Four bull bison that migrated out of Yellowstone National Park were killed by state livestock agents Wednesday - the first to be killed by the government this year under a contentious policy meant to prevent the spread of disease to livestock.

Many of Yellowstone's bison carry brucellosis, which can cause pregnant animals to miscarry. There have been no recorded transmissions of the disease in the wild from bison to cattle.

Three of the bison killed Tuesday were captured north of West Yellowstone and sent to slaughter, said Department of Livestock Executive Officer Christian Mackay.

The animals were just outside an area recently designated as year-round habitat for bull bison. Mackay said livestock agents made several attempts to haze the bulls back into the park before capturing the animals.

The fourth bull was shot at the edge of a guest ranch near the South Fork of the Madison River. Mackay said that animal had been mingling with livestock in recent days.

But Bar N Ranch manager Gayle Gavagan said the bison was more than a mile from the nearest cattle herd when it was shot.

She called the shooting "unfortunate" and said it had caused a stir among the ranch's three dozen guests.

"The buffalo are a national symbol," she said. "The cattle ranchers feel that they could be in peril, which I can appreciate. But I don't really know if the evidence is there to back them up. Is this just going to continue forever and ever? There has to be a solution."

Gavagan said the guest ranch's neighbors run cattle in the summer, but none were out yet out on Tuesday.

Brucellosis has been eradicated elsewhere in the United States. It is typically transmitted through the afterbirth of female animals that miscarry.

Over the last decade, all seven cases of brucellosis-infected cattle in the Yellowstone region were traced to diseased elk. Elk carry the disease at a lower rate than bison, but are generally not restricted in their movements.

In 2008, 1,601 Yellowstone bison were killed for brucellosis control. But with Yellowstone's bison population down sharply - about 3,000 now versus 4,700 two years ago - this spring's migration in search of food at lower elevations was smaller than in recent years.

One Yellowstone bison was killed during the winter by a Montana hunter. At least 15 of the animals were killed on U.S. Highway 191 in April, in three separate cases of vehicles driving into groups of bison.

Two weeks ago, state livestock officials said they were finished with their annual bison operation after hazing 500 to 600 of the animals about 15 miles into the park. The bulls captured Wednesday were part of a small group that continued to linger near the park's boundary.