Most visitors to the NRS’s Carpinteria Salt Marsh Reserve are impressed by the diversity of birds living in the estuary. But when Kevin Lafferty, a scientist for the U.S. Geological Survey, visits the marsh, he sees something completely different — parasites.
“If you drive by the marsh and look out the window, you see the egrets and all the other incredible bird life,” Lafferty explains. “But the biomass of the larval trematodes that live in the snails alone is greater than the biomass of all the birds living in the estuary. If you could see trematodes with binoculars, you wouldn’t bother looking at the birds because you’d be overwhelmed by the importance of the parasites in that system.”
Lafferty, together with his long-time research partner, UC Santa Barbara professor Armand Kuris, and an ever-changing group of graduate and undergraduate students, has spent almost two decades exploring the world’s parasites. This work, which began as an investigation into infected snails at the marsh, has grown to become a wide-ranging examination of the impact of parasites on ecosystems throughout the world and perhaps even on human societies.
Both Lafferty and Kuris stumbled into parasitology almost by accident. As an undergraduate at Tulane University in Louisiana, Kuris was inspired by a charismatic teacher. Lafferty, who began his career as a “standard” marine biologist, discovered the field when he was asked to teach a parasitology lab in the late 1980s. In both cases, becoming aware of parasites changed their view of the world. Their research has convinced them that much of what goes on at an estuary, such as the Carpinteria Salt Marsh, is controlled by parasites. From the number of snails grazing in the mud, to the way the fish swim, to the amount of effort a bird expends to catch a fish — parasites play a key role in each of these events. Even the bird droppings that fall on the tidal flats are little more than a delivery system for worm eggs that allow parasites to complete their life cycles. And Lafferty and Kuris are confident that the same is true for other ecosystems around the world.
They Came from the Marsh
At first glance, the 120-acre Carpinteria Marsh doesn’t look like a particularly promising locale for extracting valuable scientific information. Although it provides critical habitat for migratory waterfowl and a number of endangered birds and plants as one of the last remaining tidal estuaries on the Santa Barbara coast, it’s pinned against the shoreline by U.S. Highway 101 and the busy Southern Pacific railroad tracks. Access to the marsh is through an aging industrial park. And the water that flows through its channels is heavily affected by runoff from the agricultural fields on the surrounding hillsides and the housing developments that cluster around its edges.
Yet the marsh has provided a crucial laboratory in the evolution of Kuris and Lafferty’s investigations. “The Carpinteria Marsh is our core study area,” states Kuris. “It’s been critical to our work because we’re able to do manipulative experiments there. It’s designed for that and it’s protected, so we can work undisturbed. By combining Carpinteria with other NRS sites like Coal Oil Point, we have the opportunity to compare the workings of different estuary systems.”
Much of the pair’s early marsh-based investigations focused on the California horn snails (Cerithidea californica) that dominate the estuary’s mudflats. The snails serve as intermediate hosts for more than 20 trematodes, parasitic worms that rely upon multiple hosts to complete their life cycles. One focus of Kuris and Lafferty’s investigations was how much control the worms had over the abundance of their hosts. In the horn snails, they found the answer to be clear — a lot. Up to 40 percent of all of the marsh’s horn snails are infected by the trematodes; but even more importantly, 100 percent of the large snails are infected.
In fact, the trematodes have taken overtheir hosts, castrating them so that noenergy is wasted on reproduction and then taking advantage of this energy to grow larger. Parasitic castrators have been of particular interest to Kuris. “A typical parasite is less than 1/1,000th the size ofits host,” he explains, “while a typical parasitic castrator can weigh anywherefrom 5 to 40 percent of the weight ofits host. The castrated host gives theparasite an opportunity to get huge and,inevolutionary terms, produce many more,and higher quality, young.”
Parasites must maintain a precarious balance, because they have a vested interest in maintaining the health of their host. If it dies, they die. But, at the same time, it needs enough energy from its host to thrive. For example, every time a hookworm sucks blood from a human, it degrades its own habitat, the human does a little worse and is a little more likely to die. “Evolution says that parasites have to modulate their impact. So, what can they take away so as not to degrade their habitat?” Kuris asks, then answers his own question: “Reproductive energy. Organisms devote a huge amount of energy to reproduction, but if the host is castrated, all of that energy goes to a parasite. All it has to do is not exceed that amount of energy. It’s an interesting strategy and it’s not easy to do, so it doesn’t evolve overnight. It’s relatively rare.”
The trematodes use their snail host’s energy for their own reproduction, emerging as free-swimming larvae that seek out and attach themselves to the gills of fish. The most common parasite in the marsh, Euhaplorchis californiensis, then moves on to its next intermediate host, the California killifish, Fundulus parvipinnis. After attaching to the fish’s gills, the worm migrates into the fish’s brain. Lafferty and Kuris had long been curious about the impact that the parasite might have on the fish — might it alter its host’s behavior for its own ends? But until the mid-1990s, they hadn’t pursued the topic.
Fishy Behavior Sparks Scientific Breakthrough
“The killifish/trematode cycle was one of the dissertation topics we put aside because it seemed too unlikely to produce significant results,” Lafferty admits with a smile. “I worked directly on snails for my PhD at UC Santa Barbara. But, a few years later, we had a very bright undergraduate, Kimo Morris, who wanted to do a project. So I went through my files and said, ‘Here’s an experiment that I’ve written up and have ready to go. Why don’t you try to get something out of this?’” Lafferty wasn’t optimistic. “It was a hypothesis, but we didn’t figure much would come from it. If nothing else, it would give the student the experience of failure, which is part of any scientific investigation.”
Blissfully unaware of his mentor’s misgivings, Morris set to work catching an assortment of infected killifish from the Carpinteria Marsh and uninfected fish from Devereaux Slough at the NRS’s Coal Oil Point Reserve next to the Santa Barbara campus. (The fish there are uninfected because the slough is usually closed off to the ocean and doesn’t support the marine snails required for the parasite’s life cycle.) He then put all the fish together in a big tank and watched their behavior for hours.
Lafferty first asked Morris to list all of the fish behaviors that caught his eye. “He came up with things like, ‘Fish seems to roll on its side,’” Lafferty recalls, “or, ‘They go to the bottom,’ or, ‘They go to the surface.’” Once Morris felt comfortable that he had categorized all of the obvious fish behaviors, his next challenge was to pick a single fish out of the crowd and watch it for half an hour. As Lafferty admits, “In a tank with 40 fish that all look the same, I wasn’t sure that this was going to work. But Kimo got good enough at it that he could watch a fish, keep track of all of its behaviors, and then catch it to see if it was infected.”
The results were dramatic. The fish that exhibited conspicuous behaviors were almost all infected fish from Carpinteria. The non-infected fish from Devereaux Slough were much less likely to draw attention to themselves. This was good evidence that the fish with parasites on their brains were acting differently, but one big question remained: did the changed behaviors make the fish more likely to be caught by birds? And beyond that, were the parasites really changing fish behavior in ways that increased the likelihood that they could complete their life cycles?
To address this question, Lafferty and Morris set up an experiment in the campus lagoon at UCSB. They built two large pens in the lagoon and stocked them with a mixture of infected and uninfected fish. To estimate nonpredator-related escapes and mortality, they covered one pen. The other was left open so birds could feed freely. Then, once again, the researchers patiently sat and watched.
Lafferty recalls what happened next: “Eventually the birds got used to these enclosures and came in and ate the fish. Our hope was that we could net the surviving fish before the birds ate all of them, so that we could see if there had been selectivity on the part of the birds for the infected fish.”
Again, the results strongly supported their hypothesis. The infected fish were 10 to 30 times more likely to be eaten. In fact, the birds didn’t touch the uninfected fish. The unpromising experiment had paid off handsomely for both Lafferty, who began pursuing a whole new set of research questions, and Morris, who today has his PhD and is doing postdoctoral work in marine biology at UCLA. While the uncanny match between theory and observation pleased Lafferty, he also wanted to take the question another step, developing mathematical models that would quantify how advantageous it is for parasites to control their hosts and what evolutionary pressures could lead to this strategy.
Redrawing the World’s Food Webs
If roughly half the snails at the Carpinteria Marsh are infected by parasites … and almost all the large castrated snails in the marsh are really just parasite incubators … and the behavior of the infected killifish is being controlled in part by parasites … and if the parasite larvae alone have more biomass than all the birds at the marsh … and the parasites control all of this biomass, complete with snail shells and fish fins — then why are parasites left off of most food webs?
To Kuris, the answer is obvious: “Out of sight, out of mind. If people could see parasites, more people would study them.” And that’s why the work he and Lafferty do is unique. “We work with parasites, but we are full-on ecologists. We ask completely ecological questions, but then we go on to ask: what is the role of parasite-caused infectious disease in these sorts of things? And that’s still a rather distinctive perspective.”
This approach led them to start thinking about how traditional food webs, which trace the flow of energy through an ecosystem, would be different if the full impact of parasites was taken into account. Also, if the role of parasites is so pervasive in a small environment like the Carpinteria Marsh, could the same situation prevail elsewhere? Lafferty illustrates their logic with a simple story: “If you look at a kid’s book on basic ecology, you learn that the lion eats the gazelle who eats the grass, right? Well, the clever kid is going to ask, who eats the lion? And if you go to the Serengeti and look at fecal samples from 30 lions, you’ll find 20 species of parasites in those samples. So obviously, lots of things are eating the lion, but they’re really small and hard to see. So the assumption has been that they’re not important.”
Lafferty had already demonstrated with the killifish experiment that one type of parasite, a trematode, could have a major impact on predator/prey dynamics. His next challenge was to put all of the marsh’s parasites into a food web, then apply statistical techniques to see whether the food web would be different. Beyond the challenge of collecting all of the data, Lafferty also had to develop new statistical tools that took into account the fact that smaller organisms could eat larger organisms. In most traditional food webs, organisms at higher trophic levels have fewer predators. What’s not considered is that they are actually more vulnerable to parasites. And it’s at the mid-trophic levels, where both predators and parasites are factors, that organisms have the most natural enemies.
“How you describe these things mathematically is very complicated,” Lafferty explains, “but the bottom line is that parasites are heavily connected in food webs. They permeate through the structure in such a way that they modify it significantly.”
Connectance, the ratio of observed links to possible links in a food web, is a major factor in measuring an ecosystem’s stability. Where previous studies had indicated that parasites decreased connectance in ecosystems by an average of 27 percent, the new models showed that they actually increased connectance anywhere from 7.8 to 12.9 percent, depending upon how some interactions were categorized — for example, whether mosquitoes were considered free-living predators or parasites.
Though Lafferty and Kuris are convinced that parasites increase the connectance, and therefore the stability, of an ecosystem, some scientists still question whether those connections actually command much of the system’s energy flow. To answer this challenge, the team must not only identify all of the parasites in the marsh and what they infect, but also the abundance of the parasites and the biomass of all the different species they control.
Kuris is confident that their work and the new mathematical models will prevail. “We’re showing that, even though parasites are small, massive amounts of energy flow along the food web strands that they control. They are major players in marsh ecosystems.”
Wading Beyond Carpinteria
Kuris and Lafferty’s Ecological Parasitology Laboratory is now beginning to investigate whether the work they’ve done at the Carpinteria Salt Marsh pertains to other ecosystems as well. “The results from Carpinteria are so striking, but is it just this one marsh?” asks Lafferty. “Is it all salt marshes in general? Is it all ecosystems in general? We don’t know the answer to that. It will be interesting to find out.”
As a first step in their investigation, the team recently visited a remote, and hopefully pristine, estuary in Baja California. They’re now processing the data from this trip. In the meantime, they’re also planning another, even more ambitious effort — conducting food web studies in a range of diverse ecosystems around the world. Plans are already underway to work with data from a number of sites with rich existing data sets. Potential sites range from the Serengeti plains to Arctic lakes, from the South Pacific to Yellowstone, and from San Francisco Bay to a New England forest. They’ve even proposed studying an organic farm in England.
Kuris is confident that parasites play an important role in all of these ecosystems. “The only places where they might not be important,” he muses, “would be ephemeral systems like vernal pools or areas where the density of organisms is very low. Maybe the deep sea vents.” He stops to consider what he has said, then qualifies it: “However, those are places where parasites certainly exist, so I can’t even say for sure that parasites in those food webs wouldn’t be playing important roles.”
Kuris explains their strategy: “We are using the food web concept as a unifier for looking at a range of ecosystems. We plan to gather the data and will be collaborating with sophisticated mathematical ecologists to advance our ideas, because this concept really complicates what everybody thought about a food web. In traditional food webs, things get bigger; predators are bigger than their prey. Well, parasites are smaller, and they do it in a whole different way. So traditional food web concepts need major modification.”
Kuris is particularly excited about working with data from San Francisco Bay: “It’s the perfect place to investigate how parasites affect connectance and ecosystem stability. It’s heavily invaded, and many of those non-native species have very few of their parasites. They left them behind. So this is an ecosystem operating with fewer and fewer connections, which leads to waves of invasive clams and green crabs whose populations boom and bust. Then you have mitten crabs that multiply in such abundance they clog water intake systems. You see these huge changes because the food web is destabilized.”
Pushing Endangered Species over the Edge?
Another focus of Lafferty’s attention has been the impact of parasites and infectious diseases on endangered and threatened species. Again, his primary concern was that scientists had failed to factor parasitism into their models for predicting the persistence of endangered species. His hunch proved correct: “What we found was that if you had mortality or reduced fecundity that was affected by parasitism, but you assumed it was just background, then you would generate a much more optimistic view of persistence than would be realistic. This suggests that if you have an endangered species where infectious diseases are an issue, you might want to model infectious diseases specifically, or keep in mind that your projections might be too optimistic.”
On the other hand, Lafferty resists the knee-jerk response that “the sky is falling,” that infectious diseases are bad and global changes are making them even worse. Knowing that conservation biologists have listed infectious diseases related to parasites as one of the five main reasons for species endangerment and extinction, he and his colleagues reviewed data on thousands of extinct and endangered species in the World Conservation Union’s IUCN Red List, the most exhaustive database available that lists species of conservation concern and those documented to have become extinct in the past 500 years. The review turned up very few instances where a species had gone extinct due to disease or where disease had played a documented role at all.
“There are exceptions,” he notes. “Hawaiian birds were definitely affected by malaria, and amphibian decline is pretty clearly linked to infectious fungal diseases. So those are two exceptions. For everything else, there’s very little evidence of infectious disease playing a primary role.”
The most common role infectious diseases play in driving extinctions is ancillary. A disease can sometimes reduce a population to low numbers or densities, predisposing them to extinction by other forces. But, at that point, host-specific or density-dependent diseases, especially, would be unlikely to be the sole source of species extinction, because they typically die out when the host population falls below a threshold density.
The reasons for this disease die-out seem clear to Lafferty: “When a population drops to a low number, transmission becomes less efficient, because populations are isolated from one another and individuals don’t come in contact with each other very much. And remaining individuals, because they’re rare, may have access to a lot of resources. So things like habitat destruction, overexploitation, invasive species, and pollution are, by and large, much more important from the conservation perspective. In one sense, we’re saying that disease is important to consider; on the other hand, we’re saying that, with a few exceptions, it’s not something to panic about.”
Impact on Human Societies
While pursuing these wide-ranging investigations into the impact of parasites on ecosystems, Lafferty also began to look into the relationship between humans and parasites. “Could an infectious disease,” he wondered, “indirectly alter human culture through its effect on individual personalities?”
“You can trace this study directly back to the killifish in Carpinteria Salt Marsh,” he points out. “I was impressed with what the parasites do to the fish, and it occurred to me that there’s a very common protozoan parasite in humans, Toxoplasma gondii, that concentrates in our brains and has the same type of life cycle as the trematode in the killifish brain.”
T. gondii’s reproductive phase lives in the cells that line a cat’s intestines. The eggs then shed to the soil, where they can directly reinfect another cat or encyst in the brains of other warm-blooded vertebrates, including humans. If a cat eats the new host, the parasite will complete its life cycle and reproduce. If it is eaten by any other carnivore, it simply re-encysts, a process that can continue up the food chain. Any host, such as a human, that is not usually preyed upon by cats is a dead end for the parasite.
While field studies of infected rodents have not been conducted, lab-based experiments have clearly shown that T. gondii has a demonstrable effect on rodent neurotransmitters, changing their behavior to make them more susceptible to being preyed upon by cats. Rodents infected with the parasite were more active, first to enter traps, and less fearful of cats and their associated smells. They also have elevated levels of dopamine, a neurotransmitter shown to alter novelty-seeking and neuroticism.
What became clear to Lafferty was that this parasite had faced the same sort of evolutionary challenges as had the trematode with the killifish, and it solved them in a similar way. “When you take that parasite and throw it in a human brain,” Lafferty says, “it doesn’t know that it’s not in a rodent brain, that it doesn’t stand a chance of getting into a cat. It has nothing to lose by trying different manipulative strategies on its host. It’s under selective pressure to increase the chances that its host will be eaten by a cat.”
Humans infected by T. gondii initially experience slight flulike symptoms. But even after the parasite goes dormant, it remains in the brain tissue. Though latent toxoplasmosis is usually benign, surveys have shown that the parasite appears to have subtle effects on individual personalities. Research indicates that latent infections can cause long-term personality changes. Infected women, for example, showed higher intelligence, increased superego strength, and affectothymia (warmth, attention to others, kindliness). Infected men, on the other hand, tended to show lower intelligence, decreased superego strength, and novelty-seeking. Both men and women were more prone to feelings of guilt.
Anthropologists use four principal cultural dimensions to describe human cultures — individualism, sex roles, uncertainty avoidance, and class distinction. Some believe that these cultural dimensions correspond with aggregate personalities measured at a national level. Neuroticism in an individual, for example, would aggregate to guilt proneness, which is associated with male control, materialism, and strong rules and structure on a cultural level.
The geographic prevalence of T. gondii varies from 0 to 100 percent. It is controlled by a number of factors: climate (which affects the persistence of infectious stages in the soil), cultural practices of food preparation, and how commonly cats are kept as pets. “There is a tendency towards higher prevalence of infections in tropical areas,” Lafferty notes, “because they’re more humid and don’t freeze. Low-risk areas are places that have lots of freezing, high altitude, a dry climate, really good hygiene, or very few cats. California has relatively low prevalence of toxoplasmosis because of the dry soil, though we can modify that by irrigating.”
Because there is so much variation from country to country in the risk of exposure to T. gondii, Lafferty was able to use countries as replicates for societies and to ask whether heavily exposed societies have different types of cultures than ones that are not exposed. As Lafferty notes with a grin, “That was the unasked question, maybe unasked for a good reason. Humans are so divorced from ecosystems that we don’t think of ourselves as playing a role in nature. And this is even worse. This is nature playing a role in us that we weren’t aware of. So this enters into the fundamental nature-versus-nurture debate, which is big in anthropology.”
In an article that appeared in the Proceedings of the Royal Society, Lafferty concluded that the parasite’s subtle effect on individual personalities appears to alter a society’s aggregate personality at a population level. Just as individuals infected with T. gondii score higher in guilt-proneness, countries with high T. gondii prevalence have a higher aggregate neuroticism score. He cautions, however, that causation is impossible to confirm and that it only explains a fraction of variations in specific cultural dimensions, suggesting that other factors, such as genetics and environment, might also be involved.
Lafferty stresses that he’s not trying to label certain countries and cultures in ways that could be perceived as negative. He points out that the changes that this infectious disease may bring about in human cultures are varied and some can even be positive. “Certainly, when you look at the cultures that have high prevalence of Toxoplasma, you don’t think of them as better or worse cultures than those where it’s low. They may be different. France, for example, has a very high prevalence even though they’re First World, practice good hygiene, and have winter freezes. Their main risk of exposure comes from the practice of eating raw beef, which they do a lot of.”
Lafferty’s paper has sparked interest among social scientists as well as parasitologists. He was recently asked to give a talk to the anthropology department at UCLA. “They loved it,” he recalls. “They seemed to be very open to hearing biological reasons for human behavior.”
Connecting New Worlds
The extent to which Lafferty and Kuris have pursued their research is impressive. The broad implications they’ve drawn from their discoveries are thought provoking. In addition to all of his theoretical scientific research, Kuris also leads an ambitious applied research effort, seeking solutions for problems that range from managing infectious diseases in fisheries to controlling schistosomiasis, a devastating water-borne disease, in Africa.
Lafferty’s motivation for his wide-ranging studies comes down to the aesthetics and excitement of scientific discovery. “Science continually opens up your mind to new worlds,” observes this man who began his career as a “standard” marine biologist. “Scuba diving did that for me in a dramatic way. Another [opening occurred] when I realized the difference between invasive plants and native plants. My view of the landscape completely changed. Another great example was learning to use mathematics to think about nature. And parasites revealed another unseen world. These are real, mind-expanding, exciting things that keep me hooked.” — JB
For more information, contact:
Armand Kuris and Kevin Lafferty
Ecological Parasitology Laboratory
Department of Ecology, Evolution, and Marine Biology
University of California
Santa Barbara, CA 93106
<http://www.lifesci.ucsb.edu/eemb/labs/kuris/index.html>
References
Lafferty, K. D., and A. K. Morris. 1996. Altered Behavior of Parasitized Killifish Increases Susceptibility to Predation by Bird Final Hosts. Ecology 77:5, pp. 1,390-97.
Lafferty, K. D., A. P. Dobson, and A. M. Kuris. 2006. Parasites Dominate Food Web Links. Proceedings of the National Academy of Sciences 103:30, pp. 11,211-16.
Smith, K. F., D. F. Sax, and K. D. Lafferty. 2006. Evidence for the Role of Infectious Disease in Species Extinction and Endangerment. Conservation Biology 20:5, pp. 1,349-57.
Lafferty, K. D. 2006. Can the Common Brain Parasite, Toxoplasma gondii, Influence Human Culture? Proceedings of the Royal Society B 273, pp. 2,749-55.
|
