Red Tides Under the Microscope

Red tides are caused by the dramatic reproduction of Karenia brevis, a species of dinoflagellate that is common in Gulf waters. Every year when conditions turn favorable, populations of the unicellular alga grow rapidly, dyeing undulating patches of water a brown, green, or rusty hue. Sometimes these events come and go in a matter of weeks or months. But the bloom that Lovko, a researcher at the Mote Marine Laboratory in Sarasota, saw dotted with the corpses of fish lingered in the Gulf for more than a year. It started sometime in October 2017 and didn’t dissipate until early this year. And the fish—most likely killed by potent neurotoxins called brevetoxins produced by K. brevis—weren’t the red tide’s only victims. 

I honestly do not know if K. brevis blooms can be “prevented” based on the level of our current knowledge.

 —Karen Steidinger, retired phytoplankton ecologist
after whom Karenia brevis is named

According to statistics kept by the Florida Fish and Wildlife Conservation Commission (FFWCC), the bloom killed more than 1,000 sea turtles, about 200 manatees, and nearly 190 bottlenose dolphins, in addition to countless fish and some economically important invertebrates, such as stone crabs. Humans may have also felt the effects of Florida’s most recent red tide, with the Florida Department of Health noting a small uptick in the number of weekly emergency department visits statewide in July through November 2018 for people reporting respiratory symptoms and red tide exposure. Although a causal relationship was not formally established in these cases, brevetoxins are known to cause respiratory irritation when the compounds become airborne as wind and waves whipped the water into sea spray.

Currents first swept the 2017–2019 red tide near the Florida panhandle and then around the Florida Keys and up the Atlantic coast, dumping swaths of ruddy water into nearshore ecosystems as far north as Orlando. The bloom “was in so many places at the same time,” remembers Kate Hubbard, head of the harmful algal bloom (HAB) research and monitoring program at the FFWCC’s Fish and Wildlife Research Institute (FWRI). Phytoplankton biologist Cynthia Heil, director of the Mote Marine Laboratory’s newly formed Red Tide Institute, adds, “Local currents do impact these blooms.”

BICOASTAL BLOOM: In October 2018, at the height of the red tide that plagued Florida for more than 16 months, millions of the causative dinoflagellates teemed in waters off Florida’s panhandle, as well as on the west and east coasts of the state.

© istock.com, FrankRamspott; THE SCIENTIST STAFF

Red tides are nothing new to the Gulf. They’ve plagued the area for hundreds of years, and since the 1940s, when researchers linked K. brevis (then called Gymnodinium breve) to the Gulf’s red tide events, the scientific community has been trying to learn more about the biology of the dinoflagellate species, hoping to more accurately predict blooms and mitigate the damage to local ecosystems and human health. But many critical questions remain. Scientists have not yet fully described K. brevis’s life cycle or plausibly hypothesized why the species evolved to produce brevetoxins, nor do they have a complete understanding of the environmental and ecological drivers of bloom formation, maintenance, and termination. 

The factors at play are so numerous and dynamic that anticipating shifts in local conditions that might promote a bloom has proven difficult, to say the least. Broader concerns about how climate change might alter Florida’s red tides add to the uncertainty. All of this makes for a vexingly complex soup of unknowns surrounding K. brevis.

But new insights are emerging all the time, and the scientists who study the phytoplankton and its blooms are getting closer each year to decoding the phenomenon. Hubbard, Lovko, several of his Mote colleagues, and other researchers throughout the state and beyond are taking advantage of new technologies—such as self-propelled underwater robotic gliders that sample water and track conditions in situ, and advanced genetic tools for detecting the presence of K. brevis cells—to try to understand what triggers the phyto-plankton to undergo rapid population growths, why they make brevetoxins at all, and how best to mitigate red tides once they begin ramping up in the Gulf. 

“The implementation of those tools is going to really help us address some of those key questions,” Hubbard says. “I feel pretty optimistic that we are going to be able to make some new discoveries . . . to help us in our predictive models.”

The bloom trackers

Historical accounts suggest that populations of K. brevis in the Gulf have been undergoing annual population booms since at least the 15th and 16th centuries, when Spanish explorers in Florida described fish kills in Gulf waters that bore a striking resemblance to the scene that Lovko noted last year. In 1882, the first official, though anecdotal, documentation of fish kills, bird deaths, and human sickness caused by red tide blooms in the Gulf of Mexico—as far back as 1844—was published in the Proceedings of the U.S. National Museum. Since then, researchers have tracked the annual K. brevis blooms, which typically crop up in the late summer or autumn and vary in length. 

In the FWRI lab in St. Petersburg, Hubbard’s team of scientists is focused on monitoring K. brevis in the Gulf. They process water samples sent in by citizens or fellow researchers who notice something amiss—fish kills or discolored water, for example. FedEx shipments containing plastic containers of water are usually sparse in mid-summer, but during the 2017–2019 red tide event, Hubbard says, there was little letup. In total, her lab processed more than 14,000 of these samples over a 16-month period, she says.

READY TO BLOOM: K. brevis cells in the vegetative stage of their lifecycle are primed to undergo mitosis, increasing population numbers quickly and potentially leading to a red tide.

FLICKR.COM, FWC FISH AND WILDLIFE RESEARCH INSTITUTE

Currently, Hubbard’s team primarily uses manual cell counts for state-mandated estimates of K. brevis abundance. They also occasionally hook up a microscope to a submersible imaging flow cytometer, an automated machine that can process 5–8 mL samples in about 20 minutes, detecting a variety of phytoplankton species including K. brevis. The group also tracks toxins and phytoplankton cells in water samples using chemical analyses such as liquid chromatography and mass spectrometry. Now, in collaboration with other red tide researchers, Hubbard is working on refining a method that can detect K. brevis RNA in water samples, using a handheld device that is already showing promise in field trials for yielding quick and accurate measures of the phyto-plankton’s abundance. 

“The genetic methods can be quite tricky,” Hubbard says. “But I do foresee [the device] could be something that’s used to quickly scan samples.” Her team archives water samples so that they can be used to further develop this and other new methods of censusing K. brevis.

With the data they gather—which now includes inputs from an autonomous aquatic “glider” that samples environmental conditions in the Gulf—Hubbard’s agency puts out twice-weekly bulletins detailing which Florida beaches are affected by red tide. People with lung conditions such as asthma are particularly vulnerable to serious adverse effects when winds blow airborne toxins onshore. Barbara Kirkpatrick, the executive director of the Gulf of Mexico Coastal Ocean Observing System (GCOOS), a nonprofit with a remit of providing information about the Gulf coastal and ocean waters, is working to refine that public-facing monitoring effort. “Blooms are patchy. Conditions can change day to day and beach to beach,” she says. “We’re trying to come up with a daily forecast that updates every three hours.”

The complexity of the species’ biology—and the gaping holes in scientists’ knowledge of it—presents a challenge. “I honestly do not know if K. brevis blooms can be ‘prevented’ based on the level of our current knowledge,” Karen Steidinger, the retired plankton ecologist after whom Karenia brevis was named when its Latin binomial was changed in 2001, writes in an email to The Scientist.

Missing Puzzle Pieces The lifecycle of Karenia brevis has only been partially described. Researchers know that haploid cells undergo mitosis (a) to boost population numbers—a process that is ramped up during red tide events. As blooms progress, some of these cells replicate their genomes and divide their nuclei into two (b) before themselves splitting into so-called isogametes (c). These isogametes strike out in search of other isogametes (d) with which to fuse (e), a form of sexual reproduction that results in a diploid planozygote (f). But the next steps of K. brevis’s lifecycle and how it gets back to its vegetative, haploid state are shrouded in mystery.

THOM GRAVES See full infographic: WEB | PDF

Researchers suspect that the planozygote may become a resting cyst known as a hypnozygote, a life history strategy that several other dinoflagellate species employ to weather unfavorable environmental conditions. But a K. brevis hypnozygote has never been observed in the wild or in culture. If such a life stage does exist for this organism, it could help explain why red tides crop up every autumn, often at a similar distance from shore, with these resting cysts helping to keep populations alive before environmental conditions turn favorable again. When the putative hypnozygotes are reawakened, they would then form short-lived meiocytes, which undergo meiosis to give rise to haploid cells that can restart bloom cycles through mitosis, researchers suspect. But K. brevis meiocytes, like hypnozygotes, have never been observed in the wild.

Demystifying the red tide lifecycle

Dinoflagellate life histories are notoriously complicated, and K. brevis’s lifecycle in particular has been difficult to nail down. But by looking across more than 2,000 known species of marine dinoflagellates, scientists can identify common strategies that could start to fill in the missing details. For example, more than 10 percent of species employ a resting cyst stage, and many phytoplankton scientists suspect that K. brevis does too.

Resting cysts are analogous to seeds in terrestrial plants: they afford dinoflagellates the ability to deposit their genomes in marine sediments or bottom waters as round, featureless cells, which lie dormant until favorable conditions trigger the transition back to a planktonic and highly reproductive stage of the lifecycle. The regular seasonality of Florida red tide blooms supports the existence of this type of strategy for K. brevis, with dormant “seeds” riding out the unfavorable conditions of the spring and early summer months, reawakening closer to fall, and transforming into so-called vegetative cells that multiply rapidly to cause the sometimes-catastrophic blooms. “Whether the cysts are in the sediments or in the water column, I do think it’s reasonable to suspect that there is a resting stage of some kind,” says Cary Lopez, a phytoplankton ecologist at FWRI. It’s also possible, however, that the species goes directly from reproducing more slowly during a period of sexual reproduction to more rapidly reproducing during asexual stages, without first transitioning into a cyst. 

Determining whether the species has a resting stage could be a boon to managers seeking to predict and control red tide events as blooms in the Gulf begin to form, just as knowledge of resting cysts in other harmful algal species helps scientists manage blooms elsewhere. For example, researchers studying Alexandrium fundyense, a dinoflagellate whose blooms cause regular, toxic red tides that compromise ecological and human health along the northeastern coast of the US into Canada, have mapped out two distinct cyst beds—accumulations of resting-stage cells deposited by prior blooms. The research team that described these hideouts also noted that the size and distribution of those cyst repositories correlated with the extent of blooms that followed. Finding similar cyst deposits in K. brevis would confirm that this part of the lifecycle exists, and would allow researchers to monitor dormant populations for signs of an impending bloom in the Gulf. 

A RISING TIDE: A K. brevis bloom dyed coastal waters off of Sarasota, Florida, in August 2018, during the 2017-2019 red tide event.

Vince Lovko/Mote Marine Laboratory

The opportunity to collect and study K. brevis cysts in the lab, or to generate them from an earlier life stage, could also help determine what precipitates the change from one life stage to another. “If we could identify this resting stage and then understand what drives the transition from a resting cyst to a vegetative cell, that would be very important,” says Lopez. She adds, however, that funding is often funneled to more-pressing mitigation and monitoring research, so researchers aren’t scouring the Gulf for K. brevis cyst beds. Hubbard adds that while she and her team do keep an eye out for cysts when sifting through sediment samples, they are predominately relying on oceanographic measures, such as water temperature and the speed and direction of relevant currents, along with cell counts of K. brevis, to generate red tide forecasts.

“Right now, we’re using physical data to be able to predict what’s going to happen with blooms,” Hubbard says. “Not knowing whether there is some similar accumulation of Karenia cells and where that might be makes it really challenging to be able to predict exactly when and where blooms might start.”

Sparking and sustaining blooms

While predicting red tide blooms remains tricky, it’s clear that widespread and multifaceted factors drive their initiation each year. For decades, researchers have been amassing evidence that K. brevis blooms start near the seafloor about 10 to 40 miles offshore in the Gulf. This makes the species somewhat unique among bloom-causing algae, many of which begin to expand inshore or nearshore, flourishing in the high nutrient concentrations, warm temperatures, and sunlight that most phytoplankton require to survive and reproduce. 

What may set K. brevis apart is its ability to thrive on a variety of nutrients and to get those nutrients in a number of ways. In several papers published in a 2014 special issue of the journal Harmful Algae, researchers including Heil documented that K. brevis can subsist on nutrients from undersea sediments, decaying fish, atmospheric deposits, and estuarine water. They can consume other plankton species or use nutrients those species produce, and can absorb nutrients from the water following the decay of a filamentous cyanobacterial genus called Trichodesmium. “Karenia brevis is super flexible,” Hubbard says.

The observation that the dinoflagellate can dine on rotting Trichodesmium, which occasionally also blooms in the Gulf, links red tides in the area to events that extend far beyond the state of Florida and the Gulf of Mexico. In 2001, scientists published evidence that dust storms in the Sahara Desert in early 1999 supplied nutrients that supported subsequent blooms of Trichodesmium, which requires high iron levels to thrive. Levels of dissolved phosphorus plummeted as it was consumed by the cyanobacteria, and dissolved nitrogen increased, potentially fueling a nitrogen-hungry K. brevis bloom that reddened Gulf waters in the fall of the same year.

Blooms are patchy. Conditions can change day to day and beach to beach.

 —Barbara Kirkpatrick, Gulf of Mexico Coastal
Ocean Observing System

While it’s not known whether large, sustained red tide events are caused by one or multiple dinoflagellate populations, once K. brevis gets blooming, the phytoplankton are sometimes swept toward shore by upwelling and prevailing currents into surface waters, where they continue to proliferate. This process involves yet another suite of drivers that include nutrient inputs from fertilizers in groundwater runoff, fish killed by the bloom, faulty wastewater systems, even air pollution—and, of course, local currents. 

A recent study tracked the extensive movement of Florida’s exceptional 2017–2019 red tide event and suggested that its movement into nearshore waters skirting the state’s panhandle may have resulted from the passage of Tropical Storm Gordon across the Gulf from the southwest coast of Florida to Texas and Louisiana in early September 2018. The storm, the study reported, may have disrupted the upwelling that had brought the bloom into nearshore waters on the state’s west coast, allowing the red tide to move north toward the panhandle. When the storm passed, upwelling resumed, and strong currents swung the red tide around the Keys and into coastal waters of the Atlantic along the state’s eastern shore.

Climate change and its effects on patterns of environmental conditions—rising sea surface temperatures increasing the frequency of intense hurricanes; changes in marine ecosystem function—add another layer of complexity. “In the 20th century, it was a question of looking at how are these local changes affecting red tide,” Heil says. In the 21st century, she continues, the focus has shifted to how climate change might be altering the longstanding ecological cycling represented by Florida red tides. “There are all these different, changing dynamics.”

“Just like anything,” Hubbard adds, “it’s not necessarily entirely predictable.”

Mitigating the effects of red tides

Although plenty of discoveries lie in wait for the scientists studying the basic biology and ecology of K. brevis and the nature and evolution of red tide events, funding these days is usually earmarked for monitoring and mitigation. Heil was the recipient of some of that episodic funding last October, when the Andrew and Judith Economos Charitable Foundation donated $1 million to establish the Red Tide Institute at Mote, as the protracted K. brevis bloom churned in the Gulf and made its way around the state’s southern tip.

On a rainy July day at the facility this year, Heil’s head lab technician, Amanda Muni-Morgan, swirled several beakers filled with greenish water—it was chock-full of K. brevis cells. She added gramine, an extract from the giant cane plant (Arundo donax) that may help lyse the phytoplankton cells, but may also help mitigate the aftereffects. “Killing K. brevis cells is not difficult,” explains Heil. “The problem is, you release the toxin when you kill the cells.”

IN SEARCH OF SOLUTIONS: Amanda Muni-Morgan, a technician in Cynthia Heil’s Mote laboratory, tests the effectiveness of compounds in killing K. brevis cells and neutralizing brevetoxins.

Bob grant 

Heil says she and her colleagues plan on testing a variety of other compounds as potential treatments to mitigate the toxicity and longevity of red tides. Currently, researchers and public health officials have no options at their disposal for effectively controlling blooms. Heil adds that she’s focusing on naturally derived compounds such as gramine, as they are less likely than harsher, synthetic chemicals such as herbicides to perturb the environment when added to seawater in the field. This work is in its early stages, notes FWRI’s Hubbard. “Right now, coming up with solid, robust strategies for testing those compounds is important.”

Unfortunately, funding for phytoplankton biologists seeking to untangle that complexity is patchy, says Kirkpatrick. Large and widespread blooms like the 2017–2019 red tide attract a lot of media and public attention, but only happen periodically, and “episodic events get episodic funding.” 

The result, she says, is slowed scientific progress on the basic biological front. “Over the years, I’ve had people say to my face, ‘Why don’t you know more?’” she recalls. “It’s not for lack of wanting to know more. It’s for lack of the funding to do the studies to know more.” 

Bob Grant is editor in chief of The Scientist. Email him at rgrant@the-scientist.com