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Do Emerging Infectious Diseases Have a Role in the Decline and Extinction of Species?

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Do Emerging Infectious Diseases Have a Role in the Decline and Extinction of Species? The Role of Infectious Disease in Amphibian Population Decline and Extinction James P. Collins School of Life Sciences Arizona State University University of Tennessee Department of Forestry, Wildlife and Fisheries Center for Wildlife Health Knoxville, Tennessee 22 April 2010 OUTLINE Introduction: A grand challenge problem A model system: What is the evidence for ranaviruses as a cause of amphibian decline and extinction? A model system: What is the evidence for the amphibian chytrid fungus as a cause of amphibian decline and extinction? Conclusions Introduction: Two grand challenges for 21st century environmental biology 1. Global loss of biodiversity 2. Emerging infectious diseases Do emerging infectious diseases have a role in the decline and extinction of species? 1 A theoretical problem When is emerging infectious disease a force in extinction? Conventional theory suggests that a pathogen is unable to drive a host population to extinc tion (Kermack & McKendrick 1927, Anderson & May 1979) Assumptions: density dependent transmission homogeneous mixing no alternate hosts no environmental reservoirs Proportion of DENSITY susceptible hosts that DEPENDENT become infected TRANSMISSION Density (# infected / volume) StiblSusceptible TiiTransmission IfInfec tdted Proportion of DENSITY susceptible hosts that INDEPENDENT become infected TRANSMISSION Prevalence (# infected / total # of hosts) Empirical claims Proposed declines due to EIDs Chestnut blight Dutch elm disease Sudden oak death White nose syndrome in bats Coral bleaching disease 2 Empirical claims Proposed major extinctions due to EIDs • Hawaiian birds (Reynolds et al. 2003) • Amphibians (Stuart et al. 2004) • Pleistocene large mammals (MacPhee & Marx 1997) Proposed single species extinctions due to EIDs • Polynesian snail (Daszak and Cunningham 1999) • Sharp-snouted day frog (Schloegel et al. 2006) • Endemic Christmas Island rat (Wyatt et al. 2008) Causes of amphibian declines • Commercial use • Introduced species • Land use change • CtContam inan ts • Climate change • Infectious disease Amphibian diseases: Macroparasites • Johnson et al. flatworm parasites and deformities • Trematode-agriculture runoff hypothesis (Kiesecker et al. 2002; Johnson et al. 2007; Rohr et al. 2008) Alaria: a trematode parasite of amphibians Pacific tree frog Scan by Sessions & Ballengee 3 Amphibian diseases: Microparasites Bacteria Protozoa – Saprolegnia ferax Chytrid – a fungal pathogen of frogs and salamanders - Batrachochytrium dendrobatidis (Bd) Ranavirus – a genus of viruses infecting cold blooded vertebrates A model system: Ranavirus Do the transmission dynamics of Ambystoma tigrinum virus (ATV) place ATV-infected amphibian populations at risk for pathogen-induced extinction? Amphibian diseases: Viruses Viral groups that infect amphibians: 1. Adenoviruses 2. Caliciviruses 3. Flaviviruses 4. Parvoviruses 5. RiRetroviruses 6. Togaviruses 7. Herpesviruses Pathogenic 8. Iridoviruses Herpesviruses - cause rare renal tumors in frogs; not implicated in decline or extinction Iridoviruses - common and involved in epidemics 4 Amphibian diseases: Iridoviruses Genera of Iridoviridae: 1. Iridovirus infects invertebrates, mainly insects 2. Chloriridovirus infects mosquitoes 3. Lymphocystivirus infects fish 4. Ranavirus infects salamanders, frogs, fish, and reptiles Amphibian diseases: Iridoviruses Eight Ranavirus strains are reported from amphibians and may infect multiple species or only one: • Bohle iridovirus infects amphibians, fish, and reptiles. • Frog virus 3 is reported from almost a dozen frog species and one salamander species. • Ambystoma tigrinum virus is reported only from salamanders. Frog Ranavirus relationships 100 FV3 100 SSTIV Turtle 100 TFV Frog ATV Salamander 100 99 EHNV Fish GIV 94 100 SGIV LCDV-1 100 LCDV-C Fish ISKNV 100 OSGIV 100 RBIV CIV Insect 100 MIV 0.1 (Jancovich et al. 2003. Virology) 5 Ranavirus host range and origin ? Ranavirus genomic DNA analysis Suggests that the most recent common ancestor of Ranavirus was a fish virus followed by a jump from fish to salamanders or frogs Human involvement in Ranavirus host shifts? Movement of hosts/disease by humans? Movement of tiger salamanders as bait (Source: Picco and Collins. 2008. Conservation Biology) 6 Amphibian commerce as a source of pathogen pollution Wild populations Wild populations, lakes virus? (Source: Picco and Collins. 2008. Conservation Biology) ATV and population dynamics Host: Ambystoma tigrinum nebulosum Pathogen: Ambystoma tigrinum virus (ATV) Study area Kaibab Plateau 7 Salamander life history (Brunner et al. 2004) 8 Virus transmission ATV is transmitted by direct physical contact (bumping, biting, and cannibalism) as well as by necrophagy and indirectly via water and fomites. Larval salamanders become infectious soon after exposure to ATV and their propensity to infect others increases with time. (Source: Brunner, Schock, Collins. 2007. Transmission dynamics of the amphibian ranavirus, Ambystoma tigrinum virus. Diseases of Aquatic Organisms) Testing density dependent transmission. The experiment varied number of susceptible hosts and number of infected hosts within a 55 L aquarium. (Amy Greer) Susceptible Infected Volume (L) Density Prevalence Replicates hosts hosts (I/V) (I/N) 115510.57 885580.54 40 40 55 40 0.5 4 1 8 5580.897 8085580.094 115510.53 40 40 55 40 0.5 3 Experimental design: 1059 larvae Infected Sham infected Susceptible hosts (I) hosts (Ic) hosts (S) 5 days Volume = 55L aquarium Housed Exposure time = 24 hours Housed individually for 28 individually for 28 days Laboratory days diagnostic testing 9 Experimental design: 1059 larvae Results • 504 susceptible salamanders exposed in treatment replicates • 468 developed signs of infection and died • 36 uninfected after 28 days (no sub-lethal infections) Proportion of susceptible larvae infected at each density. Vertical bars equal 1 SE. 1 0.8 infected 0.6 ceptible hosts e 0.4 0.2 that becam Proportion of sus 0 0 10 20 30 40 Density of infected hosts (# I / 55L) 10 Estimating the transmission constant (β) for a range of transmission functions Type of Function β Additional Neg. AICc ΔAIC Akaike transmission (units) parameters log- value weight (units) likely- hood Power βSIq 1.38 q = 0.255 20.20 44.9 0.00 0.588 (H-q (dimension- day-1) less) Negative k ln 7.72 k = 0.578 20.66 45.9 0.92 0.371 binomial (1+βI/k)S (H-1 (day-1) day-1) Constant risk, asymptotic, density dependent, and frequency dependent functions were evaluated but none was significant. What explains the high transmission rate? • Transmission 1 via water? 0.9 –Asymptomatic 0.8 animals shed high 0.7 numbers of viral 0.6 le hosts infected particles per daday b 0.5 • Non-random 0.4 contact? 0.3 –Behavioral changes 0.2 at low densities Proportion of suscepti 0.1 cause clumping of 0 hosts (Brunkow and 0 5 10 15 20 25 30 35 40 45 Collins 1998) Density of infected hosts (# I / 55L) What about transmission in the field? 11 Field surveys • Mark-recapture • Tissue samples for ATV screening • Environmental data Results 100 p<0.001 80 p=0.05 Percentage of 60 p>0.05 ATV positive 40 ponds 20 0 <25% 25% - >75% 75% Percent emergent vegetation How does habitat affect transmission? Hypothesis: Habitat fragmentation buffers disease transmission by decreasing larval contact rates Prediction: e Contact rat Contact Amount of vegetation 12 Experimental design Sparse Dense vegetation vegetation • Mark-recapture by site of origin • Tissue sample Larval distribution in a pond varies with amount of emergent vegetation 14% 4% 13% 5% 6% 12% 7% 11% 8% 9% 10% Sparse Dense Results • Fragmentation • “Halo effect” A lower incidence of ATV in heavily vegetated ponds is caused by lower effective density rather than buffered transmission 13 Host – pathogen theory A pathogen is unable to drive a host population to extinction (Kermack & McKendrick 1927, Anderson & May 1979) Assumptions Density dependent transmission Yes Yes Homogeneous mixing No Yes No alternative hosts N/A Yes No environmental reservoirs No Yes Empirical tests of the theory Do the transmission dynamics of Ambystoma tigrinum virus (ATV) place ATV-infected amphibian populations at risk for pathogen- induced extinction? Best evidence suggests the answer is “No:” Amy Greer et al. (2008) Jesse Brunner et al. (2007) 14 Model system: Amphibian chytrid Do the transmission dynamics of Batrachochytrium debdrobatidis (Bd) place Bd- infected amphibian populations at risk for pathogen-induced extinction? The amphibian chytrid • By the mid-1990s it was suspected that the chytrid fungus Batrachochytrium dendrobatidis might be an emerging infectious amphibian disease (EID). • EIDs are diseases that are newly recognized, newly appeared in a population, or rapidly increasing in incidence, virulence, or geographic range. Amphibian chytrid life cycle (Source: Rosenblum et al. 2010. PLoS Pathogens) 15 Chytrid - amphibian system •Chytrid is associated with anuran declines and extinctions in Australia, Europe, Africa, Central, South, and North America, but also coexists with non- declining species. •It infects most amphibian species tested with effects varying from no clinical disease to 100% mortality. •Microenvironment affects (K. Lips) susceptibility to chytrid. p = 1 (habitat can support chytrid) p = 0 (habitat cannot support chytrid) The model was also extended using Eastern Hemisphere data. (Source: Santiago Ron. 2005) Distribution of threatened amphibians in Central America, Northern South America, and the Caribbean (Source: Global Amphibian Assessment 2004) 16 Hypothesis:
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