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Vector-borne plant diseases:
factors driving the emergence and
spread of pathogens
Rodrigo Almeida
University of California, Berkeley
Percentage of all produce (1967) and of eight
major crops (1994) lost to pests
Produce lost to diseases, insects and weeds (%)
Continent or region
1967 estimate
1994 estimate
Europe
25
28
Oceania
28
36
North/Central America
29
31
Russia and China
30
41
South America
33
41
Africa
42
49
Asia
43
47
Agrios 2005
Annual losses in the US alone
• $9.1 billion to disease
• $7.7 billion to insects
• $6.2 billion to weeds
• Estimated current losses in the US
(pre- and post-harvest) Î 40%
Agrios 2005
Estimate for world population increase
Millions
Billions
Population size
Annual increments
Annual increment
Populationsize
size
Population
Source: United Nations Population Division
Increasing world population
Need to increase food production
Expansion of farm land
New (and old)
plant and human
diseases
↑External input
Environmental damage
?
Sustainability problems
Social, economical impacts
pollution
conservation of species
deforestation
extinctions
Plant emerging infectious diseases
Pathogens
Nematode Unknown
Bacterium
Fungus
Drivers of emergence
Recombination
Habitat changes
Change in vector
population
Farming
techniques
Weather
Virus
Based on Anderson et al. 2004
Introductions
What factors affect plant disease epidemics?
M
Time
int ultit
er rop
ac h
tio ic
ns
Su
ve rro
ge un
ta din
tio g
n
Host
Pa
nt
me
on
th
o
ge
n
vir
En
Disease
Host
nt
e
em s
g
a tice
n
Ma prac
Pathogen
co Abi
nd oti
itio c
ns
Vector
Additional layers of complexity:
9
9
9
9
9
9
environment (e.g. temperature)
vector ecology
pathogen ecology
host plant ecology
outcome of various interactions
disease management
Banana bunchy top disease
Disease spread in an archipelago
–identifying factors driving an epidemicPierce’s disease of grape
Impact of an invasive vector on the spread
of an established plant disease and the
‘rise’ of new diseases
Spread of a vector-borne pathogen in Hawaii
-Banana bunchy top virus-
R. Messing
R. Messing
• BBTV
– Multi-partite ssDNA virus
– Musa is only host plant in Hawaii
– Introduced into State in 1989
• Aphid vector
– Pentalonia nigronervosa
– Established in all Hawaiian islands prior to BBTV
introduction
– Banana and few other plants are host plants
• Transmission biology
– Circulative, non-propagative
BBTV invasion of Hawaii
SPREAD HYPOTHESIS
?
1997
2005
1989
2002
1995
2004
Xylella fastidiosa
9 Xylem-limited bacterium
9 Wide plant host range - at least 28 families, most
asymptomatic
9 Causes Pierce’s disease (PD), almond leaf scorch (ALS)
and many other plant diseases
9 Spread by insect vectors
Pierce’s disease (PD)
Photo UC IPM
BGSS and GWSS
Glassy-winged sharpshooter
(GWSS)
Photo R. Krugner
Homalodisca vitripennis
First detected in CA in 1989
High numbers on citrus (>6,000 per tree)
Polyphagous (estimated > 200 host plants)
Feeds on woody tissues of grapevines and
dormant plants
Highly dispersive
Vector transmission characteristics
9 Nymphs and adults vector X. fastidiosa
9 No latent period
9 No transmission after molting
9 No transovarial transmission
9 Persistent in adults
9 Multiplication in foregut
Photo J. Clark
Incidence highest at edge of vineyard
Incidence decreases away from edge
Photo A.H. Purcell
Linear spread
Exponential spread
# diseased vines
GWSS
BGSS
time
GWSS is a less efficient vector than BGSS
BGSS
GWSS
Inoculation of two-year old wood tissue
Plant tissue
# plants
# infected plants
Transmission rate/group (%)
Green
shoot
44
Two-year old
wood
40
29
19
65.9
47.5
ar
e
n
Li
100
ad
e
r
sp
ne
i
-v
o
t
- ad
e
e
n
Vi spr
Max
75
GWSS
Xf pop
50
25
0
1
Jan
Apr
Jul
Oct
Jan
Modeling vine-to-vine spread
-acquisition is improbable
early in the season
Hill and Purcell 1997
-late season infections
recover
Feil et al 2003
What are the consequences for disease dynamics?
Current hypothesis
Probability of overwinter
persistence (solid lines)
susceptible
May
Suscept.
resistant
susceptible
resistant
Jun
Jul
Aug
Date of inoculation (previous year) or acquisition (current year)
Probability of acquisition
(dotted lines)
Window of chronic vine-to-vine spread:
Resist.
Sep
Insights from modeling approach
seasonal acquisition slightly reduces PD incidence
Number of diseased vines
recovery strongly reduces 2° spread
100
seasonal acquistion
& recovery
seasonal acquisition
constant acquisition
80
60
40
20
0
0
10
20
30
40
Time (months)
50
60
Epidemiological importance of strain/host plant relationships
Ann1
Manteca
ALS4
ALS7
Dixon
Butte
PD-
Glenn
ALS6
Contra Costa
Conn
STL
ALS+
Temecula
Baja
Traver
Bakersfield
Stanislaus
Pavichi
Buena Vista
UCLA
Fresno-ALS
Medeiros
Tulare
01
PD+
X
Invasive vector transfers X. fastidiosa to
crops of economic importance, establishing
new disease cycles
Natural vegetation
Native vectors
maintain
X. fastidiosa
Little disease, non-agricultural
disease cycle
Invasive polyphagous vector
Acquires X. fastidiosa from nonagricultural disease ‘cycles’
General impact of GWSS introduction into California
GWSS large populations
More X. fastidiosa-vector encounters
More successful infections
Higher disease incidence
New vector-pathogen associations
New diseases
 NEW DISEASES Á
Oleander
Liquidambar
Mulberry
Olive
Ornamental plum
and
many new landscape hosts? (Wong et al. 2004)
What is the threat of emerging
vector-borne plant diseases?
-citrus as an example– in US (37% of the world orange juice market)
• Citrus greening –introduction(?) – 2005
• Citrus tristeza – vector introduction – early 2000s
• Citrus variegated chlorosis – threat…
– in Brazil (48% of the world orange juice market)
• Citrus greening –introduction(?) and new strain(?) - 2004
• Citrus sudden death – etiology? possibly viral mutation –
early 2000s
• Citrus variegated chlorosis – probably new host/X.
fastidiosa combination - 1987
Are human and plant vector-borne
diseases similar in their ecology?
UH-CTAHR
Hawaii DoA
Are human and plant vector-borne
diseases similar in their ecology?
Eldrige and Edman 2000
Acknowledgments
9 Banana bunchy top
9
9
9
9
9
Mandy Anhalt
Gordon Bennett
Patrick O’Grady
CTAHR/Univ. Hawaii
Hawaii DoA
9 Pierce’s disease
9 Sandy Purcell
9 Matt Daugherty
9 UC Berkeley Vector Lab
Funding
United States Department of
Agriculture
California Department of Food
and Agriculture
University of California
American Vineyard Foundation