10/2/2018
Endemic and Other Mycoses : Genetics, Evolutionary Biology, Environment John Taylor UC Berkeley [email protected]
Endemic and Other Mycoses : Genetics, Evolutionary Biology, Environment John Taylor, Rachel Adams, Cheng Gao, Bridget Barker UC Berkeley, Northern Arizona University, TGen
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Where are the agents of endemic mycoses?
Basidiomycota - Cryptococcus
Ascomycota – Taphrinomycotina - Pneumocystis
Ascomycota – Saccharomycotina - Candida
Ascomycota – Pezizomycota – Eurotiomycetes Eurotiales - Aspergillus
Ascomycota – Pezizomycota – Eurotiomycetes Onygenales – Endemic Mycoses
Where are the agents of endemic mycoses?
Basidiomycota - Cryptococcus
Ascomycota – Taphrinomycotina - Pneumocystis
Ascomycota – Saccharomycotina - Candida
Ascomycota – Pezizomycota – Eurotiomycetes Eurotiales - Aspergillus
Ascomycota – Pezizomycota – Eurotiomycetes Onygenales – Endemic Mycoses
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Muñoz et al. 2018. Scientific Reports Coccidioides DOI:10.1038/s41598-018-22816-6 Histoplasma Onygenales Blastomyces Paracoccidioides
Coccidioides
Aspergillus
Muñoz et al. 2018. Scientific Reports Coccidioides DOI:10.1038/s41598-018-22816-6 Histoplasma Onygenales Blastomyces Paracoccidioides
Coccidioides
Aspergillus
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Muñoz et al. 2018. Scientific Reports Coccidioides DOI:10.1038/s41598-018-22816-6 Histoplasma Onygenales Blastomyces Paracoccidioides
Coccidioides
Aspergillus
What is coccidioidomycosis?
Healthy Infected
www.emedicine.com
4 10/2/2018
What is coccidioidomycosis and why should we care?
Distribution of Coccidioides species
Hector and Laniado-Laborin 2005. PLoSMedicine
What is coccidioidomycosis and why should we care?
California
Arizona
https://www.cdc.gov/fungal/diseases/coccidioidomycosis/statistics.html
5 10/2/2018
What is coccidioidomycosis and why should we care? Cooksey et al. 2017 MMWR August 11, 2017 / 66(31);833–834 2016
California
What is coccidioidomycosis and why should we care? https://www.cdph.ca.gov/Programs/CID/DCDC/CDPH%20Document%20Library/CocciEpiSummary2017.pdf
2017
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Move from the patient to the environment.
Move from the patient to the environment. Diagnostics. How dangerous is this job? Do I need a respirator?
8 10/2/2018
Move from the patient to the environment. Diagnostics. How dangerous is this job? Do I need a respirator? Pharmaceuticals. Is this area so dangerous that I need to take antifungals prophylactically?
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Today’s Question:
What is the role, if any, of native mammals in the life cycle of Coccidioides?
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Background
Small mammals
1942
Chester W. Emmons
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Granuloma in mouse lung 1942
Ashburn and Emmons 1942. Archives of Pathology 34:791-800.
1942 Emmons and Ashburn, 1942
Pocket Mouse 13% 17%
Kangaroo Rat
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1943
C. W. EMMONS
. . . it may be primarily a disease of rodents . . . certain species of rodents constitute a natural reservoir of coccidioidomycosis and by their geographical distribution determine the areas of endemicity of the disease. /
/
/
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Coccidioides immitis in the soil of the southern San Joaquin Valley. Roger O. Egeberg and Ann Frank Ely 1956 American Journal of the Medical Sciences, February 1956, 151-4
Coccidioides immitis in the soil of the southern San Joaquin Valley. Roger O. Egeberg and Ann Frank Ely 1956 American Journal of the Medical Sciences, February 1956, 151-4
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Growth patterns of Coccidioides immitis in the soil of an endemic area. Ann Frank Elconin, Roger O. Egeberg and Robert Lubarsky 1957 In: Ajello, L. et al. 1957. Proc. Symp. Coccidioidomycosis. Public Health Service Publication 575.
Total 428 31 7.4%
Growth patterns of Coccidioides immitis in the soil of an endemic area. Ann Frank Elconin, Roger O. Egeberg and Robert Lubarsky 1957 In: Ajello, L. et al. 1957. Proc. Symp. Coccidioidomycosis. Public Health Service Publication 575.
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Growth patterns of Coccidioides immitis in the soil of an endemic area. Ann Frank Elconin, Roger O. Egeberg and Robert Lubarsky 1957 In: Ajello, L. et al. 1957. Proc. Symp. Coccidioidomycosis. Public Health Service Publication 575.
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Ecological studies of Coccidioides immitis. Orda A. Plunkett and F. E. Swatek 1957 In: Ajello, L. et al. 1957. Proc. Symp. Coccidioidomycosis. Public Health Service Publication 575.
May 1954, coccidioidomycosis found in 5 UCLA anthropology students excavating an Native American midden.
Ecological studies of Coccidioides immitis. Orda A. Plunkett and F. E. Swatek 1957 In: Ajello, L. et al. 1957. Proc. Symp. Coccidioidomycosis. Public Health Service Publication 575.
May 1954, coccidioidomycosis found in 5 UCLA anthropology students excavating an Native American midden. Soil Samples from the midden were positive.
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Ecological studies of Coccidioides immitis. Orda A. Plunkett and F. E. Swatek 1957 In: Ajello, L. et al. 1957. Proc. Symp. Coccidioidomycosis. Public Health Service Publication 575.
May 1954, coccidioidomycosis found in 5 UCLA anthropology students excavating an Native American midden. Soil Samples from the midden were positive. 80 burrow samples taken near the midden – all negative.
Ecological studies of Coccidioides immitis. Orda A. Plunkett and F. E. Swatek 1957 In: Ajello, L. et al. 1957. Proc. Symp. Coccidioidomycosis. Public Health Service Publication 575.
May 1954, coccidioidomycosis found in 5 UCLA anthropology students excavating an Native American midden. Soil Samples from the midden were positive. 80 burrow samples taken near the midden – all negative. 440 pocket mice and kangaroo rats captured near the midden -- all negative.
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1957-2018
Studies of physical parameters.
Climate: temperature, water and wind
Soil
Climate: California 2000
Morbidity caused by C. immitis was best explained by the interaction between two variables, the lengths of droughts and the amounts of rainfall preceding epidemics.
Fisher MC et al. 2000 J. Clin Microbiol 38:807-813
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Climate: California Relative change 2000 in cocci morbidity Morbidity caused by C. immitis was best explained by the interaction between two variables, the lengths of droughts and the amounts of rainfall preceding epidemics.
Fisher MC et al. 2000 J. Clin Microbiol 38:807-813
Climate: California Relative change 2000 in cocci morbidity Morbidity caused by Model based on length of drought and mean annual C. immitis was best rainfall in the preceding year explained by the interaction between two variables, the lengths of droughts and the amounts of rainfall preceding epidemics.
Fisher MC et al. 2000 J. Clin Microbiol 38:807-813
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Climate: California & Arizona 2017
GeoHealth 1, 51–63 (2017)
The results indicate that in both states, coccidioidomycosis incidence is related to soil moisture levels from previous summers and falls.
Climate Coccidioides Soil
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Climate Coccidioides Soil
Climate Coccidioides Soil
Cocci has to eat.
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Background
Fungal Nutrition
de.wikipedia.org
http://www.botanicalgarden.ubc.ca/potd/2007/07/xylaria_hypoxylon_tentative.php
crampball.html
/fungi/
siegelr
/~
web.stanford.edu http://
Ascomycota, Pezizomycotina
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2009 Evolution of Gene Family Size
Eurotiales
Onygenales
Sordariomycetes
Sharpton, Stajich et al. 2009. Genome Research
Gene Family Reductions: 2009 Genes coding enzymes that digest plants
https://www.123rf.com/photo_27279678_dried-out-dead-plants-lying-in-a-dry-arid-desert-environment.html Sharpton, Stajich et al. 2009. Genome Research
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Keratin, hair, skin & connective tissue
Rock Pocket Mouse
http://www.snipview.com/q/Rock%20pocket%20mouse
www.privemillenia.com
Gene Family Reductions: 2009 Genes coding enzymes that digest animals
Perognathus longimembris
Sharpton, Stajich et al. 2009. Genome Research
Jonah Evans, Texas. Parks and Wildlife Department, http://www.inaturalist.org/photos/407437
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de.wikipedia.org
http://www.botanicalgarden.ubc.ca/potd/2007/07/xylaria_hypoxylon_tentative.php
crampball.html
/fungi/
siegelr
/~
web.stanford.edu http://
Ascomycota, Pezizomycotina
Ecology Many fungi are endophytes, they live in their plant hosts without causing apparent disease. When the leaf, stem or plant dies, the fungus becomes active, consumes the dead plant and reproduces.
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de.wikipedia.org
http://www.botanicalgarden.ubc.ca/potd/2007/07/xylaria_hypoxylon_tentative.php
crampball.html
/fungi/
siegelr
/~
web.stanford.edu http://
Ascomycota, Pezizomycotina
Ecology Many fungi are endophytes, they live in their plant hosts without causing apparent disease. When the leaf, stem or plant dies, the fungus becomes active, consumes the dead plant and reproduces.
Hypothesis, Coccidioides spp. are Endozoans, they live in their natural animal hosts without causing apparent disease. When the animal dies, the fungus becomes active, consumes the dead animal and reproduces.
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Climate Coccidioides Soil
Cocci has to eat.
Climate Coccidioides Soil
Animal
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Climate Coccidioides Soil
Animal
Climate Coccidioides Soil Animals have to eat.
Animal
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Climate Coccidioides Soil
Plant Animal
Climate Coccidioides Soil
Plant Animal
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Climate Coccidioides Soil
Plant Animal
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Avenal
Maricopa
California State Hwy 33
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California State Hwy 33
The CocciDx assay* Coccidioides-Specific PCR Assay Targeting a Transposable Element
*CocciENV Assay. Bowers et al. 2018 Med Mycol doi: 10.1093/mmy/myy007
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Avenal
Coccidioides detected in burrows at all sites
Maricopa
Avenal
Coccidioides detected at surface at two sites
Maricopa
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Avenal Sites where road workers have contracted coccidioidomycosis.
Maricopa
Avenal Sites where road workers have contracted coccidioidomycosis.
Maricopa
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Arthroconidia
Life cycle Living Dead Mammal Mammal
Taylor and Barker 2018 Med Mycol
Long distance dispersal in air
Short distance Arthroconidia dispersal in soil Life cycle Living Dead Mammal Mammal
Taylor and Barker 2018 Med Mycol
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Long distance dispersal in air
Short distance dispersal in soil Mammal inhales arthroconidia Life cycle Living Dead Mammal Mammal
Taylor and Barker 2018 Med Mycol
Long distance dispersal in air
Short distance dispersal in soil Mammal inhales arthroconidia Life cycle Living Dead Mammal Mammal
Spherules develop
Taylor and Barker 2018 Med Mycol
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Long distance dispersal in air
Short distance dispersal in soil Mammal inhales arthroconidia Life cycle Living Dead Mammal Mammal Dissemination via SpherulesSpherule fungal endospores. develops develop Short host life
Taylor and Barker 2018 Med Mycol
Long distance dispersal in air
Short distance dispersal in soil Mammal inhales arthroconidia Life cycle Living Dead Mammal Mammal Dissemination via SpherulesSpherule fungal endospores. develops develop Short host life
Containment in host granuloma. Long host life.
Taylor and Barker 2018 Med Mycol
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Long distance dispersal in air
Short distance dispersal in soil Mammal inhales arthroconidia Life cycle Living Dead Mammal Mammal Dissemination via SpherulesSpherule fungal endospores. develops develop Short host life
Containment in host granuloma. Long host life.
Taylor and Barker 2018 Med Mycol
Long distance dispersal in air
Short distance Arthroconidia dispersal in Hyphae grow in dead soil Mammal inhales host and produce arthroconidia arthroconidia Life cycle Living Dead Mammal Mammal Dissemination via SpherulesSpherule fungal endospores. develops develop Short host life
Containment in host granuloma. Long host life.
Taylor and Barker 2018 Med Mycol
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Long distance dispersal in air
Short distance Arthroconidia dispersal in Hyphae grow in dead soil Mammal inhales host and produce arthroconidia arthroconidia Life cycle Living Dead Mammal Mammal Dissemination via SpherulesSpherule fungal endospores. develops develop Short host life
Containment in host granuloma. Long host life. Taylor and Barker 2018 Med Mycol
Taylor and Barker 2018 Med Mycol
Today’s Question:
What is the role, if any, of native mammals in the life cycle of Coccidioides?
42 10/2/2018
Today’s Question:
What is the role, if any, of native mammals in the life cycle of Coccidioides?
What do other data say?
Solar Panel Farms
Carrizo Plain: Drought, Plants and Mammals
Cocci in agriculture
Carrizo Plain National Monument
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MMWR / August 24, 2018 / Vol. 67 / No. 33
MMWR / August 24, 2018 / Vol. 67 / No. 33
Nine confirmed coccidioidomycosis cases were identified among 2,410 solar farm workers in California.
The incidence among workers (1,095 per 100,000 persons/year) was 4.4 to 210.6 times higher than background county rates, providing evidence that illness was work-related.
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MMWR / August 24, 2018 / Vol. 67 / No. 33
Nine confirmed coccidioidomycosis cases were identified among 2,410 solar farm workers in California.
The incidence among workers (1,095 per 100,000 persons/year) was 4.4 to 210.6 times higher than background county rates, providing evidence that illness was work-related.
Long distance dispersal in air
Short distance Arthroconidia dispersal in Hyphae grow in dead soil Mammal inhales host and produce arthroconidia arthroconidia Life cycle Living Dead Mammal Mammal Dissemination via SpherulesSpherule fungal endospores. develops develop Short host life
Containment in host granuloma. Long host life.
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Nature Climate Change 8, pages819–824 (2018)
Nature Climate Change 8:819-824 (2018)
Here [Carrizo Plain], we quantified the responses of 423 sympatric species of plants, arthropods, birds, reptiles and mammals to California’s drought of 2012–2015—the driest period in the past 1,200 years for this global biodiversity hotspot.
Nature Climate Change 8, pages819–824 (2018)
Nature Climate Change 8:819-824 (2018)
Here [Carrizo Plain], we quantified the responses of 423 sympatric species of plants, arthropods, birds, reptiles and mammals to California’s drought of 2012–2015—the driest period in the past 1,200 years for this global biodiversity hotspot.
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Mammals (n=15)
Losers Winners
Plants (n=61)
Prugh et al. 2018 Nature Climate Change Species with changes at p < 0.05
Losers Winners Mammals (n=15)
Plants (n=61)
Prugh et al. 2018 Nature Climate Change Species with changes at p < 0.05
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Plants
Drought Index
Prugh et al. 2018 Nature Climate Change
Plants Rodents
Drought Index Drought Index
Prugh et al. 2018 Nature Climate Change
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Plants Rodents
One rodent, the Giant Kangaroo Rat, Prugh et al. 2018 Nature Climate Change was very abundant (86%) pre-drought
Rain Human Cocci Millimeters of Precipitation
Prugh et al. 2018 Nature Climate Change https://www.cdph.ca.gov/Programs/CID/DCDC/CDPH%20Document%20Library/CocciEpiSummary2017.pdf
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Climate Coccidioides Soil
Plant Animal
Is Coccidioides absent from cultivated land?
Climate Coccidioides Soil
Plant Animal
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Is Coccidioides absent from cultivated land?
Climate Coccidioides Soil
Plant Animal
Is Coccidioides absent from cultivated land?
Climate Coccidioides Soil
Plant Animal
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Is Coccidioides absent from cultivated land? 1965
Arizona Medicine 1965 22: 281-288
Kevin T. Maddy, DVM, MPH
Even in areas highly infective for man, fungus was only isolated in non-cultivated and non-irrigated soils.
Avenal
Coccidioides detected in burrows at all sites
Maricopa
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Native Soils
6 Sites
72 soil samples
8.7M ITS1 reads
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Agricultural Soils
1 site, 6 plots
102 Soil Samples
8.8M ITS1 reads
Phyla of Fungi Chytrids
Zygos Zygos Chytrids Fungi Fungi Basidios
Basidios
Ascos Ascos
Native, 3,600 OTUs Agricultural. 900 OTUs
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Classes of Ascomycota
Ascomycota Ascomycota Saccharomycetes Lecanoromycetes Pezizomycetes Pezizomycetes Leotiomycetes Leotiomycetes Dothideomycetes Sordariomycetes
Eurotiomycetes Eurotiomycetes
Sordariomycetes Dothideomycetes
Native, 1492 OTUs Agricultural 495 OTUs
Orders of Eurotiomycetes
Eurotiomycetes Eurotiomycetes
Chaetothyriales
Onygenales Eurotiales
70 OTUS Eurotiales Onygenales
21 OTUS Chaetothyriales
Native Soils, 244 OTUs Agricultural Soils, 70 OTUs
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Onygenales most common OTUs
OTU Genus % Reads OTU Genus (Taxon) % Reads Chrysosporium 21.2% Gymnoascus 31.7% Gymnoascaceae 19.0% Chrysosporium 19.9% Chrysosporium 17.3% Chrysosporium 9.7% Spiromastix 16.1% Chrysosporium 9.2% Auxarthron 2.5% Spiromastix 6.5% Coccidioides 2.2% Uncinocarpus 5.9% Chrysosporium 2.0% Chrysosporium 4.7% Spiromastix 2.0% Chrysosporium 3.9% Onygenales 2.0% Myceliophthora 3.6% Auxarthron 1.8% Onygenales 2.7% Auxarthron 1.2% Gymnoascoideus 1.0%
Native, 70 OTUs Agricultural, 21 OTUs
Onygenales most common OTUs
OTU Genus % Reads OTU Genus (Taxon) % Reads Chrysosporium 21.2% Gymnoascus 31.7% Gymnoascaceae 19.0% Chrysosporium 19.9% Chrysosporium 17.3% Chrysosporium 9.7% Spiromastix 16.1% Chrysosporium 9.2% Auxarthron 2.5% Spiromastix 6.5% Coccidioides 2.2% Uncinocarpus 5.9% Chrysosporium 2.0% Chrysosporium 4.7% Spiromastix 2.0% Chrysosporium 3.9% Onygenales 2.0% Myceliophthora 3.6% Auxarthron 1.8% Onygenales 2.7% Auxarthron 1.2% Gymnoascoideus 1.0%
Native, 70 OTUs Agricultural, 21 OTUs
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Onygenales most common OTUs
OTU Genus % Reads OTU Genus (Taxon) % Reads Chrysosporium 21.2% Gymnoascus 31.7% Gymnoascaceae 19.0% Chrysosporium 19.9% Chrysosporium 17.3% Chrysosporium 9.7% Spiromastix 16.1% Chrysosporium 9.2% Auxarthron 2.5% Spiromastix 6.5% Coccidioides 2.2% Uncinocarpus 5.9% Chrysosporium 2.0% Chrysosporium 4.7% Spiromastix 2.0% Chrysosporium 3.9% Onygenales 2.0% Myceliophthora 3.6% Auxarthron 1.8% Onygenales 2.7% Auxarthron 1.2% Gymnoascoideus 1.0%
Native, 70 OTUs Agricultural, 21 OTUs
Climate Coccidioides Soil
Plant Animal
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Climate Coccidioides Soil
Plant Animal
Climate Coccidioides Soil
Plant Animal
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• Anita Sil • Rachel Brem • Clarissa Nobile • Peggy Lemaux • Katrina Hoyer • Cheng Gao • Aaron Hernday • Liliam Montoya • Josh Fierer • Devin Coleman-Derr • Jason Stajich • Jeff Dahlberg • Bridget Barker • Vishnu Chaturvedi • Jessie Uehling
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• Anita Sil • Rachel Brem • Clarissa Nobile • Peggy Lemaux • Katrina Hoyer • Cheng Gao • Aaron Hernday • Liliam Montoya • Josh Fierer • Devin Coleman-Derr • Jason Stajich • Jeff Dahlberg • Bridget Barker • Vishnu Chaturvedi • Jessie Uehling
Questions?
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Cocci found in Native American middens
Cocci absent from surrounding soil and rodents ?
63 10/2/2018
A midden is an old dump for domestic waste which may consist of animal bone, human excrement, botanical material, and remnants of food, pottery, tools and other artifacts and ecofacts associated with past human occupation. ?
Our findings of elevated nutrients in middens along the Chesapeake Bay . . . and other studies . . . demonstrate a global, albeit variable, trend of soil enrichment at and around archaeological middens that can subsequently influence the composition and abundance of modern plant communities.Although our limited sample size constrains our ability to contrast middens of different ages, these data suggest that the effects of ancient humans on the plant community can persist for over 3,000 years. ? https://sercblog.si.edu/?p=5008
Cook-Patton, S, Landscape Ecology
64 10/2/2018
OurOur findings findings of elevated of nutrients elevated in middens nutrientsalong the in middens along the Chesapeake Chesapeake Bay . . . and other studies . . . demonstrate a global,Bay albeit . . .variable, and other trend of studiessoil enrichment . . .at demonstrate and around a global, albeit variable, archaeologicaltrend of middens soil enrichmentthat can subsequently at and influence around the archaeological middens that composition and abundance of modern plant communities.Althoughcan subsequentlyour limited influence sample size the constrains composition our and abundance of ability to contrast middens of different ages, these data suggestmodern that the planteffects of communities. ancient humans on the plant community can persist for over 3,000 years. ? https://sercblog.si.edu/?p=5008
Cook-Patton, S, Landscape Ecology
OurOur findings findings of elevated of nutrients elevated in middens nutrientsalong the in middens along the Chesapeake Chesapeake Bay . . . and other studies . . . demonstrate a global,Bay albeit . . .variable, and other trend of studiessoil enrichment . . .at demonstrate and around a global, albeit variable, archaeologicaltrend of middens soil enrichmentthat can subsequently at and influence around the archaeological middens that composition and abundance of modern plant communities.Althoughcan subsequentlyour limited influence sample size the constrains composition our and abundance of ability to contrast middens of different ages, these data suggestmodern that the FUNGALeffects of ancientcommunities. humans on the plant community can persist for over 3,000 years. ? https://sercblog.si.edu/?p=5008
Cook-Patton, S, Landscape Ecology
65 10/2/2018
OurOur findings findings of elevated of nutrients elevated in middens nutrientsalong the in middens along the Chesapeake Chesapeake Bay . . . and other studies . . . demonstrate a global,Bay albeit . . .variable, and other trend of studiessoil enrichment . . .at demonstrate and around a global, albeit variable, archaeologicaltrend of middens soil enrichmentthat can subsequently at and influence around the archaeological middens that composition and abundance of modern plant communities.Althoughcan subsequentlyour limited influence sample size the constrains composition our and abundance of ability to contrast middens of different ages, these data suggestmodern that the FUNGALeffects of ancient communities. humans on the plant community can persist for over 3,000 years. ? https://sercblog.si.edu/?p=5008 Although our limited sample size constrains our ability to contrast middens of different ages, these data suggest that the effects of ancientCook -humansPatton, S, Landscape on the Ecology plant community can persist for over 3,000 years.
Cocci found in Native American middens
Cocci absent from surrounding soil and rodents ?
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Coccidioides Texeira et al. 2016 doi 10.3201/eid2206.151565 Engelthaller et al. 2016 doi 10.1128/mBio.00550- 16 Histoplasma Sepúlveda et al. 2017. doi 10.1128/mBio.01339- 17 Blastomyces Jiang et al. 2018. doi 10.1007/s13225-018-0403-y Paracoccidioides Muñoz et al, 2016. doi 10.1128/mSphere.00213- 16 Emergomyces Schwartz et al. 2018. doi 10.1007/s12281-018- 0308-y
Coccidioides Histoplasma Blastomyces Paracoccidioides Emergomyces
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Response to one year of drought
Winners
Losers Birds
Mammals Arthropods Plants
Prugh et al. 2018 Nature Climate Change
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