UNIVERSITY PARK, Pa. — In 2000, when a team of scientists led by Robert Ross studied the response of birds to the beginning of hemlock tree decline in the Delaware Water Gap National Recreation Area, Matt Toenies was just seven years old, and the ecological havoc wreaked by invasive species was the farthest thing from his mind.

Ross, a scientist employed by the U.S. Geological Survey, conducted research on habitat use by breeding birds in hemlock forests threatened by infestations of hemlock woolly adelgid, an aphid-like insect accidentally introduced from Japan. Seventeen years ago, the hemlocks were just starting to decline, victims of the sap-sucking invasives. Ross' study looked at 80 locations across 22 forest stands — 11 deciduous and 11 hemlock.

Now Toenies, a master's degree student in Penn State's intercollege graduate degree program in ecology, is leading a research team that is finishing up a similar research project, following in Ross' footsteps. Researchers have been measuring bird activity in the same plots that Ross' team did and comparing the results.

"Using the unique approach of examining the same hemlock stands both before and after degradation by the hemlock woolly adelgid, we found that hemlock decline drove changes in vegetation structure and bird communities," said Toenies, who is advised by David Miller, assistant professor of wildlife population ecology in the College of Agricultural Sciences. "Hemlock stands declined significantly since the pre-infestation baseline, with the severity of decline varying across stands."

Researchers correlated hemlock decline with changes in vegetation structure, including a denser deciduous understory, decreased live hemlock foliage in the canopy, and a greater number of standing dead hemlocks. The hemlock decline also changed the bird community, with the number of "hemlock specialists" falling and most other species growing, especially those associated with a dense shrub layer, the forest edge and deciduous forests.

Ultimately, Toenies noted, the species composition of the avian community in hemlock stands shifted toward that of neighboring deciduous stands, highlighting a trend of long-term homogenization of the bird community in regions affected by hemlock decline. "The unique species assemblages associated with hemlock forests continue to disappear," he said.

Species that showed the greatest increases were those associated with the shrub layer (veery, worm-eating warbler and wood thrush); those associated with the forest edge (blue jay, great crested flycatcher and brown-headed cowbird); and those belonging to both groups (rose-breasted grosbeak and cedar waxwing).

However, the numbers of five species associated specifically with hemlock showed negative responses to hemlock decline. They are the Acadian flycatcher, Blackburnian warbler, black-throated green warbler, hermit thrush and blue-headed vireo.

"We organized species into these groups to determine which habitat variables within dying forests are driving the restructuring of bird communities over time," Toenies explained. "Because we observed the strongest trends in groups associated with the shrub layer, woodland edge and the declining forest type, these changing features in dying forests may be most influential in shaping bird communities as die-offs progress."

The die-off of hemlocks resulting in the opening of intact canopies just adds to the threats already faced by declining populations of many forest-interior bird species, Toenies pointed out. Because of the higher presence of nest predators and brood parasites near edges, this is a typical pattern across forested landscapes.

Although the dwindling of hemlock-associated birds represents a loss of biodiversity in eastern Pennsylvania forests, Toenies has seen reassuring trends in his research that he believes wildlife managers will want to keep in mind. Dying hemlocks, it turns out, are better than none.

Even in hemlock stands heavily degraded by the adelgid, researchers didn't find many places in their study area where the trees were completely dead (although in nearby spots the hemlocks are completely dead and being replaced by hardwoods). But they saw many places where the trees were in poor condition.

"The adelgids defoliate the lower branches of the hemlocks first — they do this in a pretty systematic way — and we often see a tight little clump of hemlock needles at the top of the tree, and then it dies," he said.

"Still, we had a lot of these hemlock-associated bird species hanging around. So on a local scale where we are managing, like in a national park, for example, if we can keep enough hemlocks alive, they don't necessarily have to be that healthy. And if we have just a few hemlocks but we invest heavily in keeping them in good shape, that also is beneficial for keeping hemlock-dependent birds, at least on a very small scale."

Also participating in the research are Miller; Matt Marshall, National Park Service, Inventory and Monitoring Division, Eastern Rivers and Mountains Network; and Glenn Stauffer, intercollege graduate degree program in ecology, Department of Ecosystems Science and Management.

The National Park Service supported the research.