This document discusses disease transmission models and how they relate to amphibian extinction by the emerging infectious disease chytridiomycosis. It is presented that extinction was thought to be impossible if transmission was density-dependent and contact was homogeneous, but these assumptions may not always hold true. Habitat fragmentation can increase contact rates and transmission effectiveness. A study on the Arizona tiger salamander found populations in more sparse and modified ponds had higher incidence of infection. While extinction is a natural process, loss of biodiversity can negatively impact ecosystems and human welfare through reductions in resources like food and medicine.

1. Is the end near for amphibians? The effect of humans and pathogens Bongsoo Park David Place Oscar Bedoya Laura Goodfield 2/16/2010 2010 Spring Integrative Biosciences Colloquium [http://untitledname.com/2006/07/kermit-2]00 1 1

2. Introduction & Disease transmission models Bongsoo Park 2

3. Dr. Collin’s research focus is host-pathogen biology and its relationship to the global decline of amphibians James P. Collins B.S. from Manhattan College in 1969 Ph.D. from The University of Michigan in 1975 Professor in Ecology, Evolution, & Environmental Science 3 [http://www.collinslab.asu.edu/] 3

4. Host-Pathogen Interaction Host Pathogen Amphibians (Ex. Frogs, Salamanders) Fungus, Bacteria, Virus (Ex. Batrachochytrium dendrobatidis) [http:// static.howstuffworks.com/gif/frog-1.jpg] [http://en.wikipedia.org/wiki/File:Batrachochytrium_dendrobatidis.jpg] 4

5. Infected Frog by Chytrid fungus The fungus infects the skin of frogs destroying its structure and function. [http://www.dpiw.tas.gov.au/inter.nsf/WebPages/LJEM-673V89?open] 5

6. Emerging infectious diseases may reduce biodiversity and may account for at least some species extinctions The question of whether pathogens can cause host extinction is a key issue in epidemiological theory 6

7. The question of whether pathogens can cause host extinction is a key issue in epidemiological theory Extinction is impossible via an infectious pathogen if two assumptions are met (Kermack and McKendrick 1927; Anderson and May 1979) 7

8. Extinction is impossible via an infectious pathogen if two assumptions are met Disease transmission is density dependent (McCallum et al. 2001; Begon et al. 2002) Host contact is homogeneous (O’Keefe 2005) 8

9. Disease transmission models [McCallum, H. 2001] 9

10. Disease transmission is density dependent Population (N) Susceptible : Unresistant to some stimulus, influence Infected : Contaminated with a disease-producing agents (Merriam-webster.com) [McCallum, H. 2001] 10

11. Disease transmission is density dependent Population (N) Transmission rate = βSI (β: Transmission coefficient) [McCallum, H. 2001] 11

12. Disease transmission is density dependent Assumption : Infected and susceptible hosts mix completely with each other and move randomly within an arena of fixed size [McCallum, H. 2001] 12

13. Density dependent disease transmission is ‘Mass Action’ High School Chemistry : Water(H20) [McCallum, H. 2001] 13

14. Disease transmission is frequency dependent Population (N) Transmission rate = βSI / N (β: Transmission coefficient) [de Jong et al, 1995] 14

15. The summary of basic Disease transmission models βIS (‘mass action’) Transmission in which the number of new infections per unit time is proportional to the product of the density of infected hosts I and the density of susceptible hosts S. β IS/N (‘Pseudo mass action’) Frequency-dependent transmission is proportional to the product of the density of infected hosts(I) and the proportion(or frequency) of hosts that are susceptible. [McCallum, H. 2001] 15

16. Extinction is impossible via an infectious pathogen if two assumptions are met Disease transmission is density dependent (McCallum, Barlow&Home2001; Begon et al. 2002) Host contact is homogeneous (O’Keefe 2005) 16

17. Host contact is homogenous? Pathogen Host Host Host 17

18. Actually, host contact is not homogenous Host Pathogen Host Host 18

19. Actually, host contact is not homogenous Host 2 Host 1 Host Host Host Host Host Host Host Host Host Host Host Host Host Host Host Host Host 19

20. Actually, host contact is not homogenous “For example, we may expect that a cold will spread faster through a dense neighborhood than a rural one because more handshakes and other casual contact occur in the dense neighborhood.” State college 40,000 Philadelphia 5,000,000 [ O’Keefe, K.J. 2005 ] 20

21. Extinction is impossible via an infectious pathogen if two assumptions are met When two assumptions are not met, extinction would be possible via an infectious pathogens 21

22. When two assumptions are not met, extinction would be possible via an infectious pathogens Host extinction can be accommodated within the framework of the basic theory by relaxing the two assumptions (de Castro and Bolker 2005) 22

23. Pathogen-Associated Extinction by Chytridiomycosis David Place (Wake and Vredenburg 2008) 23

24. Mass Die-Offs Resulting from Batrachochytrium dendrobatidis Infection (Lips et al. 2005) 24

25. Rapid mortality begins in October 2004 at El Copé (Lips et al. 2005) 25

26. Rapid Die-Offs Coincide With Detection of B. dendrobatidis (Lips et al. 2005) 26

27. Batrachochytrium dendrobatidis is the Causative Agent of Chytridiomycosis Free-Living Stage (Rosenblum et al. 2008) 27

28. Bd Grows Strictly in the Keratinized Tissues of Tadpoles (Mouth) and Skin of Adults Figure 1 “Thickness of normal stratum corneum is 2–5 μm, but here it is about 60 μm. “ D= Discharge Tubes S= Sporangia Figure 2 Death hypothesized to be due to impaired respiration, osmoregulation, or uptake of fungal toxins. (Berger et al. 1998) 28

29. Under the Proper Conditions, Bd Can Lead to Host Extinction (Kate M. Mitchell. 2008) 29

30. Five Year Study at Monteverde Cloud Forest Preserve in Costa Rica 20 Species Driven to Extinction Bufo periglenes – Golden Toad Atelopus varius - Harlequin Frog (http://rana.biologia.ucr.ac.cr/ingles/gallery.html) (http://rana.biologia.ucr.ac.cr/ingles/gallery.html) (Wake and Vredenburg. 2008) 30

31. Bd is successful in many climates but does not necessarily drive all populations to extinction Bd Infects over 400 species of amphibians and is currently widespread (Fisher et al. 2009) 31

32. Bd Is More Lethal at Lower Temperatures 16 frogs exposed to B. dendrobatidis At 17°C and 23°C, all died 4 of 8 exposed frogs at 27°C died (Berger et al. 2004) 32

33. Human associated pathogen transmission Oscar Bedoya Reina 33

34. Emerging infection diseases (EIDs) of free living animals can be classified into three major groups [http:// cache.gawker.com] Spilled over from domestic animals to wildlife population [http:// www.africanwilddoglearningzone.com] Related to host or parasite translocation Adapted from [http://www.canids.org] Emerged without overt human involvement [Daszak et al. 2000] 34

35. Emerging infection diseases (EIDs) of free living animals can be classified into three major groups Spilled over from domestic animals to wildlife population [http://www.hillmanwonders.com] [Ginsberg et al. 1995] [http:// www.africanwilddoglearningzone.com] 35 35

36. Emerging infection diseases (EIDs) of free living animals can be classified into three major groups Related to host or parasite translocation [http://www.dpi.qld.gov.au] [http://www.ecoalimenta.com] Adapted from [http://www.canids.org] 36

37. Disease induced host extinction is impossible via infectious diseases Disease transmission is density dependant and host contact is homogenous Host extinction is unexpected because pathogen transmission is inefficient 37

38. Fragmentation of habitat could change density across landscapes affecting host contact Habitat fragmentation as a result of biotic or abiotic factors controls pathogen transmission 38

39. In amphibian fragmentation could increase the effective disease transmission If biotic and abiotic factors result in differences in host density between ponds, contact rates and pathogen transmission could be different 39

40. In amphibian fragmentation could increase the effective disease transmission If biotic and abiotic factors result in differences in host density between ponds, contact rates and pathogen transmission could be different 40

41. What can be said about fragmentation in amphibian habitats? Fragmentation increase the contact between individuals Abiotic and biotic factors fragment the ponds 41

42. Could fragmentation drive to extinction? Arizona tiger salamander: 1) Populations live in ponds. 2) The species has an obligate pathogen. 3) Populations are endangered. 42

43. Could fragmentation drive to extinction? Arizona tiger salamander: 1) Populations live in ponds. 2) The species has an obligate pathogen. 3) Populations are endangered. [http://media.photobucket.com] sparse [http://blog.thepondguy.com] Pounds can be fragmented dense 43

44. Could fragmentation drive to extinction? Arizona tiger salamander: 1) Populations live in ponds. 2) The species has an obligate pathogen. 3) Populations are endangered. Reintroduced to the ponds by infected adults ATV ATV infection is stochastic 44

45. Could fragmentation drive to extinction? Arizona tiger salamander: 1) Populations live in ponds. 2) The species has an obligate pathogen. 3) Populations are endangered. Modify natural ponds Human action Create artificial ponds 45 45

46. Could fragmentation drive to extinction? Arizona tiger salamander: 1) Populations live in ponds. 2) The species has an obligate pathogen. 3) Populations are endangered. Abiotic factors [http://www.uwyo.edu/] Species habits 46

47. Fragmented habitats are more likely to have higher incidence of ATV infections Studied 4 ponds in Arizona, taking the following variables: ATV presence Palmer drought severity index Amount of emerging vegetation Alteration for management Presence of cannibals 47

48. Fragmented habitats are more likely to have higher incidence of ATV infections Studied 4 ponds in Arizona, taking the following variables: ATV presence Palmer drought severity index Amount of emerging vegetation Alteration for management Presence of cannibals [http://www. wildanimalsonline.com/] Adapted from [http://www. wildanimalsonline.com/] NEGATIVE POSITIVE 48 48

49. Fragmented habitats are more likely to have higher incidence of ATV infections Studied 4 ponds in Arizona, taking the following variables: ATV presence Palmer drought severity index Amount of emerging vegetation Alteration for management Presence of cannibals -4 +4 49

50. Fragmented habitats are more likely to have higher incidence of ATV infections Studied 4 ponds in Arizona, taking the following variables: ATV presence Palmer drought severity index Amount of emerging vegetation Alteration for management Presence of cannibals 50 0% 100%

51. Fragmented habitats are more likely to have higher incidence of ATV infections Studied 4 ponds in Arizona, taking the following variables: ATV presence Palmer drought severity index Amount of emerging vegetation Alteration for management Presence of cannibals 0 1 51 51

52. Fragmented habitats are more likely to have higher incidence of ATV infections Studied 4 ponds in Arizona, taking the following variables: ATV presence Palmer drought severity index Amount of emerging vegetation Alteration for management Presence of cannibals [Adapted from Michimae, H. and Wakahara 2001] 1 HWL/LHW>0.9 0 HWL/LHW<0.86 [http://www.uwyo.edu/] [http://www. wildanimalsonline.com/] 52

53. What can be said about fragmentation in amphibian habitats? [Adapted from Greers and Collins 2008] Drought and management are positively correlated with an increase of ATV, and the amount of emergent vegetation is negatively correlated 53

54. What can be said about fragmentation in amphibian habitats? [Adapted from Greers and Collins 2008] Drought years presented a significant higher incidence of ATV 54

55. What can be said about fragmentation in amphibian habitats? [Adapted from Greers and Collins 2008] Modified sinkholes presented a significant higher incidence of ATV 55

56. What can be said about fragmentation in amphibian habitats? [Adapted from Greers and Collins 2008] The percentage of ATV decreased as vegetation score increase 56

57. ATV occurrence is modeled by the main effect of two variables [Adapted from Greers and Collins 2008] The amount of emergent vegetation and management alteration fit the data well 57

58. Tiger salamander showed different distribution patterns Significantly more animals were captured <2m from the pond’s edge, and is more frequent in ponds with sparse vegetation 58

59. Ponds with sparse vegetation and altered management for livestock have higher incidence of ATV Lower emergent vegetation causes an halo effect, and high densities Ponds with modified management are deeper and steeper 59

60. Ponds with sparse vegetation and altered management for livestock have higher incidence of ATV Stock tanks and other modified habitat could increase connectivity of populations Vegetation can act as paths by which adult move around the pond 60

61. Conclusions Contrarily to the original hypothesis: “Complex habitats would create microhabitats that separated larvae into patches”, they found that ponds with sparse vegetation is fragmented 61

62. Conclusions The intensity of ponds alteration for livestock and the amount of vegetation are positively related to the ATV incidence 62

63. The Big Picture: Implications of Extinction {Clip Art from Microsoft 2007} Laura Goodfield 63

64. The relationships between species in an ecosystem are varied but usually tie species together in a unique and complex manner. (Lavigne. 2007) 64

65. Keystone species can be defined as species that contribute more proportionally to their ecosystem than they take up biomass. [Dovel 2008] 65

66. Endangered Species have been determined by the IUCN and added to the Red List. [Table adapted from IUCN, 2009] 66

67. When it comes to abiotic causes, extinction is normal! 50% of all species 83% of all species 48% of all species 50% of all species 57% of all species (The Discovery Channel, 2010) 67

68. “Biodiversity is defined as the totality of different organisms, the genes they contain, and the ecosystems they form.” E.O. Wilson, 1986 [Myers 2000] 68

69. High levels of endangered and extinct species inversely correlate to biodiversity levels. [IUCN 2008] 69

71. Consequences of Change in Biodiversity will directly affect us and the world around us. (F.S. Chapin III et al, 2000) 71

72. Summary Disease transmission models suggest that extinction could be possible if host contact is not homogenous or disease transmission is not dependant on density. The newly emergent pathogen Bd is appears to be able to cause extinction in wild populations of amphibians. ATV infection was positively related with anthropic modifications and with habitat fragmentation. Although extinction is natural, the loss of biodiversity can result in series of changes, most of which affect us negatively.

73. What will happen if amphibians become extinct?

74. References Berger et al. (1998). Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proc NatlAcad Sci. 95(15): 9031–9036. Berger L., Speare R., Hines H., Marantelli G., Hyatt A.D., et al. (2004). Effect of season and temperature on mortality in amphibians due to chytridiomycosis. Aust. Vet. J. 82:31–36 Chapin F.S. III et al (2000) Consequences of changing biodiversity . Nature 405, 234-242. de Castro F. and Bolker B. (2005) Mechanisms of disease-induced extinction. Ecology Letters, 8, 117–126. de Jong, M.C.M. et al. (1995) How does transmission of infection depend on population size? In Epidemic Models: Their Structure and Relation to Data (Mollison, D., ed.), pp. 84–94, Cambridge University Press. Dovel G. (2008) The Truth about Our Wildlife Managers’ Plan to Restore “Native” Ecosystems. The Outdoorsman, 30. Fisher M.C., Garner T.W.J., Walker S.F. (2009). Global Emergence of Batrachochytriumdendrobatidis and Amphibian Chytridiomycosis in Space, Time, and Host. Annu. Rev. Microbiol. 63:291-310. Ginsberg J.R., Mace G.M. and Albon S. (1995). Local Extinction in a Small and Declining Population: Wild Dogs in the Serengeti. Proceedings: Biological Sciences. 262(1364):221-228. Greer A.L., Collins J.P. (2008). Habitat fragmentation as a result of biotic and abiotic factors controls pathogen transmission throughout a host population. Journal of Animal Ecology. 364-369 74

75. References Greer A.R and Collins J.P. (2008) Habitat fragmentation as a result of biotic and abiotic factors controls pathogen transmission throughout a host population. Journal of Animal Ecology, 77, 364-369. IUCN (2008) Broadening the coverage of biodiversity assessments. Accessed at http://cmsdata.iucn.org/downloads/broadening_the_coverage_of_biodiversity_assessments_factsheet_en.pdf IUCN (2009) Accessed at http://iucn.org/about/work/programmes/species/red_list/?4143/Extinction-crisis-continues-apace Lavigne D., Natural Sciences and Engineering Research Council (2007) Cod Food Web Accessed at http://www.visualcomplexity.com/vc/project.cfm?id=47. Lips K.R. et al. (2005). Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. PNAS. 103:9 McCallum, H., Barlow, N. & Hone, J. (2001) How should pathogen transmission be modelled? Trends in Ecology and Evolution, 16, 295–300. Michimae H. and Wakahara M. (2001). Factors Which Affect the Occurrence of Cannibalism and the Broad-Headed "Cannibal" Morph in Larvae of the Salamander Hynobiusretardatus. Behavioral Ecology and Sociobiology 50(4):339-345. Mitchell K.M. (2008). Persistence of the emerging pathogen Batrachochytriumdendrobatidis outside the amphibian host greatly increases the probability of host extinction. Proc. R. Soc. B. 275, 329–334 . 75

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