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Researchers Led by ODU Biologist Alex Greenwood Find Disease as Cause of Mammal Extinction

Three Old Dominion University researchers are among the authors of a new study demonstrating for the first time that disease can lead to extinction in a mammal. The ODU authors of the article, published Nov. 5 in the public access journal PLoS One, are from the Department of Biological Sciences and led by Alex Greenwood, assistant professor. Other authors are Wayne Hynes, interim chair and professor; and Kelly Wyatt, graduate researcher.

The article, "Historical Mammal Extinction on Christmas Island Correlates with Introduced Infectious Disease," examines the demise of native rats on this island in the eastern Indian Ocean. It presents an interesting storyline based partly on scientific observations in an isolated locale more than a century ago, and also on recent DNA studies.

Numerous news media here and abroad published or broadcast reports about the findings soon after the article was published.

PLoS One is produced by the Public Library of Science, a nonprofit organization of scientists and physicians committed to making the world's scientific and medical literature a public resource.

It took less than a decade for native rats to become extinct on the previously uninhabited Christmas Island once Eurasian black rats jumped ship there at the turn of the 20th century. But the genetics researchers involved in the new study show that this story is more than the typical tale of direct competition causing species to disappear. They argue that the invasive black rats carried a pathogen that exterminated two endemic species, Rattus macleari and Rattus nativitatis.

The study supports the hypothesis proposed a decade ago that "hyperdisease conditions"-unusually rapid mortality from which a species never recovers-can lead to extinction.

"This study puts into play pathogenic organisms as mediators of extinction," said Greenwood, who also works with the Division of Vertebrate Zoology at the American Museum of Natural History. "Our study is the first to correlate a pathogen with an extinction event in mammals, although we know about disease-associated extinction in snails and disease-associated population declines in amphibians."

Black rats were introduced to Christmas Island via the S.S. Hindustan in 1899. A parasitologist noted a few years later that fleas on these rats carried a pathogenic protozoan related to the same organism that causes sleeping sickness in humans. The black rats were well adapted to this protozoan, known as Trypanosoma lewisi, but quite clearly, R. macleari and R. nativitatis were not. The native species were soon seen staggering around on footpaths, evidently very ill, and by 1908 it was clear to biologists on the island that both were extinct. Extinction of island-bound mammals is not uncommon: more than 80 per cent of the mammals that have gone extinct in the last 500 years were from islands.

Although the parasitologist's findings have occasionally been cited in the specialist literature, scientists have been unable to agree that disease-rather than hybridization or competition between rat species-was the actual culprit. Greenwood and colleagues used ancient DNA procedures to determine if a rat-specific trypanosome could be detected in museum samples and if trypanosomiasis could have caused the extinction of these species.

The team collected samples from 21 specimens to see if the infectious agent existed in the population before and after contact with black rats. None of the three pre-contact samples were infected with the protozoan, but six of the 18 post-contact samples were infected. This suggests a very high rate of infection. Results were confirmed by sending a subset of the samples to a laboratory at the University of Copenhagen in Denmark for independent testing. Finally, the group investigated the possibility of hybridization by testing for the distinctive genomes of the native rats in black rat species, but no evidence of this was found.

"This is not a case of humans over-hunting-I don't think anyone was that hungry," says Ross MacPhee, a curator of vertebrate zoology at the American Museum of Natural History who proposed "hyperdisease conditions" as a mediator of extinction in 1997. "Within nine years of contact, these abundant, endemic species were evidently completely knocked out by an introduced disease-nothing else was around at the time that could have done the job. This study puts something else on the table as a reason for extinction."

The results of this study contrast with most scientists' view of the effect of pathogens on species. Most pathogens are self-limiting either because the disease burns itself out as the number of new hosts declines, or because resistant individuals increase proportionally as susceptible individuals die out.

Yet at least one mammalian species, the Tasmanian devil, shows signs of undergoing a collapse due to disease right now, in this case, from an apparently infectious form of cancer. At least a quarter of the total population have died out within the past decade, and some biologists predict the Tasmanian devil's extinction within a few years if the cancer continues to spread.

"This study should get people to think about the spread of pathogen pollution," says Greenwood. "Pathogen pollution is the introduction of animal or plant diseases into a new environment. This pollution could affect many species that are in decline or in small numbers, ranging from accidental to active introduction like the building of Pleistocene Park in Russia or the repopulation of species for conservation purposes."

The research in this paper was funded by the National Science Foundation. In addition to Greenwood, Hynes, Wyatt and MacPhee, authors include Paula Campos and Thomas Gilbert of the Department of Biology at the University of Copenhagen; Sergios-Orestis Kolokotronis and Rob DeSalle of the Sackler Institute for Comparative Genomics at the American Museum of Natural History; and Peter Daszak of the Consortium for Conservation Medicine at the Wildlife Trust.

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