Community ecology of disease: Barley Yellow Dwarf viruses in west coast

grasslands

Eric SeabloomElizabeth BorerParviez Hosseini

Dept. of ZoologyOregon State University

Host-pathogen interactions are often studied in isolation

HostPathogen

Vector

However, pathogens act within a community context

Resource

Host

Host

Pathogen

Pathogen

Vector

Vector

Community context of host-pathogen interactions

Resource supply: Abiotic resources can alter host, vector, and community dynamics.

Host Community: Most emerging human and plant diseases are host generalists

Vector Community: Many emerging animal and plant diseases are vector transmitted

Pathogen Community: Most host species are co-infected by multiple pathogens and co-infection can alter transmission and host mortality rates

Community context of host-pathogen interactions: B/CYDV in California

grasslands

1. Host Community: How do changes in the host community affect host-pathogen dynamics?

2. Resource supply: How does nitrogen alter the host community and pathogen prevalence?

System Overview:

Invasion of California Grasslands

• 9.2 million ha of California grasslands invaded by exotic annual grasses for at least 150 years

• Persistence and abundance of annuals generally interpreted as evidence of competitive superiority

• However, recent work shows native perennial grasses are better competitors and can invade stands of exotic annual grasses1

1Seabloom et al. 2003. PNAS,

The conundrum: How did competitively inferior species invade and dominate in this system?

Recent experiments show that exotic annual grasses can increase prevalence of Barley Yellow Dwarf Virus in native grasses1,2

Can disease allow persistence of competitively-inferior exotic annual grasses?1Malmstrom et al. 2005. Oecologia,

2Malmstrom et al. 2005. New Phytologist.

Barley and Cereal Yellow Dwarf Viruses• One of the most economically

important diseases of grasses worldwide

• One of the most prevalent of all viral diseases

• Over 150 hosts including cereal crops, exotic grasses, and native grasses

• RNA luteoviruses that infect sieve tubes of grasses

• Causes stunting, yellowing, increased mortality, and decreased fecundity

• Obligate vectors are aphids

Irwin and Thresh. 1990. Annual Review of Phytopathology. D'Arcy and Burnett 1995.

B/CYDV Strain and Vector Communities

http://www.ento.csiro.au/http://www.biokids.umich.edu/http://www.viarural.com.ar/

Sitobion avenae

I. SGV

I. MAV

I. PAV

II. RPV

II. RMV

Rhopalosiphum padi

Schizaphis graminum

Rhopalosiphum maidis

Community context of host-pathogen interactions: BYDV in California

grasslands

1. Host Community: How do changes in the host community affect host-pathogen dynamics?

2. Resource supply: How does nitrogen alter the host community and pathogen prevalence?

3. Vector and Pathogen Community: How do vector and pathogen interactions affect pathogen prevalence and coexistence?

1. How do changes in the host community affect host pathogen dynamics?

Resource

Host

Host

Pathogen

Pathogen

Vector

Vector

Disease Effects on CompetitionConceptual Model

Discrete Time– Survival between seasons– Reset of system Loss of Disease

Continuous Time– Growing (Winter Rainy) Season – Ongoing infection processes (SI model)– Competition (Lotka-Volterra)

Integro-Difference EquationsParameterized with data from field experiments

The Ugly Math: Between seasons

t

t

IPSPtS dtFFbp 1,

t

t

SStS dtGFP 1,

t

t

IaSAtS dtHHba 1,

01, tIp

t

t

IItI dtGFP 1,

01, tIa

The Ugly Math: Growing season

SpppS

S pVdt

dptF )( spspp

II pVp

dt

dptF )(

SpS

S PVdt

dPtG )( Sp

II PV

dt

dPtG )(

SaaaS

S aVdt

datH )( Sasaa

II aVa

dt

datH )(

IsaPIsapIsaaa PPppaa 1

IspPIspaIsppp PPaapp 1

III PpaV

Dominance mediated by Disease

• Without Disease– Perennials invade

– And replace annuals

Healthy Annuals

Healthy Perennials

Diseased Annuals

Diseased Perennials

• With Disease– Annuals invade

– Dominate system

– High disease prevalence

Borer et al. 2007. PNAS

2. How does nitrogen alter host community and pathogen prevalence?

Resource

Host

Host

Pathogen

Pathogen

Vector

Vector

Host community•Annual dominated•Perennial dominated

Nitrogen addition•Control•4 g N m-2 yr-1

Treatments started in 2000

BYDV prevalence•exotic annual B. hordeaceus monitored from 2002-2003•native perennial E. glaucus monitored from 2002-2005

Experimental manipulation of host community composition and nitrogen

Nitrogen increased annual grass abundance and BYDV prevalence in the native perennial, Elymus glaucus

Community context of host-pathogen interactions: BYDV in California

grasslands

1. Host Community: BYDV presence was a necessary precondition to allow invasion by exotic annual grasses in California

2. Resource supply: Nitrogen increases both exotic annual invasion and BYDV prevalence in native grasses

Community context of host-pathogen interactions: general implications

1. Host Community: there can be strong feedbacks between changes in the host community and pathogen dynamics.

2. Resource supply: changing supply of abiotic resources can indirectly affect pathogens via effects on host communities

All this is well and good, but we are still lacking a large-scale experimental test of the model predictions

Hopland

McLaughlin

Finley

Basket Slough

Sierra Foothills

Experimental Test of Resource Supply and Host Community effects on Disease

•Replicated at five Sites with two replicates per site•N and P added in factorial combination•Monitor Disease incidence in 3 congeneric pairs of annual and perennial grasses

We have good estimates for end of season status for discrete time portion of model

A key challenge is to track within season growth rates used in disease model as sites are widely scattered.

Hopland

McLaughlin

Finley

Basket Slough

Sierra Foothills

Experimental Test of Resource Supply effects on Disease

•Remote meteorological stations will allow us to track changes in light interception, a surrogate for plant biomass.

•These continuous data will allow us to estimate the effects of resource supply (rainfall, nitrogen, phosphorous) on the phenology of annual and perennial grasslands.

Sensor setup for one reserve (site)

NP plot

Neon Wireless Platform: light, soil moisture, rainfall, temperature senors and compactrio, wireless, and power (solar & battery),…

Radio Relay: may be necessary to compete connection to internet point of contact

Internet point of contact: Cheap CPU with wireless antenna. This point will have power available.

Ground-level light and soil moisture sensors in and out of N&P fertilization plot with ambient light, rain, and temp sensors at platform

Example workflow for BYDV models

1. Collection of raw sensor data from met stations2. Data processing in R3. Model fitting and parameter estimation of

growth models in R4. Run disease model simulations in R5. Produce graphics from model output in R

General features for REAP to consider from BYDV case study

1. Need for continuous data from remote locations2. Well-documented workflows between raw data, data

processing, parameter fitting with statistical models, and analytical/simulation models

3. Ability to use a wide range of sensor configurations.

Considerations not well-represented in current case study

1. Mobile sensor/data loggers as in the case with GPS radio collars

2. High density networks of sensor spatial sensor grids3. Need for adaptive real-time reconfiguration of sensor

networks

Funding•NSF/NIH EID 05-25666 (Borer, Dobson, Mitchell, Power, and Seabloom)

•Murdock Foundation (Borer and Engler)

•USDA NRICGP 2003-35316-13767 (Briggs and Borer)

•NSF DEB 02-35624 (Reichman, Seabloom, and Schimel)

•NSF DEB 04-44639 (Power and Mitchell)

People•Field work: T. Yoshida, A. Borcher, J. Quinn, T. Mizerek, G. Creager, A. Brandt, B. Martin

•ELISAs: Kai Blaisdell and Craig Kahlke