Sex change artists
of the Bay of Fundy
By Travis Webb

OTTAWA — This shrimp has traveled a long way. She was born and raised on the mudflats of the Bay of Fundy – an inlet off the Atlantic enclosed by the coast of Nova Scotia and New Brunswick.

They may be small, but Corophium play a pivotal role in the the Bay of Fundy.

Last summer, the tiny shrimp – she’s no larger than a dime – made the 900 km journey to Ottawa.

Now, she spends her time in a bar fridge that sits on a lab bench in Carleton University’s Nesbitt Building. She lies there quietly, waiting for her big day.

When they’re ready for her, she’ll be whisked onto a sterile, brightly-lit operating surface. Moments later, the procedure will begin.

They want her ovaries.

“It’s a lot of work,” says Mark Forbes, the Carleton biologist responsible for the shrimp’s ordeal.

But it’s work with a purpose.

After all, these shrimp may hold a key to the survival of one of Canada’s most important ecosystems.

More than mud

From the highway, Peter Hicklin says the Bay of Fundy mudflats look pretty barren. Wet deserts, he calls them.

But walk out onto a flat and he says it’s a different story.

“It’s like standing in a bowl of Rice Krispies,” says Hicklin, a research scientist with the Canadian Wildlife Service in New Brunswick. “You hear snap, crackle, pop . . . It’s alive.”

Much of that life is Forbes’ shrimp, Corophium volutator. By mid-summer, Hicklin says the mudflats swell with more than seven billion of them.

With these incredible numbers come great responsibility: The shrimp work the pumps at one of the biggest gas stations in the world.

Each summer, two or three million Semipalmated Sandpipers descend upon the mudflats to fuel up. The bay is their only stop on their trip from the Arctic to Brazil, says Hicklin, who has studied the birds for more than 20 years.

“The sandpipers feed almost exclusively on Corophium,” says Forbes. “They double their weight . . . and use that fat to fly 4,000 kilometres non-stop down to South America.”

Take the shrimp out of Fundy and the birds could be facing a serious fuel crisis.

Mudflats like the one in Johnson's Mills, N.B. are home to millions of sandpipers every summer.

But serving the sandpipers is only the most dramatic example of Corophium’s importance to Fundy. According to Hicklin, the shrimp help provide nutrients for Right whales living in the bay. Forbes says 15 species of intertidal fish rely on Corophium as a food source.

Research even suggests the burrows the shrimp dig help keep the mudflats – and the habitat they provide for other organisms – from washing away.

“Corophium is so central to the food web that we call it a key species,” says Forbes. “If they were to go (extinct), it could have some very severe ecological consequences.”

It’s a threat Forbes says isn’t that far-fetched. Corophium populations in Europe have collapsed in the past and Forbes says Fundy has experienced some small localized crashes in recent years.

“(Corophium populations) blink on and off,” he says. “(My lab) is interested in trying to figure out what the factors are and determine whether parasites are one of them.”

Parasites enter the picture

Forbes is a parasitologist. By definition, he says a parasite lives in or on another organism. Having established a home, the parasite uses its host to derive its own nutrient requirements. In the process, it causes some degree of harm to its gracious provider.

But Forbes is interested in more than just these individual effects. Instead, he explores ecological parasitology – the study of how parasites affect the distribution and abundance of organisms in an ecosystem.

Much of Forbes' research focuses on species which hold ecological or economic importance.

Over the course of his career, Forbes has worked with several species including dragonflies and frogs. He says most of the hosts he studies hold some sort of economic or ecological importance.

His work with Corophium in the Bay of Fundy is no different.

Still, Robert Poulin, a parasitologist at the University of Otago in New Zealand, says the European Corophium extinctions show the reach of Forbes’ research.

“Corophium and their close relatives are hugely abundant in intertidal mudflats all over the world,” says Poulin. “(Forbes’) work has potential implications that extend beyond the Bay of Fundy.”

David Marcogliese, a parasitologist with Environment Canada, agrees. He also says much of Forbes’ research – including his Corophium studies – can be applied to more general host-parasite relationships.

“(Forbes’ work) is conceptually and theoretically interesting,” says Marcogliese. “He’s not just going out there and measuring things. In that sense, his work is quite novel and progressive.”

But for now, Forbes says he’s not focused on these peripheral benefits.

He just wants to wrap his head around the Corophium dating scene.

Battle of the sexes

Corophium males have it pretty good.

They’re surrounded by enormous numbers of friends and family – sometimes as many as 60,000 of them per square meter.

Better yet, most of the company is female.

During mating season, Corophium males investigate neighbouring burrows searching for females.

Depending on the location, Forbes says there are anywhere from four to 12 females for every male. While this might sound good for the guys, it presents a potentially serious problem.

“If you have too few females, the population may not grow as quickly,” says Forbes. “We may get so many females that males are actually limiting and (Corophium) can have these localized crashes.”

In this limiting scenario, Corophium males aren’t able to fertilize enough females to sustain the population. An added complication, says Forbes, is that Corophium mate on a lunar cycle. Males only get one chance a month to meet as many females as they can.

It’s a situation akin to asking one mailman to complete 12 routes all in one shift. Some female shrimp will get their delivery, but by the end of the day, many will be left staring disappointedly into an empty mailbox.

With so many potential mothers ignored, population crashes in Fundy become a possibility.

Forbes turned to his specialty for an explanation.

The idea isn’t without precedence. Marcogliese says research out of England has shown that a certain parasite alters the sex ratio of another species of crustacean.

“There’s all kinds of interesting things going on with (feminizing) parasites,” says Marcogliese. “They can have profound impacts on populations of organisms.”

But could this be happening in Corophium?

“Oh, it’s quite possible,” says Marcogliese.

So Forbes and his lab – specifically post-doc Selma Mautner – set out to harvest shrimp from Fundy last summer. Back in Ottawa, the team began cutting open Corophium and removing ovaries from females and testes from males.

It’s a delicate process, but it allows them to extract and identify the DNA contained in the sex organs of the shrimp. If an invading parasite is present, its genetic code will show up in the DNA analysis.

“We found a parasite that is found only in the ovaries of Corophium females,” says Forbes.

Early returns

In the initial group of 37 Corophium males , none carried a parasite in their testes. Meanwhile, a parasite was detected in the ovaries of seven of the 25 females.

“We believe the parasite feminizes (male Corophium) and continues its life cycle by being passed on in daughters, granddaughters, and great granddaughters,” says Forbes.

According to Forbes, the parasite can only survive in the nutrient-rich ovaries of Corophium females. When the female’s eggs are fertilized, the parasite sees an opportunity to pass on its own offspring.

But if the parasite’s progeny enters an egg destined to become male, it panics. It can’t live in that environment. As the young Corophium grows, the parasite flips the shrimp’s gender. A genetic male develops into a female.

Corophium ovaries provide ideal accomodation for Forbes' microscopic parasite.

Forbes says the parasite may perform this trick by altering hormone secretions at a sensitive stage of development. But this theory is pure guesswork – the parasite is too small to study at Carleton.

As a result, Forbes says he knows little about details like what harm the parasite brings its Corophium host. To learn more, the team sends samples of the parasite to England, where they are examined under a scanning electron microscope.

For now, Forbes and his team must satisfy themselves with what the DNA sequence of the parasite tells them.

“It’s quite different from anything we know about,” he says. “This parasite is new to science.”

According to Forbes, the DNA sequence also indicates the parasite belongs to a group of single-celled parasites called the Microsporidia. Given its genetic similarity to these parasites, one can get a picture of how Forbes’ parasite may operate in Corophium.

For example, Microsporidian parasites reproduce by ejecting spores. When a spore encounters a host cell that appeals to them, it pricks the cell with a needle-like tube and the parasite is injected inside.

This is likely how Forbes’ parasite reproduces.

But these details aren’t Forbes’ immediate concern. Instead, he and his team want to document the presence of the parasite in the most female-biased populations in Fundy. Collecting this data would be a first step towards definitively attributing skewed sex ratios to the parasite.

If this is established, it may be possible to link the parasite to population crashes among Corophium. So far, he says the numbers indicate as much.

“We’ve actually seen evidence of a population crash and as far as we know, (the parasite) is more prevalent there than anywhere else we’ve seen yet,” he says.

Forbes says they have yet to find a skewed population the parasite hasn’t infected. At the same time, however, he hasn’t been able to find a population with a one-to-one sex ratio.

Discovering such a population would help Forbes test his theory. If the parasite hadn’t infected these Corophium, it would add weight to the idea that the parasite feminizes the shrimp and threatens their numbers.

Positive parasitism?

Dean McCurdy, a researcher at Albion College in Michigan and a collaborator with Forbes on the Corophium Project, says the parasite may not be a threat at all. He says by feminizing shrimp, the parasite may actually facilitate Corophium’s enormous population.

“If you (have) nine females and one male that can fertilize all of them . . . than all of the females produce offspring,” he says.

With an equal ratio, five males have to compete for five females. Consider that five factories can’t produce as much as nine factories, assuming they have the staff to operate them.

Similarly, nine Corophium females can produce more offspring than five.

“It’s possible this micro parasite is driving the whole system,” says McCurdy.

Forbes says it’s a possibility but adds it would only work at low levels of infection.

Still, these are the kinds of effects Forbes wants to explain. While his project isn’t there quite yet, Robert Poulin says Forbes’ work should provide a richer understanding of Corophium and feminizing parasites.

“There are still many important questions to be asked about these parasites,” he says. “I’m certain Forbes’ work will take some original directions.”

The Bay of Fundy mudflats would be dramatically different without Corophium.

Meanwhile, Peter Hicklin says parasites aren’t a serious threat to Corophium populations. A more immediate concern, he says, is human-influenced changes in sedimentation rates in the Bay of Fundy. According to Hicklin, these changes may be re-shaping the shrimp’s habitat.

Regardless, Hicklin says any Corophium research is worthwhile.

“I have great respect for that little creature,” he says. “The more work is done on them, the more we can appreciate the (need for) its conservation.”

In the end, Forbes says there wouldn’t be much he could do if there was a population crash in the near-future.

Instead, he says a Corophium collapse may actually provide a good opportunity for further research into the tiny shrimp holding the Fundy food web together.

“(We want to be) at least somewhat prepared for documenting the effects of those crashes,” he says. “We want to be Johnny-on-the-spot if they do occur.”