The accidental parasitologist

Having a parasite that lives in the rectums of Moroccan tortoises named after him is one of the more unusual of the many honours that have been bestowed on the 2013 recipient of University of Otago's Distinguished Research Medal.

Professor Robert Poulin (Zoology) has been awarded the University's highest research honour for the remarkable quality and quantity of his research on parasite ecology and evolution over the past two decades. He will be presented with the medal at a public lecture he will deliver in November.

Poulin describes himself as “an accidental parasitologist”. He studied aquatic biology at McGill University in Montreal and at Université Laval in Quebec City before switching to the study of parasites.

“At the very beginning of my postgraduate studies on the growth and mortality of young fish, I noticed external parasites on the fish I was studying. My supervisor said, 'Remove them with tweezers and discard them. They are irrelevant.' But I put some of the fish with and without parasites in aquaria and it became clear to me that the parasites changed the behaviour of the fish. So I decided to do my PhD on that instead.”

The French-Canadian held fixed-term positions at two universities in Quebec province before he and his wife and the first of their two sons emigrated to New Zealand in 1992 to join the Department of Zoology. (Both boys have gone on to study worms and viruses at Otago: not in zoology, but in computer science.)

“I was looking around for permanent positions and came across an advertisement for a job at Otago. I found out that I knew of three people here [in the Department of Zoology]. And New Zealand was already on our short-list of places that my wife and I absolutely wanted to visit.”

Two decades later Poulin is regarded as a world leader in the study of parasite ecology and evolution. His prolific publishing record includes writing, co-writing or editing six books, and writing or co-writing 25 book chapters and about 450 peer-reviewed journal articles. One of his books, Evolutionary Ecology of Parasites, a 342-page second edition of which was published by Princeton University Press in 2007, is an international standard text in its field.

“My initial interest was on the impact of parasites on fish, but as I delved into the biology of the parasites I found out that they are not just these disgusting little beasts that have no other purpose than to suck energy from the host. They actually have a very complex biology of their own.So the research we do now is split between the biology of the parasite and the impact of the parasites on the biology of the host species.”

Poulin says the research programme in parasite ecology and evolution he has established at Otago has three main branches, reflecting his main long-term interests.

“First, we are investigating the forces shaping the evolution of parasites, including their ability to manipulate host behaviour. Many parasites can pull the strings and make the host do what they want it to do. That might sound like science fiction, but it is a very common phenomenon.”

Poulin gives the example of water-loving worms that grow inside land-loving weta. Once the worms have used up all of the resources inside the weta and are ready to come out, somehow the signals in the wetas' brains are altered to compel the insects to jump into water. The adult worms then emerge and the expedient weta soon die.
“And if you grab the weta and you remove it from the water and you put it back on land it's going to reorientate itself, find the water again and jump back in,” Poulin adds. “It's crazy.”

Another area of research on parasite evolution involves documenting transmission routes of numerous parasitic worms from host to host and their impacts on the survival and reproduction of key marine and freshwater animal species.

Poulin cites the case of trematodes (flatworms or flukes) that are transmitted from snails to whitebait to eels. Inside the aquatic snails the parasites castrate their hosts and transform them into parasite factories. The parasite larvae emerge from the snails and swim in the water until they contact the skin of young non-migratory galaxiids or whitebait and burrow inside, where they deform their hosts' spines. The whitebait can't swim properly and are easy prey for freshwater eels. Once inside the eels the parasites grow to become adult worms and their eggs pass out in the faeces of the eels, hatch into small larvae that infect the snails and the cycle starts all over again.
Such stories help explain why Poulin and his students are more interested in studying parasites than cuddly pandas or cutesy penguins.

“The second major area we are studying is the role of parasites in coastal ecosystems, including how parasitism may interact with climate change to influence the properties of ecosystems.”

Poulin says as temperatures increase and oceans become more saline and more acidic, some species could disappear locally as a result of an increase in the number of parasites, which thrive in warmer temperatures, and a decrease in the hosts' resistance to them because of changes in water temperature and quality.

“Third, I have long been exploring large-scale patterns of parasite biodiversity and biogeography, in the hope of better understanding the processes behind the diversification and distribution of parasites and diseases.

“We are interested in figuring out why, for instance, if you look at the five or six thousand species of birds that are currently known, some of them are parasitised by 50 or 60 different parasite species, whereas others only have two or three.”

Poulin and his Evolutionary and Ecological Parasitology Research Group of research fellows, researchers and postgraduate students have made significant contributions and discoveries, including identifying parasites new to science.

“Since we are the first group to work on parasites of wildlife in this part of the world, every time we look at a new animal we find new parasites."

For instance, the most common freshwater fish in New Zealand is a little fish called the common bully. These things are infected with parasites that no one had seen before. In Tomahawk Lagoon there are bullies that are so heavily infected with parasites that up to 25 per cent of the mass of the fish is actually parasite, and the species that accounts for most of these is a completely new species.

Despite their negative press, Poulin says parasites can play a positive role – and not just as a contrived form of pest control.

“For instance, we found that in Otago Harbour the impact of one parasite species on the burrowing ability of cockles has, through a domino effect, had a positive consequence on the biodiversity of the inter-tidal mudflats. More cockles stranded at the surface make the habitat more suitable for a range of other little crustaceans, providing more food for fish and birds.”

The Distinguished Research Medal is the latest in an impressive list of honours granted to Poulin. In 2001 he was elected a Fellow of the New Zealand Royal Society and he received the New Zealand Association of Scientists' Research Medal. The following year the Royal Society awarded him one of its prestigious James Cook Research Fellowships. The Parasitology Section of the Canadian Society of Zoologists presented him with the Robert Arnold Wardle Award in 2007 in recognition of his outstanding contribution to parasitology. And he was honoured with the New Zealand Royal Society's Hutton Medal for excellence in animal sciences in 2011.

Ethics (and a sense of modesty in most) prevent researchers from naming newly discovered species after themselves, but one of the side benefits of academic success is the honour of your peers naming new species after you. That's what happened to Poulin in 2003 when two admiring French parasitologists gave the name Tachygonetria poulini to a species of pinworm they had discovered while researching parasites in North African tortoises.

IAN DOUGHERTY