BUFFALO, N.Y. -- Primate tourism, an economic benefit and conservation tool in many habitat countries, has exploded in popularity over the past two decades in places like China, Borneo, Uganda, Rwanda, Northern Sumatra, Madagascar, Gabon and Central America.
New research by scientists in the United States, China and Japan, however, has found that some primate tourism practices are inappropriate because they provoke an unprecedented level of adult aggression that is proving deadly for infant monkeys.
The 19-year study, "Primate Tourism, Range Restriction and Infant Risk Among Macaca thibetana at Mt. Huangshan, China" augments findings by previous researchers that some forms of wildlife tourism are counterproductive because they lead to disease transmission, disrupt social behavior and actually increase the risk of habitat destruction.
The authors are Carol Berman, Ph.D., professor of anthropology at the University at Buffalo, and Consuel Ionica, Ph.D., UB Department of Anthropology; Jinhua Li and Huabao Yin, School of Life Sciences, Anhui University, China, and Hideshi Ogawa, Faculty of Liberal Arts, Chukyo University, Japan. The study, which will be published in the October edition of the International Journal of Primatology, draws two primary conclusions.
One is that infant mortality is a useful indicator of the impact of primate tourism on primate groups. The second is that the specific practice of combining range restriction with provisioning (stocking food in a particular area of the range to increase tourist viewing opportunities) is inappropriate for primate management.
The subjects of the study were Tibetan macaques, Old World monkeys that belong to the world's most widespread primate genus. The group under observation lives in the Mt. Huangshan Scenic Area in China's Anhui province.
Like most primates used for tourism, the Huangshan Tibetan macaques were subjected to various management practices, which Berman says involved relocating them to a new area adjacent to their natural range, providing them with regular provisions in a specific location, restricting their range to varying degrees and exposing them to greater numbers of staff and tourists.
The research team observed the monkeys for six years before they were used for tourism (1986-91), for 12 years during which they were used for tourism (1992-2002 and 2004) and for one year (2003) during which tourism was suspended.
Infant mortality was virtually nil in the six years before management began, Berman says, noting that the only significant death rate for infants was in 1988 when disease swept the group killing four of six infants.
Infant mortality went up to about 20 percent in 1992 when the group was translocated. During the years of management (1992-2002, 2004) it fluctuated considerably, but peaked sharply twice: in 1994, the year that tourism and consistent range restriction began, and in 2002, the year in which the group's range was severely restricted. It decreased sharply in 2003, the year management was temporarily suspended.
The overall rate of infant mortality during management years was 54.6 percent, significantly higher than the 14.8 percent rate of pre-management years. The researchers found that the increases in infant death rates were related to adult aggression toward the young monkeys following fights among adults in the provisioning area, and that the aggressive behavior was related to level of range restriction (inconsistent, consistent, severe) at various times during the observation period.
It also found that most of the infants who died during management were severely injured shortly before their deaths. No infant deaths were attributed to wounding before 1992, the year that management for tourism began.
"Infant mortality rates during the management years were significantly higher than they were in the years before management began and also in the year in which it was suspended," Berman says, pointing out that monkeys with artificially reduced ranges become highly dependent on provisioned food and are likely to compete intensely over it.
"After management began, we observed serious attacks on infants shortly before they were found dead and a large proportion of infant corpses had bite wounds," Berman says.
"Typically, infants were wounded after aggression broke out among adults in the provisioning area used for tourist viewing," she says, "and adult aggression rates in the provisioning area were positively correlated with infant mortality over time.
"We did not witness each attack on the infants, but we had no reason to believe that the infant injuries were caused by poaching, attacks by tourists or staff, capture, predation or inter-group aggression between the infants," she says.
"The team tested several hypotheses about the affects of specific factors on infant mortality, among them, numbers of tourists, degree of range restriction, demographic changes, changes in alpha males -- factors that may have been harmful to the infants.
Berman says, "We found that range restriction alone accounted for 54 percent of the variation in infant mortality and that it was more closely associated with both mortality and aggression than any other factor examined."
The study found that rates of female-female aggression, male-male aggression and female-male aggression all were notably higher when the monkeys were in the provisioning area than when they were in the forest, away from that area. It found, too, that there was a strong positive correlation between high rates of infant mortality and both high rates of adult aggression and relative degrees of range restriction.
Post hoc analyses suggested that rates of aggression in the provisioning area were significantly lower before translocation and in the early period of management when tourists were absent and range restriction was inconsistent, than when tourism and consistent range restriction were in full force. Aggression rates were significantly higher during 2002 (when the group's range was severely restricted) than in any other time period.
"Primate tourism has been praised for its potential to achieve conservation goals and financial and educational benefits for local communities," Berman says, "but there has been little research about its impact on the primate groups themselves, which is why we undertook this evaluation. "We would like to believe that primate tourism can be beneficial to both human economic and conservation interests, but it is imperative that we understand which specific practices serve those ends and which are counterproductive," she says.
Even before the study by Berman and colleagues, conservation biologists argued that stress caused by contact with large numbers of people has detrimental effects on the behavior and biology of wild primates, and sometimes resulted in the primates avoiding tourist areas altogether.
"In addition," Berman says, "overhabituation and hyperaggression often result in changes in the primates' habitat activity patterns and communicative behavior. This in turn can affect predator-prey relationships, intergroup relationships, diet or social development.
"The strongest reason for caution involves disease transmission," she says, "because close contact has been blamed for outbreaks of disease among monkeys, great apes and humans.
"In addition to infant death, disease transmission and the disruptive consequences on their activity, relationships and social development, primate tourism also may contribute to habitat destruction," she says, "particularly when tourism demands result in the housing and feeding of tourists within the normal primate habitat."
Berman is the author "Kinship and Behavior in Primates" (Oxford University Press, New York, 2004), and of many journal articles and book chapters. She teaches graduate and undergraduate courses in primate social behavior, animal communication, ethology and advanced physical anthropology. Besides primate tourism, her interests include offspring relations, social structure, dominance style and conflict management among Old World monkeys and apes. She currently is engaged in research on parent-offspring relations among free-ranging rhesus monkeys on Cayo Santiago, Puerto Rico, and on dominance-style patterns among the Huangshan macaques.
The University at Buffalo is a premier research-intensive public university, the largest and most comprehensive campus in the State University of New York. UB's more than 27,000 students pursue their academic interests through more than 300 undergraduate, graduate and professional degree programs. Founded in 1846, the University at Buffalo is a member of the Association of American Universities.