USA. From a spring 2011 study, we examine HICO-detected spatial patterns in phytoplankton optical properties along an environmental gradient defined by upwelling flow patterns and along a temporal gradient of upwelling intensification. From a fall 2011 study, we use HICOs enhanced spatial and spectral resolution to distinguish a small-scale ―red tide‖ bloom, and we examine bloom expansion and its supporting processes using other remote sensing and in situ data. From a spectacular HICO image of the Monterey Bay region acquired during fall of 2012, we present a suite of algorithm results for characterization of phytoplankton, and we examine the strengths, limitations, and distinctions of each algorithm in the context of the enhanced spatial and spectral resolution.