Devil facial tumour disease

Devil facial tumour disease causes tumours to form in and around the mouth, interfering with feeding and eventually leading to death by starvation.

Devil facial tumour disease (DFTD) is an aggressive non-viral transmissible parasitic cancer—which likely originated in Schwann cells—that affects Tasmanian devils.^[1][2][3][4] The first "official case" was described in 1996, in Australia. In the subsequent decade the disease ravaged Tasmania's wild devils, with estimates of decline ranging from 20% to as much as a 50% of the devil population, across over 65% of the state.^[5][6] Affected high-density populations suffer up to 100% mortality in 12–18 months.^[7] The disease has mainly been concentrated in Tasmania's eastern half. Visible signs of DFTD begin with lesions and lumps around the mouth. These develop into cancerous tumours that may spread from the face to the entire body. The tumours interfere with feeding, and the affected animal may starve to death. At present the population has dwindled 70% since 1996. Numbers as of 2010 show an 80% rate of infection throughout the population. Six females have been found with a partial immunity. Breeding in captivity has begun to try to save the population.^[8] It is spread by devils biting each other's heads when fighting over food.

Characteristics

Tasmanian devil cells have 14 chromosomes, while the tumour cells contain 13.^[9] Researchers identified the cancer as a neuroendocrine tumor, and found identical chromosomal rearrangements in all the cancer cells.^[10] The karyotype anomalies of DFTD cells are similar to those of cancer cells from canine transmissible venereal tumour (CTVT), a cancer of dogs that is transmitted between canines by physical contact.^[10]

Ultimately the idea that cancer cells themselves are an infective agent (the Allograft Theory^[11]) turned out to be correct, with transmission of the disease occurring by biting, feeding on the same material, and aggressive mating. Final confirmation of this came when researcher Anne-Maree Pearse and colleagues found an infected animal that had a chromosomal abnormality in its non-tumorous cells that did not appear in its tumour cells, proving that the tumour cells could not have descended from the animal's own cells.^[12][13] Pearse believes that this may prove vital to the survival of the devils. Since June 2005, three females have been found that are partially resistant to DFTD.^[14]

Further research from the University of Sydney has shown that the infectious facial cancer may be able to spread because of low diversity in devil immune genes (MHC class I and II).^[15] The same genes are also found in the tumours, so the devil's immune system does not recognise the tumour cells as foreign.^[16][17] There are at least nine strains of the cancer, showing that it is evolving, and may become more virulent.^[18] The strains may also complicate attempts to develop a vaccine, and the mutation of the cancer may mean that it could spread to other related species, like the quoll.^[19]

In a paper published in the January 2010 issue of Science,^[20] an international team of researchers announced that devil facial tumour disease likely originated in Schwann cells, a type of cell found in the peripheral nervous system that is essential for the functions of nerve cells in the peripheral nervous system.^[21][22] The researchers sampled 25 tumours and found that the tumours were genetically identical.^[21] Using deep sequencing technology, the team profiled the tumours' transcriptome, the set of genes that are active in tumours. It closely matched that of Schwann cells.^[22] The genetic markers identified by the team will enable veterinarians to more easily distinguish DFTD from other types of cancer (a malady to which devils are unusually susceptible) and may eventually help identify a genetic pathway that can be targeted to treat it.^[22]

Due to the decreased life expectancy of the devils due to DFTD, they have begun breeding at younger ages in the wild, with reports that many only live to participate in one breeding cycle.^[23] A study has suggested that Tasmanian devils have changed their breeding habits in response to the disease. Females previously started breeding at the age of two, then annually for about three more years until dying normally. Now they commonly breed at the age of one, and die of tumours shortly thereafter. It is speculated that the disease is spread by devils biting each other during the mating season.^[24] Social interactions have been seen spreading DFTD in a local area.^[25] It is one of three contagious cancers.

Pathology

Growth of large tumours impedes feeding, and starvation is a common cause of death in affected devils. Organ involvement and additional infections may also be a factor in death, as regional lymph node involvement and systemic metastasis is common. The cancer invades the heart.^[26]

The tumours are capable of dissolving parts of the skull.^[27]

Preservation response

Wild Tasmanian devil populations are being monitored to track the spread of the disease and to identify changes in disease prevalence. Field monitoring involves trapping devils within a defined area to check for the presence of the disease and determine the number of affected animals. The same area is visited repeatedly to characterise the spread of the disease over time. So far, it has been established that the short-term effects of the disease in an area can be severe. Long-term monitoring at replicated sites will be essential to assess whether these effects remain, or whether populations can recover.^[6] Field workers are also testing the effectiveness of disease suppression by trapping and removing diseased devils. It is hoped that the removal of diseased devils from wild populations should decrease disease prevalence and allow more devils to survive beyond their juvenile years and breed.^[6] A study felt that the current system of culling did not impede the disease's spread.^[28]

Two "insurance" populations of disease-free devils are being established at an urban facility in the Hobart suburb of Taroona and on Maria Island off the east coast of Tasmania. Captive breeding in mainland zoos is also a possibility. The decline in devil numbers is also seen as an ecological problem, since its presence in the Tasmanian forest ecosystem is believed to have prevented the establishment of the red fox, illegally introduced to Tasmania in 2001.^[29] It is believed that Tasmanian devil young would be vulnerable to red fox predation, as they are left alone for long periods of time.^[30]

In response to the impact of DFTD on Tasmanian devil populations, 47 devils have been shipped to mainland Australian wildlife parks to attempt to preserve the genetic diversity of the species. The largest of these efforts is the Barrington Tops "Devil Ark"; an initiative of the Australian Reptile Park. This project aims to create a set of one thousand genetically representative devils, and is now a major focus of the insurance policy.^[31] In addition, the Tasman peninsula is being considered as a possible "clean area" with the single narrow access point controlled by physical barriers. The Tasmanian Department of Primary Industries and Water is experimenting on culling infected animals with some signs of success.^[32][33]

In 2008, a devil named Cedric was thought to have a natural immunity to the disease, but in late 2008 he developed two tumours on his face. The tumors were removed^[34] and officials thought Cedric was responding well until September 2010 when he it was discovered that the cancer had spread to his lungs. He was euthanized upon the discovery.^[35] A diagnostic blood test was developed in mid-2009 to screen for the disease.^[36] In early 2010, scientists found some Tasmanian devils, mostly in the north-west of Tasmania, that are genetically different enough for their bodies to recognise the cancer as foreign. They have only one Major Histocompatibility Complex, whereas the cancerous cells have both.^[37]

At present with the population reduced by 70% since 1996, if a cure is not found then scientists predict they will become extinct by 2035.^[8]

A study recommended oocyte banking be used in the conservation effort for Tasmanian devils, as the survival rate of the oocytes in their study was 70%.^[38]

In 2010, there was hope that EBC-46, a drug which cures facial tumours in dogs, cats, and horses, may be a cure for DFTD.^[39]

Vaccination with irradiated cancer cells has not proven successful.^[40]

Research published in the Proceedings of the National Academy of Sciences on June 27, 2011, suggests picking a genetically diverse breeding stock, defined by the genome sequence, for conservation efforts.^[41]

In 2011, Principal Investigator David Phalen, (Wildlife Health and Conservation Centre, University of Sydney) and Stephen Pyecroft (Department of Primary Industries and Water in Tasmania) along with Antony Moore and Angela Frimberger (Veterinary Oncology Consultants) were awarded a Tasmanian Government Project Management Grant for their project Investigation into Chemotherapy Agents Effective Against the Tasmanian Devil Facial Tumour.^[42]

History

Spread of the disease as of 2007.^[43] Individual cases are represented as points, and the disease front is represented as a dashed line. (Annotated in Ukrainian)

In 1996, a photographer captured several images of devils with facial tumours near Mount William in Tasmania's north-east. At around the same time, farmers reported a decline in devil numbers.^[44] Menna Jones first encountered the disease in 1999^[45] near Little Swanport, in 2001 capturing three devils with facial tumours on the Freycinet Peninsula. The devil population on the peninsula decreased dramatically. In March 2003 Nick Mooney wrote a memo to be circulated within the Parks and Wildlife Services calling for more funding for the study of the disease, but the call for funding was edited out before the memo was presented to Bryan Green, then Minister for Primary Industries, Water and Environment.^[46][47] In April 2003, a working group was formed by the Tasmanian Government to respond to the disease.^[48] In September 2003, Nick Mooney went to the Tasmanian daily newspaper The Mercury, informing the general public of the disease and proposing a quarantine of healthy Tasmanian devils. At the time, it was thought that a retrovirus was a possible cause. David Chadwick of the state Animal Health Laboratory said that the laboratory did not have the resources needed to research the possibility of a retrovirus. The Tasmanian Conservation Trust criticised the Tasmanian Government for not providing sufficient resources to research the disease, and suggested that the DFTD could be zoonotic, posing a threat to livestock and humans.^[27] On 14 October 2003, a workshop was held in Launceston.^[49] In 2004, Kathryn Medlock found three oddly shaped devil skulls in European museums and found a description of a devil in London Zoo dying which showed a similarity to DFTD.^[50]

A virus was initially thought to be the cause of DFTD,^[27] but no evidence of such a virus could be detected in the cancer cells.^{[citation needed]} Calicivirus, 1080 poison, agricultural chemicals, and habitat fragmentation combined with a retrovirus were other proposed causes.^[51] Environmental toxins had also been suspected.^[52] In March 2006 a devil escaped from a park into an area which was infected with DFTD. She was recaptured with bite marks on her face, and returned to live with the other devils in the park. She wounded a male and by October both devils were observed to have the disease, which was subsequently transferred to two other devils. This incident helped test the viability of the allograft theory of transmission.^[53] In 2006, DFTD was classed a List B notifiable disease under the Animal Health Act 1995.^[54] Also in 2006, the strategy of developing an insurance population in captivity was developed. It was reassessed in 2008.^[55] A 2007 investigation into the immune system of the devils found that when combatting other pathogens, the response from the immune system was normal, leading to suspicion that the devils were not capable of detecting the cancerous cells as "non-self".^[56] In 2007, it was predicted that populations could become locally extinct within 10 – 15 years of DFTD occurring, and predicted that the disease would spread across the entire range of the Tasmanian devils. This study also predicted that Tasmanian devils would become extinct within 25–35 years.^[57]

In 2008, high levels of potentially carcinogenic flame retardant chemicals were found in Tasmanian devils. Preliminary results of tests ordered by the Tasmanian government on chemicals found in fat tissue from 16 devils have revealed high levels of hexabromobiphenyl (BB153) and "reasonably high" levels of decabromodiphenyl ether (BDE209).^[58]

In other animals

Transmissible cancer, caused by a clone of malignant cells rather than a virus, is extremely rare. The only other known types are canine transmissible venereal tumour (CTVT), which is passed between dogs via sexual activity and has been known to science for about 100 years, and contagious reticulum cell sarcoma of the Syrian hamster,^[59] which can be transmitted from one Syrian hamster to another by means of the bite of the mosquito Aedes aegypti.^[60] CTVT mutes the expression of the immune response, whereas the Syrian hamster disease spreads due to lack of genetic diversity.^[61] The mutation of devil facial tumour disease may mean that it could spread to other related species, like the quoll.^[19]

See also

• HeLa cells – an immortal cell line used in biomedical research

References

1. ^ Zimmer, Carl (December 31, 2009). "Findings on Origin of a Cancer in Tasmanian Devils". New York Times. http://www.nytimes.com/2010/01/01/science/01devil.html. Retrieved 2009-12-31. "The Tasmanian devil, the spaniel-size marsupial found on the Australian island of Tasmania, has been hurtling toward extinction in recent years, the victim of a bizarre and mysterious facial cancer that spreads like a plague." 
2. ^ Loh, Richmond. 2003. Tasmanian Devil (Sarcophilus harrisii) facial tumour (DFT). Paper prepared for the Devil Facial Tumour Disease Workshop, Sir Raymond Ferrall Centre, University of Tasmania, Newnham, 14 October 2003, p. 2.
3. ^ Experts tackle the devil's tumour, BBC News, 20 February 2007.
4. ^ Weiss, Rick (11 August 2006). "Study Finds That a Type of Cancer in Dogs Is Contagious". The Washington Post. http://www.washingtonpost.com/wp-dyn/content/article/2006/08/10/AR2006081001535.html. Retrieved 11 August 2006. 
5. ^ DPIWE. 2005. Devil Facial Tumour Disease – Update June 2005
6. ^ ^{a b c} DPIWE. 2005. Tasmanian Devil Facial Tumour Disease, Disease Management Strategy
7. ^ DPIWE. Disease Affecting Tasmanian Devils
8. ^ ^{a b} Scientists find 'immune' Tassie Devils 14:00 AEST Wed Mar 10 2010 by ninemsn
9. ^ "Bites spread fatal 'devil' cancer". BBC News. 2006-02-02. http://news.bbc.co.uk/2/hi/science/nature/4674446.stm. 
10. ^ ^{a b} Bostanci, A. (2005). "A Devil of a Disease". Science 307 (5712): 1035. doi:10.1126/science.307.5712.1035. PMID 15718445. 
11. ^ Pearse, A-M., Swift, K. (2006). "Allograft theory: Transmission of devil facial-tumour disease". Nature 439 (7076): 549. doi:10.1038/439549a. PMID 16452970. 
12. ^ Tasmanian devils felled by rare cancer, New Scientist, 1 February 2006.
13. ^ Gramlin, Carolyn: Poor Devils: Critters' fights transmit cancer, Science News, 4 February 2006.
14. ^ Dennis, Carina (2006-02-02). "Endangered species: Time to raise the devil". Nature 439 (7076): 530. doi:10.1038/439530a. PMID 16452951. 
15. ^ "Tasmanian devil epidemic: cause isolated?". Cosmos Magazine. 27 June 2007. http://www.cosmosmagazine.com/node/1412. 
16. ^ Leung, Chee Chee: Extinction warning for Tassie devils, The Age, 4 October 2007.
17. ^ "Scientists make progress in understanding Tasmanian devil disease". New York Times. 2007-10-09. http://www.iht.com/articles/2007/10/09/news/devil.php. "Australian researchers have made a breakthrough in understanding a rapidly spreading facial cancer that has killed a large percentage of the Tasmanian devil population." 
18. ^ http://northerntasmania.yourguide.com.au/news/local/news/environmental-issues/disease-setback-for-tasmanian-devil-tumour-evolving-with-nine-strains-now-identified/1227014.aspx
19. ^ ^{a b} "New Tas devil tumour strands 'harder to vaccinate' – ABC News (Australian Broadcasting Corporation)". ABC.net.au. 2008-07-25. http://www.abc.net.au/news/stories/2008/07/25/2315094.htm. Retrieved 2010-01-03. 
20. ^ Murchison, E. P.; Tovar, C.; Hsu, A.; Bender, H. S.; Kheradpour, P.; Rebbeck, C. A.; Obendorf, D.; Conlan, C. et al. (2009). "The Tasmanian Devil Transcriptome Reveals Schwann Cell Origins of a Clonally Transmissible Cancer". Science 327 (5961): 84–87. doi:10.1126/science.1180616. PMC 2982769. PMID 20044575. http://www.pubmedcentral.nih.gov/articlerender.fcgi?tool=pmcentrez&artid=2982769.  edit
21. ^ ^{a b} Kinver, Mark (1 January 2010). "Tasmanian devil facial cancer origins 'identified'". BBC. http://news.bbc.co.uk/2/hi/science/nature/8433645.stm. 
22. ^ ^{a b c} Walsh, Bryan (1 January 2010). "Decoding the Tasmanian Devil's Deadly Cancer". Time. http://www.time.com/time/health/article/0,8599,1950787,00.html?xid=rss-topstories. 
23. ^ Owen and Pemberton, p. 6.
24. ^ Kinver, Mark (15 July 2008). "Tumours 'alter devils' sex lives'". BBC News. http://news.bbc.co.uk/2/hi/science/nature/7505244.stm. 
25. ^ http://www.environment.gov.au/biodiversity/threatened/publications/recovery/pubs/draft-for-comment-tasmanian-devil.pdf
26. ^ O'Neill, Iain D. (2010). "Tasmanian devil facial tumor disease: Insights into reduced tumor surveillance from an unusual malignancy". International Journal of Cancer 127 (7): 1637. doi:10.1002/ijc.25374. 
27. ^ ^{a b c} Wood, Danielle (1 September 2003). "Tassie devil under threat". The Mercury (Hobart Town, Tasmania): p. 1. 
28. ^ Lachish, Shelly; McCallum, Hamish; Mann, Dydee; Pukk, Christy E.; Jones, Menna E. (2010). "Evaluation of Selective Culling of Infected Individuals to Control Tasmanian Devil Facial Tumor Disease". Conservation Biology 24 (3): 841–851. doi:10.1111/j.1523-1739.2009.01429.x. PMID 20088958. 
29. ^ Bostanci A (2005). "A Devil of a Disease". Science 307 (5712): 1035. doi:10.1126/science.307.5712.1035. PMID 15718445. 
30. ^ "DPIW – Fox Impact on Wildlife". Dpiw.tas.gov.au. 2010-05-25. http://www.dpiw.tas.gov.au/inter.nsf/WebPages/SJON-52J8U3?open. Retrieved 2010-09-11. 
31. ^ "The Tasmanian Devil Needs a Saviour". Devil Ark. http://www.devilark.com.au/. Retrieved 2011-04-19. 
32. ^ Scientific American, March 2007
33. ^ Contagious cancer: the evolution of a killer, David Quammen, Harper's Magazine, April 2008.
34. ^ BBC – Fence hope for Tasmanian Devils. Retrieved 5 January 2009.
35. ^ "Cancer-related death for Cedric the devil – ABC News (Australian Broadcasting Corporation)". ABC.net.au. 2010-09-01. http://www.abc.net.au/news/stories/2010/09/01/2999309.htm. Retrieved 2010-09-11. 
36. ^ "A pre-tumour diagnostic test for DFTD". Tassiedevil.com.au. 2009-06-15. http://www.tassiedevil.com.au/tasdevil.nsf/TheProgram/4836FF3FB8C7A885CA2576D20003AEFA?OpenDocument. Retrieved 2010-09-11. 
37. ^ Matthew Denholm (2010-03-10). "Genetic study raises hopes for Tasmanian devils hit by facial tumour disease". The Australian. http://www.theaustralian.com.au/news/health-science/genetic-study-raises-hopes-for-tasmanian-devils-hit-by-facial-tumour-disease/story-e6frg8y6-1225839047676. Retrieved 2010-09-11. 
38. ^ Czarny, N.A.; Rodger, J.C. (2010). "Vitrification as a method for genome resource banking oocytes from the endangered Tasmanian devil (Sarcophilus harrisii)☆". Cryobiology 60 (3): 322–5. doi:10.1016/j.cryobiol.2010.02.007. PMID 20219455. 
39. ^ "Devil cure hope in rainforest". The Mercury. 2010-06-20. http://www.themercury.com.au/article/2010/06/20/153431_tasmania-news.html. Retrieved 2010-10-08. 
40. ^ http://www.nature.com/news/2009/091231/full/news.2009.1169.html
41. ^ Miller, Webb; et al. (27). "Genetic diversity and population structure of the endangered marsupial Sarcophilus harrisii (Tasmanian devil)". Proceedings of the National Academy of Sciences 108 (30): 12348. doi:10.1073/pnas.1102838108. 
42. ^ http://www.vetoncologyconsults.com/Tassie%20devils.htm
43. ^ McCallum H (2008). "Tasmanian devil facial tumour disease: lessons for conservation biology". Trends Ecol Evol. 23 (11): 631–7. doi:10.1016/j.tree.2008.07.001. PMID 18715674. 
44. ^ Owen and Pemberton, pp.170–171
45. ^ "Tasmanian devils threatened by facial tumour disease". Science Show (Australian Broadcasting Corporation). 2007-04-21. http://abc.com.au/rn/scienceshow/stories/2007/1902683.htm. Retrieved 2010-10-08. 
46. ^ Owen and Pemberton, p.177
47. ^ Tasmania, Parliamentary Debates, House of Assembly, 29 October 2003, part 2, pages 31–104. (part 2) 3:30 pm (Jeremy Rockliff, Shadow Minister for Primary Industries, Water and Environment; Nick McKim, Tasmanian Greens; Bryan Green, Minister for Primary Industries, Water and Environment).
48. ^ Tasmania, Parliamentary Debates, House of Assembly, 20 August 2003, part 1, pages 1–29, (Bryan Green, Minister for Primary Industries, Water and Environment). (10:58 am) (part 1)
49. ^ "Wildlife specialists concerned about Tassie Devil disease". Australian Broadcasting Corporation. 2003-10-14. http://www.abc.net.au/worldtoday/content/2003/s966941.htm. Retrieved 2010-10-08. 
50. ^ "Devil Disease". Stateline Tasmania. Australian Broadcasting Corporation. 2004-09-10. http://www.abc.net.au/stateline/tas/content/2003/s1196883.htm. Retrieved 2010-10-08. 
51. ^ Owen and Pemberton, p.178
52. ^ Owen and Pemberton, p.184-185
53. ^ http://tasmaniantimes.com/images/uploads/obendorf_eur_j_oncol_4-08.pdf
54. ^ http://www.tassiedevil.com.au/tasdevil.nsf/file/DD87BEF28EFEF6C3CA2576D20004BB2C/$file/FAQs%20Devil%20Facial%20Tumour%20Disease.pdf
55. ^ Conservation Breeding Specialist Group (2008). "Tasmanian Devil PHVA Final Report" (PDF). Apple Valley, Minnesota: IUCN/SSC Conservation Breeding Specialist Group. http://www.cbsg.org/cbsg/workshopreports/23/tasmanian_devil_phva_2008.pdf. Retrieved 2 October 2010. 
56. ^ Woods, Gregory M.; Kreiss, Alexandre; Belov, Katherine; Siddle, Hannah V.; Obendorf, David L.; Muller, H. Konrad (2007). "The Immune Response of the Tasmanian Devil (Sarcophilus harrisii) and Devil Facial Tumour Disease". EcoHealth 4 (3): 338. doi:10.1007/s10393-007-0117-1. 
57. ^ McCallum, Hamish; Tompkins, Daniel M.; Jones, Menna; Lachish, Shelly; Marvanek, Steve; Lazenby, Billie; Hocking, Greg; Wiersma, Jason et al. (2007). "Distribution and Impacts of Tasmanian Devil Facial Tumor Disease". EcoHealth 4 (3): 318. doi:10.1007/s10393-007-0118-0. 
58. ^ Denholm, Matthew (2008-01-22). "Cancer agents found in Tasmanian devils". News.com.au. http://www.news.com.au/story/0,23599,23087523-421,00.html. Retrieved 2010-03-16. 
59. ^ COPPER, H.L.; MacKay, CM; Banfield, WG (1964-10-01). "CHROMOSOME STUDIES OF A CONTAGIOUS RETICULUM CELL SARCOMA OF THE SYRIAN HAMSTER". J Natl Cancer Inst 33: 691–706. PMID 14220251. 
60. ^ Banfield, William G.; Woke, PA; MacKay, CM; Cooper, HL (1965-05-28). "Mosquito Transmission of a Reticulum Cell Sarcoma of Hamsters". Science 148 (3674): 1239–1240. doi:10.1126/science.148.3674.1239. PMID 14280009. http://www.sciencemag.org/cgi/content/abstract/148/3674/1239. 
61. ^ Siddle, H. V.; Kreiss, A.; Eldridge, M. D. B.; Noonan, E.; Clarke, C. J.; Pyecroft, S.; Woods, G. M.; Belov, K. (2007). "Transmission of a fatal clonal tumor by biting occurs due to depleted MHC diversity in a threatened carnivorous marsupial". Proceedings of the National Academy of Sciences 104 (41): 16221. doi:10.1073/pnas.0704580104. 

Further reading

• Australian Government (February 2010) State party report on the state of conservation of the Tasmanian Wilderness World Heritage Area (Australia) pp. 29–32
• Bender, Hannah S. (2010). "Devil Facial Tumour Disease (DFTD): Using Genetics and Genomics to Investigate Infectious Disease in an Endangered Marsupial". Marsupial Genetics and Genomics. pp. 499. doi:10.1007/978-90-481-9023-2_23. ISBN 978-90-481-9022-5. 
• Bode, M., C. Hawkins, T. Rout, and B. Wintle. 2009. Efficiently locating conservation boundaries: Searching for the Tasmanian devil facial tumour disease front. Biological Conservation 142:1333–1339.
• Bradshaw, C. J. A. and B. W. Brook. 2005. Disease and the devil: density-dependent epidemiological processes explain historical population fluctuations in the Tasmanian devil. Ecography 28:181–190.
• Department of primary industries, water and environment (February 2005) Tasmanian Devil Facial Tumour Disease (DFTD) Disease Management Strategy
• Jones, Menna E.; Cockburn, Andrew; Hamede, Rodrigo; Hawkins, Clare; Hesterman, Heather; Lachish, Shelly; Mann, Diana; McCallum, Hamish; Pemberton, David. (2008). "Life-history change in disease-ravaged Tasmanian devil populations". Proceedings of the National Academy of Sciences of the United States of America 105 (29): 10023–7. doi:10.1073/pnas.0711236105. PMC 2481324. PMID 18626026. http://www.pubmedcentral.nih.gov/articlerender.fcgi?tool=pmcentrez&artid=2481324. 

External links

• Save the Tasmanian Devil website