Wing pathology of white-nose syndrome in bats suggests life-threatening disruption of physiology

BMC Biology

Volumn 8, Issue , 2010, Pages

  Cryan, Paul M ^a   Meteyer, Carol U ^b   Boyles, Justin G ^c   Blehert, David S ^b  

^a FORT COLLINS SCIENCE CENTER   (United States)

^b NATIONAL WILDLIFE HEALTH CENTER   (United States)

^c UNIVERSITY OF PRETORIA   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHIBIA; FUNGI; GEOMYCES;

ANIMAL; ANIMAL DISEASE; ARTICLE; ASCOMYCETES; BAT; BLOOD FLOW; DEHYDRATION; ENERGY METABOLISM; FORELIMB; HIBERNATION; HOMEOSTASIS; MICROBIOLOGY; MYCOSIS; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; THERMOREGULATION; VASCULARIZATION;

ANIMALS; ASCOMYCOTA; BODY TEMPERATURE REGULATION; CHIROPTERA; DEHYDRATION; ENERGY METABOLISM; HIBERNATION; HOMEOSTASIS; MYCOSES; REGIONAL BLOOD FLOW; WATER LOSS, INSENSIBLE; WING;

EID: 78549277122     PISSN: None     EISSN: 17417007     Source Type: Journal    
DOI: 10.1186/1741-7007-8-135     Document Type: Article

References (49)

1. Blehert DS, Hicks AC, Behr M, Meteyer CU, Berlowski-Zier BM, Buckles EL, Coleman JT, Darling SR, Gargas A, Niver R, Okoniewski JC, Rudd RJ, Stone WB. Bat white-nose syndrome: an emerging fungal pathogen?. Science 2009, 323:227. 10.1126/science.1163874, 18974316.
2. Reichard JD, Kunz TH. White-nose syndrome inflicts lasting injuries to the wings of little brown myotis (Myotis lucifugus). Acta Chiropterol 2009, 11:457-464.
3. Courtin F, Stone WB, Risatti G, Gilbert K, Van Kruiningen HJ. Pathologic findings and liver elements in hibernating bats with white-nose syndrome. Vet Pathol 2010, 47:214-219. 10.1177/0300985809358614, 20110222.
4. Turner GR, Reeder DM. Update of white-nose syndrome in bats, September 2009. Bat Res News 2009, 50:47-53.
5. Frick WF, Pollock JF, Hicks AC, Langwig KE, Reynolds DS, Turner GR, Butchkoski CM, Kunz TH. An emerging disease causes regional population collapse of a common North American bat species. Science 2010, 329:679-682. 10.1126/science.1188594, 20689016.
6. Gargas A, Trest MT, Christensen M, Volk TJ, Blehert DS. Geomyces destructans sp. nov. associated with bat white-nose syndrome. Mycotaxon 2009, 108:147-154.
7. Meteyer CU, Buckles EL, Blehert DS, Hicks AC, Green DE, Shearn-Bochsler V, Thomas NJ, Gargas A, Behr MJ. Histopathologic criteria to confirm white-nose syndrome in bats. J Vet Diagn Invest 2009, 21:411-414.
8. Puechmaille SJ, Verdeyroux P, Fuller H, Ar Gouilh M, Bekaert M, Teeling EC. White-Nose Syndrome fungus (Geomyces destructans) in bat, France. Emerg Infect Dis 2010, 16:290-293. 2958029, 20113562.
9. Wibbelt G, Kurth A, Hellmann D, Weishaar M, Barlow A, Veith M, Prüger J, Görföl T, Grosche L, Bontadina F, Zöphel U, Seidl HP, Cryan PM, Blehert DS. White-nose syndrome fungus (Geomyces destructans) in bats, Europe. Emerg Infect Dis 2010, 16:1237-1243. 10.3201/eid1608.100002, 20678317.
10. Reeder WG, Cowles RB. Aspects of thermoregulation in bats. J Mammal 1951, 32:389-403.
11. Carey HV, Andrews MT, Martin SL. Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiol Rev 2003, 83:1153-1181.
12. Jaeger R. Serological, hematological and immunological research on hibernating bats. Experientia 1963, 19:596-598. 10.1007/BF02151011, 14101525.
13. Prendergast BJ, Freeman DA, Zucker I, Nelson RJ. Periodic arousal from hibernation is necessary for initiation of immune response in ground squirrels. Am J Physiol Regul Integr Comp Physiol 2002, 282:R1054-R1062.
14. Bouma HJ, Carey HV, Kroese GM. Hibernation: the immune system at rest?. J Leukocyte Biol 2010, 88:619-624. 10.1189/jlb.0310174, 20519639.
15. Geiser F. Metabolic and body temperature reduction during hibernation and daily torpor. Annu Rev Physiol 2004, 66:239-274. 10.1146/annurev.physiol.66.032102.115105, 14977403.
16. Davis WH. Hibernation: ecology and physiological ecology. Biology of Bats 1970, 1:265-300. New York: Academic Press, Wimsatt WA.
17. Ransome R. The Natural History of Hibernating Bats 1990, London: Christopher Helm.
18. Boyles JG, Storm JJ, Brack V. Thermal benefits of clustering during hibernation: a field test of competing hypotheses on Myotis sodalis. Funct Ecol 2008, 22:632-636.
19. Makanya AN, Mortola JP. The structural design of the bat wing web and its possible role in gas exchange. J Anat 2007, 211:687-967. 10.1111/j.1469-7580.2007.00817.x, 2375846, 17971117.
20. Quay WB. Integument and derivatives. Biology of Bats 1970, 2:1-56. New York: Academic Press, Wimsatt WA.
21. Richardson MD, Shankland GS. Rhizopus, Rhizomucor, Absidia and other agents of systemic and subcutaneous zygomycoses. Manual of Clinical Microbiology 1999, 7:1242-1255. Washington DC: American Society for Microbiology Press, Murray PR, Baron EJ, Pfaller MA, Tenover FC, Yolken RH.
22. Kallen FC. Some aspects of water balance in the hibernating bat. Annales Acad Scient Fenn 1964, 71:259-267.
23. Thomas DW, Cloutier D. Evaporative water loss by hibernating little brown bats, Myotis lucifugus. Physiol Zool 1992, 65:443-456.
24. Licht P, Leitner P. Physiological responses to high environmental temperatures in three species of microchiropteran bats. Comp Biochem Physiol 1967, 22:371-387.
25. Webb PI, Speakman JR, Racey PA. Evaporative water loss in two sympatric species of vespertilionid bat, Plecotus auritus and Myotis daubentonii: relation to foraging mode and implications for roost site selection. J Zool Soc Lond 1995, 235:269-278.
26. Bassett JE. Control of postprandial water loss in Myotis lucifugus lucifugus. Comp Biochem Physiol 1980, 65:497-500.
27. Twente JW. Some aspects of habitat selection and other behavior of cavern-dwelling bats. Ecology 1955, 36:706-732.
28. Webb PI. The comparative ecophysiology of water balance in microchiropteran bats. Symp Zool Soc Lond 1995, 67:203-218.
29. Yoder JA, Benoit JB, Denlinger DL, Tank JL, Zettler LW. An endosymbiotic conidial fungus, Scopulariopsis brevicaulis, protects the American dog tick, Dermacentor variabilis, from desiccation imposed by an entomopathogenic fungus. J Invertebr Pathol 2008, 97:119-127. 10.1016/j.jip.2007.07.011, 17880996.
30. Cortese TA, Nicoll PA. In vivo observations of skin appendages in the bat wing. J Invest Dermatol 1970, 54:1-10. 10.1111/1523-1747.ep12551469, 5416675.
31. Murphy RC. Fluorescence studies in the wing of the living bat. Anat Rec 1960, 136:127-136. 10.1002/ar.1091360207, 14425408.
32. Sisk MO. A study of the sudoriparous glands of the little brown bat, Myotis lucifugus lucifugus. J Morphol 1957, 101:425-455.
33. Speakman JR, Thomas DW. Physiological ecology and energetics of bats. Bat Ecology 2003, 430-490. Chicago: University of Chicago Press, Kunz TH, Fenton MB.
34. Thomas DW. The physiological ecology of hibernation in vespertilionid bats. Symp Zool Soc Lond 1995, 67:233-244.
35. Thomas DW, Dorais M, Bergeron JM. Winter energy budgets and cost of arousals for hibernating little brown bats, Myotis lucifugus. J Mammal 1990, 71:475-479.
36. Speakman JR, Racey PA. Hibernal ecology of the pipistrelle bat: energy expenditure, water requirements and mass loss, implications for survival and the function of winter emergence flights. J Anim Ecol 1989, 58:797-813.
37. Kallen FC. The cardiovascular systems of bats: structure and function. Biology of Bats 1977, 3:289-483. New York: Academic Press, Wimsatt WA.
38. Neuweiler G. The Biology of Bats. English edition 2000, New York: Oxford University Press.
39. Herreid CF, Bretz WL, Schmidt-Nielsen K. Cutaneous gas exchange in bats. Am J Physiol 1968, 215:506-508.
40. Szewczak JM. Matching gas exchange in the bat from flight to torpor. Am Zool 1997, 37:92-100.
41. Szewczak JM, Jackson DC. Apneic oxygen uptake in the torpid bat, Eptesicus fuscus. J Exp Biol 1992, 173:217-227.
42. Thomas DW, Cloutier D, Gagné D. Arrhythmic breathing, apnea and non-steady-state oxygen uptake in hibernating little brown bats. J Exp Biol 1990, 149:395-406.
43. Boyles JG, Willis CKR. Could localized warm areas inside cold caves reduce mortality of hibernating bats affected by white-nose syndrome?. Front Ecol Environ 2010, 8:92-98.
44. Boyles JG, Dunbar MB, Whitaker JO. Activity following arousal in winter in North American vespertilionid bats. Mammal Rev 2006, 36:267-280.
45. Yin J, Wang H, Racey P, Zhang S. Distribution and ultrastructure of Merkel cell of the fishing bat (Myotis ricketti). Sci China C-Life Sci 2009, 52:802-806. 10.1007/s11427-009-0118-0, 19802737.
46. Zook J. The neuroethology of touch in bats: cutaneous receptors of the bat wing. Neurosci Abstr 2005, 78.21.
47. Scott D, Miller W, Griffin C. Muller and Kirk's Small Animal Dermatology 2001, Philadelphia, PA: WB Saunders, 6.
48. Rosenblum EB, Voyles J, Poorten TJ, Stajich JE. The deadly chytrid fungus: a story of an emerging pathogen. PLoS Pathogens 2010, 6:e1000550. 10.1371/journal.ppat.1000550, 2813266, 20126439.
49. Voyles J, Young S, Berger L, Campbell C, Voyles WF, Dinudom A, Cook D, Webb R, Alford RA, Skerratt LF, Speare R. Pathogenesis of chytridiomycosis, a cause of catastrophic amphibian declines. Science 2009, 326:582-585. 10.1126/science.1176765, 19900897.