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Study Shows that Introduced Foxes Transformed Vegetation on the Aleutian Islands from Lush Grassland to Tundra

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arctic fox taking a least auklet
Above: Introduced arctic fox taking a least auklet, a seabird breeding in the Aleutian Islands, Alaska Maritime National Wildlife Refuge. Fox predation decimated seabird populations and reduced the guano supplied by seabirds to the Aleutians, transforming the vegetation on the islands from productive plant communities dominated by grasses to less productive communities dominated by low-lying shrubs. Photograph by Anthony DeGange, USFWS. [larger version]

Grass-dominated plant communities in the Aleutian Islands (left) have been transformed to communities dominated by low-lying shrubs (right) due to reduced nutrient inputs.
Above: Grass-dominated plant communities in the Aleutian Islands (left) have been transformed to communities dominated by low-lying shrubs (right) due to reduced nutrient inputs. Foxes introduced for the Alaska fur trade decimated breeding seabird populations on the islands, leading to reduced nutrient input from seabird guano. Photographs by Croll and UCSC staff. [larger version]

Huge colonies of seabirds accustomed to nesting on islands free of predators began disappearing when fur traders started introducing foxes onto islands in the Aleutian archipelago in the 18th century. The ground-nesting birds made easy meals for the foxes. A study published in the March 25 issue of the journal Science (v. 307, no. 5717, p. 1959-1961) now shows that the effects of the introduced foxes rippled through entire island ecosystems, transforming the vegetation from lush grasslands to scrubby, low-growing tundra.

It turns out that the nutrient-poor volcanic soils of the Aleutian archipelago can support dense grasslands only if they receive regular doses of fertilizer in the form of bird droppings. On islands without foxes, seabirds transfer nutrients from the ocean to the land by feeding on marine fish and invertebrates and spreading nutrient-rich guano around the islands. Add foxes, and the indirect effects on the whole ecosystem are as dramatic as the direct effects on the seabirds.

"Introduced species are a global phenomenon, and we tend to focus on the direct effects, such as the reduction or extinction of species that are consumed by an introduced predator. This study shows how the effects of introduced species can spread throughout an ecosystem in unpredictable ways," said Donald Croll, an assistant professor of ecology and evolutionary biology at the University of California, Santa Cruz (UCSC), and first author of the Science paper.

Efforts by the U.S. Fish and Wildlife Service (USFWS) to remove introduced foxes from the Aleutian Islands have been largely successful. Seabirds are beginning to make a comeback on islands previously colonized by foxes, and in some places the vegetation has begun to look lusher. But it is likely to take decades for the ecosystems to fully recover from the effects of the foxes, said James Estes, adjunct professor of ecology and evolutionary biology at UCSC and research wildlife biologist at the U.S. Geological Survey (USGS), who is a coauthor of the paper.

"Most seabirds only have a single offspring each year, so their capacity for population increase is quite low. The foxes are mostly off the islands now, but we will probably continue to see the effects for a long time," Estes said.

In addition to Croll and Estes, the authors of the Science paper include UCSC graduate student Eric Danner, University of Montana plant ecologist John Maron, and USFWS biologist Vernon Byrd. The study grew out of conversations between Estes, who has been doing research in Alaskan coastal waters for decades, and Byrd, supervisory biologist for the Alaska Maritime National Wildlife Refuge. While working to save the endangered Aleutian Canada goose, which the foxes were driving toward extinction, Byrd had noticed the differences between islands with and without foxes and speculated that nutrients might play a role.

"He had these interesting ideas about foxes and birds and nutrient chains, and I thought we should do some studies to see how robust the idea is," Estes said.

The team of researchers, accompanied by a small army of student assistants, conducted extensive surveys on the islands for several weeks each summer over three years. They surveyed dozens of islands from one end of the archipelago to the other. Estes said the differences were striking between fox-free and fox-infested islands (defined as those where self-sustaining populations of foxes persisted into the late 1990s).

"When you go to an island that had foxes, it's very easy to walk around because the plants don't grow much higher than your ankles. But on the other islands, it's hard work just to get through the vegetation. It was exhausting just trying to get around on those islands," he said.

The researchers found that the density of breeding seabirds on fox-free islands was two orders of magnitude higher than on fox-infested islands. The resulting difference in nutrient inputs was reflected in soil phosphorus levels that were more than three times higher on fox-free islands. The vegetation on the islands also showed significant differences in nutrient content.

Evidence that more ocean-derived nutrients were cycling through the ecosystems of fox-free islands than on fox-infested islands came from analyses of nitrogen isotopes in soil, plant, and animal samples.

"The terrestrial ecosystem was being subsidized by marine-derived nutrients, and the foxes basically cut off the subsidies by interrupting the flow of nutrients coming from offshore," Croll said. "It transformed the plant community from one that does well in nutrient-rich conditions to one that does well in nutrient-depleted conditions."

Foxes were first introduced to some of the islands by Russian fur traders in the mid- to late-18th century as a way to supplement the declining harvest of sea-otter pelts. But the practice escalated between the 1890s and the 1930s, when the U.S. Government worked to establish fox-farming businesses on the islands. Mostly arctic foxes and smaller numbers of red foxes were introduced to more than 400 islands.

Byrd, who has been involved in restoration efforts in the Aleutian Islands since 1971, said that most of the islands had major breeding colonies of seabirds before the arrival of foxes. About 26 species of seabirds regularly nest on the islands, he said, including surface nesters, such as gulls and terns, that lay their eggs on the ground; burrow nesters, such as puffins, that dig burrows in the soil for their nests; and crevice nesters, such as auklets, that nest in boulder piles and rock crevices.

According to Byrd, surface nesters and burrow nesters tended to disappear completely from islands with foxes, whereas populations of crevice nesters were reduced but not eliminated. Ledge nesters such as murres and kittiwakes, which nest on steep cliff faces, were less affected by the foxes, he said.

"Wherever the puffins and gulls have come back after the removal of the foxes, the vegetation has started to become lusher again," Byrd said. "The terrestrial ecosystem was probably modified in more ways than we know, and maybe it won't be exactly like it was, but the conditions are there for a successful restoration of the native biodiversity."

About the author: Article author Tim Stephens, who holds degrees from the University of California, Santa Barbara (B.A., botany), and Cornell University (M.S., plant pathology), is a science writer in the UCSC Public Information Office.

Related Web Sites
Introduced Predators Transform Subarctic Islands from Grassland to Tundra
Science Vol. 307, no. 571
Alaska Maritime National Wildlife Refuge
U.S. Fish & Wildlife Service
Western Ecological Research Center
U.S. Geological Survey (USGS)
Ecology and Evolutionary Biology
University of California, Santa Cruz (UCSC)

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