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Twenty-eight years after intense selective logging stopped in the region now known as Uganda's Kibale National Park, the red-tailed guenon (Cercophithecus ascanius) is a primate still in decline. The logging practice, scientists report in a new study, changed the ecological balance for these monkeys, leading to behavioral changes and opening the door for multiple parasitic infections.

The researchers focused on three primate species, collecting 1,076 fecal samples from the heavily logged area and from an undisturbed, nearby forest from August 1997 to August 2002 as part of a longitudinal study of logging's impact. The samples came from red-tailed guenon, red colobus (Piliocolobus tephrosceles) and black-and-white colobus (Colobus guereza) and were analyzed for the eggs and larvae of worms and protozoan cysts.

The study appears online ahead of publication in the Journal of Applied Ecology.

While the three primate species were subject to a higher risk of infections, only the guenons (pronounced GWINN-ins) suffered from an increased number of parasites, including three parasites not found in undisturbed forest. In the selective-logging area, more than 50 percent of the trees, many of them the food sources for the mostly fruit-eating guenons, had been removed.

"We saw dramatic changes in the prevalence of infection and in the frequency of multiple infections in these logged areas," said lead researcher Thomas R. Gillespie, a postdoctoral fellow in veterinary pathobiology at the University of Illinois at Urbana-Champaign. "When you see infection characteristics like these, they can be associated with very detrimental effects on the host."

Since the logging period of the late 1960s, red-tailed guenons have been appearing in much lower densities, he said.

What once were large groups with multiple males and females are now fragmented, with much smaller groups living isolated and spread out more widely than in undisturbed forest , where often the three species share trees.

"When we look at their numbers over time, they continue to decline 28 years later," Gillespie said. "The red colobus numbers declined at first but are now recovering. The black-and-white colobus, perhaps due to a release of competition, have increased in the logged forests."

Because the two colubus species primarily eat leaves, it is believed that they can adapt more easily to disruptions in their habitat, he said.

Gillespie initiated the research as an EPA fellow and doctoral student at the University of Florida. He continues the work at Illinois to better understand the interplay between habitat disturbance and primate conservations and health in Uganda. He is collaborating with veterinary pathobiologist Tony Goldberg and other researchers at Illinois, where state-of-the-art facilities and faculty expertise are uniquely suited for studying disease emergence, zoonotic diseases and the consequences of land-use changes.

In August, Gillespie will become the first director of the new Earth & Society Initiative on Emerging Disease & Ecosystem Health at Illinois. The initiative coordinates a diverse assemblage of the university's centers, programs, laboratories and individuals whose current interests focus on the interface between emerging infectious diseases, anthropogenic environmental change and conservation.

The researchers have monitored the three species, gathering data immediately after logging, 12 years later and again 28 years after the logging ended.

"We know land-use change is affecting wildlife species," Gillespie said. "We know that there is a conservation issue. It's been difficult to understand what is taking place. No one had really looked at how parasites and disease might be affecting this relationship. We were surprised to find dramatic patterns across the board, where the species of primates doing poorly in logged areas had a much higher prevalence of parasitic infection and more types of parasites affecting them simultaneously."

Gillespie and co-authors Colin A. Chapman of McGill University in Canada and Ellis C. Greiner of the University of Florida found that red-tailed guenons had a much higher prevalence of infection with seven gastrointestinal parasites in the logged forest than in the undisturbed one.

The parasites found in the guenons were Trichuris sp. (whipworms), Oesopohagostomum sp. (nodular worms), Entamoeba coli, Entamoeba histolytica, Iodamoeba buetschlii, Strongyloides fulleborni and Streptopharagus sp.

Additionally, the red-tailed guenons in the logged forest were the only primates of the three species infected with Chilomastix mesnilia, Giardia lambila and a Dicrocoeliid liver fluke. These parasites did not appear in guenons in the undisturbed forest.

The researchers also noted that the patterns of forest regeneration in the aftermath of logging appear to be more favorable for colobus monkeys than for the guenons. Citing their own as-yet unpublished data, and that of Karen Rode of Washington State University, the researchers suggest that reduced food availability has led to dietary stress. The guenons in the logged forest, they report, are getting much less protein and vital minerals than their counterparts in undisturbed forests.

Recovery of the forest also has been hampered by the growth of acanthus, an invasive shrub that has overwhelmed much of the forest floor where trees were removed, Gilllespie said. Because elephants love to eat the shrub, they trample through the clearings, adding yet another obstacle for the growth of new trees, he said.

"Knowledge of how particular species are affected by various forms of ecological change is essential to promote land-use policy that is compatible with animal and human health and biodiversity conservation," Gillespie, Chapman and Greiner wrote in the conclusion of their study.



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