Fungal Diseases in Two North-West Spain Vineyards: Relationship with Meteorological Conditions and Predictive Aerobiological Model

ag onomy
A icle
Fungal Diseases in Two No h-Wes Spain Vineya ds:
Rela ionship wi h Me eo ological Condi ions and
P edic i e Ae obiological Model
Jose A. Co iñas Rod íguez 1, Es e anía González-Fe nández 1,
Ma ía Fe nández-González 1,2,* , Rosa A. Vázquez-Ruiz 3and Ma ía Jesús Ai a 4
1Depa men o Plan Biology and Soil Sciences, Sciences Facul y o Ou ense, Uni e si y o Vigo, As Lagoas
s/n, 32004 Ou ense, Spain; [email p o ec ed] (J.A.C.R.); [email p o ec ed] (E.G.-F.)
2Ea h Sciences Ins i u e (ICT), Pole o he Facul y o Sciences Uni e si y o Po o, 4169-007 Po o, Po ugal
3
Depa men o Bo any, Highe Poly echnic School, Uni e si y o San iago o Compos ela, 27002 Lugo, Spain;
[email p o ec ed]
4
Depa men o Bo any, Biology Facul y, Uni e si y o San iago o Compos ela, 15782 San iago o Compos ela,
Spain; [email p o ec ed]
*Co espondence: [email p o ec ed]
Recei ed: 19 Decembe 2019; Accep ed: 28 Janua y 2020; Published: 3 Feb ua y 2020


Abs ac :
G ey mould, powde y mildew, and downy mildew a e he mos equen ungal diseases
among ineya ds wo ldwide. In he p esen s udy, we analysed he in luence o he ungi causing hese
diseases (Bo y is, E ysiphe, and Plasmopa a, espec i ely) on wo i icul u e a eas om No h-wes e n
(NW) Spain du ing h ee g ow h seasons (2016, 2017, and 2018). The ob ained esul s showed
he p edominan concen a ion o he Bo y is ai bo ne spo es, mainly om he beginning o he
In lo escence eme ge phenological s age (S-5) un il he end o he Flowe ing phenological s age
(S-6). E ysiphe and Plasmopa a ai bo ne spo e peak concen a ions we e mo e localised a ound
Flowe ing (S-6) and De elopmen o ui s (S-7) phenological s ages. We applied a Spea man’s
co ela ion es and a P incipal Componen Analysis o de e mine he in luence o he me eo ological
pa ame e s on he concen a ion o ai bo ne spo es. Taking in o accoun he a iables wi h he highes
co ela ion coe icien , we de eloped mul iple eg ession models o o ecas he phy opa hogenic
ungal spo e concen a ions. The Bo y is model eg ession equa ion explained be ween 59.4–70.9%
o spo e concen a ion a iabili y. The E ysiphe equa ion explained be ween 57.6–61% and he
Plasmopa a explained be ween 39.9–55.8%. In gene al, we ound be e p edic ion esul s o mean
daily concen a ions han spo adic spo e peaks.
Keywo ds: Bo y is; E ysiphe; Plasmopa a; ineya ds; incidence; mul iple linea eg ession
1. In oduc ion
Among he c yp ogamic diseases, he ungal g ey mould, powde y mildew, and downy mildew
epidemics ha e he highes incidence in Eu opean ineya ds [
1
–
4
]. G ey mould caused by Bo y is spp.
Pe s.: F . ( eleomo ph: Bo yo inia uckeliana (de Ba y) Whe zel) a ec s mo e han 200 plan s, mainly
dico plan s, and i can cause se ious economic damage, especially in g ape ines [
5
–
7
]. In addi ion o an
impo an c op yield loss, his disease can also educe he wine quali y by p o iding an uns able colou ,
oxida i e damages, p ema u e aging, unpleasan la ou s, and cla i ica ion di icul ies [
8
]. The Bo y is
in ec ions, due o he ungal laccase enzyme oxida ion, can comp omise bo h he g apes and wine
quali y [
9
]. This ungus o e win e s as scle o ia and mycelium in buds o unk c acks, in ec ing plan s
again in he ollowing sp ing mainly h ough wounds caused by hails ones, mechanical inju ies o
insec s [10–12].
Ag onomy 2020,10, 219; doi:10.3390/ag onomy10020219 www.mdpi.com/jou nal/ag onomy
Ag onomy 2020,10, 219 2 o 18
Powde y mildew caused by E ysiphe neca o Schwein.: (anamo ph: Oidium ucke i Be k) came
om he Uni ed S a es o Eu ope h ough England in 1845, sp eading o he en i e Medi e anean
egion and o he geog aphical a eas [
13
]. The Ame ican na i e g ape ine has a high esis ance le el
agains his pa hogen, while he Eu opean species Vi is ini e a is suscep ible as i can p esen se e e
disease symp oms in di e en plan pa s [
14
]. This ungus no ably dec eases he g ape yield and
quali y, al e ing he mus and wine o ganolep ic cha ac e is ics as i educes he soluble solids and
inc eases he o al acidi y [
15
]. In ed wines, in ec ed ui s a he beginning o ipening each a lowe
phenolic compounds con en , which also has an impac on hei senso y p ope ies [16].
Finally, Plasmopa a i icola (Be k. & Cu is) Be l. & De Toni, esponsible o downy mildew, is an
obliga e oomyce e ha o e win e s as oospo es in soil lea es and ege al deb is. These p opagules
ma u e as a unc ion o empe a u e and p ecipi a ion, causing subsequen seconda y in ec ions.
Plasmopa a is na i e o No h Ame ica and was i s de ec ed in Spain in 1878. Since hen, i has been
conside ed as one o he wo s g ape ine diseases ha occu du ing a ou able wea he condi ions [
17
].
The ungus bea s ui only on he hos plan su ace, as such, i can be only diagnosed by obse ing
spo ula ion o ui ing on he plan [
18
]. I causes di ec in lo escence and bunch losses o indi ec
dec eases o pho osyn he ic ac i i y on a ec ed lea es. In se e e a acks, he plan s su e pa ial
desicca ion esul ing in he p ema u e alling o lea es, and he wi he ing o b anches [19].
The incidence o hese h ee ine pa hogens was widely s udied, as well as conside ing he analysis
o cul u al con ol p ac ices. Di e en measu es, such as d ainage imp o emen , g een p uning nea o
lowe ing, de olia ion nea o e aison o he imp o emen o en ila ion o bunches, and he use o a
aining sys em o achie e app op ia e ai ci cula ion, can educe he pa hology se e i y caused by any
o hese ungi [
20
–
22
]. The plan igou can be con olled by a oiding excessi e g ow h and ege a i e
de elopmen is also bene icial o educe he incidence o phy opa hogens [
23
]. Rega ding chemical
con ol, con ac p oduc s, such as coppe in he o m o we able powde and applied in a olia sp ay
o sulphu as a powde o dus ing, should be used as in ec ion p e en ion sys ems, al hough hei
use should be a oided du ing lowe ing as i can a ec ui se [
24
]. Howe e , when diseases a e
e iden i is necessa y o apply pene a ing and sys emic ea men s wi h cu a i e e ec s, egula ing
hei equency acco ding o he pa hogen’s in ensi y [25].
The main goals o his esea ch wo k a e o analyse he incidence o hese h ee ungal g ape ine
diseases (g ey mould, powde y mildew, and downy mildew) in No h-wes e n (NW) Spain ineya ds
and o de elop p edic ion models o de ec he ai bo ne spo e p esence ha ungi p oduce. Besides
cos educ ion in g ape p oduc ion, his kind o s udy also impac s en i onmen al p o ec ion and
quali y since i allows a phy osani a y ea men applica ion when a eal in ec ion is de ec ed [26,27].
2. Ma e ials and Me hods
2.1. Loca ion and Clima ic Cha ac e is ics o he S udy A ea
The p esen s udy was conduc ed in wo wine-making egions, Ribei o and Ribei a Sac a, in he
Cenlle (117 m a. s.l. 42
◦
18
0
55.7” N; 8
◦
6
0
2.54” W) and O Ma o (332 m a. s.l. 42
◦
30
0
32.3” N; 7
◦
30
0
3.02”
W) ineya ds, espec i e ly (Figu e 1) du ing 2016, 2017 and 2018.
Ag onomy 2020,10, 219 3 o 18
Ag onomy2020,10,xFORPEERREVIEW3o 19

Figu e1.Loca iono  heRibei o(Cenlle)andRibei aSac a(OMa o)Designa ionO igina easin he
No hwes e nSpain.
Thep e ailingcul i a in heCenlle ineya disGodello,andinOMa o ineya di isMencía,
bo hincludedin hep e e en ialca ego yacco ding o heDesigna iono O iginRibei o(DOGN°
149,2009)andRibei aSac a(DOGN°194,2009) egula ions.TheGodellocul i a hasahigh igou 
andane ec bea ing( ending og owmo e e ically hanho izon ally)wi hanea lysp ou and
ma u a ion.Conside ing hepa hogensuscep ibili yo  heplan acco ding o he h eeca ego ies
es ablishedin heclassi ica iono  heGodellocul i a isclassi iedasha inglowsensi i i y o
Bo y is,mediumsensi i i y oPlasmopa a,andsensi i i y oE ysiphe.TheMencíacul i a hasa
medium igou wi hea lysp ou ingandsemi‐la ema u a ion.Thiscul i a issensi i e o he h ee
conside ed ungalpa hogens[28].
Fo clima iccha ac e iza ion,weconside ed heme eo ologicalda ao  hemaximum,minimum
andmean empe a u e, ela i ehumidi y,dayligh (sunshine)hou s, ain allandwind‐speed
a iables(Table1),p o idedby wos a ionsloca ed e yclose o hes udied ineya ds, heLei o
andMon o es a ionsbelonging o hewea he se iceMe eogaliciah ps://www.me eogalicia.gal
(accessedon21/06/2019).
Table1.Me eo ologicalpa ame e s,maximum empe a u e,minimum empe a u e,a e age
empe a u e,a e age ela i ehumidi y,sunshine,windspeedand ain all,in hes udya ea(2016–
2018).
Ribei oRibei aSac a
Yea 201620172018201620172018
AnnualA e age
Me eo ologicalDa a
MaxT(°C)22.823.923.720.621.921.4
MinT(°C)7.36.48.26.76.17.3
MeanT(°C)13.813.915.212.813.113.7
MeanRH(%)78.475.875.980.976.978.6
Sunshine(hou s)5.35.94.98.18.48.4
Wind‐Speed(Km/h)2.11.82.22.11.82.5
AnnualTo alRain all(L/m
2
)1211.8814.5775.2940.4616.2660.5
MaximumDaily ain all(l/m
2
)49.0100.839.442.877.525.7
Da e10Jan10Dec28

Feb10

Jan10Dec11Ma 
Maximum empe a u e(MaxT),minimum empe a u e(MinT),a e age empe a u e(MeanT),
a e age ela i ehumidi y(MeanRH).
Figu e 1.
Loca ion o he Ribei o (Cenlle) and Ribei a Sac a (O Ma o) Designa ion O igin a eas in he
No hwes e n Spain.
The p e ailing cul i a in he Cenlle ineya d is Godello, and in O Ma o ineya d i is Menc
í
a,
bo h included in he p e e en ial ca ego y acco ding o he Designa ion o O igin Ribei o (DOG N
◦
149,
2009) and Ribei a Sac a (DOG N
◦
194, 2009) egula ions. The Godello cul i a has a high igou and an
e ec bea ing ( ending o g ow mo e e ically han ho izon ally) wi h an ea ly sp ou and ma u a ion.
Conside ing he pa hogen suscep ibili y o he plan acco ding o he h ee ca ego ies es ablished in
he classi ica ion o he Godello cul i a is classi ied as ha ing low sensi i i y o Bo y is, medium
sensi i i y o Plasmopa a, and sensi i i y o E ysiphe. The Menc
í
a cul i a has a medium igou wi h
ea ly sp ou ing and semi-la e ma u a ion. This cul i a is sensi i e o he h ee conside ed ungal
pa hogens [28].
Fo clima ic cha ac e iza ion, we conside ed he me eo ological da a o he maximum, minimum
and mean empe a u e, ela i e humidi y, dayligh (sunshine) hou s, ain all and wind-speed a iables
(Table 1), p o ided by wo s a ions loca ed e y close o he s udied ineya ds, he Lei o and Mon o e
s a ions belonging o he wea he se ice Me eogalicia h ps://www.me eogalicia.gal (accessed on
21/06/2019).
Table 1.
Me eo ological pa ame e s, maximum empe a u e, minimum empe a u e, a e age
empe a u e, a e age ela i e humidi y, sunshine, wind speed and ain all, in he s udy a ea (2016–2018).
Ribei o Ribei a Sac a
Yea 2016 2017 2018 2016 2017 2018
Annual A e age
Me eo ological
Da a
Max T (◦C) 22.8 23.9 23.7 20.6 21.9 21.4
Min T (◦C) 7.3 6.4 8.2 6.7 6.1 7.3
Mean T (◦C) 13.8 13.9 15.2 12.8 13.1 13.7
Mean RH (%) 78.4 75.8 75.9 80.9 76.9 78.6
Sunshine (hou s) 5.3 5.9 4.9 8.1 8.4 8.4
Wind-Speed (Km/h)
2.1 1.8 2.2 2.1 1.8 2.5
Annual To al Rain all (L/m2)1211.8 814.5 775.2 940.4 616.2 660.5
Maximum Daily ain all (l/m2)49.0 100.8 39.4 42.8 77.5 25.7
Da e 10 Jan 10 Dec 28 Feb 10 Jan 10 Dec 11 Ma
Maximum empe a u e (Max T), minimum empe a u e (Min T), a e age empe a u e (Mean T), a e age ela i e
humidi y (Mean RH).
Ag onomy 2020,10, 219 4 o 18
2.2. Fieldwo k and Labo a o y Analysis
We s udied he phenological s ages o bo h g ape ine cul i a s ollowing he [
29
] scale adop ed
by he BBCH (Biologische Bundesans al , Bundesso enam and Chemical indus y) as a s anda dized scale.
Phenological obse a ions we e applied on 10 ines o each cul i a and his in o ma ion was co ela ed
wi h a mosphe ic spo e (o spo angia o Plasmopa a) concen a ions.
The s udy was ca ied ou du ing he ac i e g ape ine cycle, om he 1
s
o Ma ch o he g ape
ha es da e in he mon h o Sep embe . We used a olume ic me hod by means o a Hi s ype
Lanzoni VPPS-2000
®
(Lanzoni s. .l., Bologna, I aly) pollen-spo e ap [
30
] o he sampling o ai bo ne
ep oduc i e s uc u es. The olume ic aps we e placed a a heigh o wo me e s, acco ding
o he ine’s olia a angemen on each s udied ineya d. We iden i ied and quan i ied he h ee
conside ed pa hogens spo es/spo angia (Bo y is,E ysiphe and Plasmopa a) in he collec ed samples.
We ollowed he Spanish Ae obiology Ne wo k (REA) p oposed p o ocol [
31
] o spo e coun and
sample p epa a ion. Slide coun s we e pe o med on wo longi udinal ansec s along he slides and
he ai bo ne ungal spo e concen a ions we e exp essed as a daily a e age o ungal spo es/m
3
o ai
ecommended e ms we e used o he ae obiological e minology [32].
Table 2shows he phy ochemical ea men s applied in he plo s o he s udy. In he Ribei o D.O:
(Cenlle), a mean o h ee ea men s/yea agains Bo y is was applied om s age 6 ( lowe ing), six
ea men s/yea agains Mildew +Oidium mainly om s age 5 (in lo escence eme ges), and wo speci ic
ea men s/yea agains Mildew in he 7 h and 8 h s ages (de elopmen o ui s and ipening o be ies).
In he Ribei a Sac a D.O. (O Ma o), no ea men s agains Bo y is we e applied, ou ea men s/yea
(none in 2017) agains Mildew +Oidium, mainly in s age 5 (In lo escence eme ge) and ou speci ic
ea men s/yea agains Mildew (none in 2017). Fo all cases, he ungicides used un il Flowe ing (E6)
a e o he sys emic ype in yea s ha had a high incidence o ungi, and om his momen o con ac
(mainly sulphu -based powde p oduc s un il F ui se , and coppe in we dus un il So ening o
be ies).
Table 2. Numbe o phy osani a y ea men s applied in he s udied plo s.
Agains S0 S1 S5 S6 S7 S8
Bo y is
Cenlle 2016 1 2
Cenlle 2017 1 1
Cenlle 2018 2 2 1
O Ma o 2016
O Ma o 2017
O Ma o 2018
Mildew +Oidium
Cenlle 2016 2 2 2
Cenlle 2017 2 1 3 1
Cenlle 2018 1 1 1 1 2
O Ma o 2016 1 2 1
O Ma o 2017
O Ma o 2018 2 1 2
Mildew
Cenlle 2016 1
Cenlle 2017 2
Cenlle 2018 2 2
O Ma o 2016 2 2
O Ma o 2017
O Ma o 2018 1 1 2
Phenological s ages: Bud de elopmen (S0), Lea de elopmen (S1), In lo escence eme ge (S5), Flowe ing (S6),
De elopmen o ui s (S7) and Ripening o be ies (S8).
2.3. S a is ical Analysis
In o de o de e mine he in luence o he main me eo ological a iables on ai bo ne spo e
concen a ions, we applied Spea man’s co ela ion es , as he conside ed a iables didn’ show a
Ag onomy 2020,10, 219 5 o 18
no mal dis ibu ion. We conside ed he co ela ions o he same day and he p e ious 1–7 days as
spo e p oduc ion can be di ec ly a ec ed by me eo ological condi ions o indi ec ly h ough i s e ec
on he colonised subs a es [
26
]. Mo eo e , we applied a P incipal Componen Analysis (PCA) o
complemen he analysis o hese a iables, conside ing he me eo ological in luence o all a iables
as a whole. Fo his analysis we conside ed o bo h ineya ds he maximum, mean, and minimum
empe a u es; ela i e humidi y; ain all; and wind-speed me eo ological pa ame e s, independen o
he ineya d loca ion.
Wi h he ob ained esul s, we de eloped models based on Lineal Reg essions using he
me eo ological a iables wi h he highes co ela ion coe icien s as es ima o s o he ungal spo e
concen a ions. Fo model alida ion, we ca ied ou an in e nal alida ion and we s udied he esidual
sco es as hey show he di e ences be ween obse ed and p edic ed da a o each analysed yea .
3. Resul s
3.1. To al Spo e Concen a ions and Spa ial Dis ibu ion
The ac i e g ape ine pe iod sligh ly a ied acco ding o he ineya d loca ion and he conside ed
yea . The sp ou ing phenological phase (S-0) began be ween mid-Ma ch o he beginning o Ap il,
while he ha es da e occu ed be ween he end o Augus o mid-Sep embe . Wi hin hese da es,
he collec ion o ae obiological samples was ca ied ou and he ungal spo es we e coun ed.
The Bo y is Seasonal Spo e In eg al (SSIn) was ma kedly highe han o he o he conside ed
pa hogens, wi h a maximum o 49,620 spo es in he O Ma o ineya d in 2018 and SSIn alues o
27,656 and 17,240 spo es o he 2016 and 2017 yea s, espec i ely. The E ysiphe SSIn no ed a eco d in
2016 o bo h s udied ineya ds o 17,269 spo es in Cenlle and 12,946 spo es in O Ma o. Plasmopa a was
he pa hogen wi h he lowes a mosphe ic p esence. The highes SSIn alue was eco ded in 2018 a
he O Ma o ineya d wi h 5656 spo es, a ying be ween 1363 o 2017 and 3618 o 2016 SSIn, and om
679 o 2017 o 3605 o 2018 SSIn alues in Cenlle (Table 3).
Taking in o accoun he maximum daily alues we also ound a clea Bo y is spo e’s dominance
wi h a maximum o 1547 spo es/m
3
in O Ma o on 9 June 2018. The highes daily peaks o E ysiphe and
Plasmopa a we e eco ded du ing he 2016 season in he O Ma o ineya d, wi h 597 E ysiphe spo es/m
3
on 3 June 2016 and 502 Plasmopa a spo es/m3on 7 July 2016.
Conside ing he pa hogen ela ion wi h he di e en g ape ine phenological phases, we ound a
conside able a iabili y depending on he pa hogen, season, and ineya d loca ion. The Bo y is and
E ysiphe ai bo ne spo e p esence we e almos cons an ly along he g ape ine g ow h cycle, while he
Plasmopa a spo angia did no show a con inuous daily eco d. Fo he conside ed 2016–2018 pe iod,
we ound 29 days/season a e age o Plasmopa a 0- eco d in Cenlle, and 20 days/season in O Ma o.
The highes Bo y is incidence was de ec ed om he in lo escence eme gence (S-5) phenological
s age un il he end o lowe ing (S-6). A he Cenlle plo , he maximum a mosphe ic Bo y is spo e
peak was eco ded in mid-June in 2016, he end o May in 2017, and se e al spo e peaks we e de ec ed
be ween he beginnings o June and he end o July in 2018, wi h a maximum peak on 7 July. A he O
Ma o plo , he Bo y is spo e peaks occu ed wi hin he May–July pe iod, wi h he maximum peaks
on 27 May 2016, on 4 June 2017, and 9 June 2018. We also ound ea ly in ec ions du ing he lea
de elopmen (S-1) phenological s age a he Cenlle ineya d in 2017, and a he O Ma o ineya d in
2016 and 2017 (Figu e 2).

Ag onomy 2020,10, 219 6 o 18
Table 3.
SSIn da a, daily maximum spo e concen a ion and maximum da e o Bo y is,E ysiphe, and
Plasmopa a in Ribei o (Cenlle) and Ribei a Sac a (O Ma o) DOs du ing he s udy pe iod (spo es/m
3
o ai ).
Cenlle Bo y is E ysiphe Plasmopa a
S udy Pe iod 19 Sep embe 2016 o 18 Sep embe 2016
SSIn 16,806 17,269 1910
Daily Maximum 637 399 104
Maximum Da e 22 June 16 May 8 June
S udy Pe iod 16 Ma ch 2017 o 30 Augus 2017
SSIn 15,378 3344 679
Daily Maximum 696 423 54
Maximum Da e 28 May 2017 26 May 2017 8 May 2017
S udy Pe iod 29 Ma ch 2018 o 10 Sep embe 2018
SSIn 24,214 3116 3605
Daily maximum 1210 316 460
Maximum da e 7 July 2018 4 June 2018 7 July 2018
O Ma o
S udy pe iod 24 Ma ch 2016 o 30 Sep embe 2016
SSIn 27,656 12,946 3618
Daily Maximum 1435 597 502
Maximum Da e 27 May 2016 3 June 2016 7 July 2016
S udy Pe iod 04 Ma ch 2017 o 08 Sep embe 2017
SSIn 17,240 1686 1363
Daily Maximum 826 108 45
Maximum Da e 4 June 2017 19 June 2017 3 June 2017
S udy Pe iod 07 Ap il 2018 o 07 Sep embe 2018
SSIn 49,620 5632 5656
Daily Maximum 1547 197 345
Maximum da e 9 June 2018 29 May 2018 22 July 2018
SSIn—Seasonal Spo e In eg al.
Mos o he E ysiphe and Plasmopa a in ec ions coincided wi h he end o lowe ing (S-6) and
de elopmen o ui s (S-7) phenological s ages. A he Cenlle ineya d, he e we e se e al E ysiphe
and Plasmopa a spo e peaks de ec ed in he May–July pe iod in 2016, while he maximum E ysiphe
spo e peak was on 26 May 2017 and 4 June 2018, and he maximum Plasmopa a spo angia peaks we e
egis e ed a he beginning o May in 2017, and du ing July in 2018. A he O Ma o ineya d, he highes
E ysiphe spo e peaks we e also de ec ed in he May–July pe iod in 2016 wi h a maximum spo e peak on
3 June. In 2017 and 2018, he highes daily spo e peaks we e lowe han in 2016, egis e ed on 19 June
and 29 May, espec i ely. The Plasmopa a highes spo angia peaks occu ed a he beginning o July in
2016 and he end o July in 2018, while in 2017 he peak was de ec ed a he beginning o June, wi h a
ma kedly lowe alue (Figu e 2).
Ag onomy 2020,10, 219 7 o 18
Ag onomy2020,10,xFORPEERREVIEW7o 19

Figu e2.Phenology,spo econcen a ions,andphy osani a y ea men sappliedin he h ees udy
yea s o Ribei o(Cenlle)andRibei aSac a(OMa o) ineya ds.
Mos o  heE ysipheandPlasmopa ain ec ionscoincidedwi h heendo  lowe ing(S‐6)and
de elopmen o  ui s(S‐7)phenologicals ages.A  heCenlle ineya d, he ewe ese e alE ysiphe
andPlasmopa aspo epeaksde ec edin heMay–Julype iodin2016,while hemaximumE ysiphe
spo epeakwason26May2017and4June2018,and hemaximumPlasmopa aspo angiapeakswe e
egis e eda  hebeginningo Mayin2017,anddu ingJulyin2018.A  heOMa o ineya d, he
highes E ysiphespo epeakswe ealsode ec edin heMay–Julype iodin2016wi hamaximum
spo epeakon3June.In2017and2018, hehighes dailyspo epeakswe elowe  hanin2016,
egis e edon19Juneand29May, espec i ely.ThePlasmopa ahighes spo angiapeaksoccu eda 
hebeginningo Julyin2016and heendo Julyin2018,whilein2017 hepeakwasde ec eda  he
beginningo June,wi hama kedlylowe  alue(Figu e2).
3.2.Analysiso Me eo ologicalPa ame e s
Takingin oaccoun  heannuala e agemaximum empe a u e alue,i washighe inRibei o
(Cenlle)wi ha2°Cdi e enceo e Ribei aSac a(OMa o) o  hesameconside edyea s.Thesame
occu edwi hminimumandmean empe a u esbu wi h helowes di e encein hiscase,a ound
1°C.Fo bo h ineya ds,CenlleandOMa o,2017waswa me  han heo he  woconside edyea s
wi hamaximum empe a u eo 23.9°Cand21.9°C espec i ely.Meanandminimum empe a u es
we ehighe in2018,wi h15.2°Cand13.7°Cmean empe a u es,and8.2°Cand7.3°Cminimum
empe a u es, espec i ely.Thea e age ela i ehumidi ywashighe inRibei aSac a haninRibei o,
eachingi smaximumin2016wi h80.9%.Thesamehappenedwi h hesunshinehou s,wi h he
maximum alues o Ribei aSac a oundin2017and2018.The ainies yea was2016 o bo hRibei o
Figu e 2.
Phenology, spo e concen a ions, and phy osani a y ea men s applied in he h ee s udy
yea s o Ribei o (Cenlle) and Ribei a Sac a (O Ma o) ineya ds.
3.2. Analysis o Me eo ological Pa ame e s
Taking in o accoun he annual a e age maximum empe a u e alue, i was highe in Ribei o
(Cenlle) wi h a 2
◦
C di e ence o e Ribei a Sac a (O Ma o) o he same conside ed yea s. The same
occu ed wi h minimum and mean empe a u es bu wi h he lowes di e ence in his case, a ound 1
◦
C.
Fo bo h ineya ds, Cenlle and O Ma o, 2017 was wa me han he o he wo conside ed yea s wi h
a maximum empe a u e o 23.9
◦
C and 21.9
◦
C espec i ely. Mean and minimum empe a u es
we e highe in 2018, wi h 15.2
◦
C and 13.7
◦
C mean empe a u es, and 8.2
◦
C and 7.3
◦
C minimum
empe a u es, espec i ely. The a e age ela i e humidi y was highe in Ribei a Sac a han in Ribei o,
eaching i s maximum in 2016 wi h 80.9%. The same happened wi h he sunshine hou s, wi h he
maximum alues o Ribei a Sac a ound in 2017 and 2018. The ainies yea was 2016 o bo h Ribei o
(wi h 1211.8 mm) and Ribei a Sac a (940.4 mm) a eas. Ne e heless, he ainies day was 10 Decembe
2017 o bo h ineya ds (Table 1).
3.3. S a is ical Resul s
The s a is ical analysis be ween he spo e daily concen a ions and he daily alues o he main
me eo ological a iables along he g ape ine ep oduc i e cycle was conduc ed, while also conside ing
he daily alues o he me eo ological a iables du ing he p e ious 7 days in ega ds o he p esence
o spo es in he a mosphe e o he ineya d. The s a is ical analysis be ween he spo e concen a ions
and he main me eo ological a iables showed ha ain all and ela i e humidi y had a s a is ically
signi ican in luence in mos cases. Ne e heless, he in luence sign was no so clea o empe a u e,
Ag onomy 2020,10, 219 8 o 18
as we ound he same numbe o posi i e and nega i e co ela ions o maximum and mean empe a u e.
The pa ame e s wi h he highes in luence on each pa hogen a ied depending on he ineya d loca ion
and he s udy yea .
Wi hin he signi ican Bo y is co ela ions, we ound he highes Spea man’s posi i e coe icien s
o he Bo y is spo es ob ained ou days be o e (Bo y is-4) s. ain all, and Bo y is-4 s. ela i e
humidi y co ela ions o Cenlle in 2017. In he same Cenlle ineya d in 2018, we ound he Bo y is-1
s. minimum empe a u e, and Bo y is s. mean empe a u e co ela ions. We also ound a high
Spea man’s posi i e coe icien o he Bo y is-2 s. ela i e humidi y co ela ion a he O Ma o
ineya d in 2016. Fo he E ysiphe ai bo ne spo es we ound ha he highes Spea man’s signi ican
coe icien was nega i e, co esponding o E ysiphe-2 s. minimum empe a u e, and E ysiphe-2 s.
mean empe a u e co ela ions a Cenlle ineya d in 2016. A he O Ma o ineya d, we ound also high
co ela ions, posi i e in his case, be ween E ysiphe s. minimum empe a u e, and E ysiphe s. mean
empe a u e in 2017. The s onges co ela ions ound o Plasmopa a ai bo ne spo angia co esponded
o Plasmopa a s. minimum empe a u e, Plasmopa a s. mean empe a u e posi i e co ela ions a
he Cenlle ineya d in 2017, and Plasmopa a-6 s. ain all, Plasmopa a-2 s. ela i e humidi y posi i e
co ela ions a he O Ma o ineya d in 2016. Howe e , we also ound conside able nega i e co ela ions
o Plasmopa a-7 s. maximum empe a u e and Plasmopa a-7 s. mean empe a u e a he O Ma o
ineya d in 2016 (Table 4).
In bo h analyzed a eas, he P incipal Componen s PC1 and PC2 included me eo ological a iables
and he PC3 g ouped he h ee phy opa hogenic ungi spo e concen a ions. Fo Cenlle, PC1 includes
he maximum and mean empe a u es, humidi y, and ain all and PC2 includes he minimum
empe a u e and wind speed. In he case o O Ma o, PC1 include he empe a u es and he wind speed,
whe eas PC2 includes he wa e - ela ed pa ame e s. Mos o he a iables had signi ican posi i e
loads, excep wind speed (PC2 in Cenlle and PC1 in O Ma o). Fo g aphic ep esen a ion, we selec ed
PC2 e sus PC3 o he Cenlle ineya d, and PC1 e sus PC3 o he O Ma o ineya d (Figu e 3).
In he ob ained cha s we showed in de ail he ela ion be ween ungal ai bo ne spo es and he main
me eo ological a iables. In bo h ineya ds we obse ed a high posi i e associa ion deg ee be ween
me eo ology and ungal spo es coun s.
Ag onomy 2020,10, 219 9 o 18
Table 4.
Spea man’s ank co ela ion o di e en pa ame e s o he s udied cul i a s. Spo e concen a ions (Bo y is,E ysiphe and Plasmopa a) and he main
me eo ological pa ame e s. (ple el: * <0.05; ** <0.01; N.S.: no signi ica i e).
2016 2017 2018
Cenlle Bo y is E ysiphe Plasmopa a Bo y is E ysiphe Plasmopa a Bo y is E ysiphe Plasmopa a
Rain all −0.167 *
Bo y is
−0.365 *
E ysiphe-7
0.355 *
Plasmopa a-2
0.401 **
Bo y is-4
0.196 *
E ysiphe-7
0.172 *
Plasmopa a-4
−0.190 *
Bo y is-1 N.S. −0.255 **
Plasmopa a
RH 0.382 *
Bo y is-2
−0.321 *
E ysiphe-2
0.342 *
Plamopa a-2
0.507 **
Bo y is-4
0.248 **
E ysiphe-5 N.S. 0.263 **
Bo y is-5
0.203 **
E ysiphe−7N.S.
T max 0.288 **
Bo y is
0.440 **
E ysiphe-2
−0.335 *
Plasmopa a-2
−0.228 **
Bo y is-4
−0.180 *
E ysiphe-7
−0.300**
Plasmopa a-6
0.387 **
Bo y is N.S. 0.387 **
Plasmopa a
T min 0.323 **
Bo y is
−0.674 *
E ysiphe-2
0.346 *
Plasmopa a-2 N.S. N.S. −0.411 **
Plasmopa a-7
0.634 **
Bo y is-1
0.197 *
E ysiphe
0.489 **
Plasmopa a
T mean 0.307 **
Bo y is
−0.666 **
E ysiphe-2 N.S. −0.188 *
Bo y is-4
−0.154 *
E ysiphe-5
−0.362 **
Plasmopa a-6
0.556 **
Bo y is N.S. 0.480 **
Plasmopa a
O Ma o
Rain all 0.365 **
Bo y is-5
0.394 **
E ysiphe-6
0.227 **
Plasmopa a-6 N.S. −0.272 **
E ysiphe-2 N.S. 0.224 **
Bo y is-6
0.231 **
E ysiphe-7 N.S.
RH 0.593 **
Bo y is-2
0.491**
E ysiphe-6
0.377**
Plamopa a-2
0.224 **
Bo y is-3
−0.354 **
E ysiphe-2
0.163 *
Plasmopa a-4
0.373 **
B o y is-7
0.359 **
E ysiphe-6 N.S.
T max −0.386 **
Bo y is-7
−0.476 **
E ysiphe-7
−0.309 **
Plasmopa a-7 N.S. 0.483 **
E ysiphe
0.186 *
Plasmopa a N.S. −0.297 **
E ysiphe-6 N.S.
T min −0.153 *
Bo y is-7
−0.231 **
E ysiphe-6
−0.177*
Plasmopa a-7
0.248 **
Bo y is
0.509 **
E ysiphe
0.209 **
Plasmopa a
0.331 **
Bo y is N.S. N.S.
T mean −0.367 **
Bo y is-7
−0.439 **
E ysiphe-7
−0.332 **
Plasmopa a-7
0.224 **
Bo y is
0.582 **
E ysiphe
0.218 **
Plasmopa a
0.169 *
Bo y is
−0.251 **
E ysiphe-6 N.S.
The P incipal Componen Analysis (PCA) esul ed in he ex ac ion o h ee P incipal Componen s (PC) o bo h Cenlle and O Ma o ineya ds. The accumula ed explained a iance o he
o iginal da a in Cenlle was 70.9% and 67.6% in O Ma o (Table 5).
Ag onomy 2020,10, 219 16 o 18
18.
Camb a, M.; Be nal, I. Plasmopa a Vi icola (Be k. y Cu is) Be l. & de Toni. Mildiu de la id. Fichas de Diagn
ó
s ico
en Labo a o io de O ganismos Noci os de los Vege ales. Ficha 64, 2nd ed.; MAPA: Mad id, Spain, 2006.
19.
Rossi, V.; Ca i, T. E ec o wa e on ge mina ion o Plasmopa a i icola oospo es. Plan Pa hol.
2007
,56,
957–966. [C ossRe ]
20.
D
í
az, T.; Riquelme, A. Con ol In eg ado en el cul i o de u a de mesa en la Regi
ó
n de Mu cia. Phy oma
2012
,
239, 48–54.
21.
Lucas, A. Con ol in eg ado de plagas y en e medades en el iñedo. Dossie ges i
ó
n in eg ada. Vida Ru al, 4
Decembe 2012, pp. 46–51.
22.
Me le , H.; Na a o, A.; Rosales, J. Manual T
é
cnico P oduc i o y Econ
ó
mico Vid. 2016, (Pub. CIREN N
◦
193).
A ailable online: h p://www.biblio ecadigi al.ci en.cl/handle/123456789/26087 (accessed on 3 Feb ua y 2020).
23.
Gonz
á
lez-Dom
í
nguez, E.; Ca i, T.; Cilibe i, N.; Rossi, V. A mechanis ic model o Bo y is cine ea on g ape ines
ha includes wea he , ine g ow h s age, and he main in ec ion pa hways. PLoS ONE 2015,10, e0140444.
24.
Po as, A. Mejo a de la Tecnolog
í
a de la Pul e izaci
ó
n de P oduc os Fi osani a ios sob e Plan aciones de id
en Espalde a. Ph.D. Thesis, Uni e sidad de Có doba, Có doba, Spain, 2006.
25.
Rojas, V.; Dennis, M. Nue as Al e na i as de Con ol Pa a el o
í
dio de la id (Uncinula Neca o Schw.); Uni e sidad
de Chile, Fac. de CC. Ag onomicas: San iago, Chile, 2003; p. 58.
26.
Rod
í
guez-Rajo, F.J.; Ja o, V.; Fe n
á
ndez-Gonz
á
lez, M.; Ai a, M.J. The use o ae obiological me hods o
o ecas ing Bo y is spo e concen a ions in a ineya d. G ana 2010,49, 56–65. [C ossRe ]
27.
A a a , K.H. Applica ion o s a is ical model o o ecas ing powde y mildew o g apes unde Egyp ian
condi ions based on me eo ological da a. In . J. Plan Pa hol. 2015,6, 48–57. [C ossRe ]
28.
MAPAMA. Minis e io de Ag icul u a y Pesca, Alimen aci
ó
n y Medio Ambien e, Regis o de Va iedades
Come ciales. 2017. A ailable online: www.mapama.gob.es (accessed on 3 Feb ua y 2020).
29.
Lo enz, D.H.; Eicho n, K.W.; Bleiholde , H.; Klose, R.; Meie , U.; Webe , E. Phänologische En wicklungss adien
de Wein ebe (Vi is ini e a L. ssp. ini e a). Codie ung und Besch eibung nach de e wei e en BBCH–Skala.
Vi ic. Enol. Sci. 1994,49, 66–70.
30. Hi s , J.M. An au oma ic olume ic spo e– ap. Ann. Appl. Biol. 1952,36, 257–265. [C ossRe ]
31.
Gal
á
n, C.; Ca iñanos, P.; Alc
á
za , P.; Dom
í
nguez, E. Manual de Calidad y Ges i
ó
n de la Red Española de Ae obiolog
í
a;
Se icio de Publicaciones, Uni e sidad de Có doba: Có doba, Spain, 2007; p. 61.
32.
Gal
á
n, C.; A ia i, A.; Bonini, M.; Clo , B.; C ouzy, B.; Dahl, A.; Fe nandez-Gonz
á
lez, D.; F enguelli, G.;
Geh ig, R.; Isa d, S.; e al. Recommended e minology o ae obiological s udies. Ae obiologia
2017
,33,
293–295. [C ossRe ]
33.
Ga gallo, P.; Ga c
í
a-Casa ejos, N. Impac os ambien ales y medidas de mi igaci
ó
n en el sec o i i in
í
cola
español. E3S Web o Con e ences 50, 01029. In P oceedings o he XII Cong eso In e nacional Te oi ,
Za agoza, Spain, 18–22 June 2018.
34.
Gau am, H.R.; Bha dwaj, M.L.; Robi ash, K. Clima e change and i s impac on plan diseases. Cu . Sci.
2013
,
105, 1685–1691.
35.
Casano a, J. Si uaci
ó
n ac ual de la Vi icul u a Ecol
ó
gica: T
é
cnicas de p oducci
ó
n de la u a y p oduc os
au o izados. Vida Ru al 2003,171, 41–45.
36.
P
é
ez-Sanz, R.; Manzano, Y.; San iago, L.; de La Iglesia, G.; Campillo, C.; Albe e, L.; Mi anda, J.S.; Ju
á
ez, I.
Me odolog
í
a pa a la Validaci
ó
n de Modelos de Desa ollo asociados al clima pa a el seguimien o del Mildiu,
Oidio y Pod edumb e G is en Viñedos de Cas illa y Le
ó
n. In P oceedings o he XXVIII Jo nadas de
Vi icul u a y Enolog
í
a de la Tie a de Ba os: Cul u al San a Ana, Cen o Uni e si a io, Almend alejo, Spain,
8–12 May 2006.
37.
O landini, S.; Maga ey, R.D.; Pa k, E.W.; Spo lede , M.; K oschel, J. Me hods o ag oclima ology: Modeling
app oaches o pes s and diseases. In Ag oclima ology: Linking Ag icul u e o Clima e; Ha ield, J.L.,
Si akuma , M.V.K., P uege , J.H., Eds.; Ag on. Monog . 60; ASA, CSSA, and SSSA: Madison, WI,
USA, 2017.
38.
Fe n
á
ndez-Gonz
á
lez, M.; Rod
í
guez-Rajo, F.J.; Ja o, V.; Ai a, M.J. Incidence o ungals in a ineya d o he
denomina ion o o igin Ribei o (Ou ense NW Spain). Ann. Ag ic. En i on. Med. 2009,16, 263–271.
39.
Calonnec, A.; Ca ola o, P.; Naulin, J.M.; Bailey, D.; Langlais, M. A hos –pa hogen simula ion model: Powde y
mildew o g ape ine. Plan Pa hol. 2008,57, 493–508. [C ossRe ]

Ag onomy 2020,10, 219 17 o 18
40.
Dugan, F.M.; Lupien, S.L.; G o e, G.G. Incidence, agg essi eness and in plan a in e ac ions o Bo y is cine ea
and o he ilamen ous ungi quiescen in g ape be ies and do man buds in cen al Washing on S a e.
Phy opa hology 2002,150, 375–381. [C ossRe ]
41.
Gessle , C.; Pe o , I.; Pe azzolli, M. Plasmopa a i icola: A e iew o knowledge on downy mildew o
g ape ine and e ec i e disease managemen . Phy opa hol. Medi e . 2011,50, 3–44.
42. Gale , P. P écis de Vi icul u e, 7 h ed.; Imp. JF: Mon pellie , F ance, 2000.
43.
Boso, S.; San iago, J.L.; Villa e de-Alonso, V.; Gago, P.; Ma
í
nez, M.C.; Rod
í
guez, E. E aluaci
ó
n de la
incidencia a en e medades
ú
ngicas en di e en es clones del c . Alba iño (Vi is ini e a L.). Phy oma
2009
,210,
1–5.
44.
D
í
az, M.R.; Iglesias, I.; Ja o, M.V. Ai bo ne concen a ions o Bo y is,Uncinula and Plasmopa a spo es in a
ineya d in Lei o-Ou ense (N.W. Spain). Ae obiologia 1997,13, 31–35. [C ossRe ]
45.
D
í
az, M.R.; Iglesias, I.; Ja o, M.V. Seasonal a ia ion o ai bo ne ungal spo e concen a ions in a ineya d o
No h-Wes Spain. Ae obiologia 1998,14, 221–227. [C ossRe ]
46.
Oli ei a, M.; Gue ne -Mo ei a, J.; Mesqui a, M.M.; Ab eu, I. Impo an phy opa hogenic ai bo ne ungal
spo es in a u al a ea: Incidence o Bo y is cine ea and Oidium spp. Ann. Ag ic. En i on. Med.
2009
,16,
197–204.
47.
Rod
í
guez-Rajo, F.J.; Seijo Coello, M.C.; Ja o, V. Es udio de los ni eles de los p incipales i opa
ó
genos pa a
la op imizaci
ó
n de cosechas de Vi is ini e a en Valdeo as Ou ense (1998). Bo anica Complu ensis
2002
,26,
121–135.
48.
Fe n
á
ndez-Gonz
á
lez, M.; Rod
í
guez Rajo, F.J.; Ja o, V.; Ai a, M.J.; Ribei o, H.; Oli ei a, M.; Ab eu, I.
Fo ecas ing ARIMA models o a mosphe ic ineya d pa hogens in Galicia and No he n Po ugal: Bo y is
cine ea spo es. Ann. Ag ic. En i on. Med. 2012,19, 255–262. [PubMed]
49.
Ma
í
nez, C.; Boso, S. E aluaci
ó
n de la Vi ulencia de Dis in as Poblaciones de Hongos Responsables del Mildiu, o
í
dio
y Bo y is en Dis in as Denominaciones de O igen Gallegas; G upo de Vi icul u a de la MBG–CSIC: Pon e ed a,
Spain, 2015.
50.
Co iñas, J.A.; Ai a, M.J.; Fe n
á
ndez–Gonz
á
lez, M.; Rod
í
guez-Rajo, F.J.; V
á
zquez–Ruiz, R.A. Po en ial
sus ainable wine–g owing model in he Ribei a Sac a D.O. (NW Spain). Cienc. Tec. Vi i inic.
2018
,33,
114–145.
51.
La o e, B.A.; Rioja, M.E. E ec o de la empe a u a y humedad ela i a sob e la ge minaci
ó
n de conidias de
Bo y is cine ea.Cien. In . Ag ic. 2001,29, 67–72.
52.
Moli o , D.; Baus, O.; Ho mann, L.; Beye , M. Me eo ological condi ions de e mine he he mal- empo al
posi ion o he annual Bo y is bunch o epidemic on Vi is ini e a L. c . Riesling g apes. OENO One
2016
,50,
231–234. [C ossRe ]
53.
Kelle , M.; Vi e , O.; Cole, M. Bo y is cine ea in ec ion in g ape lowe s: De ense eac ion, la ency and disease
exp ession. Phy opa hology 2003,93, 316–322. [C ossRe ]
54.
Vi e , O.; Kelle , M.; Jaudzems, V.G.; Cole, F.M. Bo y is cine ea in ec ion o g ape lowe s: Ligh and elec on
mic oscopical s udies o in ec ion si es. Phy opa hology 2004,94, 850–857. [C ossRe ]
55.
La o e, B.A.; Rioja, M.E.; Lillo, C. E ec o de la empe a u a en el desa ollo de la in ecci
ó
n p oducida po
Bo y is cine ea en lo es y bayas de u a de mesa. Cien. In . Ag ic. 2002,29, 145–151. [C ossRe ]
56.
Cilibe i, N.; Fe maud, M.; Languasco, L.; Rossi, V. In luence o ungal s ain, empe a u e, and we ness
du a ion on in ec ion o g ape ine in lo escences and young be y clus e s by Bo y is cine ea.Phy opa hology
2015,105, 325–333. [C ossRe ]
57.
Calonnec, A.; Ca ola o, P.; Poupo , C.; Dubou dieu, D.; Da ie , P. E ec s o Uncinula neca o on he yield
and quali y o g apes (Vi is ini e a) and wine. Plan Pa hol. 2004,53, 434–445. [C ossRe ]
58.
Campbell, P.; Bendek, C.; La o e, B.A. Risk o powde y mildew (E ysiphe neca o ) ou b eaks on g ape ines
in ela ion o clus e de elopmen . Cien. In . Ag ic. 2007,34, 5–11. [C ossRe ]
59.
Fe n
á
ndez-Gonz
á
lez, M.; Piña–Rey, A.; Gonz
á
lez–Fe n
á
ndez, E.; Ai a, M.J.; Rod
í
guez-Rajo, F.J.
Fi s assessmen o Goidanich Index and ae obiological da a o Plasmopa a i icola in ec ion isk managemen
in no h-wes Spain. J. Ag ic. Sci. 2019,157, 129–139. [C ossRe ]
60.
Thind, T.S.; A o a, J.K.; Mohan, C.; Raj, P. Epidemiology o powde y mildew, downy mildew and an h acnose
diseases o g ape ine. In Diseases o F ui s and Vege ables Volume I; Sp inge : Do d ech , The Ne he lands,
2004; pp. 621–638.
Ag onomy 2020,10, 219 18 o 18
61.
Chellemi, D.O.; Ma ois, J.J. E ec o ungicides and wa e on spo ula ion o Uncinula neca o .Plan Dis.
1991
,
75, 455–457. [C ossRe ]
62.
Si apalan, A. E ec s o impac ing ain d ops on he g ow h and de elopmen o powde y mildew ungi.
Plan Pa hol. 1993,42, 256–263. [C ossRe ]
63.
Ja is, W.R.; Guble , W.D.; G o e, G.G. Epidemiology o Powde y Mildews in Ag icul u al Pa hosys ems.
In The Powde y Mildews: A Comp ehensi e T ea ise; B
é
lange , R.R., Bushnell, W.R., Dik, A.J., Ca e , T.L.W.,
Eds.; Ame ican Phy opa hological Socie y, APS P ess: S . Paul, MN, USA, 2002; pp. 169–199.
64.
Campbell, P. E ec o de Fac o es Ambien ales y M
é
odos de Con ol Sob e la Ge minaci
ó
n y Desa ollo de
Uncinula neca o en Vi is ini e a. Mas e ’s Thesis, Facul ad de Ag onom
í
a e Ingenie
í
a Fo es al, Uni e sidad
Ca ólica de Chile, San iago, Chile, 2003.
65.
Almend o, J.P.
Í
ndices clim
á
icos p opios de la id en el sec o cen al de ie a de ba os. In Ac as de las IV
Jo nadas de His o ia de Almend alejo y Tie a de Ba os; Asociaci
ó
n His
ó
ica de Almend alejo: Almend alejo,
Spain, 2013; pp. 121–131.
66.
Thiessen, L.D.; Thiessen, L.; Neill, T.M.; Maha ee, W.F. Assessmen o E ysiphe neca o ascospo e elease
models o use in he Medi e anean clima e o Wes e n O egon. Plan Dis.
2018
,102, 1500–1508. [C ossRe ]
67.
Maga ey, P.A.; Maga ey, R.D.; Emme , R.W. P inciples o managing he oliage diseases o g ape ine wi h
low inpu o pes icides. In P oceedings o he 6 h In e na ional Cong ess on O ganic Vi icul u e, Basel,
Swi ze land, 25–26 Augus 2000; p. 140.
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