The (accidental) marine disease ecologist

Blue crabs, Callinectes sapidus.
Blue crabs, Callinectes sapidus. (Image courtesy of Donald Behringer.)

University of Florida marine ecologist Donald Behringer, Ph.D., has held a fascination with crustaceans since childhood. Back then, he caught crayfish and crabs while exploring the creeks around his house and the nearby Chesapeake Bay. Later, as a Ph.D. student at Old Dominion University he studied Caribbean spiny lobsters, and as a UF professor he now explores the ecology of lobsters and crabs globally.

But along the way, as he studied these marine creatures, he also came to know the growing list of parasites to which they play host. Behringer may not have set out to become a leader in the growing field of marine disease ecology, but with each new discovery, he grew into one.

In 2020, he was the lead editor of Marine Disease Ecology, an academic book published by Oxford University Press. “When Oxford published our book, it was a recognition that this was a mature field that had reached the stage where it was time for a book to pull the state of knowledge to together in one place,” Behringer said.

The book was a milestone for a journey that began 14 years earlier with the publication of a portion of his dissertation in Nature. In 2006, Behringer had reported the discovery of the first virus known to infect Caribbean spiny lobsters — Panulirus argus Virus 1, or PaV1 — and how it altered their behavior.

The experience hooked Behringer on a career journey investigating marine parasites and their hosts.

Eurpean spiny lobsters, Palinurus elephas
Behringer studied European spiny lobsters, Palinurus elephas, in Spain as a Fulbright Scholar in 2015-2016. (Image courtesy of Donald Behringer.)

Parasite and host ecology and evolution

The Behringer lab for marine and disease ecology, which is located in the UF School of Forest, Fisheries, and Aquatic Sciences, studies a wide array of issues. At the broadest level Behringer’s agenda focuses upon how parasites affect the ecology of their hosts. But his team also investigates the role of environmental drivers on host-pathogen relationships, and a few times a year they get the thrill of reporting a newly discovered parasite. Behringer is a faculty member of the UF Emerging Pathogens Institute.

Recently, Behringer coauthored a paper in BioScience which reviewed various strategies animals use to avoid acquiring an infectious disease. Many animals, including marine crustaceans, have used physical distancing long before it became popularized among humans during the COVID-19 pandemic.

“A healthy lobster can determine when another one is infected with PaV1, and they stay away from it,” Behringer said. “That behavior is actually triggered before the infected animal becomes infectious. It’s a very effective mechanism at reducing transmission risk.”

In general, avoidance behaviors are understudied in marine animals when compared to land-dwelling animals. And yet, when researchers such as Behringer look in oceans, rivers, and lakes, avoidance behaviors are widely used in aquatic environments. They help marine and freshwater creatures alike to evade infectious agents such as parasites, fungi, protists, bacteria and viruses.

Caribbean spiny lobster, Panulirus argus, congregate beneath a coral head.
Caribbean spiny lobster, Panulirus argus, congregate beneath a coral head. (Image courtesy of Donald Behringer.)

In work recently published by the Philosophical Transactions of the Royal Society B, Behringer and former lab member Jamie Bojko, Ph.D.—who is now a faculty member of Teesside University in the United Kingdom—reviewed alignment between avoidance behaviors in aquatic and terrestrial animals.  Behringer and Bojko also explored how environmental characteristics affect behaviors to help marine animals avoid infections. Given the recent acceleration of emerging and re-emerging infectious agents, understanding avoidance behaviors in marine animals is an important step for forming an understanding of marine disease ecology and epidemiology.

Crab parasites and habitat health

Another avenue of research Behringer’s lab is exploring is how environmental degradation alters relationships between hosts and parasites. Environmental change, ocean warming and acidification, and fishing practices can alter the habitat in which marine creatures live. And habitat changes can influence changes in health or disease for the creatures that call it home.

In the waters around the Florida Keys, for example, stone crabs can be affected by harmful algae blooms. These events are caused by an over proliferation of cyanobacteria which turns the water pea green. These blooms alter the marine communities where the stone crabs live.

Behringer and his Ph.D. student, Elizabeth Duermit-Moreau, hypothesize that crabs are unable to feed on their normal fare during these events. This causes them to switch to new prey items and potentially be exposed to new pathogens.

“We are interested to know how habitat degradation changes their foraging patterns,” Behringer explained. “How the condition of habitats they feed in, and the types of things they feed on, might potentially reflect the parasites they then acquire.”

Two men sit in a boat offshore and study blue crab movements.
Behringer and UF marine ecologist, Douglas Marcinek, study blue crab movements offshore of Jacksonville, Fla. (Image courtesy of Donald Behringer.)

Crab and lobster viruses, temperature, and hemispheres

The Behringer lab also studies how temperature and oceanographic distance affect the relationship between hosts and viruses. For example, blue crabs (Callinectes sapidus) can become infected with CsRV1, a lethal reovirus, but prevalence rates appear to vary throughout the crab’s extremely wide range.

Blue crabs span the northern and southern hemispheres, from Maine to Argentina. Straddling such a wide distribution means that this species has adapted its life history to different temperatures. In the far northern and southern parts of its range, where water temperatures fall below about 50-degrees Fahrenheit, blue crabs overwinter by hibernating in the mud. But in warmer tropical waters, they stay active throughout the year.

This line of research showed how climate and seasonality affect where CsRV1 is found in the northern and southern hemispheres. The virus was first detected in North Atlantic waters but has since been found in crabs off the coast of Brazil and Uruguay. There are gaps in knowledge about where the virus occurs between these wide-ranging places, but it appears the virus is only transmitted between crabs on the ocean floor.

“It only infects the crabs cruising around on the bottom,” Behringer said. “The virus does not appear to infect the larval crabs in the water column.”

In a paper recently published in the Marine Ecology Progress Series, Behringer and collaborators report that CsRV1 is prevalent throughout the range of blue crabs but was significantly higher in the northern and southern parts of their range compared to the tropics. They did not find it in any related Callinectes species.

To better understand how the blue crab’s lifecycle affects CsRV1 infection dynamics, Behringer’s lab is engaged in field collections and laboratory transmission experiments. Their field surveys showed that the virus is present at a lower rate in crabs that hibernate during the winter.

A man holds a blue crab with an acoustic tag.
A blue crab with an acoustic tag, about to be returned to its habitat for study. (Image courtesy of Donald Behringer.)

“We want to understand how the virus transmits and affects the blue crab hosts, when they are overwintering,” Behringer explained. “When an infected crab is hibernating, does the virus also remain largely dormant? Or does it kill the crabs before they emerge from hibernation? This could have important implications for the evolution of virulence in CsRV1.”  

The lab is also investigating if or how infection with CsRV1 affects the movement of blue crabs. By attaching acoustic tags or “little pingers” to them and then using hydroacoustic receivers, his team can determine the speed and direction of their movements. They then compare the movements of healthy crabs in the wild with experimentally infected ones in a laboratory.

“Then we can ask questions and draw inferences using mathematical models,” Behringer said. “We can say, for example, ‘The sick guys are moving X% less so what is the likelihood they will get from one bay to the next,’ based on the relative difference in movement.”

The big-picture goal is to build a model that simulates how blue crabs move on the ocean floor, how their larvae move through the water column, and how the virus infects them over a broad geographic rage with large temperature gradients. Partners on the project include the University of Maryland and Shedd Aquarium with support from the National Science Foundation.

Caribbean spiny lobsters also have a large geographic range and studies have shown that up to 17% of adult lobsters are infected with PaV1 across the wider Caribbean. Working with researchers from the University of Miami and Old Dominion University, Behringer contributed to a study that investigated how PaV1 might disperse over large regions of the ocean with complicated water movements.

The team modeled whether the virus was more likely to have spread through water currents outside of a host, or within infected post-larval stage lobsters. They then compared the model results to the Caribbean distribution and genetic structure of the virus to evaluate how it most likely spreads.

A man in scuba gear records data in the ocean.
Behringer records data during a survey of juvenile European spiny lobsters in the Columbretes Islands with colleagues from the Centre Oceanogràfic de les Balears in Spain. Behringer was in the United Kingdom and Europe as a Fulbright Scholar 2015-2016. (Image courtesy of Donald Behringer.)

Detecting and describing novel marine pathogens

Inevitably, by conducting field research on marine animals, new pathogens tend to turn up. Sometimes they are entirely new to science, and other times they may be known but are found for the first time in a new host. Behringer works with colleagues at the Emerging Pathogens Institute to genetically sequence novel viruses and other parasites.

His team, along with EPI collaborators from the UF Veterinary Medical School, recently reported that PaV1, along with two similar DNA viruses that infect freshwater demon shrimp and European shore crabs, are part of a distinct family of viruses for which they proposed the new name Mininucleoviridae. PaV1, it turned out, was also the first virus in a whole new family of viruses.

Behringer’s lab has also described a new RNA virus detected within the parasite of a Sargassum shrimp, and they contributed to the first report of a new nudivirus that infects demon shrimp. They found an entirely new lineage of microsporidia infecting Florida crayfish, and a new DNA virus that is likely from a new genus and infects flat-back mud crabs.

“We sometimes find new things by doing targeted surveys— but it’s often serendipity,” Behringer said. “You can’t go looking for something that you don’t know exists yet. But it’s always exciting when you stumble across something that just looks different.”

The thrill of discovery is not all that different, Behringer reflected, from how he felt when exploring the Maryland creeks all those years ago.

He looks forward to working with fellow EPI faculty member Sadie Ryan on an upcoming project that will explore how parasites influence biological invasions in crayfish.

Written by: DeLene Beeland