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Parasites as Indicators of Coastal-Ecosystem Health

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Horn snails in a salt marsh
Hosts: Horn snails, like these in a salt marsh in Morro Bay, CA, are hosts to 17 different kinds of trematode worms. Photo by Kevin D. Lafferty, USGS.
When USGS scientist Kevin Lafferty visits a salt marsh at low tide, he sees much more than algae-green-tinted mudflats, tidal sloughs, and brine-adapted pickleweed. Like other visitors, he sees the bustle of life around the mudflats—from clams, snails, and crabs to shorebirds and long-legged waders, and gobies and killifish in the shallows of the estuary. Unlike most visitors, however, Lafferty focuses his thoughts on the parasites that are an integral, though often unnoticed, part of a healthy salt marsh.

According to Lafferty and his research colleagues, parasitic trematodes—a type of worm—are like puppeteers directing the lives of the animals that use the salt-marsh environment. The parasites' lifestyle is one of "body snatching" and mind control of their hosts, the envy of science-fiction horror movies. Apart from having fascinating science-fiction life cycles, however, these parasites serve as barometers of the well-being of a salt marsh.

"Paradoxically, healthier, less degraded ecosystems tend to have more parasites with complex life cycles than do altered systems, because these parasites depend on functioning natural systems," said Lafferty, a marine biologist at the USGS' Western Ecological Research Center Field Station in Santa Barbara, CA.

Most trematodes, said Lafferty, must infect three different host animals—first, intermediate, and final—to develop into egg-producing adults. If one of the host animals is missing, as it may be in a degraded ecosystem, the parasite cannot complete its life cycle.

"Changes to parasite communities can profoundly alter natural systems," said Lafferty. Changes most likely to affect parasite communities are alterations in the communities of the parasite hosts, the animals that the parasite uses to complete its life cycles. Today, these changes are most likely to occur because of climate change and environmental degradation, including habitat fragmentation, pollution, overharvesting of marine species, and introduced nonnative species.

In 2001, Lafferty and colleagues at the University of California, Santa Barbara (UCSB), began research funded by the U.S. Environmental Protection Agency to develop tools using parasites to monitor the health of salt marshes. New funding from the National Science Foundation and the National Institutes of Health will support student research during the next 5 years, under the direction of three principal investigators, Lafferty, Armand Kuris (professor of zoology at UCSB), and Andrew P. Dobson (professor of zoology at Princeton University). They are examining 17 different kinds of trematodes found in horn snails, an abundant snail in salt marshes in California and Mexico and on the Gulf Coast.

Using Trematodes as Indicators

"A measure of the trematode community, gathered from dissecting snails that act as the first host of these worms, provides a single, integrated snapshot of host species that have been in an estuary over the average lifespan of the snails that occur there," said Lafferty. Intact trematode communities are assurances of the healthy integrity and diversity of species within the salt marsh.

trematode cercaria
Parasite: This free-swimming stage of a parasite larva, a trematode cercaria, leaves an infected snail to encyst on a fish brain. View is 0.267 mm across. Courtesy of Todd Huspeni, University of California, Santa Barbara.
Trematode infection begins as a horn snail grazing on algae incidentally ingests worm eggs, perhaps from a bird dropping. The eggs hatch into worms that prevent the snail's own reproduction. Instead, the infected snail nourishes the growing larval worms, which eventually develop into a free-swimming stage and leave the snails to seek their second, or intermediate, host.

"Depending on the worm species, the intermediate host might be a crab, fish, bird, or another species of snail," Lafferty noted. The most common salt-marsh trematode infects California killifish. By traveling to the fish's brain, the worm causes the fish to behave differently from other killifish. "An infected fish will sometimes move about jerkily near the water's surface, turning on its side and flashing its light-colored belly. This behavior attracts predators like herons; capturing infected fish is 10 to 30 times easier for the heron than capturing healthy fish," Lafferty said.

The heron, in turn, becomes the host to the adult worm, said Lafferty. The adult trematode takes up final residence in the bird's gut, releasing thousands of eggs that are deposited by way of bird droppings back into the salt marsh, completing the life cycle of the parasite.

The scientists will use mathematical models, molecular tools, laboratory experiments, field experiments, and large-scale comparative field studies in their investigation. In addition to work at two UCSB natural reserves, Carpinteria Salt Marsh and Coal Oil Point, research will take place in estuaries in California's Morro Bay and Mugu Lagoon, along the Pacific Coast of Baja California, Mexico, and in Japan.

salt marsh at Bahia Falsa de San Quitin, Baja, Mexico
Parasite ecologists are studying the health of this salt marsh at Bahia Falsa de San Quitin, Baja, Mexico. Photo by Kevin D. Lafferty, USGS.

While this research is specifically geared toward understanding the role of parasites in a functioning ecosystem, another study is examining how altered parasite communities may place wildlife at risk.

Species Conservation and Disease

"Understanding the way disease influences wildlife populations is an important tool for addressing conservation questions," Lafferty said. Writing in the June issue of Conservation Biology, Lafferty and Leah Gerber, an assistant professor at Arizona State University, Tempe, found that an important step in determining a wildlife population's status and designing recovery measures for a population at risk of becoming endangered or extinct is to analyze a species' vulnerability to infectious disease.

"Not all diseases will be of concern for the conservation of a species," Lafferty points out. "We examined situations in which disease affected rare species or caused common species to become rare. In most cases, ironically, diseases specific to rare species tend not to be so much of a problem as environmental changes occur, because when individual animals become increasingly isolated from one another as their population numbers decrease, transmission of infectious diseases becomes more difficult."

Yet, cautions Lafferty, introduced, nonnative diseases can and do put a species at risk. For example, he said, rare species are likely to be most affected by diseases normally found in domestic animals.

California Sea Otter Health

When California sea otters were hunted to the brink of extinction by the fur trade, Lafferty suggests, their natural diseases may also have been largely eliminated. The remaining California otters increased in the 20th century and expanded their range, but in recent decades, they have become accidental hosts for several non-otter diseases, parasites for which they are not a natural host.

"These are among diseases that are newly emerging owing to human changes to the environment," said Lafferty.

Examining data from necropsies conducted by pathology teams between 1967 and 1989, Lafferty and Gerber found that nearly half of the stranded-sea-otter deaths were associated with disease. A significant percentage—26 percent—of deaths came from diseases that do not normally occur in sea otters.

Sample container holding segment of a bird intestine filled with acanthocephalan worms
Acanthocephalan worms: Segment of a bird intestine filled with acanthocephalan worms. When in a sea otter, the worms can bore through the intestinal wall and cause death. Photo by Kevin D. Lafferty, USGS., USGS.
Many sea otters (14 percent) died from being infected by a parasitic acanthocephalan worm found in sand crabs the sea otters ate when other, more natural prey was scarce. The acanthocephalan worm normally completes its life cycle when the sand crab is eaten by a shorebird. In sea otters, however, the parasite punctures the intestines, leading to peritonitis, an often-fatal infection. Lafferty and Gerber found that years in which the acanthocephalan worms were common were followed by years with high sea-otter mortality, suggesting that this parasite contributes to high death rates that can lead to reduced population growth in otters.

Other otters (8 percent) died from protozoan parasites called Toxoplasma gondii, which they acquired from cat feces that had been washed to sea. Cats are the usual final host of this protozoan, but other mammals—including humans—and birds can become intermediate hosts. This parasite causes toxoplasmosis, a flulike disease that is known to change behavior in its host and can alter personality in infected humans. Recent research indicates that the otters' risk of this disease is highest in areas where freshwater runoff enters sea-otter habitat.

In addition, some (4 percent) of the sea otters the researchers examined had suffered from valley fever. They were infected in the same manner as humans are, by inhaling spores of a soil fungus in dust blown to sea from construction and agriculture.

Although Lafferty and Gerber found that disease is an important factor in limiting sea-otter population growth, researchers have not been able to determine yet whether disease is driving the recent California sea-otter decline. Entanglement or entrapment in coastal fishing gear, starvation, disease, and contaminants may all have contributed to the recent sea-otter decline, say USGS sea-otter researchers.

Lafferty and Gerber suggest that less exposure to contaminants that could suppress otter immune systems, and to dust and sewage, could help the otters better resist disease. However, there may be no way to prevent infection from acanthocephalan worms, the most prevalent of the new diseases.

Lafferty warns that other diseases may emerge as risks to California sea otters in future years. "Canine distemper virus is a possibility, and if the otters eventually expand their range to the southern Channel Islands, they may encounter new diseases associated with warmer waters."

Related Sound Waves Stories
California Sea Otter Numbers Slide for Second Straight Year
July 2002
Where Disease May Mean Good Health—The Role of Parasites in Natural Ecosystems
April 2002
What's Wrong with the California Sea Otter?
February 2002

Related Web Sites
Using Parasites to Monitor Ecosystem Health
U.S. Geological Survey (USGS)
Department of Ecology, Evolution, and Marine Biology (EEMB)
University of California, Santa Barbara
Department of Ecology and Evolutionary Biology
Princeton University

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Southern California Offshore Hazards Survey

Mapping Georges Bank

Research Ground Water Diesel Fuel Contamination

Parasites as Indicators of Coastal-Ecosystem Health

Outreach Florida's Hillsborough River

Climate-Change Effects Lecture

Meetings Coral-Reef Meeting

usSEABED - Seabed Characteristics

Awards Lake Mead Poster

von Huene Receives Prestigious Award

Staff & Center News Hapke's Thesis Defense

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