154 Alternative fungicides for Botrytis cinerea Australian Journal of Grape and Wine Research 16, 154–172, 2010

Review: Alternatives to synthetic fungicides for Botrytis cinerea

management in vineyards
M.A. JACOMETTI,1 S.D. WRATTEN1 and M. WALTER2
1
Bio-Protection Research Centre, PO Box 84, Lincoln University, Canterbury 7647, New Zealand
2
Plant & Food Research, PO Box 51, Lincoln, New Zealand
Corresponding author: Dr Marco Jacometti, fax + 64 3 325 3696, email: marco.jacometti@lincoln.ac.nz

Abstract
Botrytis cinerea (Pers.: Fr), the causal agent of botrytis bunch rot, is an important disease of grapevines
worldwide, with canopy management and the prophylactic use of fungicides being the most common
control methods. The latter has resulted in fungicide resistance and is increasingly raising concerns
regarding residues in wine and effects on human and environmental health. Research-led alternatives to
this practice are beginning to emerge, including a range of biotic and abiotic treatments that induce vine
resistance to B. cinerea and inundative applications of biological control agents such as Trichoderma,
Bacillus, Ulocladium and Streptomyces species. Also, habitat manipulation techniques that aim to improve
the effectiveness of naturally occurring biological control are being developed using mulches brought into
the vineyard, as well as mulched cover crops. These can accelerate decomposition of botrytis mycelium
and sclerotia on the vineyard floor in winter. The challenges of these different techniques and the
prospects for habitat manipulation for this fungal disease are discussed. Extensive tables on synthetic
fungicides, biofungicides, essential oils and plant extracts effective against B. cinerea are included.

Keywords: biological control, Botrytis cinerea, habitat manipulation, induced resistance,

mulch, sustainable viticulture

Botrytis cinerea – epidemiology and current
control practices _67 154..172
Botrytis bunch rot, caused by Botrytis cinerea (Pers.: Fr), is
an important disease of grapevines in temperate climates
worldwide and can cause extensive economic losses
through grape desiccation, rot and biochemical changes
that reduce wine quality (Mullins et al. 1992). The patho-
gen overwinters as mycelium or sclerotia on dead canes,
or as mycelium in cane inner bark, dormant buds, mum-
mified berries, rachides, tendrils or other plant debris on
the vineyard floor, as well as on necrotic tissues of other
plant species (Elmer and Michailides 2004). In spring,
under favourable environmental conditions (15–20°C,
95% relative humidity [RH]), large numbers of conidia
are produced on this debris and are dispersed by wind and
water into the grapevine (Pearson and Goheen 1988).
These spores can travel long distances, but in vineyards,
95% of spores travel less than 1 m from the ground
source (Seyb 2004).
The vine tissues most vulnerable to early-season infec-
tion are flowers and young shoots, and leaves (McClellan
and Hewitt 1973, Nair and Hill 1992, Nair et al. 1995),
but the spread of early-season infections in the grapevine
is usually limited because of heightened physical and
chemical defence systems (Nicholas et al. 1994) which
stimulate the pathogen to become latent in the host tissue
(Williamson 1994). Senescing floral tissues are highly
doi: 10.1111/j.1755-0238.2009.0067.x
© 2009 Australian Society of Viticulture and Oenology Inc.
susceptible to the disease (Keller et al. 2003) and are
often a source of secondary infections (Nair and Hill 1992,
Seyb 2004). These tissues can become a major source of
infection as grape bunches develop (Seyb 2004), espe-
cially post-veraison when bunch humidity (Mullins et al.
1992) and sugar concentrations increase (Elmer and
Michailides 2004), and concentrations of anti-fungal
compounds decrease in berries (Bavaresco et al. 1997).
Bunch infection is heightened by rain (Gubler et al. 1987)
and berry damage, the latter allowing B. cinerea to bypass
a suite of biophysical and biochemical barriers in the plant
(Webber and Gibbs 1989). Berry damage can be caused by
a range of edaphic events, such as frost, hail, wind-blown
sand (Nair and Hill 1992) or excessive rain, which can
cause berry split (Elmer and Michailides 2004), or biotic
events, such as damage by birds, snails, plant pathogens
and insects (Elmer and Michailides 2004), the latter of
which can also vector B. cinerea spores, either on their
bodies or in their faeces (Fermaud and Le Menn 1992,
Fermaud and Gaunt 1995, Louis et al. 1996).
Botrytis cinerea infection creates several biochemical
changes in the juice that alter the flavour, odour and clarity
of the wine. The most important of these changes is the
production of laccases (phenol oxidases), which reduce
wine clarity and oxidise other compounds in the wine that
contribute to the appearance, taste, mouth-feel, fragrance
and antimicrobial properties of the wine (Jackson 1994c).
Jacometti et al. Alternative fungicides for Botrytis cinerea 155

Habitat Manipulation
Mulches Fertilisation rate Plant Defence Stimulants:
Cover crops Irrigation rate Plant hormones
Soil management Trellis Design Abiotic stimulants
Leaf Trimming/thinning Plant extracts
Grape variety Compost extracts
Rootstock

B. cinerea Vine Vigour Vine Resistance:

primary
inoculum
Æ Chemical
Resistance
Canopy humidity Frost B
Physical resistance
Bunch humidity Hail e
Wind-blown sand r
Berry split r
Birds y Figure 1. Viticultural inputs
Snails that influence Botrytis cinerea
Pathogens D
a
development in grape vines,
m modified from Jackson and
a Lombard (1993)
g
Insects e

B. cinerea development in vines VECTOR

Synthetic
Elemental (eg. Bordeaux)
Bacterial toxins (eg. Bt)
Plant toxins (eg. Pyrethrum) Biofungicide
Mineral oils (eg. Stylet-OilTM)
Plant oils (eg. Thyme)
Animal oils (eg. Fish)
Fungicides

The presence of laccases limits the use of thermovinifica-
tion, a technique used to release anthocyanins from the
grape skin, which enhances wine colour, especially in
delicate varieties such as Pinot noir (Jackson 1994b).
Laccases are readily soluble, so are not easily removed
through most clarification techniques. An exception being
ultrafiltration (0.2–0.05 mm nominal pore size), which is
avoided by makers of premium wine because of loss of
important pigments and tannins in red wines (Cattaruzza
et al. 1987) and a perceived loss of flavour, although there
is little experimental evidence for this (Jackson 1994d).
Botrytis cinerea is most commonly managed through a
variety of cultural techniques that reduce canopy humid-
ity and inoculum sources (Figure 1) and through the
use of synthetic fungicides (Rosslenbroich and Stuebler
2000). Synthetic fungicides affect various aspects of
pathogen development and comprise up to ten chemical
groups (Young 2008) (Table 1). They are broadly categor-
ised into two main classes: systemic and contact. Systemic
fungicides do not require contact with the pathogen as
they are absorbed and translocated through the plant,
whereas contact fungicides require direct contact and
therefore good spray coverage and penetration into the
canopy are required for effective control (Brink et al.
© 2009 Australian Society of Viticulture and Oenology Inc.
2007). Most fungicide groups are highly restricted or
unavailable to the grape industry because of fungal resis-
tance (Pappas 1997, Wilson et al. 1997, Leroux 2004),
public concerns about the possible effects of synthetic
chemicals on human health (Becker and Schwinn 1993,
Fokkema 1993, Johnson 1994, Elmer and Michailides
2004, Farquhar et al. 2009) and environmental pollution
(Howell 2001, Elmer and Michailides 2004). Conse-
quently, viticulturalists are beginning to require alterna-
tives for disease management. These have been most
readily adopted in organic viticulture, as the use of
synthetic fungicides is prohibited in this sector of the
industry.
The most commonly used products in organic viticul-
ture have been two copper-containing compounds: Bor-
deaux mixture (copper sulphate and hydrated lime) and
copper sulphate (Jackson 2008b), but copper is now
avoided by many viticulturalists (Darriet et al. 2001). This
is because it can reduce concentrations of important
varietal aroma compounds of wine, alter wine flavour
(Jackson 2008e) and can augment hydrogen sulphide
accumulation, which can cause off-odours in wine
(Darriet et al. 2001, Jackson 2008b). Copper can also be
phytotoxic (Rathore and Khan 2000) and can accumulate
 156

Table 1. The New Zealand trade names, active ingredients, chemical group, mode of action, application information for grapes and risk of resistance of synthetic fungicides
used in the management of Botrytis cinerea in New Zealand. All information in this table has been sourced from Young (2008).

New Zealand trade names Active ingredients Chemical Properties/mode of action Application Withholding Resistance
group period (days)

Amistar WG
Captan 80W, Captan Flo, Merpan
Addstem, Agpro Carbendazim, Chief,
Goldazim 500SC, MBC 500 Flo,
MBC 50 WP, MBC 800 WDG,
Prolific, Protek, X-Spore, Zelam
Carbendazim, Topsin M-4 A
Azoxystrobin Strobilurin Broad spectrum, systemic 10 to14-day intervals from early flowering 14 High risk
translaminar, anti-sporulant to preharvest.
Captan Cyclic imide Broad spectrum 10 to 14-day intervals from when shoots 21 High risk
are 5–8 cm long to harvest.
Carbendazim (Addstem and Benzimidazole Broad spectrum, systemic one application between flowering and 7 High risk
MBC 500 also contain harvest.
ethylene glycol and
Prolific formaldehyde)
Tiophanate methyl Benzimidazole Broad spectrum, systemic one application between flowering and 7 High risk
harvest.
Alternative fungicides for Botrytis cinerea

Balear 500SC, Barrack 720, Chlorothalonil (Balear also contains Chloro nitrile Protectant 10 to 14-day intervals from bud burst. 28 Low risk
Barrachlor 720, Barrier, Blizzard, ethylene glycol and Max Cl
Bravo Weatherstick, Cavalry, mancozeb)
Chlorotek, Elect 750 SC, Harrier,
Max CL
Defence 500, Fortify, Hawk, Ippon Iprodione Dicarboximide Broad spectrum, contact 1–2 times between veraison and harvest. 1 High risk
500 SC, Rapid 500, Rovral Flo,
Rovral Gold
Euparen Multi Tolyfluanid Sulphamide Broad spectrum, contact, protectant one application at 5% and 80% flowering. Do not apply after High risk
flowering
Pyrus 400SC, Scala Pyrimethanil Anilinopyrimidine Specific botrycide, contact, Apply at flowering, pre-bunch closure, 7 High risk
translaminar and fumigant, verasion and pre-harvest. No more than
protectant. two applications per season.
Shirlan Fluazinam Pyridinamine Narrow spectrum, protectant. Apply at early and late flowering, pre- 28 High risk
bunch closure, and verasion.
Switch Cyprodinil and Anilinopyrimidine Botrycide, protectant and systemic Apply at 5% flowering, 80% flowering or Do not apply after High risk
flodioxonil and phenylpyrrole action, inhibits spore germination, pre-bunch closure. No more than two pre-bunch closure
penetration of germ tube and applications per season.
mycelial growth.
Teldor Fenhexamid Hydroxyanilide Specific botrycide, protectant, inhibits Apply at pre-bunch closure and verasion, 21 Medium risk
germ tube and mycelium growth. or, verasion and 14 days after verasion.
No Fungus Thiram, Thiram 40 F, Thiram Disulphide Broad spectrum, multi-site action, 10 to 14-day intervals from budburst to 7 Low risk
Thiram DF contact fungicide harvest, application closer than 3 weeks
before harvest may affect fermentation.

© 2009 Australian Society of Viticulture and Oenology Inc.

Australian Journal of Grape and Wine Research 16, 154–172, 2010
Jacometti et al.
in agricultural soils (Rathore and Khan 2000, Jackson
2008d), resulting in leaf chlorosis in vines (Jackson
2008d) and decreased soil biological activity (Parat et al.
2002). B. cinerea can develop resistance to copper under
laboratory conditions (Parry and Wood 1958), but there
appear to be no instances of B. cinerea resistance to copper
in vineyards. Despite this, the above environmental and
wine quality concerns have led to a movement away from
copper-based fungicides in viticulture (Jackson 2008b).
With the loss of many synthetic fungicides and
copper-containing products, conventional and organic
growers are seeking alternatives to manage B. cinerea. This
review will discuss alternative techniques and products
for B. cinerea management in vineyards and will focus on
biological control, essential oils, habitat manipulation and
various biotic and abiotic compounds that induce vine
resistance to B. cinerea. Information on the effects of
animal oils (e.g. fish oils) on the suppression of B. cinerea
is largely anecdotal, and so is not included in this review.
Alternatives to fungicides
Biological control
There are three main types of biological control: classical,
inundative and conservation. Classical biological control
has been defined by Eilenberg et al. (2001) as ‘The inten-
tional introduction of an exotic, usually co-evolved, biological
control agent for permanent establishment and long-term pest
control’. Because of the widespread occurrence of B.
cinerea (Pearson and Goheen 1988), its rapid growth rate
and the low rates of parasitism commonly observed (Elad
and Stewart 2004), classical biological control agents
(BCAs)have not been extensively researched for this
disease. In contrast, inundative biological control, defined
by Eilenberg et al. (2001) as ‘The use of living organisms to
control pests when control is achieved exclusively by the released
organisms themselves’ is the dominant method (Elmer and
Michailides 2004, Williamson et al. 2007). No research
appears to have been published on B. cinerea in grapes
using conservation biological control, defined by Eilen-
berg et al. (2001) as the ‘Modification of the environment or
existing practices to protect and enhance specific natural enemies
or other organisms to reduce the effect of pests’.
Inundative biological control usually involves the
mass-release of a BCA and can be effective in suppressing
B. cinerea in grapes (Schilder et al. 2002) and other crops
(Ingram and Meister 2006). These organisms can operate
through one or a combination of mechanisms, either
directly, through parasitism (Wisniewski et al. 1991, Elad
1995, Howell 2003) or attachment to B. cinerea surfaces
(Wisniewski et al. 1991, Elad 1996), or indirectly through
competition (Blakeman 1993, Elad et al. 1994, Elad
1996), induction of plant disease resistance (Korolev et al.
2008), production of inhibitory compounds (Nelson and
Powelson 1988, Edwards and Seddon 1992) or alteration
of the local environment’s physical properties (Edwards
and Seddon 1992). An example of the latter is the ability
of Bacillus brevis (Migula) to reduce the wetability of
Chinese cabbage and therefore restrict the period suitable
for B. cinerea infection (Edwards and Seddon 1992). These
© 2009 Australian Society of Viticulture and Oenology Inc.
Alternative fungicides for Botrytis cinerea 157
mechanisms can suppress B. cinerea through reducing its
saprophytic ability (Zimand et al. 1996), spore production
(Morandi et al. 2000) and virulence (Elad and Freeman
2002).
Improvements to inundative biological control have
been achieved through the use of mixtures of BCAs or
multiple isolates of the same BCA (Elad et al. 1998,
Guetsky et al. 2001). These different organisms can target
different stages of the B. cinerea lifecycle (Elad et al. 1994)
or occupy different environmental niches (Janisiewicz
1996), which improves the range of climatic conditions
under which they are effective (Elmer and Michailides
2004). Improvements in the substrate in which the BCA
is stored and applied has increased product shelf life, ease
of application and longevity in the field (Kolombet et al.
2008), all of which have improved BCA efficacy (Elmer
and Reglinski 2006). Formulations can be in the form of
dusts, granules, pellets, prills, wettable powders, emulsi-
fiable liquids or gels (Vidhyasekaran 2004). Once regis-
tered, these products are often called ‘biofungicides’ (Lee
et al. 2006), several of which are registered for B. cinerea
management in grapes in New Zealand (Table 2).
Biological control agents of B. cinerea are most com-
monly filamentous fungi from the genera Trichoderma,
Ulocladium and Gliocladium, bacteria from the genera
Bacillus and Pseudomonas and yeasts from the genera Pichia
and Candida (Elmer and Michailides 2004), the most well-
studied of which are Trichoderma fungi (Vinale et al.
2008). Biofungicides are predominantly preventative
treatments and are generally not effective post-infection
(Whipps and Lumsden 2001) so need to be applied when
climatic conditions are conducive to vine colonisation by
the BCA, before periods of high vine vulnerability, such as
flowering and leaf plucking/trimming, and after veraison
(Whipps and Lumsden 2001). This need for BCA coloni-
sation requires certain climatic conditions, and variation
in these conditions reduces efficacy (Elad and Stewart
2004). For this reason, biological control is inherently
less consistent than synthetic fungicides (Elmer and
Michailides 2004, Elmer and Reglinski 2006). Also, in
contrast to systemic fungicides, most biofungicides require
contact with the pathogen, so disease-control efficacy is
commonly reduced after bunch closure, when penetra-
tion of the biofungicide becomes inefficient. After this
time, the biological control agent is unlikely to persist
inside the bunch until harvest (Holz and Volkmann
2002), when grapes are most susceptible to infection
(Nicholas et al. 1994). This drop in efficacy after bunch
closure has created interest in microbially induced disease
response in plants, a systemic mechanism in which BCAs
can suppress plant pathogens without direct contact and a
useful method to suppress latent infections (see Microbial
induction).
The lack of field consistency of biofungicides has been
a major hurdle in the adoption of this technology, but
these products can be used effectively in conjunction with
other techniques, including synthetic fungicides (Jackson
2008b). Biofungicides have a minimal impact on vine
physiology and leave no chemical residues in wine,
although little consideration has been paid to the concen-
158 Alternative fungicides for Botrytis cinerea Australian Journal of Grape and Wine Research 16, 154–172, 2010

Table 2. The organism, selected trade names and documented modes of action of biofungicides that can suppress
Botrytis cinerea in grapes.

Organism Selected trade names Documented modes of action

Filamentous fungi and oomycetes

Ampelomyces quisqualis
Gliocladium catenulatum
Pythium oligandrum
Trichoderma atroviride
Trichoderma harzianum
Trichoderma harzianum and
Trichoderma polysporum
Trichoderma harzianum and
Trichoderma viride
Trichoderma viride
Trichoderma virens
Ulocladium oudemansi
Yeasts
Candida oleophila
Candida saitoana
Cryptococcus albidus
Metschnikowia fructicola
Saccharomyces chevalieri
Bacteria
Bacillus subtilis
Pseudomonas fluorescens
Pseudomonas syringae
Streptomyces griseoviridis
AQ10 (Vidhyasekaran 2004)
PrimaStop, PreStop (Vidhyasekaran 2004)
Polygandron (Mohamed et al. 2007; Vidhyasekaran
2004)
Sentinel*‡ (Young 2008)
Harzian 10, Harzian 20, F-stop, Plantsheild,
Rootshield, Supraavit, T2, T-22G, T-22B, T-35,
Topshield, Trichodermin, Trichodex (Elad 2000;
Harman et al. 1996); Utkhede and Mathur 2002;
Vidhyasekaran 2004)
Binab (Vidhyasekaran 2004)
Trichodowels, Trichoject, Trichopel, Trichoseal
(Calderon et al. 1993; Vidhyasekaran 2004)
Bip T, Trichopulvin (Elmer and Reglinski 2006;
Sesan et al. 1999; Vidhyasekaran 2004)
GlioGard and SoilGard (Harman et al. 1996;
Vidhyasekaran 2004)
Botry-Zen*§ (Young 2008)
Aspire (Saligkarias et al. 2002)
Bio-Coat†, Biocure† (Schena et al. 2004) in (Elmer
and Reglinski 2006)
Yeild Plus (Helbig 2002)
Shemer† (Karabulut et al. 2004; Kurtzman and
Droby 2001)
Saccharopulvin (Sesan et al. 1999)
Bactophyt, Epic, (BM 1600), Kodiak, Serenade
Max*¶, System 3 (GBO3) (Vidhyasekaran 2004;
Young 2008)
BioCoat, Conqueror (Trotel-Aziz et al. 2008;
Vidhyasekaran, 2004)
Bio-save (Elmer and Reglinski 2006; Long et al.
2005)
Mycostop (Vidhyasekaran 2004; White et al. 1990)
Parasitism (Morando et al. 2000)
Antibiosis (Machowicz-Stefaniak 1998)
Parasitism, induces host defences (Vidhyasekaran
2004)
Competitive exclusion (Young 2008)
Competitive exclusion, antibiosis, enzyme
interruption, induces host defences
(Vidhyasekaran 2004)
Competitive exclusion, antibiosis, enzyme
interruption, induces host defences
(Vidhyasekaran 2004)
Competitive exclusion, antibiosis, enzyme
interruption, induces host defences
(Vidhyasekaran 2004)
Induces host defences (Calderon et al. 1993)
Mycoparasite, (Baek et al. 1999), induces host
defences (Howell et al. 2000)
Competitive exclusion (Young 2008)
Competitive exclusion (Mercier and Wilson 1994)
Parasitism, antibiosis and induces host defences
(Ahmed et al. 1998)
Parasitism (Elad 1996)
Competitive exclusion (Blachinsky et al. 2007;
Kurtzman and Droby 2001)
Antagonism, prevents spore germination, germ tube
elongation and germ tube penetration.
(Vidhyasekaran 2004)
Induces host defences, antibiosis (Vidhyasekaran
2004)
Induces host defences, antibiosis (Elad and Stewart
2004)
Parasitism (Tapio and Pohtolahdenpera 1991)

*Registered for use on B. cinerea in grapes in New Zealand.

†Post harvest.
‡Apply at flowering, pre-bunch closure, verasion and pre-harvest.
§Apply early and late bloom, at pea-size berry stage and bunch closure.
¶Apply 7 to 10-day intervals early in the season, don’t apply at flowering.

trations of mycotoxins that are likely to persist in wine,
and what impact these toxins can have on human health
(Jackson 2008b). Despite improvement in biofungicides
and increasing evidence that they can be used in conjunc-
tion with other techniques, many viticulturalists still
regard them as inferior products (Elmer and Reglinski
2006). These growers are likely to adopt these products
only through the withdrawal of synthetic fungicides
(Elmer and Reglinski 2006). In contrast, other growers
see these products as a viable alternative to synthetic
fungicides and are trialling and adopting these products in
commercial vineyards (Elmer and Michailides 2004).
© 2009 Australian Society of Viticulture and Oenology Inc.
Jacometti et al. Alternative fungicides for Botrytis cinerea 159

Oils carcinogenic compounds, but both at sufficiently low

Essential oils. Essential (volatile or ethereal) oils are the
concentrated oils of plants that contain volatile aroma
compounds. These oils naturally contain bioactive com-
pounds that can effectively manage B. cinerea (Table 3),
but the concentrations required to be effective are often
toxic to the plant (Walter et al. 2001, Plotto et al. 2003) or
leave residues (Elmer and Reglinski 2006), the latter of
which can alter the taste and odour of grapes and wine
(Redl and Bauer (1990) in Jackson (2008b)). Many
essential oils have been shown to be effective at inhibiting
B. cinerea in vitro (Walter et al. 2001, Bouchra et al. 2003,
Daferera et al. 2003, Tegegne and Pretorius 2007), but to
the authors’ knowledge, thyme oil (Thymus capitatus (L.))
and massoialactone, derived from the bark of the tree
Cryptocarya massoia, are the only essential oils to have
inhibited B. cinerea infection in grape bunches and in
leaves in planta (Walter et al. 2001). In this work, pre-
inoculated bunches and leaves were submersed in a
0.33% essential oil emulsion at veraison, a method that
ensured complete penetration of the oil into the bunch
and leaf surface but not representative of the penetration
or coverage achieved with standard spray equipment. The
following year, the same emulsion was sprayed into the
canopy at 8 to 10-day intervals from flowering to harvest.
This treatment was effective at inhibiting B. cinerea in
leaves and bunches, but was phytotoxic in bunches,
which caused bunch thinning, thereby changing bunch
architecture and reducing bunch humidity, an effect that
may have confounded the observed suppression of the
pathogen.
There has been little consideration of the health effects
of residues left by essential oils in wine, especially
products derived from non-food plants. Gold et al.
(1992) extensively compared plant-based and synthetic
pesticides and found them to contain equal levels of
levels to be deemed safe. Until the issues of safety, phy-
totoxicity and alterations in flavour and odour in wine
are resolved, these products cannot be seen as an effective
alternative to conventional botryticides.
Mineral oils
Mineral (white or paraffin) oils can be effective at sup-
pressing B. cinerea (Dell et al. 1998) and other plant dis-
eases (Beattie et al. 2002). Applications of these oils are
effective at low dosages because of their excellent spread-
ing and sticking properties (Calfouzos 1966) and, if highly
refined, are quite disease-specific (Northover and Timmer
2002). If applied at high concentrations, they can have
phytotoxic impacts on crops, especially if less refined oils
are used (Northover and Timmer 2002). One of the most
commonly used commercial products, JMS Stylet-OilTM
(JMS Flowers Farms, Inc., Vero Beach, Florida, USA), is a
highly refined mineral oil with an unsulphonated residue
of 99.1% (Dell et al. 1998). It has been demonstrated to
be effective for the control of powdery mildew and B.
cinerea in grapevines (Dell et al. 1998), both on its own
and in combination with synthetic fungicides, including
benzimidazole, dicarboximide (Bourbos et al. 1994) and
iprodione (Dell et al. 1998). The use of Stylet-OilTM oil
with these fungicides improved B. cinerea suppression
compared with the fungicide products used alone. Stylet-
OilTM does, however, have the potential to reduce photo-
synthesis, decrease the accumulation of soluble solids in
grape (Finger et al. 2002) and alter wild yeast populations
on grape clusters (W. D. Gubler, unpublished data, cited
in Dell et al. 1998). Another mineral oil, marketed under
the name ‘Ultra Fine Sun Spray’, can be mixed with
sodium bicarbonate to provide control of powdery

Table 3. A list of some of the essential oils tested against Botrytis cinerea, the level of control obtained, the medium it
was tested on and the target of inhibition.

Species Common name† Level of Medium‡ Target of Reference¶,††

control obtained inhibition§

Aegle marmelos L. Bael High GM M 8

Ageratum conyzoides L. Billygoat-weed, chick weed, Moderate GM M 8
goatweed, whiteweed
Ammomum subulatum Roxb. Big cardamom Moderate GM M 8
Anethum graveolens L. Dill High GM M, G 3, 6
Azadirachta indica A. Neem tree Moderate GM M 8
Caesulia axillaries Roxb. NA Very high GM M 8
Callistemon lanceolatus DC. Bottlebrush, red bottlebrush bush Low GM M 8
Chenopodium ambrosioides L. Epazote, wormseed, Jesuit’s tea, Very high GM M 8
Mexican tea
Cinnamomum zeylanicum L. Cinnamon Very high V G 11
Citrus medica L. Citron Low GM M 8
Citrus reticulata L. Mandarin, satsuma Low GM M 8
Coriandrum sativum L. Coriander High V M 6

© 2009 Australian Society of Viticulture and Oenology Inc.

160 Alternative fungicides for Botrytis cinerea Australian Journal of Grape and Wine Research 16, 154–172, 2010

Table 3. Continued

Species Common name† Level of Medium‡ Target of Reference¶,††

control obtained inhibition§

Cryptocarya massoia L. Massoi Very high Pg S 1, 10

Cuminum cyminum L. Cumin High GM M 3
Cymbopogon citrates DC. Citronella grass, lemongrass Very high GM, V M, S, G 6, 8, 9
Cymbopogon martini Stapf Palmarosa Very high V G 11
Elettaria cardamomum Maton. Cardamomum green High GM M 8
Eucalyptus citriodora Hook. Lemon-scented gum, spotted gum, Very high GM M 8
lemon eucalyptus
Eupatorium cannabinum L. Hemp-agrimony, hemp agrimony Very high GM M 8
Foeniculum vulgare Mill. Fennel Very high V, GM M, G 5, 7
Heteranthemis viscidehirta Schott. Sticky oxeye Very high GM M 3
Hyptis suaveolens L. Pignut Low GM M 8
Jasminum grandiflorum L. Catalonian jasmine, Spanish jasmine, Moderate GM M, G 1
royal jasmine
Laurus nobilis L. Bay laurel, bay leaf, true laurel, High GM M 3
laurel, sweet bay
Lavandula angustifolia L. Common lavender, English lavender, Moderate GM M 1, 4
true lavender
Lawsonia inermis L. Henna, hina Very high GM M 8
Leptospermium scoparium Forst Manuka, tea tree Moderate GM M, G 1
Lippia alba Mill N. B. Bushy lippia, verbena white, white Low GM M 8
lippia
Melaleuca alternifolia L. Narrow-leaved paperbark, narrow- Moderate GM, V M, G 1
leaved tea-tree, narrow-leaf
ti-tree, snow-in-summer
Melaleuca leucodendron L. Cajaput Low GM M 8
Mentha cardiaca L. Spearmint, scotch spearmint Very high GM M, G 6
Mentha poperita L. Peppermint High V G 11
Mentha pulegium L. Pennyroyal Moderate GM M 2, 4
Mentha spp. Mint Very high V G 7
Murraya koenigii L. Curry Tree, curry-leaf tree, kadipatta, High GM M 8
karivepallai
Nepeta hindostana Roth Haines Cal mint Moderate GM M 8
Ocimum basilicum L. (cv.) Cinnamon basil High GM M, G 6
Ocimum basilicum L. Basil, basilico, bush basil, common High GM, V M, G 6, 7, 8
basil, sweet basil, wild basil.
Ocimum canum Sims Hairy basil Very high GM M 8
Ocimum gratissimum L. African basil Very high GM M 8
Ocimum sanctum L. Holy basil Very high GM, Pg M, G 8
Origanum dictamnus L. Dictamnus Very high GM M 4
Origanum majorana L. Marjoram High GM M 4
Origanum vulgare L. Oregano Very high GM, V, Pt M, G 2, 4, 6, 11
Pelargonium roseum Willd. Rose geranium Very high V G 7
Pimpinella anisum L. Aniseed, anise Very high V G 7
Prostanthera rotundifolia R. Br. Australian mint, native mint, High GM M, G 1
roundleaf mint bush
Prunus persica L. peach Very high GM, Pg M, G 8
Rosa spp. Bois de rose Moderate GM M, G 1
Rosmarinus officinalis L. Rosemary Low GM M 1, 4, 6
Salvia fruticosa L. Greek sage Moderate GM M 4, 5
Lavandula angustifolia L. Common lavender, English lavender, Moderate GM M 1, 4
true lavender

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Jacometti et al. Alternative fungicides for Botrytis cinerea 161

Table 3. Continued

Species Common name† Level of Medium‡ Target of Reference¶,††

control obtained inhibition§

Lawsonia inermis L. Henna, hina Very high GM M 8

Leptospermium scoparium Forst Manuka, tea tree Moderate GM M, G 1
Lippia alba Mill N. B. Bushy lippia, verbena white, white Low GM M 8
lippia
Melaleuca alternifolia L. Narrow-leaved paperbark, narrow- Moderate GM, V M, G 1
leaved tea-tree, narrow-leaf
ti-tree, snow-in-summer
Melaleuca leucodendron L. Cajaput Low GM M 8
Mentha cardiaca L. Spearmint, scotch spearmint Very high GM M, G 6
Mentha poperita L. Peppermint High V G 11
Mentha pulegium L. Pennyroyal Moderate GM M 2, 4
Mentha spp. Mint Very high V G 7
Murraya koenigii L. Curry Tree, curry-leaf tree, kadipatta, High GM M 8
karivepallai
Nepeta hindostana Roth Haines Cal mint Moderate GM M 8
Ocimum basilicum L. (cv.) Cinnamon basil High GM M, G 6
Ocimum basilicum L. Basil, basilico, bush basil, common High GM, V M, G 6, 7, 8
basil, sweet basil, wild basil.
Ocimum canum Sims Hairy basil Very high GM M 8
Ocimum gratissimum L. African basil Very high GM M 8
Ocimum sanctum L. Holy basil Very high GM, Pg M, G 8
Origanum dictamnus L. Dictamnus Very high GM M 4
Origanum majorana L. Marjoram High GM M 4
Origanum vulgare L. Oregano Very high GM, V, Pt M, G 2, 4, 6, 11
Pelargonium roseum Willd. Rose geranium Very high V G 7
Pimpinella anisum L. Aniseed, anise Very high V G 7
Prostanthera rotundifolia R. Br. Australian mint, native mint, High GM M, G 1
roundleaf mint bush
Prunus persica L. peach Very high GM, Pg M, G 8
Rosa spp. Bois de rose Moderate GM M, G 1
Rosmarinus officinalis L. Rosemary Low GM M 1, 4, 6
Salvia fruticosa L. Greek sage Moderate GM M 4, 5
Salvia officinalis L. Broadleaf sage, common sage, Moderate GM M, G 6
culinary sage, Dalmatian sage,
garden sage, kitchen sage, purple
sage, red sage
Syzygium aromaticum L. Clove High GM, V M, G 1, 11
Thymbra spicata L. Black thyme High GM M 3
Thymus capitatus L. Thyme Very high GM, V, M, G 1, 4, 6, 10
Pg, Pt
Thymus glandulosus Lag. NA Very high GM M 2
Thymus zygis Loefl. NA Very high V G 11
Zingiber cassumunar Roxb. Ginger cassumunar, zingiber Very high GM M 8
Zingiber officinale Rosc. Garden giner, ginger Very high GM, Pg M, G 8

†NA, not applicable.

‡GM, growth medium (Potato Dextrose Agar [PDA]); V, volatile/vapour in lab on growth medium; Pg, suppressed disease in grape; Pt, suppressed disease in tomato.
§M, mycelium; G, germination; S, sporulation.
¶1, Antonov et al. (1997); 2, Bouchra et al. (2003); 3, Chebli et al. (2004); 4, Daferera et al. (2003); 5, Ozcan (2003); 6, Plotto et al. (2003); 7, Tanović et al. (2005);
8, Tripathi et al. (2008); 9, Tzortzakis and Economakis (2007); 10, Walter et al. (2001); 11, Wilson et al. (1997).
††Studies by Plotto et al. (2003) and Tripathi et al. (2008) examined post-harvest disease.

© 2009 Australian Society of Viticulture and Oenology Inc.

162 Alternative fungicides for Botrytis cinerea
mildew in grapes at a level similar to the fungicide flusi-
lazole (Henriquez et al. 1998).
Further information on the chemistry and formula-
tion of these oils, their phytotoxicity and physiological
impact on plants, on human health and on the environ-
ment, compatibility with other pesticides, use as an adju-
vant and impact on pest and disease control can be found
in a recent review of the topic by Beattie et al. (2002).
Plant defence stimulants
Various biotic and abiotic compounds, reviewed recently
by Elmer and Reglinski (2006), can elicit a plant defence
response that can be highly effective at suppressing B.
cinerea in grapes in the field (Reglinski et al. 2005). These
compounds include plant hormones, abiotic stimulants,
plant and microbial extracts, and microbes.
Plant hormones
Plant hormones can be highly effective at suppressing
B. cinerea in the field. The most common of these com-
pounds, salicylic acid and ß-aminobutyric acid, can sup-
press B. cinerea in grapes (Reglinski et al. 1997) and
Arabidopsis plants (Zimmerli et al. 2001). Plant-induced
resistance with salicylic acid has recently been reviewed
by Vasyukova and Ozeretskovskaya (2007). Jasmonic
acid, another plant hormone, is known to induce stilbene
production in grapes (Larronde et al. 2003), which sup-
presses B. cinerea infection (Baarlen et al. 2004). The
effects of jasmonates and their application in horticulture
has recently been reviewed by Rohwer and Erwin (2008).
These compounds induce resistance through stimulating
a change in grapevine physiology (Hammerschmidt
1999); therefore, grape quality can also be impacted and
can cause retarded berry development (Kraeva et al.
1998), reduced berry weight (Elmer and Reglinski 2006)
and decreased phenolics content (Duxbury et al. 2004).
Jasmonates can also leave residues in wine (Kast 2000)
and can be phytotoxic at a high application rate (Reglinski
et al. 1997). Because of the high level of plant sensitivity
to these compounds, there is a narrow margin separating
phytotoxicity and the application rate required for effec-
tive control of plant pathogens (Reglinski et al. 1997,
Elmer and Reglinski 2006), which is a concern for the use
of these hormones in viticulture. Also, issues of delayed
ripening caused by the jasmonates (Kraeva et al. 1998)
are likely to only postpone the B. cinerea infection and
further increase the risks of loss associated with late
harvesting. This is a particular concern for growers in
temperate vineyards who are anxious to harvest as early
as possible to reduce the risk of loss from botrytis. These
stimulants, in their current state, are likely to be consid-
ered by the industry as being too risky and impractical for
use in commercial vineyards.
Abiotic stimulants
Various inorganic compounds have been demonstrated to
induce a systemic resistance response in wine grapes.
These include fertilisers containing nitrogen which can
Australian Journal of Grape and Wine Research 16, 154–172, 2010
affect B. cinerea, recently reviewed by Mundy (2008), as
well as phosphorus, potassium (Reuveni and Reuveni
1998) and potassium phosphate (Reuveni and Reuveni
1995) for the control of powdery mildew, particularly
when used in conjunction with Bordeaux mixture and a
sulphur fungicide (Soyez 2002). Calcium, which assists
the maintenance of grape cell wall integrity, improves
resistance to B. cinerea (Miceli et al. 1999). Soluble forms
of silicon, also implied to increase cell wall strength of
grape leaves, improves resistance to powdery mildew
(Bowen et al. 1992), an effect likely to also increase resis-
tance to B. cinerea (Miceli et al. 1999, Jacometti et al.
2007b). Copper can suppress B. cinerea through eliciting
peroxidise, phenol, resveratrol and anthocyanin accumu-
lation in grapevines (Coulomb et al. 1998).
Induced plant disease response to calcium and silicon is
a generally underutilised technique for suppression of B.
cinerea. These compounds do not have a large impact on
vine growth, physiology or wine quality (Jackson 2008a),
although wines with very high calcium levels can become
musty in the bottle because of calcium tartrate instability
(Jackson 2008g) or calcium oxalate precipitation, but this
does not occur commonly and can be remedied (Jackson
2008f). Elicitation through the use of copper, however, has
many environmental and wine quality issues, as discussed
previously, and for this reason should be avoided.
Plant extracts
Plant extracts (Table 4) can be potent plant defence stimu-
lants. Extracts from giant knotweed (Reynoutria sachalinen-
sis (F. Schmidt) Nakai), registered as ‘Milsana’ (5%
ethanolic extract), are effective at suppressing powdery
mildew in many crops, such as zucchini (Bokshi et al.
2008), tomato (Bardin et al. 2008), strawberry (Carlen
et al. 2004) and cucumber (Fofana et al. 2002, Bokshi
et al. 2008, Lin et al. 2009), and B. cinerea in crops such as
tomato (Ingram and Meister 2006, Bardin et al. 2008),
strawberry (Carlen et al. 2004), cucumber (Konstantini-
dou Doltsinis et al. 2002) and grapes (Schilder et al. 2002,
Schmitt et al. 2002). In a German vineyard, Milsana
applied every 7–10 days reduced the disease incidence of
powdery mildew and B. cinerea to the same or lower levels
than sulphur or a copper-containing agent, FW 450 (Dow
AgroSciences) (Schmitt et al. 2002). Eight applications of
Milsana in vineyard trials in the USA reduced powdery
mildew on leaves by 75% compared to untreated vines,
while four applications of Milsana, applied between pre-
bunch closure and harvest, reduced botrytis bunch rot by
50% (Schilder et al. 2002). Seaweed extract and AlCl3,
marketed under the trade name ‘Synermix’ (Goëmar
Laboratories, Saint Malo, France), have been shown to
elicit resveratrol accumulation in detached grape leaves
and enhance the efficacy of iprodione fungicide against B.
cinerea in vineyard trials (Jeandet et al. 1996, Jeandet et al.
2000). Croplife® (Croplife, Canberra, Australia), a citrus
and coconut extract, when applied with GNS Plantfood®
(GNS, Milan, OH, USA), a foliar fertiliser, provided mod-
erate to good suppression of B. cinerea in vineyard trials in
MI, USA (Schilder et al. 2002).
© 2009 Australian Society of Viticulture and Oenology Inc.
Jacometti et al. Alternative fungicides for Botrytis cinerea 163

Table 4. A list of some of the plant extracts tested against Botrytis cinerea, their levels of activity, medium on which they
were tested and the target of inhibition.

Species Common name Family Level of Test Target of Reference††

activity medium§ inhibition¶

Adenocalyma alleaceum Garlic creeper Bignoniaceae Very high V G 4

Aglaia odorata Perfume plant Meliaceae High V G 4
Allium ampeloprasum Elephant garlic Liliaceae Very high V G 4
Allium cepa Potato onion Liliaceae High V G 4
Allium fistolops Welsh onion Liliaceae High V G 4
Allium ramosum Fragrant-flower garlic Liliaceae Very high V G 4
Allium sativum Serpent garlic Liliaceae Very high V G 4
Allium schoenoprasum Chive Liliaceae High V G 4
Allium tuberosum Chinese chive Liliaceae High V G 4
Calamintha origanifolia Calamint Labiatae Moderate GM M, G 1
Capsicum annuum Capsicum† Solanaceae Very high V G 4
Capsicum annuum Capsicum‡ Solanaceae High V G 4
Capsicum chinense Pepper ‘Habanero’ Solanaceae Very high V G 4
Capsicum frutescens Pepper ‘Tabasco’ Solanaceae Very high V G 4
Chloranthus japonicus Chloranthus Chloranthaceae High Pt M, G 2
Clematis paniculata Sweet autumn clematis Ranunculaceae High V G 4
Clematis trichotoma No common name Ranunculaceae Low Pt M, G 2
Corchoropsis psilocarpa No common name Sterculiaceae Moderate Pt M, G 2
Corydalis ochotensis Variety ‘raddeana’ Fumariaceae Low Pt M, G 2
Dolichos kilimandscharicus No common name Fabaceae Moderate GM M 3
Helianthus tuberosus Jerusalem artichoke, Compositae Low Pt M, G 2
sunchoke
Hesperis matronalis Sweet rocket Cruciferae High V G 4
Inula viscosa Inula Compositae Moderate/high GM, Pa M, G 1
Isatis tinctoria Dyer’s woad Cruciferae High V G 4
Isodon inflexus No common name Labiatae Moderate Pt M, G 2
Juglans nigra Black walnut Junglandaceae High V G 4
Liquidambar styraciflua Sweet gum Hamamelidaceae High V G 4
Lysimachia clethroides Gooseneck loosestrife Primulaceae Low Pt M, G 2
Maerua subcordata No common name Capparaceae Low GM M 3
Matricaria sp. ‘Barths’ Compositae High V G 4
Micromeria juliana Savory Labiatae Low GM M, G 1
Micromeria nervosa Emperor’s mint Labiatae Very high GM, Pa M, G 1
Origanum syriacum Wild marjoram Labiatae Very high GM, Pa M, G 1
Oxalis europaea European yellow wood sorrel Oxalidaceae High V G 4
Patrinia scabiosaefolia Golden lace Patrinia, golden Valerianaceae High Pt M, G 2
valerian
Patrinia villosa White patrinia Valerianaceae Moderate Pt M, G 2
Paulownia coreana Korean paulownia Scrophulariaceae High Pt M, G 2
Phytolacca dodecandra African soapberry Phytolaccaceae Low GM M 3
Plumbago maritima Leadwort Plumbaginaceae Very high GM, Pa M, G 1
Prunus persica Peach Rosaceae High V G 4
Pyrus communis Pear Rosaceae High V G 4
Ruta sp. Rue Rubiaceae Low/moderate GM M, G 1
Satureja acinos Mother of thyme Labiatae High V G 4
Sideritis pullulans Ironwort Lamiaceae Moderate/high GM M, G 1
Taxus canadensis American yew Taxaceae High V G 4
Taxus media Anglo–Japanese yew Taxaceae High V G 4
Tulbaghia violacea Society garlic Liliaceae Very high V G 4
Urginea maritima Sea onion Asphodelaceae Low GM G 1

†Varieties: chile, jalapeno, piquin, sandia, sweet and tepin.

‡Varieties: Anaheim, ancho, big jim, Cayenne, floral gem, fresno chile grand, holiday time, Hungarian yellow wax, large cherry, mirasol, Santa Fe, serrano, super chile,
sweet roumanian and yatsafusa.
§GM, growth medium (Potato Dextrose Agar [PDA]); V, volatile/vapour in lab on growth medium; Pa, suppressed disease in avocado; Pt, suppressed disease in tomato.
¶M, mycelium; G, germination.
††1, Abou-Jawdah et al. (2004); 2, Gyung et al. (2004); 3, Tegegne and Pretorius (2007); 4, Wilson et al. (1997).

© 2009 Australian Society of Viticulture and Oenology Inc.

164 Alternative fungicides for Botrytis cinerea
Plant extracts have the potential to alter chemical
balances in produce, which in grapes may impact wine
quality. Milsana has been shown to alter the fatty acid
content in wheat (Renard-Merlier et al. 2009) and res-
veratrol levels in grapes (Jeandet et al. 1996, Jeandet
et al. 2000). Plant extracts also have the potential to
disrupt biological control of pests in vineyards. For
example, applications of Milsana can cause reductions in
the fecundity and populations of two predatory mites:
Phytoseiulus persimilis (Acarina: Gamasida) and Typhlodro-
mus pyri (Acarina: Phytoseiidae) (Siggelkow and Jackel
1998). A methanolic extract of R. sachalinensis mildly
reduced the parasitism rates of Trichogramma cacoeciae
(Hymenoptera: Trichogrammatidae) (Hafez et al. 1999),
an egg parasitoid of many Lepidopteran pests found in
grapevines and other crops (Pizzol and Pintureau 2008).
This organism is also known to be a good indicator organ-
ism for a variety of other beneficial insects (Hafez et al.
1999). A water extract of R. sachalinensis had no effect on
the parasitoid.
The plant extracts described previously have the
potential to develop into effective disease management
tools in vineyards. They have the ability to suppress mul-
tiple pathogens (Schilder et al. 2002), are compatible with
other products, including synthetic fungicides (Jeandet
et al. 1996, Jeandet et al. 2000) and biofungicides (Bardin
et al. 2004, Bardin et al. 2008), and pathogen suppres-
sion can range from moderate (Schilder et al. 2002) to
levels achieved by conventional fungicides (Schmitt et al.
2002). The compatibility with other products and vari-
ability in suppression levels lends these extracts to being
part of an integrated pest management system.
Compost extracts
Compost extracts can suppress diseases either directly,
through antifungal activity, or indirectly through induc-
ing plant defences (Elmer and Reglinski 2006). Little is
known about the role microbes play in the activation of
plant defences, but pasteurisation has been shown to
reduce the effect (Elad and Shtienberg 1994) and it can be
nullified after sterilisation, so microbial populations are
likely to have an important function (Hoitink et al. 1997).
Extracts from animals and plants have been used to
control various plant pathogens including B. cinerea as
well as downy and powdery mildew (Elad and Shtienberg
1994). An extract made from grape marc and horse and
cattle manures can suppress B. cinerea on detached grape
leaves by up to 95% (Elad and Shtienberg 1994), and on
detached grapes by up to 70% (Ketterer et al. 1992).
When applied on its own, this extract was less effective
under field conditions, but when applied with casein or
pine oil, efficacy was equal to a conventional fungicide
(Ketterer et al. 1992).
The mechanism of suppression of B. cinerea and other
plant pathogens by compost extracts is not well under-
stood and is currently under-researched. The compost
technology has shown potential to suppress B. cinerea
in the laboratory (Elad and Shtienberg 1994) and field
(Ketterer et al. 1992), and is complementary with other
products like essential oils (Ketterer et al. 1992) and bio-
Australian Journal of Grape and Wine Research 16, 154–172, 2010
logical control agents (Scheuerell and Mahaffee 2000).
These characteristics are ideal for inclusion into an inte-
grated pest management system. More information on
the various impacts and applications of compost extracts
in horticulture and agriculture can be found in four
recent reviews (Scheuerell and Mahaffee 2002, Litterick
et al. 2004b, Litterick et al. 2004a, Mahaffee and Scheuer-
ell 2006).
Microbial induction
Microorganisms have been shown to induce a plant-
defence response in plants (Elad 2000, Yedidia et al.
2003). This can be caused by non-pathogenic microor-
ganisms, a phenomenon known as induced systemic
resistance (ISR), or by pathogenic microorganisms, a phe-
nomenon known as systemic acquired resistance (SAR)
(van Loon 2007). The plant response can either be a
systemic (De Meyer et al. 1998, Elad 2000) or a local
reaction (Elad et al. 1994, Elad and Kapat 1999). A
review of ISR and SAR from the plant disease manage-
ment perspective has been recently published by Manon-
mani et al. (2007). ISR can be a component of the
mechanism of action of disease-suppressive microorgan-
isms that are primarily released into the canopy as bio-
logical control agents (Elad 2000, Yedidia et al. 2003). For
example, cellulase production from the BCA Trichoderma
viride has been shown to induce resveratrol accumulation
in grape cell cultures (Calderon et al. 1993) and peroxi-
dise isozyme accumulation in grape leaves and stems
(Barcelo et al. 1996). Trichoderma harzianum T39 reduced
downy mildew by 63% in grape, when applied more than
once 48–72 h before inoculation, without a direct inhibi-
tion of the pathogen (Perazzolli et al. 2008), which sug-
gests that this BCA is stimulating ISR.
In an example of SAR, Trichoderma hamatum and
three binucleate Rhizoctonia species effectively inhibited
botrytis blight in geraniums to the same degree as a fun-
gicide control, under moderately conducive conditions to
the pathogen, by inducing systemic resistance in the host
(Olson and Benson 2007). As this mechanism is sys-
temic, direct contact with the pathogen is not required.
This is very important in grapes after bunch closure
when spray application is very unlikely to penetrate the
bunch. Utilising this plant-defence response mechanism
effectively, in conjunction with the other mechanisms
used in biological control that have been discussed pre-
viously, is likely to make biofungicides more robust and
consistent in their efficacy under field conditions than
ones that act through a single mechanism (Elmer and
Reglinski 2006).
Habitat manipulation
Habitat manipulation, also termed restorative biological
control (Everett et al. 2005), commonly shares tech-
niques with conservation biological control but the dis-
ciplines are not synonymous (Gurr et al. 2000).
Conservation biological control attempts to reduce popu-
lations of the pest species exclusively through the promo-
tion of predators, parasitoids and competitors of the pest
(top–down regulation), whereas habitat manipulation
© 2009 Australian Society of Viticulture and Oenology Inc.
Jacometti et al.
can either promote these species or regulate the pest
through limiting the resources available to it (bottom-up
regulation), like food and shelter (Gurr et al. 2000). The
use of habitat manipulation can reduce the incidence of B.
cinerea directly, through altering the vine canopy, e.g. leaf
plucking, or indirectly through altering vine vigour or the
local environment, e.g. cover crops.
Canopy management
Canopy density and bunch humidity are directly influ-
enced by trellis design (Savage and Sall 1984, Gubler
et al. 1987), grape variety, pruning techniques, leaf
trimming (‘hedging’) and leaf removal (leaf plucking)
(Elmer and Michailides 2004). Pruning techniques and
leaf/trimming removal have also been shown to reduce
berry-to-berry contact in bunches (Martin 1990). These
increase epicuticular wax and cuticle thickness (Percival
et al. 1993), which reduces the incidence of B. cinerea
in bunches (Martin 1990). Increased light penetration
into the canopy also increases ultraviolet exposure, which
stimulates phytoalexin production (Langcake 1981),
compounds inhibitory to B. cinerea and other pathogens
(Daniel and Purkayastha 1995). Compact bunches have
been shown to increase the incidence of B. cinerea
(Fermaud et al. 2001), and this compactness can be influ-
enced by various biotic and abiotic factors, including
excessive nitrogen (Keller et al. 2001), rootstock (Ferreira
and Marais 1987), cultivar (Jackson 2008b) and canopy
management techniques (discussed below).
Local environment manipulations
Habitat manipulation can reduce the incidence of B.
cinerea in grapevines by reducing inoculum levels in
the vineyard or reducing vine vigour, the latter of
which alters canopy density and conditions conducive to
B. cinerea. Vine vigour is influenced by grape variety
(Jackson 1994a), rootstock selection (Pearson and
Goheen 1988), irrigation regimes (Elmer and Michailides
2004) and fertilisation, especially with respect to nitrogen
(Keller et al. 2001). These techniques are well understood
and established in viticultural practice. The use of cover
crops can also reduce vine vigour (Tan and Crabtree 1990,
Wolpert et al. 1993), as can mulches through changes in
the C : N ratio of soil (Jacometti et al. 2007b).
Landscape features can also be important. Topo-
graphic features, such as slope and vineyard orientation,
will determine exposure to sun and wind, which affects
canopy humidity and B. cinerea development (Jackson
2008c). Similarly, shelter belts affect wind flow and
canopy humidity, and can also disturb insect movement,
such as that of the predatory hover fly (Diptera: Syr-
phidae) (Wratten et al. 2003).
The addition of organic (plant-based) mulches and
cover crops mulched in situ can be highly effective at
managing B. cinerea incidence in vineyards (Jacometti
et al. 2007a,b,c) Organic mulches placed under vines in
a certified organic vineyard in New Zealand reduced
B. cinerea primary inoculum through competition from
elevated soil biota and host degradation (Jacometti et al.
2007a), and improved vine resistance to disease through
© 2009 Australian Society of Viticulture and Oenology Inc.
Alternative fungicides for Botrytis cinerea 165
greater soil nutrition and water availability (Jacometti
et al. 2007b). The mulches used in these trials consisted of
anaerobically or aerobically composted grape marc (grape
pressings), shredded office paper or mulched grass, all
of which are waste products sourced on-site or locally.
Aerobic marc, anaerobic marc and shredded paper, the
most efficient of these mulches, increased soil biological
activity by 2–4 times as measured by bait lamina probes
(Kratz 1998) and biolog ecoplates (Girvan et al. 2003).
This effect was largely attributed to elevated soil moisture,
nutrient availability and cation exchange capacity
(Jacometti et al. 2007b). The increased soil biota com-
peted for space and resources with the pathogen and
subsequently B. cinerea conidiophore coverage on vine
debris decreased to 66–95% of that of the control (Jacom-
etti et al. 2007a). This increase in soil biological activity
also enhanced the biological degradation of vine debris,
an effect that, in turn, reduced the incidence of B. cinerea
primary inoculum.
In continuation of this work, the same mulches were
assessed for their influence on a range of vine develop-
ment parameters that could affect resistance to B. cinerea.
Vine canopy density was decreased in the shredded paper
treatment by up to 30% of that of the other treatments,
an effect linked to a higher C : N ratio of the soil under
this high-carbon mulch type. This decrease in canopy
density was likely to have increased light penetration,
elevated canopy temperature and photosynthesis rate,
and lowered canopy humidity. These changes, coupled
with changes in soil biota, nutrient levels and soil mois-
ture, increased grape skin strength by up to 10% in the
paper mulch treatment. The altered soil and vine envi-
ronment under the marc and paper treatments led to a
reduction of up to 97% in B. cinerea infection compared to
the control, averaged over two consecutive harvests.
Under high disease pressure at harvest, the paper and
marc treatments reduced B. cinerea severity on the grapes
to below the economic threshold on Riesling grapes in
New Zealand (Figure 2) (Jacometti et al. 2007b). This
increase in grapevine resistance to B. cinerea is similar to
the concept of suppressive soils, where mulches, crop
rotations, fumigants or soil solarisation techniques are
used to stimulate existing soil biota and increase the resis-
tance of crops grown on this soil to plant pathogens
(Whipps 1997).
Mulched cover crops can also enhance the soil and
vine environment (Jacometti et al. 2007c). Compared
with a bare ground control, phacelia (Phacelia tanacetifolia
Benth., cv. Balo) and perennial ryegrass (Lolium perenne
(L.), cv. Kingston) grown in situ then mulched into the
under-vine area, reduced B. cinerea primary inoculum on
vine debris and increased vine debris degradation rate
and soil biological activity. As a result of the use of these
mulches, B. cinerea severity was reduced in vine inflores-
cences at flowering and in grapes at harvest (Figure 3). B.
cinerea severity in these Chardonnay grapes was below
the economic threshold for all treatments. This reduction
was partly attributed to decreases in primary inoculum
but also to probable changes in vine physiology and resis-
tance (Jacometti et al. 2007b).
166 Alternative fungicides for Botrytis cinerea Australian Journal of Grape and Wine Research 16, 154–172, 2010
Severity of B. cinerea sporulation on grapes at harvest

12
A

Year 1
10
Year 2
(no. of grapes infected/vine)

AB Figure 2. Percentage of
bunches infected with
8
sporulating Botrytis cinerea on
vines under difference organic
mulch treatments under low
6 Economic threshold disease pressure (Year 1) and
B B B
high disease pressure (Year 2),
and the economic threshold for
4 botrytis control in Riesling
grapes in New Zealand. Letters
denote least significant
2 differences (LSD) calculated
a
ab through Fisher’s protected LSD
bc
c c (P < 0.05). (Reprinted from
0 Jacometti et al. (2007b) with
permission.)
c

c
l

ss

c
ss

r
r

ro
ro

pe
pe
ar

ar
ar

ar
ra
ra

nt
nt

m
m

Pa
Pa

g
g

Co
Co

ic

ic

ic

ic
n

n
ow

ow
ob

ob

ob

ob
er

er
er

er
M

M
A

A
na

na
A

Mulch treatments

16 a Mulches and mulched cover crops can be effective at

Mean % B. cinerea sporulation area/conidiophore

Flowers reducing B. cinerea infections in an organic vineyard within

14
Grapes 1 or 2 years of mulch application. They are likely to be
12 compatible with the other techniques discussed in this
review as they are achieved through subtle changes in soil
10
biology and vine physiology. In conventional vineyards,
coverage

8
6 b
4
2 b
0
Control Phacelia
Figure 3. Percentage of vine inflorescences infected with Botrytis
cinerea (incubated under laboratory conditions) and percentage of
bunches with botrytis bunch rot at harvest, under different mulched
cover crops. The industry economic threshold for botrytis bunch rot
on Chardonnay grapes in New Zealand is shown. (Reprinted from
Jacometti et al. (2007c) with permission.)
For effective in situ mulching, the species of cover crop
chosen for a particular vineyard needs to produce suffi-
cient biomass. Such information for cover crops grown in
California has been presented by Bugg et al. (1996), and
reviewed by McGourty and Reganold (2005), Ingels
(1998) and Rous (1993). Other factors that also need to
be considered on a site-by-site basis are the level of com-
petition the crop will have with the vine, which can
reduce yield (Tan and Crabtree 1990, Wolpert et al.
1993), how the cover crop will suit agronomic practices
(Bugg et al. 1996), and how it will effect soil attributes
(Bugg et al. 1996, Jacometti et al. 2007b).
the soil microbial community could be less well developed
than organic systems, so mulching could require a longer
period of time to achieve the same results. Over this time,
Economic threshold
the viticulturalist may be dependent on some of the other
alternatives discussed in this review. The use of those
a
methods would be unlikely to disturb soil organisms and
c b therefore would allow the vine microbial community to
re-populate the rhizosphere under the mulches. If
Ryegrass Control Phacelia Ryegrass
mulches are used in conjunction with conventional fun-
Mulch treatments
gicides, the benefits proposed are likely to be limited to
some extent by the effects of the fungicides on the soil
microflora, the negative effects of which are well docu-
mented (Vyas 1988, Chen et al. 2001).
Soil management is also an important part of keeping
the integrity of this system, as overworked soil has
reduced structure, organic matter and biological activity
(McLaren and Cameron 1994). These changes typically
lead to a reduction in available soil moisture and the
concentrations and availability of nutrients (Li et al.
2004). It is therefore recommended that if cover crops are
used to provide the mulch in situ, they should be directly
drilled or drilled with minimum tillage (McLaren and
Cameron 1994). It is important to note that soils are
highly modified through climate and local topography
and are not heterogeneous through space and time
(Chamran et al. 2002), thus management techniques dis-
cussed previously need to be customised to the character-
istics of the local soil.
The use of mulches and cover crops could potentially
be applicable to other horticultural systems and can be
© 2009 Australian Society of Viticulture and Oenology Inc.
Jacometti et al.
able to manage other diseases. Grapevine fungal patho-
gens that have similar characteristics to those of B. cinerea,
especially downy mildew, which overwinters in leaf litter
on the vineyard floor and favours warm, humid weather
(Magarey et al. 1994), provide added incentive to develop
this technology further. The use of cover crops could also
be integrated into other habitat manipulation techniques,
such as the employment of flowering plants to supply
nectar and pollen for beneficial insects in vines and other
crops. These plants, initially providing floral resources to
enhance the efficacy of arthropod BCAs (Landis et al.
2000, Zehnder et al. 2007, Jonsson et al. 2008), could
subsequently be mulched with vine prunings into the
below-vine area. The physiological changes in grape
disease resistance reviewed here, such as increases in skin
strength and the probable increase in berry defence
chemicals (e.g. phenolics) could also reduce insect pest
damage (Read et al. 2003) and secondary infections as a
result of that damage (Baker et al. 1994).
The deployment of mulches would need to be care-
fully considered in areas where voles (Microtus spp.) and
other rodents are pests in grapevines. These species can
cause extensive damage to young grapevines, through
eating the bark to the cambium layer, resulting in a partial
or full girdling of the vine (Salmon et al. 1992). These
pests find shelter and food under dense undergrowth and
therefore mulches could provide a resource for them,
resulting in increased population densities and subse-
quent vine damage (Salmon et al. 1992).
Mulches may also be disadvantageous in areas that are
prone to early frosts, since bare ground is effective at
accumulating heat over the day, which can be released
over the night and reduce the impact of frosts (Jackson
2008b). The cooler, moister soils that arise from mulched
ground, compared to bare areas, could also hinder the
initiation of vine growth in the spring (Jackson 2008b).
Conclusion
A change from current viticultural practices, heavily
dependent on synthetic fungicides, is inevitable. Fungi-
cide resistance, market and regulatory pressure regarding
residues and concerns of environmental and human
health are increasing, so new management techniques
will need to be adopted. All alternative products and
techniques discussed in this review can have some role to
play in this, with the exception of essential oils, because
of taint issues, and plant hormones, which are too sensi-
tive for commercial application in their current state.
Biofungicides have been shown to be compatible with
other products, to be stable on the shelf and in the field,
and to operate through a variety of mechanisms.
However, there is a limited range of these products
because of the excessive cost of commercialisation, pro-
duction challenges and regulatory issues. These factors
have been reviewed elsewhere (Fravel 1999, Stewart
2001, Gerhardson 2002). Mineral oils have been shown
to be effective by themselves, are complemented by other
products and have excellent sticking properties. They do,
however, have the potential to disturb plant function,
affect grape quality and potentially leave residues, and so
© 2009 Australian Society of Viticulture and Oenology Inc.
Alternative fungicides for Botrytis cinerea 167
need to be used in moderation. Plant defence stimulants
have been shown to be very effective at suppressing B.
cinerea and other plant pathogens, both by themselves
and in conjunction with other products, including essen-
tial oils, BCAs and synthetic fungicides. These products
can cause subtle changes in vine physiology and can alter
grape juice components, such as resveratrol levels, which
need to be managed by the viticulturalist. The use of
mulches and cover crops can effectively suppresses B.
cinerea through induced vine disease resistance, canopy
density reductions and biological control. They are com-
patible with all other techniques that do not disturb soil
biology, but may be unsuitable in areas where voles and
other rodents cause vine damage or where vines are at
high risk of frost damage. Cultural techniques, such as
pruning, leaf clipping and leaf plucking, are well estab-
lished within the industry and are effective at reducing B.
cinerea infection. These techniques, used in conjunction
with each other, suit an integrated method of pest man-
agement, a common trend in modern viticulture.
References
Abou-Jawdah, Y., Wardan, R., Sobh, H. and Salameh, A. (2004)
Antifungal activities of extracts from selected Lebanese wild plants
against plant pathogenic fungi. Phytopathologia Mediterranea 43,
377–386.
Ahmed, E.G., Wilson, C.L. and Wisniewski, M. (1998) Ultrastruc-
tural and cytochemical aspects of the biological control of Botrytis
cinerea by Candida saitoana in apple fruit. Phytopathology 88,
282–291.
Antonov, A., Stewart, A. and Walter, M. (1997) Inhibition of
conidium germination and mycelial growth of Botrytis cinerea by
natural products. Proceedings of the Fiftieth New Zealand Plant
Protection Conference (New Zealand Plant Protection Society:
Rotorua, New Zealand) pp. 159–164.
Baarlen, P., Legendre, L. and Kan, J.A.L. (2004) Plant defence
compounds against botrytis infection. In: Botrytis: Biology, pathol-
ogy and control. Eds. Y. Elad, B. Williamson, P. Tudzynski and N.
Delen (Kluwer Academic Publishers: Netherlands) pp. 143–161.
Baek, J.M., Howell, C.R. and Kenerley, C.M. (1999) The role of an
extracellular chitinase from Trichoderma virens Gv29-8 in the bio-
control of Rhizoctonia solani. Current Genetics 35, 41–50.
Baker, G., Bailey, P. and Charles, J. (1994) Lightbrown apple
moth. In: Diseases and pests. Eds. P. Nicholas, P. Magarey and M.
Wachtel (Winetitles: Marleston, South Australia) pp. 47–50.
Barcelo, A.R., Zapata, J.M. and Calderon, A.A. (1996) A basic
peroxidase isoenzyme, marker of resistance against Plasmopara
viticola in grapevines, is induced by an elicitor from Trichoderma
viride in susceptible grapevines. Journal of Phytopathology 144,
309–313.
Bardin, M., Fargues, J. and Nicot, P.C. (2008) Compatibility
between biopesticides used to control grey mould, powdery
mildew and whitefly on tomato. Biological Control 46, 476–483.
Bardin, M., Fargues, J., Couston, L., Troulet, C., Philippe, G. and
Nicot, P.C. (2004) Combined biological control against three bio-
aggressors of tomato. La Revue Technique des Pepinieristes Hor-
ticulteurs Maraichers 461, 36–39.
Bavaresco, L., Petegolli, D., Cantu, E., Fregoni, M., Chiusa, G. and
Trevisan, M. (1997) Elicitation and accumulation of stilbene
phytoalexins in grapevine berries infected by Botrytis cinerea.
Vitis 36, 77–83.
Beattie, A., Watson, D., Stevens, M., Rae, D. and Spooner-Hart, R.
(2002) Spray oils beyond 2000: Sustainable pest and disease man-
agement (University of Western Sydney: Sydney, Australia).
Becker, J.O. and Schwinn, F.J. (1993) Control of soil-borne patho-
gens with living bacteria and fungi – Status and outlook. Pesticide
Science 37, 355–363.
168 Alternative fungicides for Botrytis cinerea
Blachinsky, D., Antonov, J., Bercovitz, A., El-Ad, B., Feldman, K.,
Husid, A., Lazare, M., Marcov, N., Shamai, I., Droby, S. and
Keren-Zur, M. (2007) Commercial applications of Shemer for
the control of pre- and post-harvest diseases. Proceedings of the
meeting, Fundamental and Practice Approaches to Increase Bio-
control Efficacy (OIBC/OILB: Dijon, France) pp. 75–78.
Blakeman, J.P. (1993) Pathogens in the foliar environment. Plant
Pathology 42, 479–493.
Bokshi, A.I., Jobling, J. and McConchie, R. (2008) A single appli-
cation of Milsana followed by Bion assists in the control of
powdery mildew in cucumber and helps overcome yield losses.
Journal of Horticultural Science and Biotechnology 83, 701–706.
Bouchra, C., Achouri, M., Hassani, L.M.I. and Hmamouchi, M.
(2003) Chemical composition and antifungal activity of essential
oils of seven Moroccan Labiatae against Botrytis cinerea (Pers: Fr).
Journal of Ethnopharmacology 89, 165–169.
Bourbos, V.A., Skoudridakis, M.T., Haitas, V.C. and Fotiadis, K.S.
(1994) The possible control of Botrytis cinerea Pers. using paraffinic
oils. Brighton Crop Protection Conference – Pests and Diseases
(British Crop Protection Council: Surrey, England) pp. 797–800.
Bowen, P., Menzies, J. and Ehret, D. (1992) Soluble silicon sprays
inhibit powdery mildew development on grape leaves. Journal of
the American Society for Horticultural Science 117, 906–912.
Brink, J.C., Fourie, P.H. and Holz, G. (2007) Fungicide spray cover
in grape bunches and control of Botrytis cinerea (abstract). South
African Journal of Science 103, V–V.
Bugg, R.L., McGourty, G., Sarrantonio, M., Lanini, W.T. and Bar-
tolucci, R. (1996) Comparison of 32 cover crops in an organic
vineyard on the north coast of California. Biological Agriculture &
Horticulture 13, 63–81.
Calderon, A.A., Zapata, J.M., Munoz, R., Pedreno, M.A. and
Barcelo, A.R. (1993) Resveratrol production as a part of the
hypersensitive-like response of grapevine cells to an elicitor from
Trichoderma viride. New Phytologist 124, 455–463.
Calfouzos, L. (1966) Action of oil in the control of plant disease.
Annual Review of Phytopathology 4, 369–390.
Carlen, C., Faby, R., Karjalainen, R., Pommier, J.J. and Steffek, R.
(2004) Control of air borne diseases in strawberries with natural
and synthetic elicitors. Acta Horticulturae 649, 237–240.
Cattaruzza, A., Peri, C. and Rossi, M. (1987) Ultrafiltration and
deep-bed filtration of a red wine – Comparative experiments.
American Journal of Enology and Viticulture 38, 139–142.
Chamran, F., Gessler, P.E. and Chadwick, O.A. (2002) Spatially
explicit treatment of soil-water dynamics along a semiarid catena.
Soil Science Society of America Journal 66, 1571–1583.
Chebli, B., Hmamouchi, M., Achouri, M., Hassani, L. and Idrissi,
M. (2004) Composition and in vitro fungitoxic activity of 19 essen-
tial oils against two post-harvest pathogens. Journal of Essential
Oil Research 16, 507–511.
Chen, S.K., Edwards, C.A. and Subler, S. (2001) A microcosm
approach for evaluating the effects of the fungicides benomyl and
captan on soil ecological processes and plant growth. Applied Soil
Ecology 18, 69–82.
Coulomb, C., Lizzi, Y., Coulomb, P.J., Roggero, J.P., Coulomb, P.O.
and Agullon, O. (1998) Can copper be an elicitor? Phytoma 512,
41–46.
Daferera, D.J., Ziogas, B.N. and Polissiou, M.G. (2003) The effec-
tiveness of plant essential oils on the growth of Botrytis cinerea,
Fusarium sp. and Clavibacter michiganensis subsp. michiganensis.
Crop Protection 22, 39–44.
Daniel, M. and Purkayastha, R.P. (1995) Handbook of phytoalexin
metabolism and action (Marcel Dekker, Inc: New York, USA).
Darriet, P., Bouchilloux, P., Poupot, C., Bugaret, Y., Clerjeau, M.,
Sauris, P., Medina, B. and Dubourdieu, D. (2001) Effects of
copper fungicide spraying on volatile thiols of the varietal aroma
of Sauvignon blanc, Cabernet Sauvignon and Merlot wines. Vitis
40, 93–99.
De Meyer, G., Bigirimana, J., Elad, Y. and Hofte, M. (1998)
Induced systemic resistance in Trichoderma harzianum T39 biocon-
trol of Botrytis cinerea. European Journal of Plant Pathology 104,
279–286.
Australian Journal of Grape and Wine Research 16, 154–172, 2010
Dell, K.J., Gubler, W.D., Krueger, R., Sanger, M. and Bettiga, L.J.
(1998) The efficacy of JMS Stylet-Oil on grape powdery mildew
and botrytis bunch rot and effects on fermentation. American
Journal of Enology and Viticulture 49, 11–16.
Duxbury, M., Hotter, G., Reglinski, T. and Sharpe, N. (2004) Effect
of chitosan and 5-chlorosalicylic acid on total phenolic content of
grapes and wine. American Journal of Enology and Viticulture 55,
191–194.
Edwards, S.G. and Seddon, B. (1992) Bacillus brevis as a biocontrol
agent against Botrytis cinerea on protected chinese cabbage. 10th
International Botrytis Symp: Recent Advances in Botrytis Research
(Pudoc: Wageningen, Netherlands) pp. 267–271.
Eilenberg, J., Hajek, A. and Lomer, C. (2001) Suggestions for
unifying the terminology in biological control. BioControl 46,
387–400.
Elad, Y. (1995) Mycoparasitism. In: Pathogenesis and host speci-
ficity in plant diseases: Histpathological, biochemical, genetic and
molecular basis, Vol 2: Eukaryotes. Eds. K. Kohmoto, U.S. Singh
and R.S. Singh (Elsevier Science Ltd: Oxford, UK) pp. 289–307.
Elad, Y. (1996) Mechanisms involved in the biological control of
Botrytis cinerea incited diseases. European Journal of Plant Pathol-
ogy 102, 719–732.
Elad, Y. (2000) Biological control of foliar pathogens by means of
Trichoderma harzianum and potential modes of action. Crop Pro-
tection 19, 709–714.
Elad, Y. and Freeman, S. (2002) Biological control of fungal plant
pathogens. In: Mycota – A comprehensive treatise on fungi as
experimental systems for basic and applied research. Eds. F.
Kempken (Springer: Heidelberger, Germany) pp. 93–109.
Elad, Y. and Kapat, A. (1999) The role of Trichoderma harzianum
protease in the biocontrol of Botrytis cinerea. European Journal of
Plant Pathology 105, 177–189.
Elad, Y. and Shtienberg, D. (1994) Effect of compost water extracts
on grey mould (Botrytis cinerea). Crop Protection 13, 109–114.
Elad, Y. and Stewart, A. (2004) Microbial control of Botrytis spp.
In: Botrytis: Biology, Pathology and Control. Eds. Y. Elad, B.
Williamson, P. Tudzynski and N. Delen (Kluwer Academic
Publishers: Netherlands) pp. 223–241.
Elad, Y., Kirshner, B. and Sztejnberg, A. (1998) Management of
powdery mildew and gray mold of cucumber by Trichoderma
harzianum T39 and Ampelomyces quisqualis AQ10. BioControl 43,
241–251.
Elad, Y., Kohl, J. and Fokkema, N.J. (1994) Control of infection
and sporulation of Botrytis cinerea on bean and tomato by
saprophytic bacteria and fungi. European Journal of Plant Pathol-
ogy 100, 315–336.
Elmer, P.A.G. and Michailides, T.J. (2004) Epidemiology of Botrytis
cinerea in orchard and vine crops. In: Botrytis: Biology, pathology
and control. Eds. Y. Elad, B. Williamson, P. Tudzynski and N.
Delen (Kluwer Academic Publishers: Netherlands) pp. 243–
272.
Elmer, P.A.G. and Reglinski, T. (2006) Biosuppression of Botrytis
cinerea in grapes. Plant Pathology 55, 155–177.
Everett, K.R., Vanneste, J.L., Hallett, I.C. and Walter, M. (2005)
Ecological alternatives for disease management of fruit rot patho-
gens. New Zealand Plant Protection 58, 55–61.
Farquhar, S.A., Goff, N.M., Shadbeh, N., Samples, J., Ventura, S.,
Sanchez, V., Rao, P. and Davis, S. (2009) Occupational health
and safety status of indigenous and Latino farmworkers in
Oregon. Journal of Agricultural Safety and Health 15, 89–102.
Fermaud, M. and Gaunt, R.E. (1995) Thrips obscuratus as a poten-
tial vector of Botrytis cinerea in kiwifruit. Mycological Research 99,
267–273.
Fermaud, M. and Le Menn, R. (1992) Transmission of Botrytis
cinerea to grapes by grape berry moth larvae. Phytopathology 82,
1393–1398.
Fermaud, M., Pieri, P. and Liminana, J.M. (2001) Botrytis and
micro-climates: Propagation of Botrytis cinerea in grapes in con-
trolled climatic conditions. Phytoma 543, 40–43.
Ferreira, J.H.S. and Marais, P.G. (1987) Effect of rootstock cultivar,
pruning method and crop load on Botrytis cinerea rot of Vitis vinifera
© 2009 Australian Society of Viticulture and Oenology Inc.
Jacometti et al.
cv. Chenin blanc grapes. South African Journal for Enology and
Viticulture 8, 41–44.
Finger, S.A., Wolf, T.K. and Baudoin, A.B. (2002) Effects of hor-
ticultural oils on the photosynthesis, fruit maturity, and crop yield
of winegrapes. American Journal of Enology and Viticulture 53,
116–124.
Fofana, B., McNally, D.J., Labbe, C., Boulanger, R., Benhamou, N.,
Seguin, A. and Belanger, R.R. (2002) Milsana-induced resistance
in powdery mildew-infected cucumber plants correlates with the
induction of chalcone synthase and chalcone isomerase. Physi-
ological and Molecular Plant Pathology 61, 121–132.
Fokkema, N.J. (1993) Opportunities and problems of control of
foliar pathogens with micro-organisms. Pesticide Science 37, 411–
416.
Fravel, D. (1999) Hurdles and bottlenecks on the road to biocontrol
of plant pathogens. Australasian Plant Pathology 28, 53–56.
Gerhardson, B. (2002) Biological substitutes for pesticides. Trends
in Biotechnology 20, 338–343.
Girvan, M.S., Bullimore, J., Pretty, J.N., Osborn, A.M. and Ball,
A.S. (2003) Soil type is the primary determinant of the compo-
sition of the total and active bacterial communities in arable soils.
Applied and Environmental Microbiology 69, 1800–1809.
Gold, L.S., Slone, T.H., Stern, B.R., Manley, N.B. and Ames, B.N.
(1992) Rodent carcinogens – Setting priorities. Science 258, 261–
265.
Gubler, W.D., Marois, J.J., Bledsoe, A.M. and Bettiga, L.J. (1987)
Control of botrytis bunch rot of grape with canopy management.
Plant Disease 71, 599–601.
Guetsky, R., Shtienberg, D., Elad, Y. and Dinoor, A. (2001) Com-
bining biocontrol agents to reduce the variability of biological
control. Phytopathology 91, 621–627.
Gurr, G.M., Wratten, S.D. and Barbosa, P. (2000) Success in
conservation biological control of arthropods. In: Biological
Control: Measures of Success. Eds. G.M. Gurr and S.D. Wratten
(Kluwer Academic Publishers: Dordrecht, The Netherlands) pp.
105–132.
Gyung, J.C., Kyoung, S.J., Jin-Seok, K., Seon-Woo, L., Jun Young,
C., Kwang, Y.C. and Jin-Cheol, K. (2004) In vivo antifungal
activities of 57 plant extracts against six plant pathogenic fungi.
Plant Pathology Journal 20, 184–191.
Hafez, M.B., Schmitt, A. and Hassan, S.A. (1999) The side-effects
of plant extracts and metabolites of Reynoutria sachalinensis (F.
Schmidt) Nakai and conventional fungicides on the beneficial
organism Trichogramma cacoeciae Marchal (Hym., Trichogramma-
tidae). Journal of Applied Entomology 123, 363–368.
Hammerschmidt, R. (1999) Induced disease resistance: How do
induced plants stop pathogens? Physiological and Molecular Plant
Pathology 55, 77–84.
Harman, G.E., Latorre, B., Agosin, E., San Martin, R., Riegel, D.G.,
Nielsen, P.A., Tronsmo, A. and Pearson, R.C. (1996) Biological
and integrated control of botrytis bunch rot of grape using Tricho-
derma spp. Biological Control 7, 259–266.
Helbig, J. (2002) Ability of the antagonistic yeast Cryptococcus albidus
to control Botrytis cinerea in strawberry. BioControl 47, 85–99.
Henriquez, J.L., Montealegre, J. and Lira, W. (1998) Evaluation of
Ultra Fine Sun Spray oil to control the powdery mildew (Uncinula
necator Schw. Burr) of grapes. Investigacion Agricola 18, 25–32.
Hoitink, H.A.J., Stone, A.G. and Han, D.Y. (1997) Suppression
of plant diseases by compost. Agronomia Costarricense 21, 25–
33.
Holz, G. and Volkmann, A. (2002) Colonisation of different posi-
tions in grape bunches by potential biocontrol organisms and
subsequent occurrence of Botrytis cinerea. Bulletin OILB/SROP 25,
9–12.
Howell, C.R. (2003) Mechanisms employed by Trichoderma species
in the biological control of plant diseases: The history and evolu-
tion of current concepts. Plant Disease 87, 4–10.
Howell, C.R., Hanson, L.E., Stipanovic, R.D. and Puckhaber, L.S.
(2000) Induction of terpenoid synthesis in cotton roots and
control of Rhizoctonia solani by seed treatment with Trichoderma
virens. Phytopathology 90, 248–252.
© 2009 Australian Society of Viticulture and Oenology Inc.
Alternative fungicides for Botrytis cinerea 169
Howell, G.S. (2001) Sustainable grape productivity and the
growth–yield relationship: A review. American Journal of
Enology and Viticulture 52, 165–174.
Ingels, C.A. (1998) Cover cropping in vineyards: A grower’s hand-
book (ANR Publications: California).
Ingram, D.M. and Meister, C.W. (2006) Managing Botrytis gray
mold in greenhouse tomatoes using traditional and bio-
fungicides. Plant Health Progress July, 1–5.
Jackson, D.I. and Lombard, P.B. (1993) Environmental and
management practices affecting grape composition and wine
quality – A review. American Journal of Enology and Viticulture
44, 409–430.
Jackson, R.S. (1994a) Grape species and varieties: Grapevine
improvement. In: Wine Science: Principles and Applications. Eds.
S.L. Taylor (Academic Press: San Diego) pp. 27–33.
Jackson, R.S. (1994b) Fermentation: Prefermentation practices.
In: Wine science: Principles and applications. Eds. S.L. Taylor
(Academic Press: San Diego) pp. 283–294.
Jackson, R.S. (1994c) Specific and distinctive wine styles: Sweet
table wines. In: Wine science: Principles and applications. Eds.
S.L. Taylor (Academic Press: San Diego) pp. 434–440.
Jackson, R.S. (1994d) Postfermentation treatments and related
topics: Stabilization and clarification. In: Wine science: Principles
and applications. Eds. S.L. Taylor (Academic Press: San Diego) pp.
362–374.
Jackson, R.S. (2008a) Wine science: Principles, practice, percep-
tion. In: Wine Science: Principles and Applications. (Academic
Press: London) p. 751.
Jackson, R.S. (2008b) Vineyard practice: Disease, pest and weed
control. In: Wine Science: Principles and Applications. (Academic
Press: London) pp. 175–212.
Jackson, R.S. (2008c) Site selection and climate: Topographic influ-
ences. In: Wine Science: Principles and Applications. (Academic
Press: London) pp. 246–249.
Jackson, R.S. (2008d) Vineyard practice: Fertilization. In: Wine
Science: Principles and Applications. (Academic Press: London)
pp. 160–174.
Jackson, R.S. (2008e) Fermentation: Biochemistry of alcoholic
fermentation. In: Wine Science: Principles and Applications.
(Academic Press: London) pp. 358–402.
Jackson, R.S. (2008f) Chemical constituents of grapes and wine.
In: Wine Science: Principles and Applications. (Academic Press:
London) pp. 274–317.
Jackson, R.S. (2008g) Postfermentation treatments and related
topics: Stabilization and clarification. In: Wine Science:
Principles and Applications. (Academic Press: London) pp. 425–
441.
Jacometti, M.A., Wratten, S.D. and Walter, M. (2007a) Manage-
ment of understorey to reduce the primary inoculum Botrytis
cinerea: Enhancing ecosystem services in vineyards. Biological
Control 40, 57–64.
Jacometti, M.A., Wratten, S.D. and Walter, M. (2007b) Under-
storey management increases grape quality, yield and resistance to
Botrytis cinerea. Agriculture, Ecosystems and Environment 122,
349–356.
Jacometti, M.A., Wratten, S.D. and Walter, M. (2007c) Enhancing
ecosystem services in vineyards: Using cover crops to decrease
botrytis bunch rot severity. International Journal of Agricultural
Sustainability 5, 305–314.
Janisiewicz, W. (1996) Ecological diversity, niche overlap, and
coexistence of antagonists used in developing mixtures for bio-
control of postharvest diseases of apples. Phytopathology 86, 473–
479.
Jeandet, P., Adrian, M., Breuil, A.C., Sbaghi, M., Debord, S.,
Bessis, R., Weston, L.A. and Harmon, R. (2000) Chemical induc-
tion of phytoalexin synthesis in grapevines: Application to the
control of grey mould in the vineyard. Acta Horticulturae 528,
591–596.
Jeandet, P., Adrian, M., Joubert, J.M., Hubert, F. and Bessis, R.
(1996) Stimulating the natural defences of grape. A complement
to phytosanitary control of Botrytis. Phytoma 488, 21–25.
170 Alternative fungicides for Botrytis cinerea
Johnson, K.B. (1994) Dose-response relationships and inundative
biological-control. Phytopathology 84, 780–784.
Jonsson, M., Wratten, S.D., Landis, D.A. and Gurr, G.M. (2008)
Recent advances in conservation biological control of arthropods
by arthropods. Biological Control 45, 172–175.
Karabulut, O.A., Tezcan, H., Daus, A., Cohen, L., Wiess, B. and
Droby, S. (2004) Control of preharvest and postharvest fruit rot in
strawberry by Metschnikowia fructicola. Biocontrol Science and
Technology 14, 513–521.
Kast, W.K. (2000) Salicylic and phosphorous acid – Possible alter-
native of copper? IFOAM 2000 – The World Grows Organic.
Proceedings, 6th International Congress on Organic Viticulture
(Forschungsinstitut fur biologischen Landbau: Frick, Switzerland)
pp. 177–179.
Keller, M., Kummer, M. and Vasconcelos, M.C. (2001) Reproduc-
tive growth of grapevines in response to nitrogen supply and
rootstock. Australian Journal of Grape and Wine Research 7,
12–18.
Keller, M., Viret, O. and Cole, M. (2003) Botrytis cinerea infection
in grape flowers: Defense reaction, latency and disease expression.
Phytopathology 93, 316–322.
Ketterer, N., Fisher, B., Weltzien, H.C. and Williamson, B. (1992)
Biological control of Botrytis cinerea on grapevine by compost
extracts and their microorganisms in pure culture. Recent
Advances in Botrytis Research. Proceedings of the 10th Interna-
tional Botrytis symposium (Pudoc: Wageningen, The Nether-
lands) pp. 179–186.
Kolombet, L.V., Zhigletsova, S.K., Kosareva, N.I., Bystrova, E.V.,
Derbyshev, V.V., Krasnova, S.P. and Schisler, D. (2008) Devel-
opment of an extended shelf-life, liquid formulation of the bio-
fungicide Trichoderma asperellum. World Journal of Microbiology &
Biotechnology 24, 123–131.
Konstantinidou Doltsinis, S., Markellou, E., Petsikos Panayotarou,
N., Siranidou, E., Kalamarakis, A.E., Schmitt, A., Ernst, A.,
Seddon, B., Belanger, R.R. and Dik, A.J. (2002) Combinations of
biocontrol agents and Milsana(R) against powdery mildew and
grey mould in cucumber in Greece and the Netherlands. Proceed-
ings of the 7th Working Group Meeting, Influence of Abiotic and
Biotic Factors on Biocontrol Agents (OIBC/OILB: Dijon, France)
pp. 171–174.
Korolev, N., David, D.R. and Elad, Y. (2008) The role of phyto-
hormones in basal resistance and Trichoderma-induced systemic
resistance to Botrytis cinerea in Arabidopsis thaliana. BioControl 53,
667–683.
Kraeva, E., Andary, C., Carbonneau, A. and Deloire, A. (1998)
Salicylic acid treatment of grape berries retards ripening. Vitis 37,
143–144.
Kratz, W. (1998) The bait lamina test: General aspects, applications
and perspectives. Environmental Science and Pollution Research
5, 94–96.
Kurtzman, C.P. and Droby, S. (2001) Metschnikowia fructicola, a new
ascosporic yeast with potential for biocontrol of postharvest fruit
rots. Systematic and Applied Microbiology 24, 395–399.
Landis, D.A., Wratten, S.D. and Gurr, G.M. (2000) Habitat man-
agement to conserve natural enemies of arthropod pests in agri-
culture. Annual Review of Entomology 45, 175–201.
Langcake, P. (1981) Disease resistance of Vitis spp and the produc-
tion of the stress metabolites resveratrol, epsilon-viniferin, alpha-
viniferin and pterostilbene. Physiological Plant Pathology 18,
213–226.
Larronde, F., Gaudilliere, J.P., Krisa, S., Decendit, A., Deffieux, G.
and Merillon, J.M. (2003) Airborne methyl jasmonate induces
stilbene accumulation in leaves and berries of grapevine plants.
American Journal of Enology and Viticulture 54, 63–66.
Lee, J.P., Lee, S.W., Kim, C.S., Son, J.H., Song, J.H., Lee, K.Y., Kim,
H.J., Jung, S.J. and Moon, B.J. (2006) Evaluation of formula-
tions of Bacillus licheniformis for the biological control of tomato
gray mold caused by Botrytis cinerea. Biological Control 37, 329–
337.
Leroux, P. (2004) Chemical control of Botrytis and its resistance to
chemical fungicides. In: Botrytis: Biology, pathology and control.
Australian Journal of Grape and Wine Research 16, 154–172, 2010
Eds. Y. Elad, B. Williamson, P. Tudzynski and N. Delen (Kluwer
Academic: Dordrecht, The Netherlands) pp. 195–222.
Li, H., Parent, L.E., Karam, A. and Tremblay, C. (2004) Potential
of sphagnum peat for improving soil organic matter, water
holding capacity, bulk density and potato yield in a sandy soil.
Plant and Soil 265, 355–365.
Lin, T., Ishizaka, M. and Ishii, H. (2009) Acibenzolar-S-methyl-
induced systemic resistance against anthracnose and powdery
mildew diseases on cucumber plants without accumulation of
phytoalexins. Journal of Phytopathology 157, 40–50.
Litterick, A.M., Harrier, L., Wallace, P., Watson, C.A. and Wood,
M. (2004a) The role of uncomposted materials, composts,
manures, and compost extracts in reducing pest and disease
incidence and severity in sustainable temperate agricultural and
horticultural crop production – A review. Critical Reviews in
Plant Sciences 23, 453–479.
Litterick, A.M., Watson, C.A., Wallace, P. and Wood, M. (2004b)
Compost teas – A simple disease control solution for organic
crops? In: Organic farming: Science and practice for profitable
livestock and cropping. Ed. A. Hopkins (British Grassland Society:
Reading, UK) pp. 188–191.
Long, C.A., Wu, Z. and Deng, B.X. (2005) Biological control of
Penicillium italicum of citrus and Botrytis cinerea of grape by Strain
34-9 of Kloeckera apiculata. European Food Research and Technol-
ogy 221, 197–201.
van Loon, L.C. (2007) Plant responses to plant growth-promoting
rhizobacteria. European Journal of Plant Pathology 119, 243–
254.
Louis, C., Girard, M., Kuhl, G. and Lopez-Ferber, M. (1996)
Persistence of Botrytis cinerea in its vector Drosophila melanogaster.
Phytopathology 89, 934–939.
Machowicz-Stefaniak, Z. (1998) Antagonistic activity of epiphytic
fungi from grape-vine against Botrytis cinerea Pers. Phytopatholo-
gia Polonica 16, 45–52.
Magarey, P., Wachtel, M. and Emmett, R. (1994) Downy mildew.
In: Diseases and Pests. Eds. P. Nicholas, P. Magarey and M.
Wachtel (Winetitles: Marleston, South Australia) pp. 6–11.
Mahaffee, W.F. and Scheuerell, S.J. (2006) Compost teas: Alterna-
tive approaches to the biological control of plant diseases. In:
Microbial ecology of aerial plant surfaces. Eds. M.J. Bailey, A.K.
Lilley, T.M. Timms-Wilson and P.T.N. Spencer-Phillips (Cabi:
Wallingford, UK) pp. 165–179.
Manonmani, K., Jayasekhar, M., Justin, C.G.L. and
Thangaselvabai, T. (2007) Induced systemic resistance (ISR) in
plant disease management – A review. Agricultural Reviews 28,
42–48.
Martin, S.R. (1990) Systematic management to minimize botrytis
bunch rot in three victorian vineyards. Australian & New Zealand
Wine Industry Journal 5, 235–237.
McClellan, W.D. and Hewitt, W.B. (1973) Early Botrytis rot of
grapes: Time of infection and latency of Botrytis cinerea Pers. in Vitis
vinifera L. Phytopathology 63, 1151–1157.
McGourty, G.T. and Reganold, J.P. (2005) Managing vineyard soil
organic matter with cover crops. Proceedings of the Soil Environ-
ment and Vine Mineral Nutrition Symposium (American Society
for Enology and Viticulture: Davis, USA) pp. 145–151.
McLaren, R.G. and Cameron, K.C. (1994) Soil science (Oxford
University Press: Auckland).
Mercier, J. and Wilson, C.L. (1994) Colonization of apple wounds
by naturally-occurring microflora and introduced Candida oleo-
phila and their effect on infection by Botrytis cinerea during storage.
Biological Control 4, 138–144.
Miceli, A., Ippolito, A., Linsalata, V. and Nigro, F. (1999) Effect of
preharvest calcium treatments on decay and biochemical changes
in table grape during storage. Phytopathologia Mediterranea 38,
47–53.
Mohamed, N., Lherminier, J., Farmer, M.J., Fromentin, J., Beno,
N., Houot, V., Milat, M.L. and Blein, J.P. (2007) Defense
responses in grapevine leaves against Botrytis cinerea induced by
application of a Pythium oligandrum strain or its elicitin, oligandrin,
to roots. Phytopathology 97, 611–620.
© 2009 Australian Society of Viticulture and Oenology Inc.
Jacometti et al.
Morandi, M.A.B., Sutton, J.C. and Maffia, L.A. (2000) Effects of
host and microbial factors on development of Clonostachys rosea
and control of Botrytis cinerea in rose. European Journal of Plant
Pathology 106, 439–448.
Morando, A., Bevione, D., Morando, P. and Ravizza, G. (2000)
Powdery mildew control and collateral effects on grey mould and
acid rot. Atti Giornate Fitopatologiche (Universita degli Studi di
Bologna: Bologna, Italy) pp. 227–230.
Mullins, M.G., Bouquet, A. and Williams, L.E. (1992) Biology of
the grapevine. (Cambridge University Press: Cambridge, New
York).
Mundy, D.C. (2008) A review of the direct and indirect effects of
nitrogen on botrytis bunch rot in wine grapes. New Zealand Plant
Protection 61, 306–310.
Nair, N.G. and Hill, G.K. (1992) Bunch rot of grapes caused by
Botrytis cinerea. In: Plant diseases of international importance:
Diseases of fruit crops. Eds. J. Kumar, H.S. Chaube, U.S. Singh
and A.N. Mukhopadhyay (Prentice Hall: Englewood Cliffs, USA)
pp. 147–169.
Nair, N.G., Guilbaud-Oulton, S., Barchia, I. and Emmett, R.W.
(1995) Significance of carry over inoculum, flower infection and
latency on the incidence of Botrytis cinerea in berries of grapevines
at harvest in New South Wales. Australian Journal of Experimen-
tal Agriculture 35, 1177–1180.
Nelson, M.E. and Powelson, M.L. (1988) Biological control of gray
mold of snap beans by Trichoderma hamatum. Plant Disease 72,
727–729.
Nicholas, P., Magarey, P. and Wachtel, M. (1994) Diseases and
Pests (Winetitles: Marleston, South Australia).
Northover, J. and Timmer, L.W. (2002) Control of plant diseases
with petroleum and plant derived oils. In: Spray oils beyond 2000:
Sustainable pest and disease management. Eds. A. Beattie, D.
Watson, M. Stevens, D. Rae and R. Spooner-Hart (University of
Western Sydney: Sydney, Australia) pp. 512–527.
Olson, H.A. and Benson, D.M. (2007) Induced systemic resistance
and the role of binucleate Rhizoctonia and Trichoderma hamatum
382 in biocontrol of botrytis blight in geranium. Biological Control
42, 233–241.
Ozcan, M. (2003) Antifungal effects of some turkish spice essential
oils on Aspergillus niger and Botrytis cinerea growth. Zeitschrift fur
Arznei and Gewurzpflanzen 8, 173–175.
Pappas, A.C. (1997) Evolution of fungicide resistance in Botrytis
cinerea in protected crops in Greece. Crop Protection 16, 257–263.
Parat, C., Chaussod, R., Leveque, J., Dousset, S. and Andreux, F.
(2002) The relationship between copper accumulated in vineyard
calcareous soils and soil organic matter and iron. European
Journal of Soil Science 53, 663–669.
Parry, K.E. and Wood, R.K.S. (1958) The adaptation of fungi to
fungicides: Adaptation to copper and mercury salts. Annals of
Applied Biology 46, 446–456.
Pearson, R.C. and Goheen, A.C. (1988) Compendium of grape
diseases (APS Press: St. Paul, Minnosata, USA).
Perazzolli, M., Dagostin, S., Ferrari, A., Elad, Y. and Pertot, I.
(2008) Induction of systemic resistance against Plasmopara viticola
in grapevine by Trichoderma harzianum T39 and benzothiadiazole.
Biological Control 47, 228–234.
Percival, D.C., Sullivan, J.A. and Fisher, K.H. (1993) Effect of
cluster exposure, berry contact and cultivar on cuticular mem-
brane formation and occurrence of bunch rot (Botrytis cinerea Pers
Fr) with three Vitis vinifera L cultivars. Vitis 32, 87–97.
Pizzol, J. and Pintureau, B. (2008) Effect of photoperiod experi-
enced by parents on diapause induction in Trichogramma cacoeciae.
Entomologia Experimentalis Et Applicata 127, 72–77.
Plotto, A., Roberts, D.D. and Roberts, R.G. (2003) Evaluation of
plant essential oils as natural postharvest disease control of tomato
(Lycopersicon esculentum). Acta Horticulturae 628, 737–745.
Rathore, H.S. and Khan, A.A. (2000) Fungicide and herbicide
residue in water. In: Handbook of water analysis. Eds. L. Nollet
(CRC Press: New York, USA) pp. 609–655.
Read, J., Gras, E., Sanson, G.D., Clissold, F. and Brunt, C. (2003)
Does chemical defence decline more in developing leaves that
© 2009 Australian Society of Viticulture and Oenology Inc.
Alternative fungicides for Botrytis cinerea 171
become strong and tough at maturity? Australian Journal of
Botany 51, 489–496.
Redl, H. and Bauer, K. (1990) Prüfung alternativer Mittel auf
deren Wirkung gegenüber Plasmopara viticola und deren Einfluß
auf das Ertagsgeschehen unter österreichischen. Weinbaubedin-
gungen. Mitteilungen Klosterneuburg Rebe und Wein 40, 134–
138.
Reglinski, T., Elmer, P.A.G., Taylor, J.T., Parry, F.J., Marsden, R.
and Wood, P.N. (2005) Suppression of botrytis bunch rot in
Chardonnay grapevines by induction of host resistance and fungal
antagonism. Australasian Plant Pathology 34, 481–488.
Reglinski, T., Poole, P.R., Whitaker, G. and Hoyte, S.M. (1997)
Induced resistance against Sclerotinia sclerotiorum in kiwifruit
leaves. Plant Pathology 46, 716–721.
Renard-Merlier, D., Laruelle, F., Nowak, E., Durand, R. and Reig-
nault, P. (2009) Changes in C12:0, C18:1, C18:2 and C20:2 fatty
acid content in wheat treated with resistance inducers and
infected by powdery mildew. Plant Biology 11, 75–82.
Reuveni, M. and Reuveni, R. (1995) Efficacy of foliar application
of phosphates in controlling powdery mildew fungus on field-
grown winegrapes – Effects on cluster yield and peroxidase-
activity in berries. Journal of Phytopathology 143, 21–25.
Reuveni, R. and Reuveni, M. (1998) Foliar-fertilizer therapy – A
concept in integrated pest management. Crop Protection 17, 111–
118.
Rohwer, C.L. and Erwin, J.E. (2008) Horticultural applications of
jasmonates: A review. Journal of Horticultural Science & Biotech-
nology 83, 283–304.
Rosslenbroich, H.J. and Stuebler, D. (2000) Botrytis cinerea –
History of chemical control and novel fungicides for its manage-
ment. Crop Protection 19, 557–561.
Rous, C. (1993) Cover crops: A practical tool for vineyard manage-
ment (American Society Enology & Viticulture: Davis, California).
Saligkarias, I.D., Gravanis, F.T. and Epton, H.A.S. (2002) Biological
control of Botrytis cinerea on tomato plants by the use of epiphytic
yeasts Candida guilliermondii strains 101 and US 7 and Candida
oleophila strain I-182: in vivo studies. Biological Control 25, 143–
150.
Salmon, P.T., Clark, W.R. and Clark, D.O. (1992) Vertebrates:
Mammals. In: Grape pest management. Eds. D.L. Flaherty (ANR
Publications: California, USA) pp. 297–311.
Savage, D.S. and Sall, M.A. (1984) Botrytis bunch rot of grapes:
Influence of trellis type and canopy microclimate. Phytopathology
74, 65–70.
Schena, L., Nigro, F., Soleti Ligorio, V., Yaseen, T., El Ghaouth, A.
and Ippolito, A. (2004) Biocontrol activity of Bio-Coat and
Biosure against postharvest rots of table grapes and sweet cherries.
Central Valley Postharvest Newsletter 13, 10.
Scheuerell, S. and Mahaffee, W. (2000) Assessing aerated and
non-aerated watery fermented compost and Trichoderma har-
zianum T-22 for control of powdery mildew (Sphaerotheca pannosa
var. rosae) of rose in the Willamette Valley, Oregon (abstract).
Phytopathology 90, 69.
Scheuerell, S. and Mahaffee, W. (2002) Compost tea: Principles
and prospects for plant disease control. Compost Science & Utili-
zation 10, 313–338.
Schilder, A.M.C., Gillett, J.M., Sysak, R.W. and Wise, J.C. (2002)
Evaluation of environmentally friendly products for control of
fungal diseases of grapes. Proceedings of the 10th International
Conference on Cultivation Technique and Phytopathological
Problems in Organic Fruit-Growing and Viticulture (Foko:
Weinsberg, Germany) pp. 163–167.
Schmitt, A., Kunz, S., Nandi, S., Seddon, B. and Ernst, A. (2002)
Use of Reynoutria sachalinensis plant extracts, clay preparations
and Brevibacillus brevis against fungal diseases of grape berries.
Proceedings of the 10th International Conference on Cultivation
Technique and Phytopathological Problems in Organic Fruit-
Growing and Viticulture (Foko: Weinsberg, Germany) pp. 146–
151.
Sesan, T., Oprea, M., Podosu Cristescu, A., Tica, C. and Oancea, F.
(1999) Biocontrol of Botrytis cinerea on grapevine with Trichoderma
172 Alternative fungicides for Botrytis cinerea
spp. and Saccharomyces chevalieri. Bulletin of the Polish Academy of
Biological Sciences 47, 197–205.
Seyb, A.M. (2004) Botrytis cinerea inoculum sources in the vineyard
system. PhD Thesis, Lincoln University, Canterbury, New Zealand,
227 pp.
Siggelkow, C. and Jackel, B. (1998) Side effects of plant tonics on
predatory mites. Nachrichtenblatt des Deutschen Pflanzenschutz-
dienstes 50, 278–284.
Soyez, J.L. (2002) Lessons from the 2002 campaign on the use of
potassium phosphonate PK2 in viticulture. Progres Agricole et
Viticole 119, 511–514.
Stewart, A. (2001) Commercial biocontrol – Reality or fantasy?
Australasian Plant Pathology 30, 127–131.
Tan, S.Y. and Crabtree, G.D. (1990) Competition between peren-
nial ryegrass sod and Chardonnay wine grapes for mineral nutri-
ents. Hortscience 25, 533–535.
Tanović, B., Milijašević, S., Todorović, B., Potočnik, I. and
Rekanović, E. (2005) Toxicity of essential oils to Botrytis cinerea
Pers in vitro. Pesticidi i fitomedicina 20, 109–114.
Tapio, E. and Pohtolahdenpera, A. (1991) Scanning electron-
microscopy of hyphal interaction between Streptomyces griseoviridis
and some plant pathogenic fungi. Journal of Agricultural Science
in Finland 63, 435–441.
Tegegne, G. and Pretorius, J.C. (2007) In vitro and in vivo antifungal
activity of crude extracts and powdered dry material from Ethio-
pian wild plants against economically important plant pathogens.
BioControl 52, 877–888.
Tripathi, P., Dubey, N.K. and Shukla, A.K. (2008) Use of some
essential oils as post-harvest botanical fungicides in the manage-
ment of grey mould of grapes caused by Botrytis cinerea. World
Journal of Microbiology and Biotechnology 24, 39–46.
Trotel-Aziz, P., Couderchet, M., Biagianti, S. and Aziz, A. (2008)
Characterization of new bacterial biocontrol agents Acinetobacter,
Bacillus, Pantoea and Pseudomonas spp. mediating grapevine resis-
tance against Botrytis cinerea. Environmental and Experimental
Botany 64, 21–32.
Tzortzakis, N.G. and Economakis, C.D. (2007) Antifungal activity
of lemongrass (Cymbopogon citratus L.) essential oil against key
postharvest pathogens. Innovative Food Science and Emerging
Technologies 8, 253–258.
Utkhede, R.S. and Mathur, S. (2002) Biological control of stem
canker of greenhouse tomatoes caused by Botrytis cinerea. Cana-
dian Journal of Microbiology 48, 550–554.
Vasyukova, N.I. and Ozeretskovskaya, O.L. (2007) Induced plant
resistance and salicylic acid: A review. Applied Biochemistry and
Microbiology 43, 367–373.
Vidhyasekaran, P. (2004) Biological control – Microbial pesticides.
In: Concise encyclopedia of plant pathology. Ed. P. Vidhyasekaran
(Food Products Press: Binghamton, USA) pp. 239–270.
Vinale, F., Sivasithamparam, K., Ghisalberti, E.L., Marra, R., Woo,
S.L. and Lorito, M. (2008) Trichoderma-plant-pathogen interac-
tions. Soil Biology & Biochemistry 40, 1–10.
Vyas, S.C. (1988) Soil microorganisms and their activities. In:
Non-target effects of agricultural fungicides. Eds. C.V. Suhash
(CRC Press Inc: Florida, USA) pp. 258.
Walter, M., Jaspers, M.V., Frampton, C.M. and Stewart, A. (2001)
Control of Botrytis cinerea in grape using thyme oil. Australasian
Plant Pathology 30, 21–25.
Webber, J.F. and Gibbs, J.N. (1989) Insect dissemination of fungal
pathogens of trees. In: Insect-fungus interactions. Eds. N.
Wilding, N.M. Collins, P.M. Hammond and J.F. Webber (Aca-
demic Press: London, UK) pp. 161–189.
Australian Journal of Grape and Wine Research 16, 154–172, 2010
Whipps, J.M. (1997) Ecological considerations involved in com-
mercial development of biological control agents for soil-borne
diseases. In: Modern Soil Microbiology. Eds. J.D. van Elsas, J.T.
Trevors and E.M.H. Wellington (Marcel Dekker Inc: New York,
USA) pp. 525–546.
Whipps, J.M. and Lumsden, R.D. (2001) Commercial use of fungi
as plant disease biological control agents: Status and prospects. In:
Fungi as biocontrol agents. Eds. T. M. Butt, C. Jackson and N.
Magan (CABI: Wallingford, Oxon, UK) pp. 9–22.
White, J.G., Linfield, C.A., Lahdenpera, M.L. and Uoti, J. (1990)
Mycostop – A novel biofungicide based on Streptomyces
griseoviridis. Brighton Crop Protection Conference – Pests and
Diseases. (British Crop Protection Council: Farnham, UK) pp.
221–226.
Williamson, B. (1994) Latency and quiescence in survival and
success of fungal plant-pathogens. In: Ecology of plant pathogens.
Eds. J.P. Blakeman and B. Williamson (CAB International: Wall-
ingford, UK) pp. 187–207.
Williamson, B., Tudzynsk, B., Tudzynski, P. and van Kan, J.A.L.
(2007) Botrytis cinerea: The cause of grey mould disease. Molecular
Plant Pathology 8, 561–580.
Wilson, C.L., Solar, J.M., El Ghaouth, A. and Wisniewski, M.E.
(1997) Rapid evaluation of plant extracts and essential oils for
antifungal activity against Botrytis cinerea. Plant Disease 81, 204–
210.
Wisniewski, M., Biles, C., Droby, S., McLaughlin, R., Wilson, C.
and Chalutz, E. (1991) Mode of action of the postharvest
biocontrol yeast, Pichia guilliermondii: 1. Characterization of
attachment to Botrytis cinerea. Physiological and Molecular Plant
Pathology 39, 245–258.
Wolpert, J.A., Phillips, P.A., Striegler, R.K., McKenry, M.V. and
Foott, J.H. (1993) Berber orchardgrass tested as cover crop in
commercial vineyard. California Agriculture 47, 23–25.
Wratten, S.D., Bowie, M.H., Hickman, J.M., Evans, A.M., Sedcole,
J.R. and Tylianakis, J.M. (2003) Field boundaries as barriers to
movement of hover flies (Diptera: Syrphidae) in cultivated land.
Oecologia 134, 605–611.
Yedidia, I., Shoresh, M., Kerem, Z., Benhamou, N., Kapulnik, Y.
and Chet, I. (2003) Concomitant induction of systemic resistance
to Pseudomonas spingae pv. lachrymans in cucumber by Trichoderma
asperellum (T-203) and accumulation of phytoalexins. Applied and
Environmental Microbiology 69, 7343–7353.
Young, S. (2008) New Zealand Agrichemical manual (Agri Media
Ltd: Christchurch, New Zealand).
Zehnder, G., Gurr, G.M., Kuhne, S., Wade, M.R., Wratten, S.D.
and Wyss, E. (2007) Arthropod pest management in organic
crops. Annual Review of Entomology 52, 57–80.
Zimand, G., Elad, Y. and Chet, I. (1996) Effect of Trichoderma
harzianum on Botrytis cinerea pathogenicity. Phytopathology 86,
1255–1260.
Zimmerli, L., Metraux, J.P. and Mauch-Mani, B. (2001) beta-
aminobutyric acid-induced protection of Arabidopsis against the
necrotrophic fungus Botrytis cinerea. Plant Physiology 126, 517–
523.
Manuscript received: 9 November 2008
Revised manuscript received: 9 August 2009
Accepted: 10 August 2009
© 2009 Australian Society of Viticulture and Oenology Inc.