White nose syndrome

A little brown bat with white nose syndrome.

White-nose syndrome (WNS) is an emerging disease in North American bats which as of 2012 was associated with at least 5.7 million bat deaths.[1] The condition is named for a distinctive fungal growth around the muzzles and on the wings of hibernating bats and was first identified from a February 2006 photo taken in a cave in Schoharie County, New York.[2] It has rapidly spread.[3] As of September 2014, the fungus has been found in caves and mines of 25 states throughout the Northeastern US, as far south as Mississippi, as far west as Missouri and as far north as five Canadian provinces.[4][5]

The disease is caused by the fungus Pseudogymnoascus destructans which colonizes the bat's skin. No obvious treatment or means of preventing transmission is known,[6][7] and some species have declined >90% within five years of the disease reaching a site.[8]

The US Fish & Wildlife Service (USFWS) has called for a moratorium on caving activities in affected areas[9] and strongly recommends to decontaminate clothing or equipment in such areas after each use. The National Speleological Society maintains an up-to-date page to keep cavers apprised of current events and advisories.[10]

Impact

Little brown bat (Myotis lucifugus) affected by white nose syndrome

As of 2012 white nose syndrome was estimated to have caused at least 5.7 million to 6.7 million bat deaths in North America.[1] In 2008 bats declined in some caves by more than 90%,[11][12] Alan Hicks with the New York State Department of Environmental Conservation described the impact in 2008 as "unprecedented" and "the gravest threat to bats...ever seen."[13]

As of 2014 eleven bat species, including three endangered species and one species proposed for endangered species listing have been affected by WNS or exposed to the causative fungus, Pseudogymnoascus destructans, with impacts varying widely.[14] As of 2012 four species have suffered substantial declines and extinction of at least one species was predicted.[8] Declines included species already listed as endangered in the US, such as the Indiana bat, whose hibernaculum in many states has been affected.[15] The once-common little brown bat has suffered a major population collapse in the northeastern US.[16] In 2012 the northern long-eared myotis ("Myotis septentrionalis") was reported to be extirpated from all sites where the disease has been present for >4 years.[8] In 2009, the Virginia big-eared bat (Corynorhinus townsendii virginianus), the official state bat of Virginia,[17] and the Gray bat had yet to suffer measurable declines.

Beyond the direct effect on bat populations, WNS has broader ecological implications. The Forest Service estimated in 2008 that the die-off from white-nose syndrome means that at least 2.4 million pounds of insects (1.1 million kg) will go uneaten and become a financial burden to farmers, possibly leading to crop damage or having other economic impact in New England.[11] It is estimated that bats save farmers in the U.S. 3 billion dollars annually in pest control services. In addition, numerous bat species provide crucial pollination and seed dispersal services. [18]

In 2008, comparisons were raised to colony collapse disorder, another incompletely understood phenomenon resulting in the abrupt disappearance of Western honey bee colonies,[19][20] and with chytridiomycosis, a fungal skin disease linked with worldwide declines in amphibian populations.[21][22]

Research

2009 VOA report about the disease

Biologists of the US Fish and Wildlife Service have been collecting information at each site in regard to the number of bats affected, the geographic extent of the outbreaks and samples of affected bats. They developed a geographic database to track the location of sites, where WNS has been found.[23] The Fish and Wildlife Service has been partnering with the Northeastern Cave Conservancy to track movements of cavers that have visited affected sites in New York.[23]

In 2009, the Service advised closing caves to explorers in 20 states, from the Midwest to New England. This directive was supposed to be extended to 13 southern states. One Virginia scientist stated, "If it gets into caves more to our south, in places like Tennessee, Kentucky, Georgia and Alabama, we’re going to be talking deaths in the millions.".[17] In March 2012, WNS was discovered on some tri-colored bats (Perimyotis subflavus) in Russell Cave in Jackson County Alabama.[24]

Cause

Pseudogymnoascus destructans

The fungus Pseudogymnoascus destructans is the primary cause of WNS.[25] It preferably grows in the 4 to 15 °C range (39–59 °F) and will not grow at temperatures above 20 °C (68 °F).[26] It is cold loving or psychrophilic. It is phylogenetically related to Geomyces spp., but with a conidial morphology distinct from characterized members of this genus.[21] Early laboratory research placed the fungus in the genus Geomyces,[21][27] but later phylogenic evaluation revealed this organism should be reclassified. The genera Geomyces and Pseudogymnoascus are closely related and found in the family Pseudeurotiaceae; P. destructans was found to be most closely related to the Pseudogymnoascus species in 2013, implying that its name should be changed to Pseudogymnoascus destructans.[28]

A 2011 study found that 100% of healthy North American bats infected with the fungus cultured from infected bats exhibit lesions consistent with the disease.[27] Direct microscopy and culture analyses demonstrated that the skin of the WNS-affected bats is colonized by the fungus.[21]

The species has been found in healthy bats in Europe, although as of 2010 it was not clear whether it was introduced into North America from Europe or Asia.[29][30]

Infection

A laboratory experiment suggests that physical contact is required for one bat to infect another, because bats in mesh cages adjacent to infected bats did not contract the fungus. This implies that the fungus is not airborne, or at least is not transmitted from bat to bat through the air.[27] The primary way this fungus is spread is through bat-to-bat contact or infected cave-to-bat contact. Humans entering bat caves may also transport this fungus from one location to another. [31]

Signs of disease

The signs observed with WNS include unusual winter behavior like abnormally frequent or abnormally long arousal from torpor (temporary hibernation), flying, loss of body fat, damage and scarring of the wing membranes, and death. As early as 2011 it was hypothesized that prematurely expending the fat reserves for winter survival may be a cause for death.[32]

Pathophysiology

Until December 2014 the cause for the abnormal behavior was unclear, as no physiological data linking altered behavior to hypothesized increased energy demands existed.

The Fish and Wildlife Service published a case control study in December 2014: Of 60 little brown bats, 39 bats were randomly assigned to infection by applying conidia to skin of the dorsal surface of both wings and 21 bats remained controls. All were observed for 95 days and euthanized. 32 bats developed WNS (30 mild to moderate and 2 moderate to severe). Interestingly, the remaining 7 infected bats were PCR-positive with normal wing histology. Infected bats with WNS had higher proportions of lean tissue mass to fat tissue mass than uninfected bats in measuring an increase in total body water volume as a percent of body mass. Infected bats used twice as much energy as healthy bats, and starved to death. Direct calculations of energy expenditure failed for most bats, because isotope concentrations were indistinguishable from background. There was also no difference in torpor durations in this experiment; The average torpor duration for infected bats was 9.1 days with an average arousal of 54 min. Average torpor duration for control bats was 8.5 days with an average arousal duration of 55 min.[33] Infected bats suffered respiratory acidosis with an almost 40% higher mean pCO2 than healthy bats, and potassium concentration was significantly higher.[33] Hence the following model of infection exists: Pseudogymnoascus destructans colonizes and eventually invades the wing epidermis. This causes increased energy expenditure, and an elevated blood pCO2 and bicarbonate called chronic respiratory acidosis, possibly due to diffusion problems. Hyperkalemia (elevated blood potassium) ensues because of an acidosis-induced extracellular shift of potassium. Dying, infected cells could also leak their (intracellular) potassium into the blood. The damaged wing epidermis might stimulate increased frequencies of arousal from torpor, which removes excess CO2 and normalizes blood pH, at the expense of hydration and fat reserves. With worsening wing damage, the effects are exacerbated by water and electrolyte loss across the wound (hypotonic dehydration), which stimulates more frequent arousals in positive feedback loop that ultimately leads to death.[33]

Geographical spread

The disease was first reported in January 2007 in New York caves[19] although it was retrospectively detected in a photograph taken in early 2006. It spread to other New York caves and into Vermont, Massachusetts, and Connecticut by 2008.[34][35] In early 2009, it was confirmed in New Hampshire,[36] New Jersey, Pennsylvania,[37] Virginia,[38] West Virginia[34] and in March 2010, in Ontario Canada, Maryland,[39] Middle Tennessee, Missouri,[40] and Quebec, Canada.[41][42] In 2011, the syndrome was confirmed in Ohio,[43] Indiana,[44] Kentucky,[45] North Carolina,[38] Maine,[46] New Brunswick and Nova Scotia.[47] In the winter of 2011–2012, Alabama,[24] Delaware[48] and Arkansas[49] confirmed the disease in bats and new cases showed up in northeastern Ohio,[50] and Acadia National Park in Maine.[51] Confirmed cases appeared in 2013 in Georgia,[52] South Carolina,[53] Illinois,[54] and the Canadian Province of Prince Edward Island.[55] On March 28, 2014, WDNR and USGS staff conducting routine surveillance detected white-nose syndrome in a single mine in Grant County Wisconsin and the USGS National Wildlife Health Center later confirmed the disease.[56] On April 10, 2014, the Michigan Department of Natural Resources announced that the disease had been found in Alpena County, Mackinac County, and Dickinson County.[57] Oklahoma and Myotis velifer were removed from the list of White Nose Syndrome suspects after retesting was negative.[58]

As of 3 September 2014 the syndrome has been confirmed in 25 states and 5 Canadian provinces. The causative fungus has been confirmed in three additional states Iowa, Minnesota, and Mississippi.[59] In May, 2014, after retesting, the Myotis velifer specimen from Oklahoma and other swabs and samples from the area tested negative, and Oklahoma and the Myotis Velifer were removed from the list of White Nose Syndrome suspects.[58]

The role of humans in the spread of the disease is debated. It is likely the fungus was brought to North America by human activities, because no bats normally migrate between Europe and North America, and the fungus was first discovered in New York where there are commercial caves with thousands of visitors per year. In addition, research has shown the fungus can persist on human clothing, and thus could be carried among locations, necessitating a need for Decontamination described below. However, there is little evidence that humans have so far played a role in the spread of the fungus in North America, in that the speed and direction of spread from the initial sites in New York are consistent with what is known about normal bat movement. The lack of long distance spread (e.g. distances greater than 200 km) may be a result of reduced human movement between infected and uninfected sites or decontamination activities or both.

Decontamination

The fungus Pseudogymnoascus destructans, or a closely related species of fungus, has been found in soil samples from infected caves and suggests that it can be transported from cave to cave by soil, such as that carried by human clothing.[60] Precautionary decontamination methods are being encouraged to inhibit the possible spread of spores by humans. The WNS Decontamination Team, a sub-group of the Disease Management Working Group, published a national decontamination protocol on March 15, 2012. They revised the protocol on June 25, 2012,.[61] In May 2015, based upon laboratory tests, a recommendation was issued by to increase the temperature of the hot water treatment for submersible gear to 60 degrees Celsius for 20 minutes (up from 50 degrees Celsius).[62] All other guidance in the existing protocol should be followed.

As of 2008, cave management and preservation organizations had begun requesting that cave visitors limit their activities and disinfect clothing and equipment that has been used in possibly infected caves.[63] The current protocol goes further, and indicates that in many cases it is inappropriate to reuse even disinfected gear, and that new gear should be used.[64]:see p.3 flow chart

In some cases, access to caves is being closed entirely.[65]

See also

References

  1. 1 2 Froschauer, Ann; Coleman, Jeremy (17 January 2012). "North American bat death toll exceeds 5.5 million from white-nose syndrome" (PDF). White-Nose syndrome.org (US Fish & Wildlife Service). Retrieved 2012-02-03.
  2. ↑ Blehert, D. S.; Hicks, A. C.; Behr, M.; Meteyer, C. U.; Berlowski-Zier, B. M.; Buckles, E. L.; Coleman, J. T. H.; Darling, S. R.; Gargas, A.; Niver, R.; Okoniewski, J. C.; Rudd, R. J.; Stone, W. B. (2009). "Bat White-Nose Syndrome: An Emerging Fungal Pathogen?" (PDF). Science 323 (5911): 227. doi:10.1126/science.1163874. PMID 18974316.
  3. ↑ Raloff, Janet (9 April 2012). "Bat killer is still spreading". ScienceNews.
  4. ↑ "Three cases of bat disease discovered in Missouri". Missouri Department of Conservation. 2 April 2012.
  5. ↑ "Bat White Nose Syndrome (WNS) by Occurrence by County/District NSS WNS Map". US Fish & Wildlife Service. 5 April 2012.
  6. ↑ Coghlan, Andy (26 October 2011). "Bat killer identified". New Scientist.
  7. ↑ Ferrante, Julia. "Bucknell University professor, national research team identify cause of White-Nose Syndrome in bats".
  8. 1 2 3 Langwig, K.E.; W.F. Frick; J.T. Bried; A.C. Hicks; T.H. Kunz; A.M. Kilpatrick (2012). "Sociality, density-dependence and microclimates determine the persistence of populations suffering from a novel fungal disease, white-nose syndrome". Ecology Letters 15 (1): 1050–1057. doi:10.1111/j.1461-0248.2012.01829.x. PMID 22747672.
  9. ↑ "Cave activity discouraged to help protect bats from deadly white-nose syndrome" (PDF). US Fish and Wildlife Service.
  10. ↑ "White Nose Syndrome Page". National Speleological Society. Retrieved 9 November 2011.
  11. 1 2 Daley, Beth (2008-02-07). "Die-off of bats could hurt area crops". The Boston Globe. Retrieved 2008-02-14.
  12. ↑ Kelley, Tina (2008-03-25). "Bats Perish, and No One Knows Why". The New York Times. Retrieved 2008-03-25.
  13. ↑ Shapley, Dan (2008-02-05). "The Gravest Threat to Bats Ever Seen". The Daily Green. Retrieved 2008-02-14.
  14. ↑ "Bats affected by WNS". White-Nose Syndrome. Retrieved 2014-03-15.
  15. ↑ "Unexplained "White Nose" Disease Killing Northeast Bats". Environment News Service. 2008-01-31. Retrieved 2008-02-14.
  16. ↑ Frick, W. F.; Pollock, J. F.; Hicks, A. C.; Langwig, K. E.; Reynolds, D. S.; Turner, G. G.; Butchkoski, C. M.; Kunz, T. H. (5 August 2010). "An Emerging Disease Causes Regional Population Collapse of a Common North American Bat Species". Science 329 (5992): 679–682. doi:10.1126/science.1188594. PMID 20689016.
  17. 1 2 "Cute but contagious" The Economist, May 21, 2009
  18. ↑ "White Nose Syndrome of Bats Fact Sheet | Washington Department of Fish & Wildlife". wdfw.wa.gov. Retrieved 2016-02-03.
  19. 1 2 Hill, Michael (30 January 2008). "Bat Deaths in NY, VT. Baffle Experts". Associated Press. Retrieved 2008-02-14.
  20. ↑ Mann, Bryan (2008-02-19). "Northeast Bat Die-Off Mirrors Honeybee Collapse" (audio). All Things Considered (National Public Radio). Retrieved 2008-02-20.
  21. 1 2 3 4 Blehert DS, Hicks AC, Behr M, et al. (October 2008). "Bat White-Nose Syndrome: An Emerging Fungal Pathogen?". Science 323 (5911): 227. doi:10.1126/science.1163874. PMID 18974316. Retrieved 2008-11-02.
  22. ↑ "Newly Identified Fungus Implicated In White-nose Syndrome". Science Daily. 2008-10-31. Retrieved 2009-10-25.
  23. 1 2 US Fish & Wildlife Service, Northeast Region, "White-Nose Syndrome in bats: Something is killing our bats." http://www.fws.gov/northeast/white_nose.html (accessed April 14, 2009)
  24. 1 2 Tennessee Valley Authority (22 April 2013). "WNS in Alabama Updates | Alabama Bat Working Group". Alabamabatwg.wordpress.com. Retrieved 2014-03-15.
  25. ↑ Warnecke, L.; J.M. Turner; T.K. Bollinger; J.M. Lorch; V. Misrae; P.M. Cryan; G. Wibbelt; D.S. Blehert; et al. (2012). "Inoculation of bats with European Geomyces destructans supports the novel pathogen hypothesis for the origin of white-nose syndrome". Proceedings of the National Academy of Sciences of the United States of America 109 (1): 6999–7003. doi:10.1073/pnas.1200374109. PMID 22493237.
  26. ↑ Verant, M.L.; J.G. Boyles; W. Waldrep; G. Wibbelt; D.S. Blehert (2012). "Temperature-dependent growth of "Geomyces destructans", the fungus that causes bat white-nose syndrome". PLOS ONE 7 (1): e46280. doi:10.1371/journal.pone.0046280. PMID 23029462.
  27. 1 2 3 Lorch, Jeffrey M.; Meteyer, Behr, Boyles, Cryan, Hicks, Ballman, Coleman, Redell, Reeder, Blehert (26 October 2011). "Experimental infection of bats with Geomyces destructans causes white-nose syndrome". Nature. advanced online publication (7377): 376. doi:10.1038/nature10590.
  28. ↑ Minnis AM, Lindner DL; Lindner (July 2013). "Phylogenetic evaluation of Geomyces and allies reveals no close relatives of Pseudogymnoascus destructans, comb. nov., in bat hibernacula of eastern North America". Fungal Biology 117 (9): 638–49. doi:10.1016/j.funbio.2013.07.001. PMID 24012303.
  29. ↑ Puechmaille, Sébastien J.; Verdeyroux, Pascal; Fuller, Hubert; Ar Gouilh, Meriadeg; Bekaert, Michaël; Teeling, Emma C. (February 2010). "White-nose syndrome fungus (Geomyces destructans) in bat, France" (PDF). Emerging Infectious Diseases (Atlanta: Centers for Disease Control and Prevention) 16 (2): 290–3. doi:10.3201/eid1602.091391. ISSN 1080-6059. PMC 2958029. PMID 20113562. Retrieved 2 January 2010.
  30. ↑ Susan Young (2011-10-26). ""Culprit behind bat scourge confirmed" Nature". Nature.com. Retrieved 2014-03-15.
  31. ↑ "White Nose Syndrome of Bats Fact Sheet | Washington Department of Fish & Wildlife". wdfw.wa.gov. Retrieved 2016-02-03.
  32. ↑ "A National Plan for Assisting States, Federal Agencies, and Tribes in Managing White-Nose Syndrome in Bats" (pdf). US Fish and Wildlife Service. May 2011. p. 21. Retrieved 10 January 2015.
  33. 1 2 3 Michelle L Verant, Carol U Meteyer, John R Speakman, Paul M Cryan, Jeffrey M Lorch, David S Blehert (9 December 2014). "White-nose syndrome initiates a cascade of physiologic disturbances in the hibernating bat host". BMC Physiology 14 (10). doi:10.1186/s12899-014-0010-4. Retrieved 10 January 2015.
  34. 1 2 "White Nose Syndrome; Could cave dwelling bat species become extinct in our lifetime?". Bat Conservation and Management, Inc. Retrieved 2009-02-05.
  35. ↑ "Bat affliction found in Vermont and Massachusetts caves". Newsday. 15 February 2008. Retrieved 2008-02-20.
  36. ↑ http://www.nashuatelegraph.com/apps/pbcs.dll/article?AID=/20090223/NEWS02/302239991[]
  37. ↑ Kosack, Joe (2009). "White-nose syndrome surfaces in Pennsylvania". Retrieved 2009-02-05.
  38. 1 2 "White-Nose Syndrome Statements Archive". Dgif.virginia.gov. 2009-04-02. Retrieved 2014-03-15.
  39. ↑ Maryland Department of Natural Resources (March 18, 2010). "White Nose Syndrome Confirmed In Bats From Western Maryland Cave" (PDF). White-Nose Syndrome. Retrieved 2014-03-15.
  40. ↑ "White-Nose Syndrome in Missouri | Missouri Department of Conservation". Mdc.mo.gov. Retrieved 2014-03-15.
  41. ↑ Ontario Ministry of Natural Resources (March 19, 2010). "White Nose Syndrome Detected In Ontario Bats". Archived from the original on 24 March 2010. Retrieved 2010-03-19.
  42. ↑ Smith, Chris. "Bat in Clarksville's Dunbar Cave with deadly fungus may be migrant". The Leaf-Chronicle. Retrieved 2010-03-24.
  43. ↑ "White-nose Syndrome Detected in Ohio". Ohio DNR. 2011-03-30. Retrieved 2014-03-15.
  44. ↑ "Newsroom". State of Indiana. 2011-02-01. Retrieved 2014-03-15.
  45. ↑ "WNS spreads in Kentucky". White-Nose Syndrome. Retrieved 2014-03-15.
  46. ↑ "White Nose Syndrome". Maine Department of Inland Fisheries and Wildlife.
  47. ↑ "Early Signs of White Nose Syndrome Spreading to Bats". White-Nose Syndrome. Retrieved 2014-03-15.
  48. ↑ "White-Nose Syndrome detected in Delaware bats". DNRec.delaware.gov. Retrieved 2014-03-15.
  49. ↑ Arkansas Game and Fish Commission (28 July 2013). "Fungus that kills bats prompts continued precautions at Arkansas caves" (PDF).
  50. ↑ Galbincea, Pat (2012-02-16). "Deadly white-nose syndrome found on bats in Cuyahoga and Geauga County parks". The Plain Dealer. Retrieved 2012-02-17.
  51. ↑ Acadia National Park (20 March 2012). "Bat Disease, White-Nose Syndrome, Confirmed in Acadia National Park: Not Harmful to Humans, but Deadly to Bats" (PDF). Fish and Wildlife Service. Retrieved 2012-03-21.
  52. ↑ Georgia Department of Natural Resources News Release (12 March 2013). "Disease Deadly to Bats Confirmed in Georgia". Retrieved 2013-03-26.
  53. ↑ South Carolina Department of Natural Resources News Release (2013-03-11). "Bat disease white-nose syndrome confirmed in South Carolina". Retrieved 2013-03-26.
  54. ↑ Illinois Department of Natural Resources News Release (2013-02-28). "White-Nose Syndrome Confirmed in Illinois Bats" (PDF). Retrieved 2013-03-26.
  55. ↑ "Bat white-nose syndrome confirmed on Prince Edward Island". CBC News. 2013-02-27. Retrieved 2014-03-15.
  56. ↑ "Deadly bat disease detected in single Wisconsin site; State joins 23 others in confirming white-nose syndrome". Wisconsin Department of Natural Resources. 10 April 2014.
  57. ↑ "Detroit Free Press article". Detroit Free Press. 11 April 2014. p. 1A.
  58. 1 2 "Oklahoma removed from list of suspected bat fungus areas". Oklahoma Department of Wildlife Conservation. Retrieved 13 May 2014.
  59. ↑ "Where is it now?". White-Nose Syndrome. Retrieved 2015-01-09.
  60. ↑ Linder, Daniel; Blehert (2011-03-18). "DNA-based detection of the fungal pathogen Geomyces destructans in soils from bat hibernacula". Mycologia 103 (2): 241–246. doi:10.3852/10-262. PMID 20952799.
  61. ↑ WNS Decontamination Team. "National White-Nose Syndrome Decontamination Protocol v 06.25.2012" (PDF).
  62. ↑ Geboy, Richard. "National Decontamination Protocol Update" (PDF). Midwest Regional WNS Coordinator, US Fish & Wildlife Service.
  63. ↑ "Something is killing our bats: The white-nose syndrome mystery". US Fish and Wildlife Service. Retrieved 2008-02-14.
  64. ↑ WNS Decontamination Team. "National White-Nose Syndrome Decontamination Protocol v 06.25.2012" (PDF).
  65. ↑ Munger, Edward, Jr. (2008-02-14). "Group asking cavers to keep out". Daily Gazette. Retrieved 2008-02-14.

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