Exclusion, Sterilization and Disruption for Insect Pest Control In

Scientia Horticulturae 208 (2016) 13–27

Contents lists available at ScienceDirect

Scientia Horticulturae

journal homepage: www.elsevier.com/locate/scihorti

Going beyond sprays and killing agents: Exclusion, sterilization and

disruption for insect pest control in pome and stone fruit orchards

∗

G. Chouinard , A. Firlej, D. Cormier

Research and Development Institute for the Agri-Environment (IRDA), Saint-Bruno-de-Montarville, QC J3V0G7, Canada

a r t i c l e i n f o a b s t r a c t

Article history: Because of their perennial nature, orchards harbor one of the most complex ecosystems in agriculture.

Received 13 August 2015

Nevertheless, crop protection programs still mainly focus on pesticides (synthetic or organic-approved)

Received in revised form 3 March 2016

to prevent or limit the action of so-called noxious species in these systems. Killing agents represent the

Accepted 11 March 2016

dominant paradigm and have been used in agriculture for decades. This paper synthesizes the available

Available online 21 March 2016

literature about the other approaches, more suited to organic farming, which recognize that the radical-

ness of killing is not necessary to prevent crop losses. Exclusion barriers represent one of the most readily

Keywords:

available means of protecting the crop that way, but other behavior-based techniques have been devel-

Exclusion

oped, such as sterile insect technique and mating disruption. While there are many other possibilities,

Mating disruption

these are the three approaches that are currently getting the most interest in tree fruit production, due

Sterile insect technique

Cydia pomonella to ecological and agronomical characteristics, some of which will be detailed in this review.

Drosophila suzukii license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

1. Introduction dance with the principles of organic farming. Exclusion barriers

represent one of the most readily available means of protecting

Modern agriculture relies heavily on pesticides to prevent crop the crop that way, but other “behaviorally-based” techniques, such

losses by various organisms, from microbes to mammals that can as sterile insect technique and mating disruption, have also been

develop in these agroecosystems. Because of their perennial nature, developed. Although there are many other possibilities, these are

orchards harbor one of the most complex ecosystems in agriculture, the three approaches that are currently getting the most interest in

but nevertheless, crop protection programs still mainly focus on tree fruit production, due to ecological and agronomical character-

synthetic (conventional farming) or natural (organic farming) pes- istics that will be detailed for each one. Sprayable barriers such as

ticides to prevent or limit the action of so-called noxious species kaolin clay (Glenn et al., 1999) will not be considered, due to their

(FAO, 2009). strong similarities (deleterious effects) with pesticides.

It is not our intention to review the pros and cons of pesticides in Efforts in those research ﬁelds have been quite variable, ranging

this article, these having been and still being strongly documented from extensive (mating disruption), to limited (exclusion). Since

in various studies and reviews. However it is certainly worthwhile orchards harbor numerous pests and are subjected to high levels

to note that two approaches exist to prevent pests from forag- of pest pressure (Kogan and Hilton, 2009), tree fruit pests have fre-

ing on crops, and that “killing” is the one that has been mostly quently been the subject of studies on those recent management

used in agriculture for decades. Killing agents – chemical, but also strategies. In the following review, alternative control of the most

botanical, microbial, physical, predatory, parasitic – are present in important pome and stone fruit species or groups of insects will

both organic and conventional cropping systems and the use of be discussed: a) the codling moth, Cydia pomonella (L.), the ori-

these pesticides represent the dominant paradigm, whether they ental fruit moth, Grapholita molesta (Busck) and other tortricids

are considered safe or not. (Lepidoptera: Tortricidae); b) tephritid ﬂies (Diptera: Tephritidae);

The second approach to pest control will be the focus of this and c) drosophila ﬂies (Diptera: Drosophilidae). Complementary

review. This approach recognizes that the radicalness of killing information regarding biology, damage and economic importance

is not necessary to prevent crop losses, which is in closer accor- of those worldwide pests can be found in many review papers

and textbooks, including those by Capinera (2008), Croft and Hoyt

(1983) and Aluja et al. (2009).

∗

Corresponding author.

E-mail address: [email protected] (G. Chouinard).

http://dx.doi.org/10.1016/j.scienta.2016.03.014

14 G. Chouinard et al. / Scientia Horticulturae 208 (2016) 13–27

Table 1 Table 2

Direct fruit pests of northeastern North American apple orchards, with average dam- Expansion of codling moth exclusion systems in France apple orchards.

age at harvest in a pesticide-free plot in Quebec, Canada 1977–2000 (updated from

Year Stage Coverage Source

Vincent and Bostanian, 1998; Chouinard, unpublished data).

2005 Design n/a Romet et al., 2010

Plum curculio Conotrachelus nenuphar 51%

2006 Field validation 9 orchards Romet et al., 2010

Apple maggot Rhagoletis pomonella 42% 2007 Commercial introduction 30 ha Romet et al., 2010

Codling moth Cydia pomonella 22% 2008 Expansion—organic 150 ha Sauphanor et al., 2009

Lesser appleworm Grapholita prunivora 7.0% 2014 Expansion—organic and 2000 ha Alaphilippe et al., 2016

Tarnished plant bug Lygus lineolaris 6.3% conventional orchards

Eyespotted budmoth Spilonota ocellana 6.1%

Obliquebanded leafroller Choristoneura rosaceana 3.9%

Redbanded leafroller Argyrotaenia velutinana 3.0%

nets, had the lowest environmental impact of all four strategies,

European apple sawﬂy Hoplocampa testudinea 2.3%

as based on the International Organization for Biological Control

toxicity classes of the pesticides used (Sterk et al., 1999). However,

despite a good environmental proﬁle, exclusion systems are not

2. Exclusion (netting) totally free of sustainability issues. Siegwart et al. (2013) showed

that behavioral adaptation of codling moth to exclusion systems is

Exclusion nets have been used in agriculture since the mid- possible (see Section 2.1.1), in accordance with observations made

dle of the 20th century (Scarascia-Mugnozza et al., 2012; Merrill, in laboratory rearings of this species. Those systems also have the

1967), and more commonly since the 1990s, when they became disadvantage of being costly. The use of netting, as presented by

widespread as a protection tool against whiteﬂies in greenhouses Stevenin (2011) for an organic high-density plot of ‘Juliet’ apples in

(Berlinger et al., 2002). As an exclusion device, the main mode of France, represented 25% of planting costs over the ﬁrst three years

action of nets is to act as a barrier to deny access to the crop. Despite and 7% of annual production costs afterward. In this case, the net-

their high sustainability (Alaphilippe et al., 2016) and stable efﬁ- ting was used solely to prevent codling moth damage, a common

cacy under variable conditions, they seldom have been considered situation in Europe where this species is the key pest in terms of

economical to use. This has gradually changed over the last three fruit damage (Blommers, 1994).

decades in tree fruit production, as nets have been increasingly used

in many parts of the world to prevent damage from hail (Iglesias 2.1. Complete exclusion

and Allegre, 2006) and even mammal and insect pests (Tasin et al.,

2008). Various types of net coverings are now widely used for a 2.1.1. Species-oriented systems: codling moth, tephritid ﬂies and

range of horticultural crops in various countries around the world leafrollers

to provide protection from birds, frugivorous bats, hail, wind, frost 2.1.1.1. Codling moth. The codling moth is a severe pest of pome

and sunburn damage (Lloyd et al., 2005). Net enclosures are more fruit worldwide (Grigg-McGufﬁn et al., 2015). Most exclusion stud-

and more used in organically grown fruit to solve several produc- ies on codling moth used Alt’Carpo nets (Filpack, Vitrolles, France).

tion issues (Granatstein et al., 2015), and are currently investigated Alt’Carpo (a French designation meaning “codling moth arrest”)

as a potential solution to the devastating problems caused by the is a noncopyrighted system that exists in two forms: a full block

brown marmorated stink bug, Halyomorpha halys in the United incomplete exclusion system (Fig. 1A), and a row-by-row complete

States and many other parts of the world (Marshall and Beers, exclusion system. Alt-Carpo nets have been designed by French

2016). These agricultural nets are almost exclusively made of clear extension services in 2005 (Sévérac and Romet, 2008) in an effort to

high density polyethylene (HDPE) and have an average lifespan of reduce the number of insecticide applications speciﬁcally required

six (Sauphanor et al., 2009) to ten (Rigden, 2008) years under ﬁeld to control codling moth-12 annually, on average in southeastern

conditions. France (Sauphanor et al., 2009). This exclusion system is the ﬁrst

The characteristics and effectiveness of exclusion systems and one of the most widely used commercial exclusion systems for

adapted for tree fruit protection have been studied for many key pome fruit in the world: estimated at about 2000 ha in Southern

pests of pome and stone fruits. The various systems used can be France (mainly on apples; Table 2) and 350 ha in Italy (mainly on

classiﬁed as either complete or incomplete exclusion (Fig. 1). In pears) (Alaphilippe et al., 2016). Although both systems (complete

incomplete exclusion, the soil is not excluded from the system, thus and incomplete) are often presented as one single technique, their

allowing several key pest species (e.g. plum curculio, tephritid ﬂies, effectiveness and applicability differ considerably. For example,

European apple sawﬂy; Table 1) to complete their life cycle and the row-by-row (complete) system creates much smaller enclosed

remain inside the enclosed area. This type of exclusion is well repre- environments and does not easily allow circulation. The full block

sented by full block netting systems (Rigden, 2008) covering entire (incomplete) system is presented in Section 2.2.1.

orchards. In complete exclusion however, the soil is excluded from Complete exclusion systems aimed at controlling codling moth

the enclosed zone; this is the case for some row-by-row systems, are usually put in place just after bloom, before the emergence of

or “tunnel” netting. Incomplete and complete exclusion systems the ﬁrst adults, and kept until harvest. Nets used are typically clear

have their advantages and disadvantages, which will be discussed and have a mesh size of 2.2 × 5.4 or 5.5 mm. It is worth noting that

below. the mesh orientation and size have not been strictly deﬁned; larger

By adding a layer of complexity to their natural environment, mesh sizes and other adaptations are also used to better ﬁt indi-

netting also affects the behavior of both enclosed and excluded vidual situations (e.g. size and age of trees, orchard density and

arthropods (Dib et al., 2010; Sauphanor et al., 2012); this in turn exposure, cultivar, mode of production). Many of the reports and

can affect the development of non-target species (pests and natu- studies discussed in this review present overall properties of all

ral enemies). For example, anti-hail nets, even without side walls, variations, sometimes including full block systems.

have been found to reduce the density and damage of the codling Typical efﬁcacy of complete exclusion systems for codling moth

moth in apple (Malus domestica Borkh.) orchards (Graf et al., 1999). is high. In efﬁcacy tests with nets performed in 2010 in 23 com-

Marliac et al. (2015) deﬁned four crop protection strategies used mercial apple orchards within the southeastern France Alt’Carpo

by organic apple farmers: pesticide-based, ecologically intensive, network (Sauphanor et al., 2012), codling moth caused little fruit

technologically-intensive and integrated. The technologically- damage (0.2% infestation at harvest) as compared to the alternative

intensive strategy, which mainly consists in the use of exclusion program using 7–8 additional insecticide applications supple-

G. Chouinard et al. / Scientia Horticulturae 208 (2016) 13–27 15

Fig. 1. Examples of exclusion systems for pome and stone fruit: (A) Alt’Carpo incomplete exclusion system for the control of codling moth (Sévérac and Romet, 2008); (B)

incomplete exclusion dual system for the control of cherry ﬂies and fruit cracking (adapted from Charlot et al., 2014); (C) and (D) complete exclusion system prototypes for

the control of multiple apple fruit pests species (photos: G. Chouinard).

mented with mating disruption (2% infestation at harvest). Among in covered and uncovered crops (around 25 annual applications

41 apple orchards surveyed in 2009 by the French extension ser- for organic pears and 14 for organic and IFP apples). This can have

vices (Romet et al., 2010; Sévérac, 2014), over 85% had no fruit an important effect on the environmental impact of fruit growing.

damaged by C. pomonella and the remaining 15% had less than 1% The environmental impact, as measured by the French I-PHY pesti-

fruits damaged. In studies by these authors, exclusion was even cide index (Van der Werf and Zimmer, 1998) of growing ‘Pink Lady’

more effective than mating disruption, on average, for this pest. apples with Alt’Carpo nets to control codling moth was 25% lower

Nets also allow a signiﬁcant reduction in the number of pesticide than when they were grown using mating disruption (Sauphanor

(synthetic or organic-approved) applications needed to protect the et al., 2009).

crop from all pests. Pesticide spraying in “exclusion farms” has been Despite the fact that they are primarily designed to exclude a sin-

compared to spraying in comparable “organic” and “integrated fruit gle pest species, complete exclusion systems for C. pomonella have

production” (IFP) farms by Alaphilippe et al. (2016) in French apple some obvious effects on the entomofauna of fruit trees. Alaphilippe

and Italian pear orchards. In their study, 100% of pear farms and et al. (2016) mentioned that nets favor the development of sec-

90% of apple farms used the row-by-row exclusion system, and ondary pests such as the woolly apple aphid, Eriosoma lanigerum

pesticides applications were calculated as the sum of the number (Hausmann) (Hemiptera: Aphididae) and the summer fruit tortrix

of equivalent full-dose applications throughout the season. Over moth, Adoxophyes orana (Fischer von Röslerstamm) (Lepidoptera:

the course of two years (2011 and 2012), an average of 4.1 annual Tortricidae). In Italian organic pear orchards, the same system

insecticide treatments was applied in the 17 apple orchards cov- favors the development of other secondary pests such as the frosted

ered by nets, whereas an average of 13.7 annual treatments were moth-bug, Metcalfa pruinosa (Say) (Hemiptera: Flatidae) and lace

applied in the 12 orchards under IFP or organic management. In bugs. Sévérac and Siegwart (2013) also mentioned the apple leaf

organic pear orchards, the reduction was even more drastic: less miner, Leucoptera malifoliella (Costa) (Lepidoptera: Lyonetiidae), a

than 5 annual applications on average in ﬁve netted orchards as minor pest that can readily pass through the meshes and develop

opposed to 18 applications in six uncovered orchards. In both crops, within enclosed environments.

a high level of net efﬁcacy was observed against codling moth, espe- On the other hand, codling moth exclusion systems are known

cially for the ‘row-by-row’ system. Fungicide use remained similar to protect from birds, mirids (Alaphilippe et al., 2016) and leop-

16 G. Chouinard et al. / Scientia Horticulturae 208 (2016) 13–27

ard moths, Zeuzera pyrina (L.) (Lepidoptera: Cossidae) (Sauphanor other types of predator or parasitoid releases (chrysopids, syrphids,

et al., 2009). Pear psylla, Cacopsylla pyricola Foerster (Hemiptera: tachinids, etc.) have not been studied.

Psyllidae) reinfestations are prevented when nets are installed right Above all entomological considerations, the effect of nets on

after an initial insecticide application (Romet et al., 2010). In a ﬁeld the cultivated plants is of prime importance. The effect of clear

study conducted in 2010 and 2011 in 43 apple orchards, Sévérac and nets (mesh size 5.4 × 2.2 mm) on temperature and photosynthe-

Siegwart (2013) also observed a slight reduction in the occurrence sis has been documented by various authors. Alaphilippe et al.

◦

and intensity of apple scab, Venturia inaequalis (Cooke) G. Wint on (2016) reported an average increase in temperature (0.7 C) in Ital-

susceptible cultivars such as ‘Pink Lady’ and ‘Gala’, but were not ian conditions and a decrease in photosynthesis active radiation

able to determine the reason for this effect. (10 and 15%, respectively in Southern France and Northern Italy)

Mites also appear to be indirectly affected by exclusion nets; for fruit grown under row-by-row netting during summer 2011.

Sauphanor et al. (2009) reported that ‘Pink Lady’ apples grown A decrease in relative humidity (2.3%) was also reported for the

without nets needed two more miticide applications than apples same year in Italy. These overall ﬁgures may however mask big-

grown under Alt’Carpo nets in a side-by-side comparison. The ger effects during short periods of time. In their study, Alaphilippe

authors hypothesized that the absence of insecticides in the net- et al. (2016) mentioned that although apples grown under nets

ted plot could have beneﬁted mite predators (exclusion system were harvested ﬁve days later than apples grown without nets, no

not mentioned). Other indirect effects include postharvest dis- signiﬁcant modiﬁcation of the fruit quality and orchard yield was

eases, which are less prevalent for apples grown under complete observed, provided trees were trained (supported) and shaped to

exclusion, presumably because enclosed fruits are protected from be covered by nets. In another study, Romet et al. (2010) reported

climatic, parasitic and non-parasitic agents that are responsible for that the size of fruits produced under nets was higher compared to

creating entry ports for various diseases (Sévérac and Siegwart, fruit from uncovered trees: the proportion of ﬁrst-class grade fruits

2013). (>75 mm) increased from 40 to 48%, and that of third class grade

No clear effect of the nets has been demonstrated for fruits (<65 mm) decreased from 16 to 6%.

insects such as the rosy apple aphid, Dysaphis plantaginea Vergnani and Caruso (2015) observed that pears (cv. ‘Abate

(Passerini) (Hemiptera: Aphididae) (Sévérac, 2014), the oriental Fétel’) grown under clear nets (mesh size: 5.4 × 2.2 mm or

fruit moth, the green apple aphid, Aphis pomi de Geer (Hemiptera: 7.4 × 3.0 mm) installed in a row-by-row design have their shoot

Aphididae), and the San Jose scale, Quadraspidiotus pernicio- growth reduced by 10%; similar black nets do not produce this type

sus (Comstock) (Hemiptera: Diaspididae) (Sévérac and Siegwart, of reduction but signiﬁcantly impede fruit coloring, ﬁrmness, and

2013). Alaphilippe et al. (2016) mentioned that oriental fruit moth size (for more details on the effect of net color, see Section 2.2.3).

is favored by Alt’Carpo exclusion nets, but this only applies to full-

block systems. Sévérac and Siegwart (2013) demonstrated that

2.1.1.2. Tephritid fruit ﬂies. With the increasing number of dwarf

moths of this species can pass through the nets because the mesh

tree cherry orchards covered to prevent fruit cracking by rain, crop

size is not adapted to this smaller species.

netting has become a viable, cost-effective control method for the

Searching strategies used by arthropods to locate mates, ovipo-

European cherry fruit ﬂy, Rhagoletis cerasi (L.) (Diptera: Tephriti-

sition sites and/or food can be drastically affected by nets, creating

dae), a major pest of cherry crops in Europe (Daniel and Grunder,

small-sized environments with physical barriers. Sauphanor et al.

2012). Brand et al. (2013) and Höhn et al. (2012) have shown

(2012) found that even when mesh size was big enough to allow

that clear polyethylene nets (mesh size 1.3 × 1.3 mm) are effective

moth to enter covered rows (as revealed by lab tests that showed

against the R. cerasi as long as nets are installed prior to egg-laying

between 18 and 73% of moth escape), such entry was not frequent.

and removed right before harvest. In a high-pressure orchard, nets

Similarly, even though nets only partially prevented females from

installed in a complete exclusion fashion reduced infestation by up

laying eggs on leaves in close contact with the nets, their fecun-

to 98% (Brand et al., 2013). Assuming that a plastic cover to shel-

dity was much lower when the leaf-net contact was imperfect. The

ter the fruits against rain is already installed, the additional cost of

authors thus explained the efﬁcacy of the row-by-row netting by

installing a net (mesh size 1.3 × 1.3 mm) over a high-density plant-

the combined result of the conﬁned space around the trees, which

ing (800 trees per ha, height of ﬁrst branches: 0.5 m, tree height:

alters the reproduction of the moth, and the partial prevention of

3.5 m, canopy diameter: 3–4 m) was estimated at 511 euros/ha

moth penetration and egg laying.

(equivalent to 3 ¼ insecticide applications of acetamiprid). Charlot

Reports on the effects of complete exclusion nets on natu-

et al. (2014) also tested complete and incomplete exclusion sys-

ral enemies are often contradictory, because many factors may

tems with a net (mesh size: 1.4 × 0.95 mm) that could exclude both

interact under natural conditions, making it difﬁcult to determine

tephritid and drosophila ﬂies (see Sections 2.2.1 and 2.2.3).

the real effect (direct or indirect) of nets. Marliac et al. (2013)

reported “contrasting effects” of codling moth exclusion netting on

2.1.1.3. Leafrollers (Lepidoptera: tortricidae). Leafroller-proof nets

the natural predators (Syrphidae, Anthocoridae, Miridae and Coc-

(mesh size 3.4 × 2.2 mm, 11% shading) are commercially avail-

cinellidae) of the rosy apple aphid. Dib et al. (2010) and Romet

able (Filpack agricole, 13127 Vitrolles, France) and currently under

et al. (2010) reported lower abundance of aphid predators (mostly

study (M. Aoun, personal communication), but no study on their

Coccinellidae and Syrphidae) under netted plots than uncovered

effectiveness has been published to our knowledge.

ones. No clear effect was found by these authors on Forﬁculidae

or on aphid parasitoids (mostly Braconidae and Pteromalidae) that

were present. However, only half of the predator groups present 2.1.2. Multipurpose systems

in uncovered plots were present under nets, and populations of Few studies can be found on complete exclusion systems aimed

aphid natural allies (Formicidae) were also less abundant, this latter at controlling more than one species at a time. Research projects

observation being suggested to explain, the lower aphid popula- are however currently conducted in Quebec, Canada with com-

tions under nets. To compensate for the lack of natural enemies plete exclusion nets (mesh size: 1.0 × 1.9 mm) in a row-by-row

in the enclosed environment, Gagnon Lupien et al. (2014) sug- design, supported by simple modiﬁcations to existing apple train-

gested the release of commercially available coccinellids Adalia ing systems in high-density plantings (Chouinard, unpublished

bipunctata (L.) (Coleoptera: Coccinellidae), but were not able to data). Eastern North American orchards harbor numerous fruit

demonstrate their effectiveness against aphids due to their high pests (Table 1) and to be cost-effective, exclusion must not be lim-

mobility between netted and uncovered trees. To our knowledge, ited to codling moth control.

G. Chouinard et al. / Scientia Horticulturae 208 (2016) 13–27 17

Table 3

Characteristics of ‘Honeycrisp’ apples grown for three years under complete exclusion netting in the province of Quebec, Canada. High density planting, row-by-row design,

nets (mesh size: 1.0 × 1.9 mm) in place from one week after bud break until one week before harvest, years 2012–2014 (Chouinard, unpublished data).

A. Mean damage by fruit pests (%) B. Other types of damage (%) C. Fruit quality indices

a a a a a a a

PC AM CM EAS LR TPB MEC RUS DEF FR CO BRI FIR MA PIP

Nets 0.00 0.00 0.19 0.09 8.14 0.28 2.61 1.03 6.97 0.32 1.8 12.0 7.36 4.5 4.3

No nets 1 59 3.23 4.16 0.23 6.83 3.98 6.30 1.54 3.85 5.88 1.9 12.2 7.27 5.6 5.3

Indicates statistically signiﬁcant difference (P < 0.05) between fruits produced with and without nets for a year or more. PC: plum curculio; AM: apple maggot; CM:

codling moth; EAS: European apple sawﬂy; LR: leafroller complex; TPB: tarnished plant bug; MEC: mechanical bruising; RUS: russetting; DEF: mineral deﬁciency (Ca or

other); FR: frost injury; CO: red coloring, on a scale from 1 to 3; BRI: Brix (%); FIR: ﬁrmness (kg); MA: maturity stage, on a scale from 1 to 8 adapted from Blanpied and Silsby

(1992); PIP: number of seeds.

Under this system, nets need to be opened daily for 2–3 days to possible after the development of multiple generations under nets,

allow bee pollination during bloom. After three years of production leading to some form of “resistance” to full-block exclusion.

under those nets without any pesticides, ‘Honeycrisp’ apples were

found to be effectively protected from attacks by all direct fruit

2.2.1.2. Tephritid ﬂies. The Queensland fruit ﬂy, Bactrocera tryoni

pests, with the exception of Choristoneura rosaceana (Harris) (Lep-

(Froggatt) (Diptera: Tephritidae) is a major pest of many orchard

idoptera: Tortricidae) (Table 3A). Fruit quality was not affected by

crops in eastern Australia. Chemical control of the Queensland fruit

the presence of nets, but maturity was delayed by about one week

ﬂy using cover and bait sprays is possible but expensive; often pro-

(Table 3B).

tection is incomplete unless many treatments (5–6) are applied

Although Middleton and McWaters (1997) stated that hail nets

annually. Lloyd et al. (2005) used a clear net exclosure (mesh size:

offer no frost protection, this assertion appears not to apply to

2 × 2 mm) in a high-pressure environment to demonstrate the efﬁ-

exclusion nets, which have a smaller mesh size. In fact, under

cacy of nets against this insect. Despite hundreds of captures weekly

eastern North American conditions, exclusion nets signiﬁcantly

in the adjacent uncovered block, no damaged fruit was found fol-

reduced fruit distortion (ring frost) due to short-timed overnight

lowing the examination of more than 700 fruits from the protected

temperature drops around bloom, as well as mechanical fruit bruis-

block. The nets reduced quantum irradiance by about 20% and

◦

ing from various sources (Table 3C). They nevertheless did not

increased maximum temperatures by about 5 C. These changes

increase daytime temperature during the hotter summer months

in climatic conditions positively affected the yield, sweetness and

(Fig. 2).

color of stone fruits grown inside the nets, especially peaches,

Prunus persica (L.) Stokes and nectarines, P. persica var. nucipersica

2.2. Incomplete exclusion (Borkh.) C.K.Schneid.

2.2.1. Species-oriented systems: codling moth, tephritid ﬂies and

2.2.1.3. Drosophila ﬂies. The spotted wing drosophila, Drosophila

drosophila ﬂies

suzukii (Matsumura) (Diptera: Drosophilidae) is a major exotic pest

2.2.1.1. Codling moth. The Alt’Carpo full block system consists

of ripening sweet cherry but also peach, nectarine, apricots and

in a single-plot hail net modiﬁed to cover the entire tree

plums in Europe and North America. Extensive monitoring, chemi-

canopy (Sauphanor et al., 2012). Traditional hail nets (mesh size:

cal control and orchard sanitation are recommended management

3.0 × 7.4 mm) are typically used for the roof in this system, but the

options because crop damage can reach 100% without appropri-

sides are usually made of the ﬁner 2.2 × 5.4 mm mesh size used in

ate methods of control (Cini et al., 2012). Laboratory trials with D.

the row-by-row system. Despite its preferential attractiveness to

suzukii encaged in tubes covered by mesh of different sizes showed

growers who are already familiar with similar anti-hail systems,

that mesh measuring 1.37 × 0.81 mm was the only one success-

the full-block system is less effective against codling moth and it

ful in constraining D. suzukii whereas in the ﬁeld, a mesh size of

is not recommended anymore by its developer as such, except as

1.40 × 0.95 mm achieved excellent protection (Charlot et al., 2014;

an improvement to existing hail net structures (Capowiez, pers.

Weydert et al., unpublished data). In Canada, a little smaller mesh

comm.). Only one-tenth of all Alt’Carpo systems installed in France

size of 1.0 × 0.6 mm was used with success for small fruit produc-

are of the full-block type (Sévérac and Siegwart, 2013).

tion (Cormier et al., 2015), but a fully-protected cherry orchard with

Two major caveats affect full-block exclusion of codling moth:

mesh size 1.37 × 1.71 mm for the walls and 1.38 × 1.38 mm for the

top failed to prevent D. suzukii infestation (Weydert et al., unpub-

(1) large open spaces over the trees allows for the reproduction of lished data). Aphid infestation was also observed and the net caused

◦

moths within the enclosed environment once they enter, and the temperature to increase by 1–1.5 C during the hottest periods.

(2) the species can establish and thrive as it can complete its

life-cycle undisturbed. Sévérac and Siegwart (2013) showed

2.2.2. Anti-hail nets

that populations inside enclosed environments can reach lev-

Unmodiﬁed (ﬂat, roof-only) anti-hail nets (Baiamonte et al.,

els similar to those in uncovered plots after only two years,

2016) also show a good efﬁcacy in preventing codling moth dam-

under high-pressure conditions. For these reasons, pesticides

age, because of the altered reproductive behavior (Tasin et al., 2008)

are often needed to supplement the action of nets used in this

discussed in Section 2.1.1. Even though many colors are available

incomplete exclusion system, partially hindering environmen-

(see Section 2.2.3), those nets are typically black, with a mesh size of

tal savings that should be provided by the nets.

2 × 6 or 3 × 7 mm, and they can intercept between 18% (Baiamonte

et al., 2016) and 32% (Bosco et al., 2015) of incident photosynthet-

Siegwart et al. (2013) observed that C. pomonella populations ically active radiation.

collected from full block exclusion systems were signiﬁcantly more Hail net structures may be skirted and enclosed down to or

successful (higher fecundity and fertility) when reared in small almost down to ground level (Middleton and McWaters, 2002) to

cages (5 8 cm boxes) than those collected in nearby comparable increase the efﬁcacy against birds, rodents and other pests. Bee

orchards without nets. They hypothesized that an adaptation to hives need to be evenly distributed inside the enclosed environ-

restrained space, as suggested by Sauphanor et al. (2009), might be ment: bees are less inclined to ﬂy into orchard blocks covered by

18 G. Chouinard et al. / Scientia Horticulturae 208 (2016) 13–27

Fig. 2. Diel temperature ﬂuctuations in the canopy of apple trees grown with and without complete exclusion netting in the province of Quebec, Canada. High density

planting, row-by-row design, mesh size 1.0 × 1.9 mm; July 2013 (Chouinard, unpublished data).

hail netting than into blocks of uncovered trees (Middleton and ond year, which was attributed to insects being “forced to develop”

McWaters, 2002), especially where there is little or no gap between in the system.

the tree top and the net (Middleton and McWaters, 2001). Kelderer et al. (2010) tested row-by-row netting in an incom-

Anti-hail nets are not designed for pest management purposes, plete exclusion setting (net pegged to the ground), with nets of

but they can reduce wind speed and affect temperature, which various mesh sizes (1 × 1 mm, 2 × 6 mm and 3 × 8 mm). They found

can impact insect development. They may increase (Middleton that the ﬁner mesh produced apples with less colored skin cover-

and McWaters, 1997) or lower (Kührt et al., 2006) air temperature age. They also observed a highly signiﬁcant reduction of codling

within the canopy; however, more generally they decrease maxi- moth fruit damage for all mesh sizes, even under conditions of

mum temperatures, minimum temperatures and relative humidity high pest pressure, as long as nets were installed before the ﬁrst

(Iglesias and Alegre, 2006). Contradictory effects of hail nets on fruit ﬂight of codling moth. On dwarf ‘Braeburn’ trees, installing the

quality attributes (color, size, ﬁrmness, sweetness, etc.) have also nets (mesh sizes: 1 × 1 mm or 3 × 8 mm) before bloom resulted in

been reported in different parts of the world (Australia: Middleton a 25% decrease in the number of fruits per tree (which resulted in

and Mcwaters, 1997; Spain: Iglesias and Alegre, 2006; Slovenia: an increase in the percentage of fruits with bitter pit), but trees

Stampar et al., 2002): as a general trend, black nets most notice- still produced 45 fruits/tree. Kelderer et al. (2014) reproduced the

ably affect tree growth, yield, fruit size and color on vigorous trees experiment on ‘Gold Rush’ and ‘Golden Delicious’ trees (M9 root-

that would have shading problems even without artiﬁcial protec- stock, 0.7 × 3.5 m planting) to ﬁnd a more pronounced, but similar

tion and clear nets only marginally affect the temperature and the pattern. On ‘Golden Delicious’, trees netted before bloom produced

crop. For more details on the effect of net color, see Section 2.2.3. signiﬁcantly less fruits than unnetted trees, but fruits were sig-

niﬁcantly bigger, which resulted in a similar yield (44–52 kg/tree).

Thus, covering trees with nets before bloom has a promising thin-

2.2.3. Multipurpose systems ning potential on apple, resulting also in an increased mean fruit

2.2.3.1. Clear netting. Lawson et al. (1994a), (1994b) were the ﬁrst weight.

to experimentally design and test incomplete exclusion cages in Row-by-row protection of cherry trees using a dual

order to prevent multiple pests from attacking apple trees. Nets system—exclusion nets against insects and plastic covering against

were made of white polyester of various mesh sizes (between cracking—has been explored by Charlot et al. (2014). Although an

× ×

1.0 0.13 mm and 3 3 mm). The exclusion cages were made expensive solution, it may be relevant in the case of such high

specifically to fit single rows of five small columnar trees. Vari- added value crops. Such a system (mesh size: 1.40 × 0.95 mm)

ous measurements of environmental, plant and fruit characteristics (Fig. 1B) successfully achieved to protect a cherry orchard against

were made over two years. Although subtle differences occurred D. suzukii and R. cerasi infestations (Charlot et al., 2014).

among treatments for many of the environmental variables mea-

sured, many were not signiﬁcant. Infestation by phytophagous

insects (leafminers and leafhoppers) was reduced by all types of 2.2.3.2. Photoselective netting. Although netting used for exclusion

nets, the most effective being the one with medium-sized mesh. is usually clear, different colors exist and can have different effects.

However, some direct fruit pests were most successfully protected For example, the use of black (instead of clear) nets comparable

by ﬁne- (1.0 × 0.13 mm) and medium-sized mesh (1.0 × 1.5 mm). to those used in Alt’Carpo full-block systems (mesh size: 3.0 × 7.1

Some pests (C. rosaceana and Conotrachelus nenuphar, Coleoptera: mm) affects fruit maturity and quality (Baiamonte et al., 2016).

Curculionidae) however reached damaging levels during the sec- Fruits grown under black nets contain lower amounts of esters and

G. Chouinard et al. / Scientia Horticulturae 208 (2016) 13–27 19

acetates that are responsible for the characteristic apple-like aroma insect technique is a control strategy compatible with other organic

and ﬂavor in apple cultivars. Colored nets also come in blue, yellow methods of control (example: mating disruption, parasitoids and

and red as well as gray, white and pearl. The latter three do not predator release). Since SIR is not a grower-level method of con-

look colored to the human eye but do modify the non-visible spec- trol, it is usually not speciﬁcally mentioned in organic standards,

trum or enhance light scattering (Shahak et al., 2004). In fruit crops, but exceptions to this may exist (e.g. National Standard of Canada,

colored nets of low shading capacity (30% or less) can be used to 2015).

avoid negative effects on productivity. Photoselective nets absorb The ﬁrst successful use of SIT to control a pest came from

different spectral bands (in the visible or UV, far-red and infra-red research by Kipling on the New World screwworm, Cochliomyia

regions) and increase the relative proportion of scattered and dif- hominivorax (Coquerel) (Diptera: Calliphoridae), which was a pest

fused light; the relative content of the modified and unmodified of livestock in North America (Klassen and Curtis, 2005). The find-

light, as well as the shading factor can be selected to ﬁt the needs of ings from Kipling contributed to the implementation of the ﬁrst

each crop (Shahak, 2006). Nets with different chromatic properties AW-IPM with SIT in the 1960s, which ﬁnally eradicated the pest

can also affect various attributes of tree performance such as pro- from the United States, Mexico, and Central America after 43 years

duction, fruit size and quality, time to maturation, ﬂowering and of presence.

photosynthesis (Shahak, 2006; Stamps, 2009; Bastías et al., 2012), This success opened the gate to the development of SIT for other

and those responses may vary between cultivars and environmen- world pests like fruit ﬂies, tsetse ﬂies and mosquitoes. The method

tal conditions (Shahak, 2006). However little is known about the ﬁrst developed on Diptera species was also adapted to lepidopter-

effect of colored nets on pest infestation in fruit crops, even if the ans, but because of the high radiation levels needed to induce F0

role of light in insect ﬂight orientation and visual detection of their male moth sterility most programs use inherited sterility tech-

hosts is well documented (Antignus, 2014). In various horticultural nique, for which moth pupae subjected to low doses of radiations

crops, the effects of photoselective nets on populations of differ- develop into partially sterile males. These males are more competi-

ent insect pest species (aphids, leafhoppers, thrips and whiteﬂies) tive and their progeny shows different degrees of sterility, including

have been reported and in most cases, the risk for pest infestation near complete sterility (Bloem et al., 1999; Carpenter et al., 2005).

under nets with attractive colors appears to be lower or equal as Literature on the SIT developmental research is extensive but there

the risk under standard black shading nets (Ben-Yakir et al., 2008; is no abundance of large- or small-scale ﬁeld experiments pub-

Weintraub, 2009). lished. This may be due to SIT being usually tested over the years

in AW-IPM programs involving different countries in the world.

Also, SIT cannot be applied by growers individually as with exclu-

3. Sterile insect technique sion nets; this control technique should be used at the region or

country scale.

The sterile insect technique (SIT) is the rearing of a large number In stone fruit production, use of SIT to control some major

of individuals of a target pest species, exposing them to radiations pests like codling moth and tephritid ﬂies showed a great success.

inducing sterility, and releasing them sequentially into the wild. Promising ﬁrst results were also obtained with other pest candi-

Sterile males, by mating with wild females, provoke female steril- dates, such as the light brown apple moth, Epiphyas postvittana

ity, which can lead to population eradication without killing the (Lepidoptera: Tortricidae), and the oriental fruit moth. Recently,

pest (Dyck et al., 2005). In order for this mode of action to be effec- Dyck et al. (2005) and Vreysen et al. (2007) published extensive

tive, pre- and post-copulatory mechanisms must be achieved: the review papers on SIT and the purpose of the following section is to

sterile male must locate, court and copulate with a wild female. brieﬂy summarize the SIT knowledge applied to pests of pome and

Then either competitive sperm cells are produced by the sterile stone fruits, and to present recent advances published since 2007.

male or a mechanism that prevents females from mating again is

triggered. This is made possible if the rearing of the target pest pro- 3.1. SIT to control lepidoptera

duces high quality individuals and if the radiations do not decrease

their behavioral and biological abilities. Other factors can inﬂuence 3.1.1. Codling moth

the effectiveness of SIT and whether it is economical (cost-effective As alternatives to broad-spectrum pesticide use against codling

mass-rearing, genetic sexing system, government willpower, etc.). moth, mating disruption and the use of synthetic growth regu-

It is worth noting that most SIT programs are used to control exotic lators or microbial agents can achieve some levels of population

species in invaded areas (example: Ceratitis capitata and, Epiphyas control, but exclusion and SIT could be more effective than these

postvittana (Walker) in the USA, C. pomonella in Canada). Dyck et al. alternatives under high pest population pressure (Vreysen et al.,

(2005) made an exhaustive review of the feasibility and consider- 2010). Numerous research projects have been carried out to con-

ations about SIT. trol codling moth with SIT in the past 50 years in the world, but

The sterile insect technique is recognized among the ﬁrst bio- only two large programs in British Columbia, Canada have been

logical control methods designed for area-wide integrated pest implemented successfully (Proverbs et al., 1982; Bloem et al., 2007).

management programs (AW-IPM) which integrate various control The ﬁrst program was conducted on 320–526 ha from 1976 to

tactics against a pest population within a delimited geographical 1978 in the Similkameen Valley (Proverbs et al., 1982). From 23,600

area (Klassen, 2005). Other tactics include pesticide applications to 36,500 sterile moths/month/ha were released over the three

to reduce the size of initial populations, mating disruption, or years, leading to 98.9% (1976), 96.9% (1977) and 100% (1978) of

non-commercial wild host plant management to reduce the immi- orchards with fruit damage under the economic threshold. The pro-

gration of wild pest populations. Four strategies can be reached gram was a success but its cost was more than twice the cost of

when using SIT in AW-IPM: pest eradication, suppression, con- chemical control (Proverbs et al., 1982).

tainment or prevention (Vreysen et al., 2006). Although SIT is The second historic case that established the efﬁcacy of SIT

considered an environmentally friendly method, undesired effects for codling moth was the large program from Okanagan-Kootenay

may occur; the pre-release population suppression is often based Sterile Insect Release (OKSIR) launched in 1992 to eradicate the

on insecticide applications that can be harmful to the environment, species from 5400 ha of orchards (apple and pear) grown inside the

and SIT targeting native species can threaten biodiversity. Direct Okanagan and Kootenay valleys and enclosed urban areas (Bloem

and indirect effects of SIT on the environment are addressed in et al., 2007). The program was ﬁnancially supported by citizens,

Nagel and Peveling (2005) for both native and exotic pests. Sterile pome fruit growers and the British Columbia and Canada govern-

20 G. Chouinard et al. / Scientia Horticulturae 208 (2016) 13–27

ments. This allowed for the construction of the OKSIR mass-rearing are still an important impediment to the implementation of the

facility in Osoyoos, which became operational in March 1993. A two technique internationally. Currently, both sterile male and female

year clean-up phase to reduce wild populations (1992–1993) was codling moths are released as there is no genetic sexing system

followed by three years of sterile moth release (1994–1997) before which could improve the SIT release procedures (Marec et al., 2005).

the last phase monitoring and sterile moth periodical release to As a result, the mass rearing and ﬁeld release procedures are not as

maintain low levels of damage was carried out. The program suc- optimal and economical as they could be. However, recent advances

cessfully controlled populations; 42 and 91% of orchards had no made in genetics to create a transgenic strain susceptible to a cold

detectable damage in 1995 and 1997, respectively, and insecticide treatment allowed for the selection of males only in mass-rearings

use for codling moth was reduced by 82% from 1991 to 2001 (Bloem (Ferguson et al., 2011; Paladino et al., 2014). Steady ﬁnancial sup-

et al., 2007). port is also crucial; without strong support from governments and

Between 2002 and 2007, the International Atomic Energy growers, the implementation of SIT in AW- IPM programs is dif-

Agency (IAEA), working with different countries, started search- ﬁcult and could lead to situations such as the closing down in

ing for ways to improve codling moth SIT ﬁeld application (IAEA, 2014 of the company in charge of rearing sterile codling moths

2007). The possibility of combining SIT to other control methods in the Western Cape, South Africa (Thorpe, 2015). In 2015, OKSIR

and the success obtained by OKSIR inspired projects in Argentina was still active and pursuing sterile male codling moth releases in

and South Africa. This contributed to the progress made on ster- British-Columbia as well as supplying individuals for other coun-

ile codling moth quality control and management, allowing for tries’ eradication programs or for research purposes.

improved ﬁeld application and research to develop a genetic sexing

strain for male-only rearing (Vreysen et al., 2010). The few papers 3.1.2. Light brown apple moth

on SIT for codling moth that have been published since the review Epiphyas postvittana is a tortricid leafroller native to Australia

by Vreysen et al. (2010) are summarized below. which has recently invaded Europe and North America (Common,

Because the development of facilities used for mass-rearing of 1970; Suckling and Brockerhoff, 2010). It can have up to ﬁve gen-

sterile insects is expensive, current projects focus on the possi- erations in California and attacks apple, peach, plum, nectarine,

bility to use sterile moths produced by OKSIR to release them in cherry, and apricot (Varela et al., 2008). In 2007, laboratory trials

other countries. In Canada, the release of sterile moths ends in and a small-scale program that were implemented in Australia and

September and resumes in March, leading to a decrease in the num- New Zealand to suppress the pest showed promising results (USDA,

ber of insects produced at the Osoyoos facilities. The production 2009)

of sterile codling moths for release in the Southern Hemisphere In California, an eradication program based on sterile moths

during the Northern Hemisphere winter should provide economic combined to mating disruption was planned after the pest was

and social advantages. However, the mating compatibility between detected in 14 counties in 2007 (Varela et al., 2008). However

Canadian mass-reared codling moths and the wild population of the ﬁrst aerial release of disrupting pheromones in September

those countries must be assessed. Under laboratory conditions, 2007 resulted in about 600 health-related complaints from resi-

Taret et al. (2010) tested the mating compatibility of eleven combi- dents (Garvey, 2008). Pressure from the public, organizations and

nations of codling moths originating from seven different countries, local governments resulted in the suspension of the aerial spraying

and found that individuals reared in Osoyoos could mate with (Carey and Harder, 2013) but despite the controversy, research is

those from Argentina, Armenia, Syria, New-Zealand, Switzerland still conducted on SIT as a method to control the light brown apple

and South Africa. Bloem et al. (2010) also demonstrated that after moth, as detailed below.

48 h of transportation, sterile Canadian codling moth males are still In laboratory conditions, Soopaya et al. (2011) observed the pro-

equally attracted to calling Canadian or South African wild females. duction of highly sterile F1 males (sterile at 99%) when male moths

Moreover, the longevity of irradiated codling moths shipped from from the parent generation were partially irradiated at 250 Gy and

the Osoyoos facilities, traveling for three days, is similar to that of Jang et al. (2012) found that F1 fertility was inferior to 1% (deter-

wild South African codling moths (Blomeﬁeld et al., 2011). mined by egg hatch). Results from experiments in a wind tunnel

Because releasing mass-reared moths from diapausing larvae and release-recapture ﬁeld observations showed that the disper-

increases male competitiveness in orchards (Judd et al., 2006), sal ability of E. postvittana could be reduced after irradiation at

Carpenter et al. (2005) conducted laboratory trials in which they 250 Gy. This should be accounted for when determining the moth

studied the irradiation level needed for mass-rearing of diapaus- sterile:wild ratio (Suckling et al., 2011). Moreover, the production

ing or non-diapausing moths. They demonstrated the absence of of the major sex component in irradiated females was reduced by

difference in irradiation requirements, which could simplify the 70% when irradiated at 300 Gy and male catches decreased by 11%

year-round production of sterile moths to be used in summer and in traps with such females (Stringer et al., 2013). These results show

winter in the Northern and Southern Hemispheres, respectively. that irradiation at over than 250 Gy causes effect on E. postvittana

Phenotypic plasticity can be used to improve ﬁeld performance behavior. Also, Kean et al. (2011) developed a population model

of irradiated codling moth. Experiments on thermal tolerance which predicts that a 200 Gy dose provoking partial F0 sterility and

showed that moths have a high temperature tolerance; moth sur- nearly full F1 sterility would allow releasing only a third of the ster-

◦

vival increased from 20 to 90% when they were subjected to a 37 C ile moths that would be produced when irradiated at 300 Gy. The

◦

pre-treatment for 1 h and a 43 C pre-treatment for 2 h, respec- model also predicts a 95% population reduction when the moth

tively (Chidawanyika and Terblanche, 2011a). Chidawanyika and sterile:wild ratio exceeds 6.4:1 in pheromone traps but validation

Terblanche (2011b) also observed that laboratory cold-acclimated of this model is still needed.

◦

codling moths (20 C) released in an orchard were recaptured more

frequently in pheromone traps in cold climate, whereas warm- 3.1.3. Painted apple moth

◦

acclimated codling moths (30 C) were recaptured more frequently The painted apple moth, Teia anartoides Walker (Lepidoptera:

in traps under warm conditions. This response to temperature accli- Lymantriidae), is an Australian insect pest defoliating plants of

mation could then be used to improve the efﬁcacy of moths once importance in horticulture and forestry; it can attack apple, peach,

released in a region with climate conditions differing from the rear- plum or cherry even if these trees are not its principal hosts. This

ing conditions. pest has invaded the Auckland region of New Zealand in 1999. From

Even if the applicability of SIT to control codling moths in 1999–2006 an eradication program was implemented. It ﬁrstly

orchards was considerably improved, economic considerations began by multiple applications of Foray 48B (Bacillus thuringiensis

G. Chouinard et al. / Scientia Horticulturae 208 (2016) 13–27 21

(Berliner), subsp. kurstaki) to decrease pest populations; in 2002 SIT fruit ﬂy strains (2009–2014). A considerable amount of publica-

was integrated to the program and sterile males were released in tions resulted from these programs, which can be found in special

2003. Progeny (F1 and F2) issued from F0 males irradiated at 100 Gy issues of Florida Entomologist (2002, volume 85 and 2007, volume

after being outcrossed with fertile females were sterile (Suckling 90), Genetica (2002, volume 116) and BMC Genetics (2014, vol-

et al., 2007). By 2004, no males were trapped in the area treated ume 15). Only studies published since 2011 are summarized below

and since that time, the painted apple moth is ofﬁcially considered because Vreysen et al. (2006) and Pereira et al. (2011) reviewed pre-

eradicated from New Zealand. The SIT technique is now available vious studies on medﬂy. These recent advances show that efforts

against the painted apple moth but no research or other program are made to reinforce the use of SIT for medﬂy control in different

has been conducted on this species since this success. regions of the world producing stone fruits and other fruits.

The IAEA developed a genetic sexing strain, by using a tem-

◦

3.1.4. Oriental fruit moth perature sensitive lethal mutation (female eggs exposed to 35 C

Because G. molesta requires several insecticide treatments per would die and so, all females would be eliminated from the mass-

season in many pome and stone fruit growing regions of the world, rearing), which reduced the cost of SIT operations (Caceres, 2002;

the potential of SIT was evaluated by Genchev (2002), in collab- Franz, 2005). Since this development, the genetic sexing strains

oration with the Food and Agriculture Organization of the United VIENNA 7 and VIENNA 8 have been used for all medﬂies produced in

Nations and the IAEA. Doses of 400–500 Gy induced 96 and 97% the world and SIT effectiveness improved considerably as a result.

of eggs mortality when irradiated as pupae and adults, respec- Molecular markers targeting sperm from strain VIENNA 8 are now

tively, whereas lower doses (100–150 Gy) caused sterility on F1, available to evaluate the efﬁcacy of sterile males to inseminate wild

but only partial sterility on F0. A small-scale ﬁeld trial was realized females (Juan-Blasco et al., 2013). Scolari et al. (2014) reviewed how

in Bulgaria and both partially and fully sterile males were released functional genetics can impact medﬂy control with SIT; new genes,

separately in an orchard at a rate of 12,000 irradiated pupae per promoters and regulatory sequences are now becoming available

release, in order to have a sterile: wild ratio of 20:1 (Genchev, 2012). for the development and improvement of competitive medﬂy sex-

Damage on mid-early and late varieties was observed on 0.5–3.5% ing strains.

of the fruits treated as opposed to 19.5–35% of the untreated fruits. Research showed that the laboratory performance of sterile C.

Since this study, no research has been conducted on G. molesta, capitata males was enhanced by administering hormonal, nutri-

although the pest can be reared on C. pomonella artiﬁcial diet tional or semiochemical supplements after the irradiation process

(Chubb et al., 2012). and before their release in the wild (Pereira et al., 2011). Notably,

exposition to ginger root oil aroma increases male competitiveness

3.2. SIT to control fruit ﬂies and their mating success (Shelly et al., 2004). Paranhos et al. (2013)

showed that a dose as low as 0.1 ml of ginger oil/m is enough

3.2.1. Mediterranean fruit ﬂy to induce a high sterility level. The age of males also plays a role;

In many countries, Ceratitis capitata (Wiedemann) (Diptera: 5 days-old sterile males exposed to ginger root oil had higher mat-

Tephritidae) is one of the most serious pest of fruits and vegetables ing success and induced higher eggs sterility than 2–3 days-old

because of the high level of damage it causes to unprotected crops exposed sterile males (Steiner et al., 2013).

and because of the import restrictions in fruit ﬂy-free areas (Liquido

et al., 1990; Thomas et al., 2013). Ceratitis capitata can exploit 300

3.2.2. European cherry fruit ﬂy

different host plants; it is a multivoltine species that can live for

A ﬁrst SIT program against the European cherry fruit ﬂy was

several months. Cherry, apple, plum, apricot, peach, nectarine and

developed from 1976 to 1979 in Switzerland. The pest was com-

pear are pome and stone fruits readily attacked by this pest (Thomas

pletely controlled in a zone where 2.8 million sterile ﬂies were

et al., 2013). Fruit loss in absence of medﬂy control can reach a value

released (Boller, 1997). However, the absence of an effective R.

of $US 445 million per year in the Mediterranean region. In the same

cerasi mass-rearing facility has blocked the pursuit of SIT methods

region, over 14 years, the IAEA (2001) has estimated the economic

for this species. R. cerasi is univoltine and has an obligatory diapause

value of the loss caused by the medﬂy to be of $US 2.4 billion.

of 150 days which makes the mass-rearing difﬁcult (Daniel and

The ﬁrst SIT program that successfully eradicated the medﬂy

Grunder, 2012). However, the recent success obtained by Köppler

was implemented in Mexico from 1977 to 1982. It allowed the

et al. (2009) on the artiﬁcial rearing of R. cerasi may lead to new

creation of a fruit ﬂy-free area covering Mexico and the United

advances in the development of strategies to control this pest.

States (Klassen and Curtis, 2005). Many AW-IPM programs have

since used SIT successfully to prevent, control or suppress the med-

3.2.3. Spotted wing drosophila

ﬂy in Chile, Peru, Argentina, South Australia, Spain and Tunisia,

A study on irradiation treatments for quarantine control of D.

to name a few (Klassen and Curtis, 2005; Vreysen et al., 2007). In

suzukii (Follett et al., 2014) has recently lead to the evaluation of SIT

Mediterranean parts of the Middle East (Israel, Jordan, Lebanon, the

as a potential control method for this invasive pest in Canada and

Palestinian territories and the Syrian Arab Republic) where apple,

France, in collaboration with the IAEA. The objectives of the project

pear, plum, apricot, nectarine and cherry are grown (Enkerlin and

are to evaluate the dose-response of D. suzukii males to radiation

Mumford, 1997), the SIT-SUPP and SIT-ERAD AW-IPM programs

and to study the competitiveness of irradiated males in laboratory

have released irradiated medﬂies in stone fruit orchards (IAEA,

and semi-ﬁeld conditions (Firlej, unpublished data).

2001). The total weekly production of sterile medﬂies in the 15

facilities around the world reached several billions per week in the

late 1990s (Hendrichs, 2000). 4. Mating disruption

In the last 15 years, numerous collaborative research projects

involving the IAEA and many countries have focused on different Mating disruption consists in diffusing the synthesized sexual

aspects of SIT to simplify and improve the technique for usage pheromone of an insect pest within a crop in order to disrupt

on medﬂies. These projects aimed at (1) developing the systems reproduction. In a completely disrupted environment, females will

used to collect female fruit ﬂies so that the trapping network remain unmated or mating will be delayed, affecting negatively egg

sensitivity used in large scale SIT control programs would be laying, fertility and reproductive rates (Jones et al., 2008; Fadamiro

improved (1999–2005); (2) improving the performance of sterile and Baker, 2002). Recently, Miller and Gut (2015) extensively

males (2004–2009); and (3) developing and evaluating improved reviewed mating disruption technologies and species involved, so

22 G. Chouinard et al. / Scientia Horticulturae 208 (2016) 13–27

Fig. 3. Various standard hand-applied dispensers for mating disruption of codling moth: (A) IsomateTM; (B) CidetrakTM; (C) CheckMateTM; (D) Meso dispenser (reproduced

from Paciﬁc Biocontrol Corporation, Trécé Incorporated and Suterra web sites).

the purpose of this section will be limited to additional details on 2014). Labor availability and cost are still the major constraints in

some recent advances for pome and stone fruits. the adoption of the mating disruption technology, especially when

Organic growers were among the ﬁrst to mating disrup- hand-applied dispensers are deployed in orchards (Casado et al.,

tion when it became commercially available in the mid-1990s 2014; Thomson, 2015). Mating disruption may be a viable alter-

(Granatstein et al., 2015). The use of mating disruption has native to conventional insecticides but in some cases, the smaller

expanded substantially since then in many of the fruit producing expenses associated with reduced insecticide applications may not

areas of the world, with about 300,000 treated hectares against compensate for the cost of the pheromone product itself, especially

insect pests of pome and stone fruits (Miller and Gut, 2015). In in areas where few insecticide applications are needed to control

South Tyrol, Italy, in Argentina, in South Africa and in Washington the targeted insect (Baldessari et al., 2012). In these cases, mating

state in the United States, mating disruption is adopted by pome disruption is mostly used as a rescue tool when insecticides can no

fruit growers and about 90% of the area are treated (Thomson, longer be applied (e.g. resistance, regulatory constraints).

2015). In other countries this approach is still under evaluation, Despite thousands of published papers over 40 years of research,

or limited in use, due to the small size of orchards, which makes the mode of action of mating disruption still is not well understood

it less appropriate or effective (Andreadis et al., 2014; Kovanci, and only a few cases exist where a speciﬁc process was attributed to

G. Chouinard et al. / Scientia Horticulturae 208 (2016) 13–27 23

Table 4

Characteristics of exclusion, disruption and sterilization techniques for pest control. A: Relative advantages and disadvantages; B: Relative suitability for major fruit pests.

Suitability classes: + = suitable; − = unsuitable or not applicable; ? = under evaluation or unknown.

Exclusion netting Sterile insect release Mating disruption

Implementation costs/ha ++ +++ +

Minimum size of implementation area + +++ ++

Effect on pest population levels + +++ ++

Potential for resistance + ++ ++

Adaptability to diverse crop systems +++ + ++

Selectivity + +++ ++

Environmental footprint ++ ++ +

Perspectives for farm use ++ + +++

Codling moth +++ ++ ++

Tephritid ﬂies +++ ++ −

Leafrollers + ++ +

Drosophila ﬂies ++ ? −

Brown marmorated stink bug ++ − ?

the success of a formulation (Miller and Gut, 2015). Mating disrup- deployed uniformly at a rate of 1200 m/ha throughout the orchard,

tion involves many mechanisms operating in sequence interfering one every fourth row, starting at the border row (Brunner and Ohler,

with mate location and reproduction (Miller et al., 2010). One of 2015).

the main reasons for the rapid development of mating disruption

in pome fruits is the development of insect resistance to insecti-

cides (Brunner et al., 2002; Charmillot and Pasquier, 2002; Veronelli

4.2. Current and future uses for pest control

et al., 2012) and more recently the regulatory restrictions on broad-

spectrum organophosphate insecticides in North America (US EPA,

In pome and stone fruits, mating disruption is mostly used

2008) as well as other insecticides in Europe (Veronelli et al., 2012).

against two major pests: the codling moth and the oriental fruit

moth. Area-wide mating disruption of codling moth has been con-

4.1. Technologies ducted in many countries on most of the continents (Thomson and

Jenkins, 2014). Worldwide use of mating disruption against this

Since the ﬁrst registration of a mating disruption product against pest represents more than 200,000 treated hectares, almost half

the codling moth in 1987 (Charmillot et al., 2007), many mating of which being located in North America (Witzgall et al., 2008;

disruption products, in various dispensers, have been registered to Thomson, 2015). Hand-applied dispensers are mostly used along

control nearly 15 insect pests in pome and stone fruits. Technolo- with sprayable formulations and aerosol dispensers (Basoalto et al.,

gies have been reviewed by Miller and Gut (2015): they include (1) 2014; Baldessari et al., 2012; McGhee et al., 2012). The latter ones

hand-applied dispensers, (2) machine-applied dispensers (sprays, have been adopted 15 years ago and since have been increasingly

ﬂakes, droplets), (3) aerosol dispensers and (4) meso dispensers. used for mating disruption of the codling moth (Casado et al., 2014).

Since then, the hand-applied dispensers have been the most used Due to the high cost of using dispensers at the full rate, a cur-

by growers and are still widely used at least against codling moth rent trend is to use less hand-applied or aerosol dispensers per

(McGhee et al., 2012). New-generation hand-applied dispensers hectare and supplement them with insecticide or virus applications

are about the same size as the standard ones (Fig. 3), but contain (Charmillot et al., 2007; Miller and Gut, 2015).

a lower amount of pheromones (McGhee et al., 2012; Gut et al., Mating disruption of the oriental fruit moth is used in 60,000 ha

2014), which reduces their cost. Larger meso dispensers, contain- of pome and stone fruit orchards (Miller and Gut, 2015) and area-

ing a higher amount of pheromones than the standard dispensers, wide projects have also been conducted for this pest in Australia,

also exist (Miller and Gut, 2015). Those were developed to solve Mexico and South Africa (Thomson and Jenkins, 2014). The hand-

the various problems associated either with the labor availabil- applied dispenser method is the most widely used technology

ity, the time required to apply the various types of hand-applied against the oriental fruit moth; it requires about half the number of

dispensers, or the cost of the pheromone (Basoalto et al., 2014). dispensers normally installed to control the codling moth (Caruso

Although meso dispensers have shown similar levels of attractancy et al., 2014; Miller and Gut, 2015).

for male codling moth as that of standard dispensers (Brunner and Mating disruption has also been registered for use in some

Wiman, 2012), dispensers applied at reduced densities compro- countries against other pome and stone fruit pests – such as the

mised mating disruption mechanisms (Miller and Gut, 2015). European leafroller, Archips rosana (L.) (Lepidoptera: Tortricidae),

On the other hand, the aerosol dispensers, which have been the fruittree leafroller, Archips argyrospila (Walker) (Lepidoptera:

used in pome fruits since 1996 (Casado et al., 2014) are more Tortricidae), the lesser peachtree borer, Synanthedon pictipes

and more adopted by pome fruit growers (McGhee et al., 2014). (Grote & Robinson) (Lepidoptera: Sesiidae), the light brown apple

Aerosol dispensers are generally used in conjunction with hand- moth, Epiphyas postvittana (Walker) (Lepidoptera: Tortricidae), the

applied dispensers, the latter being distributed on the borders obliquebanded leafroller, C. rosaceana (Harris) (Lepidoptera: Tort-

of the orchard (McGhee et al., 2014). This combination prevents ricidae), the omnivorous leafroller, Platynota stultana Walsingham

the problem of uneven distribution of pheromones associated (Lepidoptera: Tortricidae), the pandemis leafroller, Pandemis pyru-

with borders (Milli et al., 1997), which leaves areas with little or sana Kearfott (Lepidoptera: Tortricidae), the peach twig borer,

no pheromone where mating is more likely to occur (Charmillot Anarsia lineatella Zeller (Lepidoptera: Gelechiidae), the peachtree

et al., 2007). Recently, the application of pheromone microcapsules borer, Synanthedon exitiosa (Say) (Lepidoptera: Sesiidae), and the

through sprinklers has provided high levels of codling moth and threelined leafroller, Pandemis limitata (Robinson) (Lepidoptera:

oriental fruit moth disruption (Gut et al., 2014). Also, a long rope Tortricidae) – but treated areas are much less important (Miller

pheromone release device is now being tested. The long rope is and Gut, 2015).

24 G. Chouinard et al. / Scientia Horticulturae 208 (2016) 13–27

Disruption formulations targeting several co-occurring sec- compared techniques, mating disruption is the one which is the

ondary pests may affect up to six pests: often a major targeted most widely used at the farm level.

pest, as the codling moth or the oriental fruit moth, and at least None of these three approaches are universal or effective for

one secondary pest (Judd and Thomson, 2012; Tasin et al., 2014). all species; there is no need to transpose the paradigm of pesti-

As pheromone products used in mating disruption are harm- cides to those new ways of managing pests. Those approaches are

less to beneﬁcial insects, the environment, workers and consumers, technology-intensive, but at the same time they have the potential

they are appealing to the public concerned about pesticide use in to signiﬁcantly reduce the need for pesticides, to minimize effects

orchards. Although the use of mating disruption against fruit pests on beneﬁcial insects and other non-targeted organisms, to increase

has increased by about 50% during the last decade (Miller and Gut, sustainability and to reduce impacts of agriculture on the health of

2015), its rate of adoption in the near future will depend, at least, consumers and growers. Few novel pest management tools offer

on its cost-competitiveness with insecticides. One way to decrease these properties for organic agriculture.

the cost associated to the pheromone product itself, or to the labor,

would be to increase the effectiveness of the technologies, such as

Acknowledgements

the long rope or the aerosol pheromone dispensers. Cost reduc-

tion may also be achieved by combining pheromones and host

We would like to thank Jonathan Veilleux for reviewing the

plant products. The behavioral effects of the mixture on adults, lar-

manuscript. Part of this work is based upon research supported by

vae, or both may enhance the efﬁcacy of mating disruption (Gurba

the Conseil de développement de l’agriculture du Québec (CDAQ),

and Guerin, 2015; Knight, 2015; Kovanci, 2015). Financial support

the Agri-Innovation and the Innov’Action agroalimentaire programs,

from governments may also help growers to adopt the mating dis-

supported by Agriculture and Agri-Food Canada and the ministère

ruption technology as was observed in Belgium, where fruit areas

de l’Agriculture, des Pêcheries et de l’Alimentation du Québec,

under mating disruption increased widely as soon as subsidies were

through the Growing Forward 2 initiative.

available (Bengels and Beliën, 2012).

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