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Historical mammal extinction on Christmas Island (Indian Ocean) correlates with introduced infectious disease.

Wyatt KB, Campos PF, Gilbert MT, Kolokotronis SO, Hynes WH, DeSalle R, Ball SJ, Daszak P, MacPhee RD, Greenwood AD - PLoS ONE (2008)

Bottom Line: In the case of mammals, however, there are still no well-corroborated instances of such diseases having caused or significantly contributed to the complete collapse of species.Hybridization between endemic and black rats was also previously hypothesized, but we found no evidence of this in examined specimens, and conclude that hybridization cannot account for the disappearance of the endemic species.This is the first molecular evidence for a pathogen emerging in a naïve mammal species immediately prior to its final collapse.

View Article: PubMed Central - PubMed

Affiliation: Biological Sciences Department, Old Dominion University, Norfolk, VA, USA.

ABSTRACT
It is now widely accepted that novel infectious disease can be a leading cause of serious population decline and even outright extinction in some invertebrate and vertebrate groups (e.g., amphibians). In the case of mammals, however, there are still no well-corroborated instances of such diseases having caused or significantly contributed to the complete collapse of species. A case in point is the extinction of the endemic Christmas Island rat (Rattus macleari): although it has been argued that its disappearance ca. AD 1900 may have been partly or wholly caused by a pathogenic trypanosome carried by fleas hosted on recently-introduced black rats (Rattus rattus), no decisive evidence for this scenario has ever been adduced. Using ancient DNA methods on samples from museum specimens of these rodents collected during the extinction window (AD 1888-1908), we were able to resolve unambiguously sequence evidence of murid trypanosomes in both endemic and invasive rats. Importantly, endemic rats collected prior to the introduction of black rats were devoid of trypanosome signal. Hybridization between endemic and black rats was also previously hypothesized, but we found no evidence of this in examined specimens, and conclude that hybridization cannot account for the disappearance of the endemic species. This is the first molecular evidence for a pathogen emerging in a naïve mammal species immediately prior to its final collapse.

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Extinction time line for Christmas Island rats (background drawing of R. macleari by Patricia Wynne).
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pone-0003602-g001: Extinction time line for Christmas Island rats (background drawing of R. macleari by Patricia Wynne).

Mentions: Uninhabited Christmas Island was sighted on several occasions in the two centuries leading up to the first recorded landing in 1857 [4]. However, actual occupation of the island did not occur until the 1890s, following discovery of commercially exploitable deposits of phosphate [4]. The endemic rats of Christmas Island, described as “abundant” when first collected in 1887 [4], [5], but never seen after 1905, are thought to have become completely extinct by 1908 [4]; [6]; Fig. 1]. Discovery to disappearance thus took much less than a quarter-century; indeed, contemporary accounts imply that the actual collapse may have spanned only a few years. Just before their final disappearance, apparently sick individuals of Rattus macleari were seen crawling along footpaths and other areas frequented by humans [4]. One explanation proffered at the time by the pioneering tropical parasitologist H.E. Durham [7], [8] was that the animals were suffering from a highly infectious and fatal typanosomiasis, perhaps carried by infected fleas on the black rat (R. rattus) thought to have been introduced in 1899 by the S.S. Hindustan [4]. According to available evidence [9], the black rat originated in tropical mainland (as opposed to insular) Asia, spreading only much later to Europe and, in recent centuries, to effectively the rest of the world. Durham supported his speculation by gross pathological analysis of a small number of specimens, including ones with pelt characteristics suggestive of hybridization [8]. Because the endemic rats disappeared so quickly, only a small number of specimens were ever collected for scientific study (see [7]); of the few known to still exist, all are housed at just three institutions: the Natural History Museum, London (NHML), and Museum of Zoology of Cambridge University (CMZ), and the Museum of Natural History of Oxford University (OMNH).


Historical mammal extinction on Christmas Island (Indian Ocean) correlates with introduced infectious disease.

Wyatt KB, Campos PF, Gilbert MT, Kolokotronis SO, Hynes WH, DeSalle R, Ball SJ, Daszak P, MacPhee RD, Greenwood AD - PLoS ONE (2008)

Extinction time line for Christmas Island rats (background drawing of R. macleari by Patricia Wynne).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2572834&req=5

pone-0003602-g001: Extinction time line for Christmas Island rats (background drawing of R. macleari by Patricia Wynne).
Mentions: Uninhabited Christmas Island was sighted on several occasions in the two centuries leading up to the first recorded landing in 1857 [4]. However, actual occupation of the island did not occur until the 1890s, following discovery of commercially exploitable deposits of phosphate [4]. The endemic rats of Christmas Island, described as “abundant” when first collected in 1887 [4], [5], but never seen after 1905, are thought to have become completely extinct by 1908 [4]; [6]; Fig. 1]. Discovery to disappearance thus took much less than a quarter-century; indeed, contemporary accounts imply that the actual collapse may have spanned only a few years. Just before their final disappearance, apparently sick individuals of Rattus macleari were seen crawling along footpaths and other areas frequented by humans [4]. One explanation proffered at the time by the pioneering tropical parasitologist H.E. Durham [7], [8] was that the animals were suffering from a highly infectious and fatal typanosomiasis, perhaps carried by infected fleas on the black rat (R. rattus) thought to have been introduced in 1899 by the S.S. Hindustan [4]. According to available evidence [9], the black rat originated in tropical mainland (as opposed to insular) Asia, spreading only much later to Europe and, in recent centuries, to effectively the rest of the world. Durham supported his speculation by gross pathological analysis of a small number of specimens, including ones with pelt characteristics suggestive of hybridization [8]. Because the endemic rats disappeared so quickly, only a small number of specimens were ever collected for scientific study (see [7]); of the few known to still exist, all are housed at just three institutions: the Natural History Museum, London (NHML), and Museum of Zoology of Cambridge University (CMZ), and the Museum of Natural History of Oxford University (OMNH).

Bottom Line: In the case of mammals, however, there are still no well-corroborated instances of such diseases having caused or significantly contributed to the complete collapse of species.Hybridization between endemic and black rats was also previously hypothesized, but we found no evidence of this in examined specimens, and conclude that hybridization cannot account for the disappearance of the endemic species.This is the first molecular evidence for a pathogen emerging in a naïve mammal species immediately prior to its final collapse.

View Article: PubMed Central - PubMed

Affiliation: Biological Sciences Department, Old Dominion University, Norfolk, VA, USA.

ABSTRACT
It is now widely accepted that novel infectious disease can be a leading cause of serious population decline and even outright extinction in some invertebrate and vertebrate groups (e.g., amphibians). In the case of mammals, however, there are still no well-corroborated instances of such diseases having caused or significantly contributed to the complete collapse of species. A case in point is the extinction of the endemic Christmas Island rat (Rattus macleari): although it has been argued that its disappearance ca. AD 1900 may have been partly or wholly caused by a pathogenic trypanosome carried by fleas hosted on recently-introduced black rats (Rattus rattus), no decisive evidence for this scenario has ever been adduced. Using ancient DNA methods on samples from museum specimens of these rodents collected during the extinction window (AD 1888-1908), we were able to resolve unambiguously sequence evidence of murid trypanosomes in both endemic and invasive rats. Importantly, endemic rats collected prior to the introduction of black rats were devoid of trypanosome signal. Hybridization between endemic and black rats was also previously hypothesized, but we found no evidence of this in examined specimens, and conclude that hybridization cannot account for the disappearance of the endemic species. This is the first molecular evidence for a pathogen emerging in a naïve mammal species immediately prior to its final collapse.

Show MeSH
Related in: MedlinePlus