Chapter 14

Grape Berry Moths in Western European

Vineyards and Their Recent Movement
into the New World
Claudio Ioriatti, Andrea Lucchi, and Lucia G. Varela

14.1

Introduction

This chapter addresses the topic of pest biology and management for cluster-feeding
Lepidoptera of European origin, from the viewpoint of applied entomologists
working in Europe and North America. We describe the main biological, morphological, and behavioral features of the Palaearctic moths harmful to grapes. Five
species of Lepidoptera feed on grape clusters in Europe. Lobesia botrana (Denis &
Schiffermller) and Eupoecilia ambiguella (Hbner) are key pests that require specific control measures. Argyrotaenia ljungiana (Thunberg), Cryptoblabes gnidiella
(Millire) and Ephestia parasitella unicolorella Staudinger are occasionally harmful to vineyards. As the five species are similar in size and occur almost in the same
ecological niche, morphological features allowing species identification are provided in Table 14.1. For comparison, a description of the North American grape
berry moth Paralobesia viteana (Clemens) is provided by Isaacs et al. (Chap. 15).

C. Ioriatti (*)
Centre for Technology Transfer, FEM-IASMA, 38010 San Michele allAdige, TN, Italy
e-mail: claudio.ioriatti@iasma.it
A. Lucchi
Department of CDSL, Section of Agricultural Entomology, University of Pisa,
Via del Borghetto 80, 56124 Pisa, Italy
e-mail: alucchi@agr.unipi.it
L.G. Varela
UC Cooperative Extension, Division of Agriculture and Natural Resources,
University of California, 133 Aviation Blvd., Suite 109,
Santa Rosa, CA 95403-2894, USA
e-mail: lgvarela@ucdavis.edu

N.J. Bostanian et al. (eds.), Arthropod Management in Vineyards: Pests, Approaches,

and Future Directions, DOI 10.1007/978-94-007-4032-7_14,
Springer Science+Business Media B.V. 2012

339

Tortricidae,
Olethreutinae

Cryptoblabes
gnidiella

Pyralidae,
Phycitinae

Eupoecilia
Tortricidae,
ambiguella
Tortricinae

Species
Lobesia
botrana

Family,
sub family

First instar
Egg
larva
Fifth instar larva
0.6 0.7 mm
1 mm
10 mm
Slightly elliptical,
Creamy white Tan to yellowish brown head
yellow straw at
with a
and prothoracic shield,
laying, gradually
black head
rear edge of the
turns to transparprothoracic shield has a
ent light gray with
darker brown to black
bright iridescent
border. White tubercles
reflections
at the base of the body
hairs. Anal comb has 56
dark brown teeth
Wingspan 1215 mm
0.6 0.8 mm
1 mm
12 mm
Forewings yellow-brown with
Light yellow when
Creamy white Reddish to brownish yellow
dark brown band. Hind wings
first laid later
with brown
with bristles over its
slate gray fringed
becoming spotted
head
whole body. Head
with bright orange
capsules and prothoracic
plate and thoracic legs
are black. Anal comb
with 67 teeth
Wingspan 15 mm
0.7 0.4 mm
1 mm
11 mm
Forewings dark gray, punctuated Subcircolar shape
Light yellow
Yellow to light brown body
by tiny black spots, veiled in
with one slightly
with brown
with two narrow
white and dotted with reddish
flatter pole. White
head
longitudinal darker bands
scales characterized by
at laying, it
on the dorsal side.
indistinct lighter bands. Hind
gradually assumes
Brown-reddish head with
wings shiny white and
a yellowish color
small black areas at the
streaked with terminal gray
base of blackish bristles
lines. Horn-shaped process on
the third male antennomerous

Adult
Wingspan 1113 mm.
Forewings tan-cream, mottled
with gray-blue, brown, and
black blotches. Hindwings
gray with a fringed border.
Wings held in a bell shape
over the abdomen at rest

Table 14.1 Main morphological features of the principal grape cluster-feeding moth pests in European vineyards

7 mm
Brown-reddish which will
turn gradually toward
the dark red. Very
sharp creamy
abdomen, distally
displays oblique
hooks

57 mm
Reddish brown.
Cremaster with 16
hooked bristles.
Female pupae
generally more stocky
and larger than males

Pupa
46 mm
Slim with the cranial and
the caudal end
rounded. Cremaster
with 8 hooked bristles.
Female pupae
generally more stocky
and larger than males

Wingspan 1216 mm
Forewing silver-white, strigulated Batches of 4050,
with gray; markings dark
yellow, turning
reddish brown, sprinkled with
brown during
black; margins of basal and
development
median fasciae irregular.
Hindwing gray

Argyrotaenia
ljungiana

Tortricidae,
Tortricinae

Wingspan 1518 mm
Fore wings light brown with
Subcircur shape,
transverse reddish brown and
white at laying
barely perceptible strips

Ephestia
Pyralidae,
parasitella
Phycitinae
unicolorella

10 mm
78 mm
White-pinkish Light yellow body with
Reddish-brown
with dark
shades of pink and
brown
numerous bristles with
head
elongated blackish hair
tubercles. Reddish head
18 mm
Clear green body. Light
Pale brown; in a silken
green or yellowish green
cocoon in spun leaves,
head. Anal comb with
or overwintering in a
68 prongs
cocoon in debris on
the ground

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C. Ioriatti et al.

14.2 Lobesia botrana and Eupoecilia ambiguella

14.2.1

Taxonomy and Occurrence

The European grapevine moth (EGVM) L. botrana was described in 1775 by Denis
and Schiffermller as Tortrix, and subsequently as Eudemis and Polychrosis.
Currently, as Lobesia Guene 1845, it is in the family Tortricidae, subfamily
Olethreutinae, tribe Olethreutini (Razowski 1995). Lobesia botrana is historically
present in Europe, Asia, and Africa (CAB 1974). Although widespread in all
grapevine-growing areas, it is economically important mostly in southern Europe.
In southern France, in central and southern Spain, Portugal, Greece, Italy, and the
islands of the Mediterranean Basin, L. botrana is the only moth species to have an
important impact on grapevine production (Thiry 2005). Recently, it has expanded
its geographic range and was found in Chile in 2008, California in 2009, and
Argentina in 2010 (Gonzales 2010; Varela et al. 2010).
The European grape berry moth (EGBM), E. ambiguella, is considered a significant insect pest in many grapevine-growing areas where it can cause considerable
damage to grapes. It is found from Britain to Japan, from the Mediterranean
Basin to the Scandinavian countries (farther north than grapevine-growing regions)
(CAB 1986). First described by Hbner in 1796 as Tinea ambiguella, it was subsequently included in the genera Cochylis and Clysia and lastly, according to
Razowski (1995), in the genus Eupoecilia. Known as Einbindiger Traubenwickler,
Polilla de la vid, Cochylis de la vigne and Tignola della vite, it was recognized as
the major grape berry pest in Europe until the 1920s. More recently, and in many
areas, it has been gradually replaced as a major pest by L. botrana. The shift started
in the Mediterranean Basin and is now extending to Switzerland, Austria and
southern Germany where populations of L. botrana and E. ambiguella overlap.

14.2.2

Host Plants

Lobesia botrana larvae feed on grapevine flowers and berries and on a number
of other plants growing in warm-dry environments, such as one finds in most
Mediterranean countries. Its host range includes about 40 species belonging to 27
different families (Coscoll 1997). The spurge flax Daphne gnidium L. is hypothesized to be its original host plant (Bovey 1966; Lucchi and Santini 2011; Tasin
et al. 2011). However EGVM is frequently associated with other hosts in habitats
where suitable host plants occur. These hosts include for example olive tree inflorescence, Virginia creeper, jujube, rosemary, evergreen clematis, dogwood, ivy,
currant (Bovey 1966; Coscoll 1997; Stavridis and Savopoulou-Soultani 1998;
Thiry 2005). Eupoecilia ambiguella is also polyphagous and shares several host
plants with EGVM. Even though mugwort, Artemisia vulgaris L., is sometimes
reported as its native host plant, grapevine is now accepted as its original host.

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343

Other cultivated and wild host plants include black and red currant, lemon citrus,
Virginia creeper, blackthorn, smooth bedstraw, wayfaring tree, highbush cranberry,
laureltinus, privet, ash, maple, dogwood, and many others (Solinas 1962). Since
grape berry moths are mostly restricted to grapevines in grapevine-growing areas,
the nutritional and ecological polyphagy of these two tortricid species needs to be
researched.

14.2.3

Life History

Eupoecilia ambiguella and L. botrana have a similar biology, but slightly different
climatic preferences: L. botrana prefers warm and dry conditions and E. ambiguella
prefers cool and humid climates (Bournier 1977). Lobesia botrana and E. ambiguella
are typical multivoltine species with facultative diapause. In northern Europe and in
the Mediterranean Basin, EGVM has 24 generations per year on Vitis vinifera L.,
depending on latitude and microclimates (Roditakis and Karandinos 2001; Harari
et al. 2007). Two to three generations per year are the rule in Germany, Switzerland,
Austria, and northern France. It has three generations in the warmer climates of
southern France, Spain, Portugal, Greece, and Italy, where the species can sometimes
give rise to a fourth flight and a fourth generation, partial or complete. In Israel,
Egypt, and Crete some EGVM populations do not undergo diapause and spend the
winter in the larval stage, continuing to feed on unharvested clusters or on alternate
hosts. EGBM usually has only two generations per year. A third generation has been
frequently observed in France and Italy (Marcelin 1985; Varner and Mattedi 2004).
Lobesia botrana moths are crepuscular insects flying at canopy levels at twilight
(6080 lux). Males are more active than females. The flight of virgin females is
interrupted by several stationary phases, in which they release a pheromone, the
main component of which is (E,Z)-7,9-dodecadienyl acetate (Roelofs et al. 1973).
Eupoecilia ambiguella moths are active from twilight to dawn, resting motionless
during daylight. They feed, call, and mate during the night and early morning.
Females lay eggs in the afternoon and evening (Bovey 1966). The main component
of the pheromone is (Z)-9-dodecenyl acetate (Arn et al. 1976; Saglio et al. 1977).
Adults of L. botrana (Fig. 14.1a) feed from emergence to sexual maturity. Mating
occurs about 24 h after emergence and oviposition starts 3 days thereafter. Mating
lasts from a few minutes to 2 h. Males mate several times with different females,
and females have a rare tendency toward polyandry. Males are much less attracted
to mated females than to virgins. On average a female lays from 50 to 80 eggs
(Fig. 14.1b, c), most of which are laid in the first week of life. The average life span
of the adult moth is approximately 1520 days, usually shorter for males than
females. The first generation of both species develops on flowers (anthophagous)
and the other generations on berries (carpophagous) (Figs. 14.1d and 14.2bd).
Single eggs are laid on bracts, caps and stems of the flower clusters in spring and
on the berries in summer. First generation larvae feed on several pre-bloom flowers

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Fig. 14.1 Lobesia botrana (a) adult, (b) egg, (c) egg in the black-head stage, (d) larva, (e) pupa

and web them together with silk. Webbing gradually thickens to form the so-called
glomerulus or nest (Fig. 14.2a).
In hot weather, E. ambiguella larvae sometimes bore into the rachis and peduncle,
seeking moisture. Within the glomerulus, EGBM larvae construct a silk case to which
they retreat during the hottest hours of the day. In these nests, the hidden larvae feed
on flowers whose remnants are used to increase the size of the case. First generation
grape berry moths eventually pupate either inside the glomerulus or on the underside
of a leaf (Figs. 14.1e and 14.3d). Their pupal stage lasts about 2 weeks.
The emerging moths (Fig. 14.3a) lay single eggs on the berries (Fig. 14.3b).
EGBM hardly ever lays eggs on the rachis or on peduncles. After hatching, the

Fig. 14.2 Lobesia botrana (a) larval nest, (b, c) injured berries, (d) grape cluster infected by gray
mold and sour rot

Fig. 14.3 Eupoecilia ambiguella (a) adult, (b) egg, (c) larva, (d) pupa

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larvae (Fig. 14.3c) feed on the berries and may cause severe damage. When disturbed they drop down on a silk thread. European grape berry moth larvae are sluggish while EGVM larvae are highly mobile. Feeding on berries promotes infection
by gray mold (Botrytis cinerea Persoon ex Fries), which leads to even greater injury
than that caused by the insect itself. Non-diapausing larvae pupate preferably within
the cluster or on the leaves. Photoperiod induces diapause that lasts for months, but
mature EGBM larvae stay for several months in a prepupal stage and low temperatures are necessary to advance to the pupal stage (Fig. 14.3d). The diapausing larvae
build their cocoons mainly under exfoliating bark, in crevices and cracks of the
trunk and cordons.

14.2.4

Economic Importance and Control

14.2.4.1

Grape Berry Moth Damage

The two species are quite similar in behavior and damage. Sometimes they are present at the same time in the same vineyard but with a different degree of population
density. Until the end of the nineteenth century, E. ambiguella was widespread in all
the southern European regions. From the beginning of the twentieth century,
L. botrana gradually became the predominant species south of the Alps.
Grape berry moth infestation levels depend on the growth characteristics of the
cultivars, the agronomic practices, the climatic conditions, and the number of generations per year. The anthophagous generation does not generally cause yield reduction.
The following carpophagous generations are the most destructive due to larval feeding
on green and ripe berries, which results in yield reduction. The presence of larvae, webbing and rotten berries, leads to downgrading of table grapes. Moreover, secondary
infections of gray mold, B. cinerea, develop rapidly on damaged berries causing bunch
rot which substantially degrades wine quality. Black aspergillis rot, Aspergillus niger
and A. carbonarius, producers of ochratoxin A (Cozzi et al. 2006), are also often related
to larval feeding activity. Because of these undesirable economic effects, L. botrana
and E. ambiguella must be managed to keep their damage at an acceptable level.

14.2.4.2

Population Density and Risk Assessment

Time of the first appearance of adults and hatching of the first eggs can be forecasted
by predictive models based on temperature requirements of individual instars and
critical conditions for oviposition (Moravie et al. 2006). Unfortunately, forecast
models based on DD are empirical and their robustness is strongly dependent on the
environment in which they have been validated. Alternative forecasting techniques
are currently under development, such as the evaluation of larval age distribution
during the previous generation in order to predict the distribution of female emergence (Delbac et al. 2010).

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347

Trapping females with food-baited traps is a valuable tool to predict the onset of
oviposition, an event used to properly time insecticide treatments (Thiry et al.
2006). However, baited-trap maintenance and monitoring are very time-consuming
chores for growers and consultants. Pheromone traps are easier to use. They are a
sensitive tool to monitor flight of males. They can be useful to time an ovicidal treatment, and to properly schedule scouting activities in the vineyard.
Forecasting models and moth trapping alone do not provide sufficient population
density information and need to be supplemented with appropriate field scouting of
eggs and young larvae (Shahini et al. 2010). Based on the resulting infestation
assessment (% of injured clusters, number of nests per inflorescence, number of eggs
and larvae per cluster, number of injured berries per cluster), insecticides are
applied according to action thresholds (AT). The action thresholds vary widely
depending on the generation, susceptibility of the cultivar to the subsequent infection by B. cinerea, as well as whether berries are produced for table grape, raisins or
wine production.
First generation larvae may not necessarily need to be controlled by chemical
treatments, especially if they develop on cultivars with abundant blossom not subject
to intense shedding. Between flowering and harvest, damage to inflorescences is
compensated by the increase in weight of uninjured berries in the majority of cultivars.
That explains the lack of a defined injury threshold for the anthophagous generation
(Moschos 2005).
Chemical control for the first generation is exclusively applied when the pest population density is particularly high or if it exceeds an AT of more than 50% infested
inflorescences (Bagnoli et al. 2009). For the following generations, the suggested AT
ranges from 5% to 15% of infested (eggs or young larvae) clusters respectively for
compact and loosely-bunched cultivars, according to their susceptibility to rot.
Knowledge of the spatial distribution of the population is important for the development of efficient sampling programs, that allow a more accurate estimate of the
damage and AT.

14.2.4.3

Natural Enemies and Biological Control

The cohort of L. botrana and E. ambiguella natural enemies varies considerably in

time and space due to insect physiology, activity and ecological niche of individual
species. Fungi of the genera Spicaria, Beauveria, Paecilomyces, Aspergillus,
Cephalosporium, Cladosporium, Penicillium, Citromyces, Verticillium and Stemphylium can infect a large percentage of overwintering pupae. The bacteria Bacillus
thuringiensis Berliner var. kurstaki (Btk) and var. aizawai are effectively and extensively used against EGVM and EGBM, both in conventional and organic vineyards
(Scalco et al. 1997; Vidal 1997; Keil and Schruft 1998; Shahini et al. 2010). Arthropods
associated with grape berry moths include predators such as spiders (Clubionidae,
Theridiidae, Tomisidae, Linyphiidae, Salticidae), mites (Thrombididae) and insects
belonging to Dermaptera, Hemiptera, Neuroptera, Diptera and Coleoptera (Solinas
1962; Coscoll 1997). Among insect parasitoids, species associated with EGVM in

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Europe belong to the Hymenoptera (Ichneumonidae, Braconidae, Chalcididae,

Pteromalidae, Eulophidae, Elasmidae, Trichogrammatidae) and Diptera
(Tachinidae). As with most natural enemies including parasitoids, the natural control achieved by each species varies greatly in time and space. Typically, the frequency of egg and larval parasitism is high in the first two generations and decreases
drastically in the overwintering generation, which is mainly affected by larval-pupal
and pupal parasitoids.
Extensive scientific efforts to develop biological control as an effective solution for practical use in the field are still needed. Egg parasitoids of the genus
Trichogramma have been mass-released in an inundative strategy with mixed results
(Castaneda-Samayoa et al. 1993; Hommay et al. 2002; Ibrahim 2004). The pteromalids Dibrachys affinis Masi and D. cavus (Walker) are gregarious generalist
larval-pupal parasitoids of Lepidoptera, Diptera and Hymenoptera that can be readily
reared in the laboratory. However, due to lack of host specificity and because they
are also hyperparasites, they are not good candidates for release. The most frequent
and efficient species in European vineyards is the larval parasitoid Campoplex
capitator Aubert (Ichneumonidae). It is regarded as the best candidate for EGVM
biological control, but to date, releases have not taken place because of the difficulties
associated with artificially mass-rearing the species (Thiry and Xureb 2004).
14.2.4.4

Chemical Control

Most insecticides applied in the past against grape berry moths have been gradually
replaced by more selective and less toxic products. New neurotoxic insecticides
(spinosyns and oxadiazines), chitin synthesis inhibitors, compounds accelerating
molting, microbial insecticides, and more recently some avermectins and anthranilic diamides, have been introduced in current integrated control strategies.
Nevertheless, the organophosphates chlorpyriphos and methyl chlorpyriphos are
still largely used in European vineyards. Control with insecticides that are larvicidal
with some ovicidal activity gives remarkable flexibility on application timing. The
efficacy of these products depends on the optimal treatment of the most susceptible
stages, so prediction of life cycle events is critical for each moth species. Because
of increasing accuracy of the forecasting tools, a single insecticide application to
control the second generation of either species is usually effective in most grapevine
districts in Europe. More treatments are needed in the southern regions to control
L. botrana. In terms of selectivity, B. thuringiensis has undoubtedly the highest
ecological value, but its use is still limited due to its short persistence. Successful
application timing can be achieved with adequate population monitoring with pheromone traps and egg field scouting.
14.2.4.5

Pheromone-Mediated Control Strategies

The use of pheromones for control of grape berry moths has increased in vineyards due to the high selectivity and low environmental impact. Mating disruption

14 Grape Berry Moths in European Vineyards

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Table 14.2 European vineyards treated with pheromone mating disruption for management of
grape berry moth pests during 2010 (IBMA 2011) in relation to the total vineyard surface of
each country (OIV 2007)
Country
Total vineyard surface (ha)
Vineyard treated with MD (ha)
% treated
Germany
102,000
70,000
68.6
France
867,000
20,000
2.3
Italy
847,000
16,500
1.9
Spain
1,169,000
14,500
1.2
Switzerland
14,800
7,000
47.3
Austria
49,900
2,400
4.8
Czech Republic
17,700
1,300
7.3
Portugal
248,000
1,200
0.5
Hungary
75,000
300
0.4
Slovakia
17,600
100
0.6
Cyprus
15,300
100
0.7
Total
3,423,300
133,400
3.9

(MD) with hand-applied dispensers is the most well-studied and widely used
pheromone-mediated control technique against grape berry moths in the European
grapevine-growing regions (Stockel et al. 1992; Neumann et al. 1993; Charmillot
and Pasquier 2000). Currently it is applied on approximately 140,000 ha in European
vineyards, i.e. about 34% of the total grapevine-growing area in the European
Union (Table 14.2). Recent MD area-wide applications have also been conducted in
Chile and California where EGVM was accidentally introduced (Witzgall et al.
2010; Ioriatti et al. 2011).
The most common hand-applied dispensers available on the market for grape
berry moths are Shin-Etsu twist-ties ropes (Isonet L, Lplus, LE in Europe;
Isomate in the US), the BASF twin ampoules (RAK1+2, RAK 2) and, for EGVM
only, the Suterra membranes. The active ingredients in these dispensers are the
main pheromone components, (E,Z)-7,9-dodecenyl acetate and (Z)-9-dodecenyl
acetate for EGVM and EGBM, respectively.
Five hundred dispensers per hectare (the number of dispensers may vary depending on manufacturer) must be deployed in the vineyards before the onset of the
first seasonal flight, because late deployment will likely cause control failures.
Dispensers must be evenly distributed in the vineyard, and should be attached to
vine shoots to ensure protection by foliage from direct exposure to sun and high
temperatures. Twice as many dispensers must be hung along the vineyard edges.
Border effects are obviously much reduced when MD is applied in area wide projects as in certain growing regions of Germany, France, Switzerland, northern Italy,
and Spain (Kast 2001; Ioriatti et al. 2008).
Depending on the vineyard layout, the time to attach the dispensers on the
vines may vary between 1.5 and 3 h/ha. The surface area of vineyards in Europe
under pheromone-mediated (MD) control of grape berry moths is still limited,
despite intensive research and substantial experience with practical applications
during the last two decades. This is because of socio-cultural and economical
conditions existing in the different vine growing areas where interest in innovative

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methods is often low. Increasing quality standards for wine and table grapes, with
respect to pesticide residues, are creating new opportunities for extensive adoption of MD in IPM programs. However, high costs of MD (about 110 /ha for
EGVM and 150 /ha for both insects) have hampered the diffusion of this method
to date. Cost reduction must be considered for a wider adoption of MD in European
vineyards.
Novel pheromone application systems to control Lepidoptera pests such as autoconfusion, lure and kill, aerosol puffers, microencapsulated sprayables, and nanofibers may represent future opportunity for grape berry moth control (Underwood
et al. 2002; Charmillot et al. 2005; Nansen et al. 2007; Anfora et al. 2008; Hein
et al. 2011). New investments in fundamental research are critical for an effective
improvement in semiochemical applications. The research should address the reproductive, physiological, and behavioral mechanisms by which the pheromone affects
the target insects, as well as explain how volatile compounds are involved in tritrophic
interactions.

14.2.4.6 Lobesia botrana as an Invasive Species in the Americas

It was first detected in Chile in April of 2008. Grapes are grown from the region of
Atacama in the north to the region of Araucana in the south. In surveys conducted
in the growing season of 20082009, moths were detected in all grapevine-growing
regions. Low levels of catches were detected in the 20102011 season in grapevinegrowing areas from Atacama to Araucana. However, large urban areas remain as
moth reservoirs. The current control strategy is to attempt eradication of the pest
and major efforts are concentrated towards vineyards and urban areas surrounding
grapevine-growing areas. After three seasons of control with insecticide and MD,
moth catches in monitoring traps have decreased significantly and the number of
foci per region has also decreased considerably.
In the United States, the first report of this pest was in September 2009 in the
Napa Valley, California. Surveys conducted in 2010 show that the highest infestation is in Napa County, with a few moths detected, and a few foci in nine other
counties of California. No detection has been made in any other US state, despite
trap-based surveillance in many of the primary grape production regions. The strategy in California is also eradication and in the first year of control populations
decreased dramatically from the first to the third generation.
It is unclear how EGVM was first introduced into Chile or California. At low population levels the damage caused by the larvae is inconspicuous. By the time the first
infestations are detected, the spread may be extensive due primarily to movement of
grapevines with undetected infestations and movement of unsanitized machinery.
In both Chile and California the primary host for EGVM is grapevine flower
clusters and berries. In extensive surveys in Chile it has only been detected in plums
next to an infested vineyard. In California, it has been detected in low numbers only
in olive flowers adjacent to vineyards. To date, surveys conducted in riparian vegetation in infested areas of California have not detected larvae in wild grapes.

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Chile began eradication programs 2 years before California. In the first year,
control measures were applied to vineyards to a radius of 5,000 m from a detection
site. This was reduced to 1,000 m the following year. The recommendations are to
make two insecticide applications for the first generation, one for the second and
one for the third generation, plus the application of pheromone dispensers for mating disruption. In urban districts surrounding grapevine-growing areas, homeowners have a choice of destroying the fruit or accepting insecticide treatments.
In California, EGVM has three generations a year. In the first year control measures were applied to a radius of 1,000 m from a detection site and it was reduced to
500 m the following year. With the goal of eradicating the pest, one insecticide
application is targeted for each of the first and second generations, when the larvae
are most exposed. To further suppress populations the use of MD dispensers (the
product registered as Isomate-EGVM in the US) is highly encouraged. Control in
urban areas has been limited to those counties with low trap catches. Homeowners
mostly adopted fruit removal as a management technique.
Given that the first flight and egg laying period is very extended, if the application
for this generation is done before egg laying or too early in the egg laying period, a
second application may be needed to cover the prolonged egg hatch. Furthermore, at
this time, the flower cluster is rapidly expanding, decreasing the surface covered by
an insecticide. Thus, it is best to wait and time the control of the first generation when
the highest proportion of larvae is about to emerge from eggs. The timing for this
event can be determined by following the male moth flight with pheromone traps and
monitoring egg development. If the insecticide used has some ovicidal properties the
recommendation is to make the application when the heads of the larvae are visible
in 20% of the eggs. When eggs are too few to monitor, treatment is applied shortly
after peak flight. Insecticides registered for organic production are strictly larvicidal
and are applied at egg hatch. Due to the short residue of organic materials, two or
more applications are recommended starting at egg hatch and weekly for as long as
larvae are detected forming glomeruli in the flower cluster.
The insecticide timing for the second generation depends on whether the insecticide has some ovicidal properties or if it is strictly larvicidal. If it is ovicidal, the
applications can start a few days after the first males of the second flight are caught
in a trap. For larvicidal insecticides (conventional or organic), the applications can
start 1014 days after the first moths of the second flight are caught, if eggs are too
few to monitor. The second generation is substantially shorter than the first, lasting
approximately 4 weeks. This makes timing for control of the second generation
easier to predict. If treatments are timed appropriately for the first and second generations, treatment of the third generation should not be necessary. Treatments for
the third generation are limited in their efficacy in California because of overlap
in generations, the difficulty in penetrating a closed cluster and the short period
between egg hatch and the larvae penetrating the berry.
The strategy of targeting control measures towards the first and second generation
supplemented with mating disruption has proven extremely successful at drastically
reducing populations. This is probably aided by the fact that all control measures
are taking place in an area wide manner since all growers are strongly encouraged

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to participate. So far, alternate hosts do not appear to contribute significantly to

population levels. In California, chlorpyriphos is not registered for seasonal use in
vineyards, and the insecticides most used to control L. botrana are insect growth
regulators, diamides and Btk, and to a lesser extent, spinosyns and avermectin. A
major concern of the program was to avoid disruption of natural control of native
pseudococcids pests. This was achieved by using selective insecticides.
A major challenge is to achieve complete control in urban areas. Another challenge is to determine when a population has truly been eradicated. Delimitation of
infestations is done using pheromone traps. Pheromone traps are effective; however
the male moth does not fly more than 100 m, with an average distance <50 m
(Roehrich and Carles 1981). This entails having a very high density of traps with no
catches during several generations. The risk of a false negative is significant since it
will be tempting to declare the pest eradicated when in reality populations are breeding at undetectable levels.
In February 2010, EGVM was also detected in the major grape production region
of the Province of Mendoza in Argentina. As of 2011, the first year of control is
underway.

14.3
14.3.1

Cryptoblabes gnidiella
Taxonomy and Occurrence

Among Pyralidae Phycitinae, the honeydew moth (HM), C. gnidiella (Fig. 14.4ae),
is the most frequent and harmful species on grapes in the Mediterranean Basin.
Described for the first time by Millire in 1867 as Ephestia gnidiella, it was then
reported by Briosi as Albinia wockiana in 1877. The current classification is due to
Hartig (1939), who redescribed the species from specimens collected in central
Italy. Widespread throughout the Mediterranean region, HM is reported from
Malaysia, New Zealand, Hawaii, some African and Asian countries, and many tropical and subtropical regions of North and South America.

14.3.2

Host Plants

Cryptoblabes gnidiella is a polyphagous species associated with about 60 different

host plants belonging to 30 families. These include Actinidia deliciosa (Chevalier),
Citrus spp., Daphne spp., Daucus carota L., Diospyros kaki L., Eriobotrya japonica
(Thunberg) Lindley, Gossypium herbaceum L., Malus spp., Persea Americana
Miller, Prunus spp., Pyrus spp., Ricinus communis L., Tamarix spp., and Vitis spp.
(Zocchi 1971; Yehuda et al. 19911992; Sing and Sing 1997). Very frequently HM
shares the host plant with other insects, either Lepidoptera (e.g., the European
grapevine moth L. botrana) or Hemiptera (aphids and pseudococcids) which

14 Grape Berry Moths in European Vineyards

353

Fig. 14.4 Cryptoblabes gnidiella (a) adult, (b) young larva, (c) mature larva, (d) pupa, (e) infested
clusters

produce honeydew of which HM larvae are active consumers, hence the common
name Honeydew moth.

14.3.3

Life History

In the Mediterranean Basin, C. gnidiella has 34 generations per year depending on

latitude, with a first flight in MayJune, a second in July, a third in AugustSeptember
and a fourth in OctoberNovember, with possible overlapping generations on
late harvest grape varieties (Bagnoli and Lucchi 2001). In Israel the species can have
up to seven generations on grapes and citrus (Avidov and Harpaz 1969). In the
grapevine-growing areas of northeast Brazil, where climatic conditions allow two
annual crops, HM can have as many as nine generations per year (Bisotto-de-Oliveira
et al. 2007). It overwinters as a larva and pupation takes place inside a silken cocoon.
The sex pheromone of Cryptoblabes gnidiella is a mixture of quaternary aldehydes
(Bjostad et al. 1981).

14.3.4

Economic Importance and Control

The economic importance of C. gnidiella varies greatly according to geographical

areas. Though it mainly occurs in coastal areas characterized by heavy infestation of

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L. botrana and Planococcus spp., it is also able to infest healthy pre-veraison grapes,
feeding on cluster stems. During ripening, larvae may feed superficially on berry
skins. Regardless of the feeding damage, since it is highly gregarious the number of
larvae determines the level of damage caused (Lucchi et al. 2011). Because of the
highly aggregated larval distribution, affected clusters are fully compromised by the
inevitable and rapid development of rots enhanced by the presence of drosophilids
and by nitidulids. In Israel and Brazil, the species is considered a key pest of vineyards (Harari et al. 2007; Bisotto-De-Oliveira et al. 2007). Protection of grapes from
C. gnidiella infestation is achieved with effective control of L. botrana. If well timed,
it eliminates the need for a specific spray against phycitin larvae. Moreover, Btk can
be usefully employed in case of asynchronous outbreaks.

14.4 Ephestia parasitella unicolorella

Larvae of E. parasitella unicolorella (Pyralidae: Phycitinae) (Fig. 14.5af) are
found within the cluster after veraison as a secondary pest on wilted or dried berries
and very often hidden within them. Winter is spent in the larval stage, in a thin
cocoon spun by the mature larva on woody structures of the vine or on support
poles. It is not yet clear where this insect resides outside the vineyard, especially
during the spring, nor the number of generations that the species has in Europe. The
economic importance of E. parasitella unicolorella is negligible. Deseo (1980)
reports that the young larva feeds on the rachis and petiole of the bunch, whereas
the older larva can penetrate and develop on a single berry, feeding on the pulp.
At harvest mature larvae are frequently found in the most internal parts of the bunch
associated with or inside rotten or dried berries, almost motionless and folded in a
C shape. Xureb et al. (2003) advised to destroy the unharvested clusters to avoid
the further development of the species in the vineyard. In a recent review the name
of Ephestia unicolorella woodiella Richard & Thomson has been proposed for this
species (Huertas Dionisio 2007).

14.5 Argyrotaenia ljungiana

Argyrotaenia ljungiana (Fig. 14.6ad) (syn. A. pulchellana Haworth) is present
throughout the Palaearctic region with the exception of Japan. Females deposit their
eggs in batches of 4050 eggs, usually on the upper surface of the leaves. Larvae
feed primarily on leaves of host plants. Pupation occurs in a silken cocoon inside
webbed leaves. In the Mediterranean region, the species has three generations per
year, the first generation occurring in April and May, the second from the end of June
to July and the third in AugustSeptember. Argyrotaenia ljungiana overwinters in
the pupal stage, inside a cocoon in debris on the ground. A highly polyphagous
species, it feeds on many wild and cultivated plants, including grapevine and apple.

14 Grape Berry Moths in European Vineyards

355

Fig. 14.5 Ephestia parasitella unicolorella (a) adult, (b, c, d) larva, (e) overwintering larva, (f) pupa

Occasionally, A. ljungiana can give rise to important outbreaks in vineyards, where

it feeds on inflorescences and berry clusters. The harmfulness of this tortricid on
grapes has been described in Italy (Varner et al. 2001), France (Marcelin 1985),
Bulgaria (Kharizanov 1976), and Hungary (Voigt 1972). On the berries it may cause
superficial but extensive excavations, which are different from those caused by the
other two tortricids, but it can also provide entry points to rots when feeding on
ripening grapes. Sometimes the larvae can deeply abrade the cluster rachis causing
desiccation of the grapes.

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Fig. 14.6 Argyrotaenia ljungiana (a) adult, (b) larva, (c, d) damage on grapes

14.6

Conclusion

Of the five Lepidoptera species feeding on clusters in European vineyards, EGVM

and EGBM have the highest adverse economic impact. The other three species
described here, two Pyralidae and one Tortricidae, are occasional or secondary
pests. EGVM has increased its geographic range in the twentieth century throughout
Europe and the Middle East, invading the Americas early in the twenty-first century.
In the Mediterranean region south of the Alps, EGBM is being replaced by EGVM
as the major lepidopteran pest. Where EGVM is established, insecticide control for
the first generation is not practiced given that, in most varieties, damage to the inflorescence has no impact on yield. Insecticidal control is targeted primarily at the
second generation larvae. In recent years, more selective insecticides have been
introduced, with some having ovicidal activity. In Europe, the area-wide approach
based on the use of pheromones to control EGVM and EGBM represents an important development in a more environmentally acceptable control of these insects. In
regions were eradication is being pursued a program combining mating disruption

14 Grape Berry Moths in European Vineyards

357

and insecticides targeted for first and second generation larvae has achieved a drastic
reduction in population levels.
Acknowledgements We are much indebted to Bruno Bagnoli and Vittorio Veronelli for productive
discussions on grape moths. Photo acknowledgments: Bruno Bagnoli: Figs. 14.1b, c; 14.3c;
14.4bd; 14.5b, c. Paolo Giannotti: Figs. 14.1a, e; 14.3a, d. Mauro Varner: Fig. 14.6b, c. Elena
Pozzolini: Fig. 14.6d.

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