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24 JULY 2008

In praise of parasites
In ecological analysis, parasites are typically just afterthoughts and also-rans. Sure, they can harm or kill the hosts they infect, but when ecologists measure food webs (as they now call food chains) parasites don't carry much clout. That could change, at least for some ecosystems, in light of new measurements of three estuaries in Baja California.

Researchers spent three years looking at randomly-chosen plots in these coastal environments, and found surprising quantities of parasites. In fact, for some pairs of parasites and hosts, the biomass controlled by the parasites was actually higher than the mass of the uninfected hosts. And in total, the mass of parasites "was much greater than that of the fish and birds that are the top predators," says Armand Kuris, the study leader. "We found that there was a surprising and substantial biomass of those parasites we could recognize in the estuarine system."

A study in Baja California finds that the mass of animals controlled by parasites can exceed the mass of uninfected hosts. Is ecology downplaying the role of parasites in food chains?

The study was the first to look closely for parasites among many of the species of plants and animals in these estuaries, according to Kuris, a professor of zoology at the University of California at Santa Barbara.

Why put parasites on the bathroom scale? Because mass matters, says Kuris. "We thought there must be unrecognized but very substantial energy flows through the [parasite] infections, and the only way to find out was to do the work." Based solely on their mass, parasites must play a significant role in who lives, who thrives, and who dies in these estuaries, and perhaps elsewhere as well.

Although Kuris uses "parasite" and "pathogen" rather interchangeably, the study looked only at multi-cellular parasites, not bacteria or viruses, and thus probably underestimates the overall punch of parasites.

Castration complex
One fearsome-sounding category of parasite jumped out from the project's data -- the "parasitic castrators" that infect certain snails. (Fess up: Was that the sound of your knees snapping shut?) Parasitic castrators infect the host's reproductive tissue, and in the estuaries, Kuris says, "they were very big players. Even for people who study parasitic castration, I don't think anybody thought they would play such a role at the ecosystem level."

In some of these snails, castrating parasites make up 13 to 39 percent of the host animal's weight.

uninfected California horn snailinfected California horn snail

Left: An uninfected California horn snail, with its shell removed, with its testes in orange. Right: In this infected snail, a "castrating parasite" has fully replaced the testes. In thee Baja estuaries, the total mass of parasites exceeds the mass of the birds that live there in the winter. Courtesy Todd Huspeni

You might ask (we did when we finally relaxed our knees), why a parasite would gain an evolutionary advantage from roadblocking reproduction in its host. But that is less harmful than it sounds, Kuris says, because it only reduces the average size of the next generation by one snail.

No biggy.

But in return, castrating confers an evolutionary advantage to the parasites, Kuris adds. Typically, parasites steal the host's resources, making it less likely to survive and thrive, but because castrating parasites are less demanding, they can produce more offspring. In fact, he says the parasites are so "physiologically sophisticated" that they may steal less energy for reproduction than what an uninfected host would normally need to make its own offspring.

Do the math. If one-quarter of a snail's weight consists of castrating parasites, and the snail lives for a decade, and each day the parasites release infectious agents into the water, then you end up with a lot of parasite -- from a snail that is not making any more snails. For these reasons, Kuris calls the castrating parasites "body snatchers": in the process of neutralizing the host's reproductive potential, they also subvert it into a factory for more worms.

Does it generalize?
The study was the first effort to look comprehensively at the mass and distribution of parasites in any ecosystem, Kuris says, and it remains to be seen whether the results apply to other ecosystems. Host density and the degree of interactions among species may affect the presence of parasites, Kuris says. Clustering of potential hosts makes disease problematic on animal farms, he says, and an intense level of interaction may explain the disease burdens in coral reefs and rain forests.

"If we don't think about parasites explicitly, we never see them."

If parasites can comprise as much biomass as top predators, they deserve new respect from ecologists, Kuris adds. "We are not saying everyone has to study them, but everyone has to consider whether they need to work on them, whether to fold them into their studies."

The study may also have medical implications, because parasites can be defined to include bacteria and even viruses. Medicine has tended to focus on specific damages due to infections, but part of the burden of disease may result from the involuntary "contributions" that the parasite extracts from its host, Kuris offers, and/or the costs of any immune reaction to the infection. If so, doctors may want to focus on slowing parasite reproduction and speeding the development of host defenses, Kuris says. "This opens a window of creativity for some very novel strategies for management of infectious disease, rather than just killing the pathogens."

The estuary study was intended to provide a holistic view of the role of parasites in an ecosystem, says Kuris. "There was a need to make parasites visible. We and lots of others have studied all sorts of effects of diseases on individual hosts, on populations and sometimes interactions between species. These only arise when somebody detects something in the host. If we don't think about parasites explicitly, we never see them, they are truly invisible."

- David J. Tenenbaum

Bibliography
• Ecosystem energetic implications of parasite and free-living biomass in three estuaries, Armand M. Kuris et al, Nature, Vol. 454|24 July 2008| doi:10.1038/nature06970


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