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Bulletin of Insectology 72 (1): 35-54, 2019
ISSN 1721-8861 eISSN 2283-0332
A review of the apple sawfly, Hoplocampa testudinea
(Hymenoptera Tenthredinidae)
Charles VINCENT1, Dirk BABENDREIER2, Weronika ŚWIERGIEL3, Herman HELSEN4, Leo H. M. BLOMMERS5
1Horticultural Research and Development Centre, Agriculture and Agri-Food Canada, Saint-Jean-sur-Richelieu,
Quebec, Canada
2Integrated Crop Management Advisor, CABI, Delémont, Switzerland
3Swedish University of Agricultural Sciences, Department of Plant Protection Biology, Alnarp, Sweden
4Wageningen University & Research, Zetten, The Netherlands
5Rhenen, The Netherlands
Abstract
The apple sawfly (ASF), Hoplocampa testudinea Klug (Hymenoptera Tenthredinidae), attacks only one host plant, the apple tree
(Malus domestica Borkh.). It is found in temperate regions of Europe as well as in Eastern North America. The flight of the ASF
adults coincides with the bloom of apple trees and larvae develop in fruitlets. As the ASF spends approximately 11 months of its
life cycle underground as a pre-pupa or pupa, management of the ASF is possible only during 1 month. The ASF is univoltine and
has an obligatory diapause that can be extended to 2, 3 or rarely 4 years. Here key publications about the ASF have been selected
for their relevance to the application of Integrated Pest Management programs. Because the ASF is dependent on living and de-
veloping tissues and because no oviposition or artificial diet is available for laboratory experimentations, research projects have to
be conducted in field or semi-field conditions. The main natural mortality factors are the ichneumonid parasitoids Lathrolestes
ensator (Brauns), present in Europe and introduced to Eastern Canada, and Aptesis nigrocincta (Gravenhorst) in Europe. The lat-
ter also acts as a hyperparasitoid of L. ensator. Management of the ASF can be based on monitoring adults with sticky traps and
with use of a simulation model. Non-insecticidal methods that can be used deliberately in an ASF management program are re-
viewed, notably nematodes, entomopathogenic fungi, and physical control methods such as cellulose barriers and exclusion net-
ting. The technical and economic reasons preventing widespread implementation of these approaches are discussed.
Key words: apple sawfly, Hoplocampa testudinea, Lathrolestes ensator, Aptesis nigrocincta, apple orchards, nematodes.
Introduction
Among insect pests associated with apple (Malus
domestica Borkh.) orchards, the apple sawfly (ASF),
Hoplocampa testudinea Klug (Hymenoptera Ten-
thredinidae) (figure 1), has a particular status. The ASF
is a pest that directly attacks the fruit and is challenging
to manage in commercial orchards because it is vulner-
able to control measures for less than a month per year.
Adults are diurnal and mainly active during bloom,
when conserving pollinators is imperative to apple fruit
production and young larvae are vulnerable only during
a short period immediately after petal fall, thus restrict-
ing possibilities for chemical treatment. Moreover, ovi-
position and larval development of the species depend
entirely on a healthy progress of the apple fruit from
pollination to subsequent fruit set. Hence, as no artificial
diet or oviposition medium has been developed for la-
boratory rearing, research has to be done under field or
semi-field conditions.
The scientific and technical literature on H. testudinea
comprises ca. 300 articles. Key early papers on the biol-
ogy of the ASF presented information from Germany
(Velbinger, 1939), England (Miles, 1932; Dicker and
Briggs, 1953), Holland (Kuenen and van de Vrie, 1951),
Austria (Böhm, 1952), and France (Chaboussou, 1956).
A series of papers on natural and biological control
were published (notably in Poland in the ‘80s by Ja-
worska), several of which are not readily accessible be-
cause they were written in various languages and were
often published in currently rare journals.
Our objective was to critically review the literature on
the biology, ecology and behaviour of the ASF, as well
as on key antagonists, with particular reference to appli-
cation in apple protection programs. We aimed to be
comprehensive but focused on key information, includ-
ing details where appropriate. We first discuss the his-
torical perspective, distribution, identification, host
plant, life cycle, and rearing of ASF. Next, the occur-
rence of natural factors such as parasitism and patho-
gens is discussed. Research and deliberate efforts lead-
ing to possible applications within an Integrated Pest
Management (IPM) program are treated under the head-
ing “Management”.
Historical perspective on pomiculture
It should be first emphasized that the old literature on
the ASF refers to apple orchards quite different from
modern ones. The traditionally large trees with tall
trunks were difficult if not impossible to sample sys-
tematically, while non-insecticidal management tools
were limited and fruit thinning was impossible on a
commercial scale (hand fruit thinning was impractical at
that scale). Alternate fruit bearing was the general situa-
tion and levels of fruit damage varied accordingly. Ex-
treme events of various sorts, for example seven ASF
larval entries in one fruitlet or ASF larvae crawling over
the orchard floor in search of a new fruitlet, are no long-
er realistic. Currently, observations and pest control
practices are much easier on small spindle trees.
36
(Continued)
37
(Figure continued)
Figure 1-10. (1) Female ASF ovipositing in an apple flower; (2) ASF caught on sticky trap, (2a) ventral view of
male and (2b) female; (3a) External appearance of fresh oviposition scar shown by red arrow, (3b) tissues of fruit-
let receptacle under egg deposition, (3c) as revealed by dissection, (3d) ASF egg in receptacle as revealed by dis-
section, (3e) ASF egg development (after Kuenen and van de Vrie 1951; see also Trapman, 2016b); (4) ASF ma-
ture larva; (5a) ASF primary damage early season, (5b) late season; (6a) Migrating ASF larva and secondary dam-
age showing frass near entry and exit holes, (6b) one ASF larva can damage several nearby fruitlets, (6c) fruitlet
cut open showing mature ASF larva and semi-liquid frass plugging hole; (7) Late season appearance of sting dam-
age caused early in the season on apple cultivar Natyra; (8a) L. ensator adult, (8b, 8c) ASF larvae parasitized by
L. ensator, red arrow show the endoparasite; (9a) ASF larvae and pupae, (9b) ASF pupa with exit hole of L. ensa-
tor; (10) Sticky white trap used to monitor ASF adults. Authors of photos: (1*, 3a*, 5b*, 9a*) Léo-Guy Simard;
(2a, 2b) Jacques Lasnier; (3b, 3c, 3d, 3e, 4, 6a, 6b, 10) Weronika Świergiel; (5a, 7) Herman Helsen, (6c) Greg
Krawczyk; (8a*) Benoit Rancourt; (8b*, 9b*) Pierre Lemoyne; (8c) Dirk Babendreier.
*Reproduction permission of figures 1, 3a, 5b, 8a, 8b, 9a, 9b of the Department of Agriculture and Agri-Food, Gov-
ernment of Canada; © Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture
and Agri-Food Canada.
38
Distribution
The ASF is native to temperate regions of Europe, from
Great Britain in the West to the Volga river (Russia) in
the East (Fauna Europaea, 2018a). It is rare in Mediter-
ranean countries, and absent in Ireland and Iceland.
The ASF was introduced accidentally to North Ameri-
ca, where its common name is European ASF. Its dam-
age was first reported on a crabapple tree in Long Is-
land, New York, in 1939, and positive identification
was made in 1942 from specimens collected in a New
York State orchard (Pyenson, 1943). Currently, the ASF
is present in all major apple-producing regions of New
England, Pennsylvania, and in neighbouring States of
Delaware, Maryland and West Virginia (Greg Kraw-
czyk, personal communication).
In Canada, the ASF was reported in 1940 on Vancou-
ver Island in Victoria, British Columbia (Downes and
Andison, 1942; Downes, 1944). There are no further
mentions of the ASF in western North America, proba-
bly because it was eradicated there before it reached the
continent. In eastern Canada, ASF was found for the
first time in 1979 in Hemmingford, Quebec (Paradis,
1980), a few kilometres from the New York State-
Quebec border. Subsequently, it was quickly found in
all major apple-producing areas of Quebec (Vincent and
Mailloux, 1988). Currently, it is found in major apple-
producing areas from Port Hope, Ontario, to Nova Sco-
tia (Vincent et al., 2016).
Identification
The genus Hoplocampa Hartig 1837 is a well-defined
and stable group within the sawfly subfamily Nematinae
(Prous et al., 2014). Hoplocampa species are associated
with Rosaceae, each with one or a few related species of
pome- or stone fruits (subfamilies Maloideae and
Prunoideae). Their life histories are similar. Keys to
adults of the North American species are presented in
Ross (1937; 1943), to the British species in Benson
(1952) and to most European species in Masutti and
Covassi (1980). Wing venation of the ASF is typical for
the genus (e.g. Prous et al., 2014). The bodies of male
and female ASF adults are black above and orange un-
derneath. H. testudinea is the largest species in the ge-
nus and the only one associated with apple trees. Adult
female ASF are larger than males. While males have a
rounded abdomen extremity (figure 2a), females have a
conspicuous brown ovipositor, the saw, that is clearly
visible ventrally even when specimens are caught on
sticky traps (figure 2b).
Miles (1932) and Lorenz and Kraus (1957) described
the larval morphology of the ASF. The neonate larva is
whitish with a black head and dorsal black marks on
three terminal segments, and clearly visible eyes. The
full-grown larva is about 12-13 mm long with a brown
head. The larvae of H. testudinea can be easily distin-
guished from other internal fruit feeders. Like other
sawfly larvae, in addition to the three pairs of true legs
on the foremost (thoracic) segments (figure 8b), they
have another 6 pairs of non-segmented prolegs on ab-
dominal segments 2-7. In contrast, lepidopteran larvae
like the codling moth (Cydia pomonella L. Lepidoptera
Tortricidae) and the fruitlet mining tortrix - several spe-
cies, including Pammene rhediella (Clerck) Lepidoptera
Tortricidae - have only 4 pairs of prolegs on segments
3-6 (Alford, 1973). The frass of ASF larvae is wetter,
sometimes almost dripping (figure 6b-c), than that of
lepidopteran larvae, while fruit with older ASF larvae
are easily recognized by a characteristic and nasty smell
resembling that of stink bugs. No other fruit-feeding
sawfly has been recorded on apple. Occasionally, the
pear sawfly, Hoplocampa brevis (Klug) (Hymenoptera
Tenthredinidae), has been observed to oviposit and de-
velop in apple ovaries in the laboratory (Velbinger,
1939), and Ametastegia glabrata (Fallen) (Hymenoptera
Tenthredinidae) cause infestations in orchards of Swe-
den (Weronika Świergiel, personal observation). The
natural history of sawflies, including the genus Hop-
locampa, their habits, and information on curation of
specimens are treated by Benson (1950) and Gauld and
Bolton (1988). Like other nematine larvae, ASF larvae
have epidermal ventral glands in protrusible sacks; one
gland is located behind each pair of legs on the first to
the seventh abdominal segment (Benson, 1950; Boevé
and Pasteels, 1985; Boevé et al., 1996). Maxwell (1955)
treats the internal larval anatomy of sawflies.
Host plant
H. testudinea is restricted to apple as a host plant. The
only attack by this pest on another tree species was re-
ported by Stritt (1943), who found foul-smelling larvae,
larger than those of the pear sawfly, in a pear orchard
near Stuttgart, Germany. The following year, he reared
a few adult female ASF out of infested pears from the
same orchard. Velbinger (1939) reported that the ASF
did not oviposit on either pear (3 cultivars) or plum
(1 cultivar), whereas the pear sawfly accepted apples
from 5 out of 6 cultivars.
As apple trees need cross-pollination, orchards are
composed of mixes of cultivars planted in a spatial lay-
out with respect to flowering time and pollination com-
patibility. Several articles mention differences in ASF
attack among apple cultivars, and some explain these
observations to be the result of ‘preference’. For in-
stance, in the Bordeaux region (France), Roussel and
Mansencal (1961) reported 20, 30 and 35% damage
caused respectively to cultivars Golden Delicious, Win-
ter Banana and Grand Alexandre.
From 14 females caged on the cultivar Gascoyne’s
Scarlet the number of eggs was 0.3 per day compared to
1.7-5.8 for susceptible cultivars (Briggs and Alston,
1969). The ratio of primary (figure 5a-b) to secondary
(figure 6a-c) damage was four times greater, suggesting
either larval mortality or slow larval development on
cultivar Gascoyne’s.
In conclusion, differences in damage levels between
apple cultivars are often due to the reaction of the ASF
to factors varying among cultivars such as flower densi-
ty and colour, flowering period and fruit set.
Life cycle
Drawing mostly on papers by Velbinger (1939; 1948),
Miles (1932), Dicker (1953), Böhm (1952), Chaboussou
(1956; 1957) and Sjöberg et al. (2015) a summarized
life cycle follows.
39
The ASF is univoltine. The adults emerge before or at
the pink stage (phenological stage BBCH 59) of early
flowering cultivars (Miles, 1932; Kuenen and van de
Vrie, 1951; Babendreier, 1998; Ciglar and Baríc, 2002).
Peak adult activity is greatest on still, sunny days (Dick-
er, 1953; Haalboom, 1983). Within 24 hour of emer-
gence, females start laying eggs into the receptacle of
open flowers when the temperature is > 11 °C (Graf et
al., 1996c). Most eggs are normally laid before the end
of bloom (BBCH 65-69) (Sjöberg et al., 2015) (figure
3a-d). Several studies report that egg deposition starts
on the king flowers of older branches (Kuenen and van
de Vrie, 1951; Gottwald, 1982; Tamošiūnas, 2014;
Trapman, 2016b). Neonate larvae mine the fruitlet su-
perficially while subsequent larval stages typically mi-
grate to other fruitlets to eat internal tissues, and eventu-
ally their seeds. Last larval instars enter the soil to form
a cocoon. The ASF overwinters as prepupae which
evolve into pupae in spring.
Adults
The emergence of adults is generally studied by con-
centrating last-instar larvae on a defined spot where they
can enter the soil and by collecting emerging adults in a
cage the following spring. Emergence is well synchro-
nized with the bloom period e.g., starting 3 days before
the pink stage of cultivar McIntosh in Quebec (Vincent
and Mailloux, 1988) and extending over approximately
2 weeks (Babendreier, 1998). In some cases, females
emerge slightly earlier than males (Stepniewska, 1939;
Vincent and Mailloux, 1988; J.-P. Zijp, unpublished). In
other cases, both sexes emerge simultaneously
(Velbinger, 1939; Niezborala, 1978; Babendreier,
1998).
Estimates of sex-ratios have been done frequently.
However, both visual inspection of trees and tapping
branches over an umbrella have given highly variable
results. For example, the latter method yielded an aver-
age of 30% (Dicker, 1953) and 75% (Velbinger, 1939)
males. More reliable figures may be obtained by allow-
ing adults to emerge under semi-field conditions. Graf
et al. (1996a) reared 68% females (n = 565) from fruit-
lets showing secondary damage (figure 6a-c).
Babendreier (1998) found sex-ratios of 66, 70 and 79%
females (n = 633). J.-P. Zijp (unpublished) recorded
emergence of 64-73% females in samples reared in an
orchard or in containers in an insectary, with an overall
average of 68% (n = 1340) across three years.
ASF adults feed on pollen or nectar of apple flowers
and take up droplets of water present on apple leaves
(Miles, 1932). They fly during day time only (Gottwald,
1982). As in other sawfly species, pheromones and oth-
er chemical stimuli are most likely involved in encoun-
ters between males and females, but none have been re-
ported so far. Mating occurs soon after emergence
(Velbinger, 1939; Böhm, 1952), and lasts on average 3
minutes in field cages (Babendreier, 1998) or approxi-
mately 5 minutes in the open field (Miles, 1932). Both
sexes spend > 80% of the daylight hours on apple flow-
ers (Babendreier, 1998).
In early May in Switzerland, Babendreier (1998) ob-
served average lifespans of 11.5 days for females and
10.0 days for males in field cages covering a flowering
apple tree. Graf et al. (2001) found the average lifespan
of females to be 24.3 days at 10.5 °C and 7.0 days at
20.5 °C.
Oviposition nearly always takes place on open flowers
(Miles, 1932; Velbinger, 1939; Dicker, 1953) (figure 1).
The females walk over the stamens for some time, then
move between the petals to the outside of the receptacle
and oviposit in the skin of the receptacle. This causes a
small funnel-shaped mark visible on fruits at harvest
(figure 7). The total time for oviposition is about 60-120
seconds (Miles, 1932; Soenen, 1952; Roitberg and Pro-
kopy, 1980), with an average of 115 seconds determined
under field cage conditions (Babendreier, 1998). Ovipo-
sition attempts lasting < 50 seconds are unsuccessful
(Roitberg and Prokopy, 1984). It was also observed that
oviposition was interrupted after ants contacted adult
ASF (Babendreier, 1998).
Using traps, Wildbolz and Staub (1986) found that
adults were attracted first to the top of the trees and then
moved down the trees for egg-laying, particularly on the
south side. Hence most eggs were found higher up in
the trees. Accordingly, larval distribution across apple
trees in an orchard was found to be aggregated
(Babendreier, 1998). This is consistent with findings of
Tamošiūnas et al. (2015) who demonstrated a strong
tendency for aggregation of adult ASF across orchards
in Lithuania, with a constant position of the clumps over
years.
Eggs
Eggs are laid singly in the base of the receptacle in a
pocket-like cavity made by the female saw (figure 3d).
Sometimes, eggs are found between stamens. The ovi-
position channel is 1-2 mm deep and the insertion mark
of about 2 mm in length turns dark within a few days
(figure 3a-b)(Velbinger, 1939; Böhm, 1952). Not all in-
sertion marks contain an egg. Niezborala (1978) count-
ed between 1 and 17.5% empty marks on various culti-
vars.
One egg is laid per flower, exceptionally two (Soenen,
1952; Niezborala, 1978; Gottwald, 1982; Weronika
Świergiel, personal observation). Direct behavioural ob-
servations have shown that females lay one or two eggs
per fruit cluster if these have 5 or 6 flowers, but always
lay only a single egg per cluster if few flowers are pre-
sent in a cluster (Babendreier, 1998). The presence of an
egg has no effect on the number of visits to the flowers.
However, females spent significantly less time on the
receptacle of an uninfested flower before attempting
oviposition, or before leaving, than did females on an
egg-infested blossom (Roitberg and Prokopy, 1984).
Following oviposition, 83% of ASF females inspect the
oviposition wound and place their mouthparts on it for a
few seconds; only 18% of females show that behaviour
when oviposition had been unsuccessful. When the ovi-
positor is withdrawn, a droplet that exudes from the
oviposition slit is often consumed by the female (Dick-
er, 1953). This exudation causes a brownish discolora-
tion of the fruitlet skin that can be visually detected by
careful examination (Miles, 1932) (figure 3a).
Velbinger (1952) and Chaboussou (1961a; 1961b)
40
have demonstrated that virgin females lay as many via-
ble eggs as mated females. Whether sex determination
is by arrhenotoky, like in most Hymenoptera (Heimpel
and de Boer, 2008), is unknown for the ASF. Several
researchers reported an average of < 30 eggs laid per
female under artificial conditions (Soenen, 1952; Böhm,
1952; Dicker, 1953; Chaboussou, 1961a; 1961b; Alford,
1973; Graf et al., 2001). However, as the ASF is syn-
ovigenic (i.e., the female continues to produce mature
eggs if she is fed adequately), egg laying capacity under
field conditions may be greater. Velbinger (1939) found
up to 78 eggs in the ovary of one female and cites Ka-
zansky (1935) who found a maximum of 87. Niezborala
(1978) reported between 16 and 116 eggs, with an aver-
age of 43. Field collected females had 25.4 fully grown
eggs on average, plus 33.8 eggs of smaller size with
yolk (J.-P. Zijp, unpublished). As these females had
been laying some eggs already and had their stomachs
filled with pollen, the potential production must have
been well over 30 eggs per female. Babendreier (1998)
found on average 8.5 eggs in the ovary of freshly
emerged females, while females fed honey and water
but deprived of apple flowers for oviposition reached a
plateau of approximately 35 eggs at about 6 days after
emergence.
As illustrated by Kuenen and van de Vrie (1951),
there are six egg stages (figure 3e) (Trapman, 2016a).
The freshly laid egg is kidney-shaped (Miles, 1932;
Böhm, 1952) and measures 1 × 0.33 mm (Babendreier,
1998). It is whitish and viscous (yoghurt-like), and the
chorion becomes transparent after 2-3 days, allowing
observation of larval development. The egg swells and
changes form as development proceeds. This causes a
rupture in the fruitlet epidermis, leaving the egg partial-
ly exposed (Miles, 1932). The embryonic development
(from egg deposition until egg hatching) spans 8-20
days, with an average of 12 days (Kuenen and van de
Vrie, 1951). Graf et al. (2002) determined that egg de-
velopment takes 85 DD (> 6.9 °C). Most eggs survive
temperatures as low as −2.5 °C, but young larvae that
have not yet penetrated the fruit are killed at < 0 °C
(Feytaud, 1924). Fungal infestations were seen to kill
eggs laid in cool and humid weather (Noack, 1993).
Larvae
There are five larval instars that can be distinguished
by the width of the head capsule. Miles (1932) provided
the following average (minimum-maximum) widths in
mm: first instar 0.392 (0.34-0.42); second 0.550 (0.53-
0.57); third 0.786 (0.76-0.82); fourth 1.106 (1.07-1.16);
fifth 1.526 (1.49-1.57). Slightly smaller head capsules
were found by Babendreier (1998) and by Hey and
Steer (1934). Growth of head capsules follows Dyar’s
law. The first instars have a light grey-brown head, the
second, third and fourth a blackish brown head and anal
plates of similar colour, and the fifth a yellowish-brown
head and a light anal plate (Velbinger, 1939). These
colours develop a few hours after moulting.
The first instars mine the fruitlet superficially, leaving
a typical meandering scar on the epidermis of the grow-
ing fruitlet (Petherbridge, 1928) (figure 5a), the primary
damage, a term coined by Dicker (1953). Like un-
harmed fruits, such fruitlets remain on the tree until har-
vest (figure 5b). Neonate larvae that hatch inside a fruit-
let generally start mining between or just below the sep-
als, while those hatching in the open start to mine
somewhere on the side of the fruitlet.
Some second but mostly third instars move to a near-
by fruitlet and burrow towards the seeds on which they
feed. These fruitlets show secondary damage, as termed
by Dicker (1953) (figure 6a-6c). Chaboussou (1961) ob-
served that about half of these larvae moved to a third
fruitlet, while Dicker (1953) observed that 17% of the
larvae moved three times (figure 6a-b). Feeding on up to
5 fruitlets, as mentioned by Kuenen and van de Vrie
(1951) is quite unlikely in a well-managed orchard.
While entering a second fruitlet, the fruit skin is not in-
gested by larvae, but scraped with the mandibles and put
aside. This is why stomach poisons like lead-arsenate
have little larvicidal effect (Kuenen and van de Vrie,
1951). Moulting occurs exclusively within the fruitlet
(Velbinger, 1939).
Larval frass is frequently found plugging the entry
hole made in the fruitlet by older larvae (figure 6a-c).
As some ASF larvae might have exited the fruitlet, only
dissections of fruitlets showing secondary damage pro-
vide a reliable indicator of larval presence (Vincent et
al., 2016). More than one ASF larva can be found per
fruit, particularly when ASF populations are high, as
reported in the early literature (Miles, 1932; Velbinger,
1939). Destruction of the seeds causes premature fruitlet
drop, generally in June, well after the larva has de-
scended into the soil.
Development of the egg and through the fifth instar
takes between 3 and 5 weeks in the field in central
and northern Europe (Velbinger, 1939; Böhm, 1952;
Dickler, 1954; Niezborala, 1978; Gottwald, 1982;
Babendreier, 1998; Sjöberg et al., 2015). The exact
time is difficult to determine because studies must be
conducted in fruitlets growing on the tree to obtain a
realistic estimate.
The last larval instars produce a characteristic odour,
akin to those emitted by several stink bug species (He-
miptera). Boevé et al. (1996) showed that disturbed lar-
vae emit four aliphatic compounds by everting their
ventral glands, but only the fifth instar produces quanti-
ties that can be easily smelled by humans. Four butanoic
compounds (i.e., 3-hydroxy-2-butanone; 3-methyl-1-
butanol; 2,3-butanediol; 1,2-butanediol) and 2-phenyl-
ethanol were found to emanate mainly from the frass of
full grown larvae (Boevé et al., 1996).
The full-grown larva (figure 4) evacuates its intestines
before leaving the fruitlet and burrows immediately into
the soil, where it may take up to an hour to find a suita-
ble spot to pupate when the soil is dry and without
cracks (Böhm, 1952). If soil structure permits, the larva
may descend up to 25 cm below ground level (Miles,
1932; Böhm, 1952; Dicker, 1953; Jaworska, 1979b;
Ciglar and Baríc, 2002). Sandy soils allow greater sur-
vival (Zijp and Blommers, 2002a). In the soil, the larva
spins a cocoon and transforms into a prepupa within a
few days (figure 9a).
41
Pupae
The ASF spends approximately 11 months under-
ground as a prepupa or pupa in a cocoon. Velbinger
(1939) extensively described the preparation of the co-
coon by the larva. The cocoon has two layers, is water
impermeable and measures 7-8 mm long by 3-4 mm
wide (Velbinger, 1939). In Europe, pupation occurs in
March or April, about 3-4 weeks before adult emer-
gence (Miles, 1932; Böhm, 1952; Zijp and Blommers,
1993). As reported for several sawfly species (Danks,
1987), some prepupae have a prolonged diapause for a
second or third year (Dicker, 1954; Niezborala, 1978;
Zijp and Blommers, 1993). Babendreier (1998) reported
proportions of 36.8, 9.2, 8.4 and 1.6% adult emergence
after 1, 2, 3 and more years underground, respectively.
Prolonged diapause may provide better chances of sur-
vival, notably in years with poor fruit set, or when lar-
vae are killed by insecticides (Kuenen and van de Vrie,
1951).
Rearing
Rearing the ASF throughout its life cycle is impeded by
its dependence on the healthy growth of apple ovaries.
However adults may be obtained from full-grown larvae
or cocoons. The latter may be collected by sampling soil
from under well infested trees, and by crumbling or by
sieving it over water. The cocoons can be easily collect-
ed because they float (Velbinger, 1939). It is easiest,
however, to collect late instars from fruitlets showing
secondary damage (figure 6a-c). These can be laid on
the ground (Velbinger, 1939) so that the descending lar-
vae go directly into the soil. They can also be put on
wire mesh placed over a bucket, so that descending lar-
vae can first be checked for parasitoids and counted be-
fore use (Babendreier, 1998). When ASF larvae are
placed on sandy soil, the cocoons can easily be collected
by sieving the soil after a few weeks. Sand particles
(i.e., quartz < 0.8 mm) should be used to allow success-
ful cocoon spinning and increased survival rate
(Weronika Świergiel, personal observation). The co-
coons are drought tolerant; to produce many adults,
ASF larvae put into small soil-filled pots stored without
covering in an outdoor insectary had to be watered only
twice in 10 months. For containment, large earthen
flower pots or wide plastic tubes filled with larvae can
be buried in the ground to study overwintering in the
orchard, while at the same time this will exclude preda-
tion by ants or moles. Reared adults can be isolated on
branches by means of sleeve cages, and the flowers
have to be pollinated by hand, as pollination by the en-
caged sawflies is insufficient.
Natural control
Parasitoids
Only ichneumonids have been reported to parasitize
the ASF (table 1). Lathrolestes ensator (Brauns) (Hy-
menoptera Ichneumonidae) is the usual larval parasitoid
of the ASF in European orchards (Fauna Europaea,
Table 1. Parasitoids reported from H. testudinea.
Species
Country
Reference*
Lathrolestes ensator (Brauns)
Germany
Velbinger, 1939
Switzerland, France
Carl and Kählert, 1993
The Netherlands
Zijp and Blommers 1993; 2002a; 2002b
Switzerland
Graf et al., 1994
Baltic area of Russia
Tchakstynia, 1968
SW USSR, Ukraine
Tchakstynia, 1968; Zerova et al., 1992
Germany
Babendreier, 1996; 1998
England
Cross et al., 2001
Canada
Vincent et al., 2001; 2002; 2013; 2016
[reported as Lathrolestes marginatus (Thomson)]
Poland
Jaworska, 1987
[reported as Lathrolestes marginatus (Thomson)]
Ukraine USSR
Karabash, 1967
[reported as Lathrolestes marginatus (Thomson)]
Ukraine USSR
Onufriejcik, 1974*
Lathrolestes luteolus (Thomson)
Moldavia USSR
Tuniekiej, 1966*
Lathrolestes citreus (Briscke)
Poland
Niezborala, 1976
Aptesis nigrocincta Gravenhorst
Switzerland
Carl and Kählert, 1993
Microcryptus nigrocinctus Gravenhorst
Moscow USSR
Skorikova, 1969*
= Aptesis
Lithuania
Zajanckauskas, 1963*
Microcryptus abdominator (Gravenhorst)
Poland
Dulak-Jaworska, 1976
Phygadeuon talitzkii Telenga
Moldavia USSR
Tuniekiej (= Talickiej), 1966*
Holocremna bergmanni (Thomson)
Poland
Dulak-Jaworska, 1976
Thersilochus jocator (F.)
Poland
Dulak-Jaworska, 1976
Hemitheles areator (Gravenhorst)
Poland
Dulak-Jaworska, 1976
Lathrostizus macrostoma (Thomson)
Switzerland
Carl and Kählert ,1993
Unidentified ectoparasites**
Germany
Velbinger, 1939
*References from Jaworska (1987). **similar parasites found on H. testudinea, H. brevis and H. minuta larvae,
which occurred in large numbers on the latter two species.
42
2018b), notably in Germany (Velbinger, 1939), Switzer-
land (Carl and Kählert, 1993), The Netherlands (Zijp
and Blommers, 1993) and the UK (Cross et al., 1999b).
In Poland, Lathrolestes marginatus (Thomson) (Hyme-
noptera Ichneumonidae), reported by Jaworska (1987;
1992), appeared to be the same species, i.e., L. ensator
(Barron, 1994; Zijp and Blommers, 2002b). Zerova et
al. (1992) refer to L. ensator as the major parasitoid of
ASF in Ukraine, while a single specimen of the parasi-
toid was reared from H. testudinea larva found in Gold-
en Delicious fruitlets near the village of Tirolo (Alto
Adige, Italy) in 1995 by Leo H. M. Blommers (personal
observation).
Two other Lathrolestes species have been reported as
important enemies of the ASF: Lathrolestes citreus
(Brischke) (Hymenoptera Ichneumonidae) in Central
Poland (Niezborala, 1976), and Lathrolestes luteolus
(Thomson) (Hymenoptera Ichneumonidae) in Moldavia
(Tuniekiej, 1966 in Jaworska, 1987). However, these
two names cannot apply to parasitoids of the ASF, as to
they pertain to tiny parasitoid species of leafmining
sawflies of linden and elm, respectively (Reshchikov,
2015).
The flight of L. ensator starts when the flight of the
ASF is almost over, i.e. around mid-May in The Nether-
lands. Emergence of adults from the host cocoon (figure
9b) in the soil occurs when temperatures at 10 cm below
ground level reach 13 °C (Jaworska, 1987). Adult males
appear first. Females are pro-ovigenic (they have fully
developed eggs at emergence) and have 88 and 120
eggs according to Babendreier (1998) and Zijp and
Blommers (2002b), respectively. How L. ensator find
its host is not known, but Babendreier (1996) observed
females hovering above the apple tree canopy and enter-
ing fruit clusters infested by the ASF significantly more
often than uninfested ones. Females were even seen to
land directly on an infested fruit in 22 out of 23 visits to
infested fruit clusters.
Although a parasitoid egg is occasionally found in
first instars ASF (Zijp and Blommers, 1993; Babendrei-
er, 1998), females oviposit mainly in second instars
(Onufreichik, 1974; Jaworska, 1987; Babendreier,
1998), which feed superficially under the fruit skin. Fe-
males L. ensator rarely oviposit in ASF larvae once
these are inside the fruitlet (Babendreier, 1998): in only
1 out of 14 observations did females successfully parasi-
tized a larva inside the fruitlet, which still was a second
instar. A delay in parasitoid emergence due to a week of
cold weather apparently forced their acceptance of third
instar ASF, as the latter had continued growing (Zijp
and Blommers, 2002b). Taking into consideration the
well synchronized development of apples and the ASF,
L. ensator has a short period to parasitize ASF larvae,
which may be modulated by suitable weather conditions
prevailing during that period. Babendreier (1998)
showed that, in 6 out of 8 mass collections, higher para-
sitism rates were obtained for larvae developing later, as
parasitism increased from 10 to 40% during the 10-day
emergence period from collected fruitlets. This suggest-
ed a lack of synchronization of host and parasitoid or a
higher performance of L. ensator at a later point in time
when temperatures are usually slightly higher. For the
ASF, this might create a selection pressure to oviposit
early.
Female L. ensator lay up to 25 eggs per day, and 60 in
4 days (Jaworska, 1987). Superparasitism is common.
The ovipositing female apparently does not avoid previ-
ously parasitized larvae and at least up to 4 eggs can be
found in one ASF larvae, although only one egg eventu-
ally develops into an adult (Jaworska, 1987; Zijp and
Blommers, 1993; Babendreier, 1998). The banana-
shaped egg is initially white, but turns black soon after
oviposition, so that it becomes visible through the host
skin (figure 8b-c). The egg remains visible in the fully-
grown host larva entering the soil but, about 2-3 weeks
later the 0.7-0.9 mm long caudate larva has hatched. In
the larval host, the size of encapsulated and non-
encapsulated eggs is 0.4 × 0.3 mm and 0.58 × 0.17 mm,
respectively (Jaworska, 1987).
The neonate parasitoid larva has a brownish head cap-
sule and a 0.2-0.3 mm long tail. Within a few weeks, by
the time the larva entirely fills up the body cavity of the
host, it completes its development. Cocoon formation
starts about 40 days after the host enters the soil (Ja-
worska, 1987). The filmy cocoon lies against the inner
wall of the host cocoon, with the head capsule and other
remains of the host in between. In The Netherlands, the
pupa of L. ensator gradually develops through winter, in
contrast to its host (Zijp and Blommers, 1993). In re-
gions experiencing cold continental winters (as in Po-
land), pupal development starts in early spring (Ja-
worska, 1987).
Like its host, some prepupae of L. ensator do not de-
velop into an adult until after two or three winters; their
cocoons are located deeper in the soil (Jaworska, 1987).
Babendreier (1998) found a strong correlation in the
proportions of pupae remaining in diapause after one
winter between L. ensator and its host, while the rate
was consistently higher for the parasitoid than for the
ASF (Babendreier, 1998; Zijp and Blommers, 2002b).
In Belarus, Onufreichik (1974) found that few parasi-
toids emerged after one winter, 35-81% after two win-
ters and 19-61% after three winters.
In The Netherlands, L. ensator is present in most ap-
ple orchards under IPM programs that harbour the ASF
(Zijp and Blommers, 1993). In Poland, Jaworska (1987)
found that parasitism was < 4% in pesticide-treated or-
chards, and ranged from 8 to 79% in untreated orchards.
Parasitism levels > 80% were reported by Karabash
(1967) in Ukraine, Zijp and Blommers (1993) in The
Netherlands, and Vincent et al. (2016) in Canada. How-
ever, larval parasitism levels between 20 and 40% are
more typical (Carl and Kählert, 1993; Graf et al., 1994).
Mass collections in 27 orchards, managed organically or
according to IPM principles, showed parasitism rates
between 0.6 and 40% with a tendency for higher rates in
orchards having fewer pesticide treatments (Babendrei-
er, 1998). Based on a tentative life table, Zijp and
Blommers (2002b) estimated that the population density
of ASF may increase 2.4 times annually, and that 60%
larval parasitism must occur in order to achieve regula-
tion of ASF populations.
Another factor detrimental to L. ensator is the vulner-
ability of parasitized ASF larvae to fungal diseases in
43
the soil. In Poland, Jaworska (1987) observed > 70%
mortality of parasitized larvae by a fungus. The highest
mortality (52%) occurred during development of the
parasitoid larva in the ASF cocoon, compared with
about 15% after the parasitoid had spun its own cocoon.
Carl and Kählert (1993) found a similar difference be-
tween unparasitized (19%) and parasitized (52%) larvae
killed by Paecilomyces farinosus. Parasitized ASF lar-
vae were sporadically killed by nematodes in the soil
(Jaworska, 1987).
A second ichneumonid parasitoid species of the ASF
is Aptesis nigrocincta (Gravenhorst) (syn. Microcryptus
nigrocinctus) (Hymenoptera Ichneumonidae) (Baben-
dreier, 2000). Few papers have been published on this
species, probably due to its cryptic life history, i.e.,
functioning as a cocoon parasitoid below ground. How-
ever, it has been found in several apple orchards in
Switzerland (Carl and Kählert, 1993; Babendreier,
1999; 2000) and in the Baltic States (Zajanckauskas,
1963, in Jaworska, 1987). Çoruh et al. (2014) found it in
Turkey but it is unclear as to whether this was in apple
orchards or other habitats. Females are brachypterous
while males are normally winged. As A. nigrocincta
females seek to parasitize the cocoons underground,
they need cracks or fissures in the soil to reach their
host (Carl and Kählert, 1993). Preliminary tests indicate
that A. nigrocincta females may follow a chemical trail
left on the ground by fifth instars ASF to find hosts
(Babendreier, 1998).
A. nigrocincta adult lifespan is on average 2 months
when given food and hosts. It is synovigenic and lays an
average of 20 eggs during its lifetime (Babendreier,
2000). After penetrating the cocoon, the eggs are laid
externally on the host. At 20 °C, larvae hatch after a few
days and larval development is completed after 11.5
days. The complete cycle is finished after about 39 days
at 20 °C. Superparasitism occurs in this species and a
major determining factor for the female decision to lay
an additional egg seems to be the encounter rate with
hosts (Babendreier and Hoffmeister, 2002).
In Switzerland, three emergence periods have been
observed for A. nigrocincta: a first period in June, well
synchronized with the descending phase of the ASF; a
second period observed during August, and; a third one
in October (Babendreier, 1999). Hibernation takes place
as mature larva in the cocoon or in the adult stage (fe-
males only). Rates of parasitism within a single genera-
tion ranged from 12.1 to 39.7 % (Babendreier, 2000).
Zajanckauskas (1963, in Jaworska, 1987) reported 33%
parasitism. The impact of this multivoltine parasitoid
accumulates on its univoltine host; consequently, A. ni-
grocincta may be a major mortality factor of ASF co-
coons. Despite seemingly having potential to play a role
in controlling ASF populations, A. nigrocincta is not
considered as a classical biological control agent be-
cause of its lack of host specificity and because it is a
hyperparasitoid of L. ensator (Babendreier and Hoff-
meister, 2003).
A related species, Microcryptus abdominator Graven-
horst (Hymenoptera Ichneumonidae), was reported by
Jaworska (1987), who reported rearing several speci-
mens of Holocremna bergmanni Thomson (now Olesi-
campe bergmanni). Little information is available on
these and other parasitoid species listed in table 1: sev-
eral were reported only once in Eastern Europe, often in
low numbers. In the absence of recent taxonomic work
on most of these species, their identification should be
treated with caution.
It may be concluded that, as far as is known, L. ensa-
tor is the only specific parasitoid of the ASF larva. It
occurs over most of the ASF distribution range in Eu-
rope, and currently in some regions of Eastern North
America.
Predators
Hanne Lindhard Pedersen (personal communication)
observed predatory insects feeding on ASF eggs in a
Danish orchard. Predatory bugs like Himacerus apterus
(F.) (Hemiptera Nabidae) were observed feeding on
young ASF larvae (Zijp and Blommers, 2002b). Lady-
birds and lacewings have also been reported to attack
ASF larvae, while ants (Lasius sp.) may kill ASF larvae
that seek to enter the soil (Velbinger, 1939). Some holes
of about 0.1 mm diameter were found in ASF cocoons
collected from the soil in Switzerland, suggesting uni-
dentified arthropod predators acting below ground
(Babendreier, 1998). To what extent the pupae are de-
stroyed by moles, shrews and other insectivorous
mammals is unknown. Velbinger (1939) mentioned spi-
ders as predators of ASF adults. Nagy (1960) also ob-
served birds taking adult plum sawfly, Hoplocampa fla-
va L.. Pedersen et al. (2004) mentioned the deliberate
use of young hens to eat insect larvae on the ground, a
method that likely impacts the ASF as well. Overall, the
impact of predators is undetermined.
Entomopathogenic fungi
Fungi that kill H. testudinea in its cocoon in the soil
can be important mortality factors. More than 70% of
the larvae may be killed by Paecilomyces fumoso-
roseus (Wize) Brown et Smith, Paecilomyces farinosus
(Dicks et Fr.) Brown et Smith and Verticillium lecanii
(Zimm.) (Jaworska, 1992). Graf et al. (1994) found 8.2-
16.2% of ASF killed by P. farinosus. Carl and Kählert
(1993) found this fungus on hibernating H. testudinea
removed from the soil, where 19% of ASF prepupae and
52% of prepupae parasitized by L. ensator were killed,
mostly by this fungus. Onufreichik (1974) found 15-
30% of hibernating larvae were killed by the fungi
Beauveria bassiana (Bals.) Vuill. and P. fumoso-roseus
under natural conditions
Nematodes
In Poland, Jaworska (1986) found dead ASF larvae
and pupae infested with mermithid, rhabditid and stei-
nernematid nematodes. Less than 2.3% of the ASF lar-
vae died due to mermithids. Diapausing ASF pupae
were also found infested with rhabditid nematodes. In
Petri dish trials, rhabditids were not consistently patho-
genic to ASF larvae. However steinernematids were
highly pathogenic. Their effect was observable 48 hours
after infection.
44
Management
Types of damage
The ASF is a pest that directly destroys the crop by
causing three types of damage. First, a mark, the so-
called “sting”, is caused by the actual oviposition (fig-
ure 3a-b). The tiny slit in the receptacle made by the
female saw results in an inconspicuous funnel-like de-
pression near the petals of the growing fruit. In the case
of unsuccessful oviposition or egg hatch, this is the only
sign of ASF presence that can be recognized on mature
fruits (figure 7). The slight deformation of the fruit does
not usually lead to quality downgrade. Second, the su-
perficial mining of the young larva leads to the typical
ribbon-like scars (Petherbridge, 1928) (figure 5a-b).
Fruits with this primary damage (Dicker, 1953) often
remain on the tree until harvest and are downgraded.
Third, on entering a nearby fruitlet the migrating larvae
(figure 6a) feed rapidly and voraciously causing sec-
ondary damage (figure 6a-c) (Dicker, 1953). Such fruit,
with internal tissues, ovary walls and even seeds having
been eaten by the older ASF larvae (figure 6c) fall in
June, allowing the ASF to complete its life cycle under-
ground (Miles, 1932).
Basic considerations
Secondary damage visible at harvest (figure 5b) pro-
vide a rough estimate of actual ASF density and the risk
of damage next year, because several factors are at play
between bloom and harvest, notably flower abundance
on different cultivars, natural control by predators and
diseases, coincidence of flowering and ASF peak flight,
and premature fruit drop. An experienced grower or an
advisor familiar with the orchard will often be able to
make an educated guess and qualitatively assess such
conditions, but a quantitative risk assessment for the fol-
lowing year is not feasible.
Before the commercial availability of synthetic insec-
ticides prior to World War II, ASF was one of the major
pests of apples because effective control was difficult if
not impossible to attain on the large fruit trees with
available means. Excessive levels of ASF damage were
not unusual, e.g., up to 90 % fruit damage (primary and
secondary) on cultivar Worcerster Pearmain in England
(Miles, 1932) and up to 60% in Victoria, British Co-
lumbia, orchards (Downes and Andison, 1942). Like-
wise, Vincent and Mailloux (1988) observed up to 85%
fruit showing secondary damage in an untreated apple
orchard in Frelighsburg, Quebec.
Kuenen and van de Vrie (1951) noted that, whereas
the ASF is one of the most important direct pests of ap-
ple orchards, its damage is unimportant in abandoned
orchards. This may be because of alternate fruit bearing
or more abundant natural enemies present in neglected
orchards. When fruitlets are scarce, necessary resources
for the completion of the ASF life cycle are limited: fe-
males do not find fruitlets for oviposition and migrating
larvae have difficulty finding a new fruitlet nearby. By
contrast, sufficient flowers and fruitlets are present an-
nually in well-managed orchards.
In general, when devising ASF management pro-
grams, a pest manager has to consider tactics that would
have adulticidal, ovicidal or larvicidal effects. It is theo-
retically possible that adults can be killed or behaviour-
ally impaired by insecticides applied before bloom. ASF
eggs and early instar larvae are mostly vulnerable to
post-bloom treatments.
Physical control methods
Some physical control methods to manage ASF have
been investigated. Hand removal of infested fruitlets
and soil tillage were common control practices in the
past (Velbinger, 1939). Removal of infested fruits as
soon as the superficial mining scars (primary damage)
appear, so as to prevent secondary damage, is currently
performed in some commercial orchards in Sweden and
Denmark (Weronika Świergiel, personal observation).
Benoit et al. (2006) tested cellulose sheets as a physi-
cal barrier that could prevent the completion of life cy-
cles of the ASF and the plum curculio (Conotrachelus
nenuphar Herbst) (Coleoptera Curculionidae). Availa-
ble in rolls, the sheets were deployed on the soil under
the canopy of apple trees such that applets naturally fall-
ing in June would fall on the sheets, preventing larvae to
enter the soil for further development. A cage put over
experimental quadrats after fruit drop allows determina-
tion of the emergence of adults the following spring.
Cellulose sheet reduced ASF adult emergence by 60 to
95% compared with the control. But as some prepupae
have a prolonged diapause and stay in the soil for sever-
al years, complete management of an ASF population
would require the use of this tactic for several consecu-
tive years.
Haalboom (1983) showed that ASF damage was lower
on trees near zinc-white traps (figure 10) but concluded
that mass trapping was too expensive as a management
method, although a similar method is currently used in
some Danish organic orchards (Weronika Świergiel,
personal observation). Cardboard sticky traps are folded
and stapled around the wires at intervals of every 2-4
trees, while fruitlets showing primary damage are re-
moved.
The application of kaolin, a hydrophobic particle film
of fine white clay marketed as Surround™ in the USA
and Europe (Glenn et al., 1999), reduces ASF damage,
but it is unclear to what extent. Repeated applications of
kaolin against apple scab disease - Venturia inaequalis
(Cooke) G.Winter - reduced high ASF damage on culti-
var J. Grieve by ca. 75% in insecticide-treated orchards
compared with controls (Markó et al., 2006; 2008).
However, it also exerted a negative effect on the larval
parasitoid L. ensator.
In testing the effect of exclusion nets covering apple
trees in studies conducted in Quebec, Chouinard et al.
(2017) obtained ambiguous results: in 2012 ASF dam-
age at harvest was 0.28% (covered) vs 0.69% (uncov-
ered), while in 2016 ASF damage was 0.14% (covered)
vs 0% (uncovered). Finally, if apple trees are few and
small such as in private gardens, successful manage-
ment can be obtained by removing all infested fruit be-
fore the third week of June, i.e. before larvae leave the
fruitlets and enter the soil (Alford, 1973).
45
Monitoring and decision making
The necessity to apply insecticides against ASF adults
before bloom is a difficult decision to make, as it chiefly
depends on observations from the previous year. How-
ever, if a drastic reduction of ASF populations is need-
ed, a pre-bloom application of an adulticide can be
made, followed by a larvicidal treatment post-bloom.
Under a post-bloom treatment scenario, the full range of
action thresholds for control of ASF becomes available.
In addition to recording infestation levels in the previ-
ous year, a pest manager can score the numbers of ASF
adults caught on visual traps and count the numbers of
flowers with eggs or fruitlets with incipient primary
damage.
Infestation levels from the previous year may be de-
termined by fruit showing primary damage at harvest or,
preferably, fruitlets showing secondary damage before
June drop. This is a first step to support decision making
the following year. For example, van den Ende et al.
(1996) proposed monitoring ASF adults with visual
traps when damage to the previous year’s harvest was >
1% and no detrimental side effect on ASF eggs or larvae
is expected from insecticide applications targeted
against other pests.
The use of visual traps to monitor the ASF flight has a
long history. Kuenen and van de Vrie (1951) observed
that few eggs are deposited in flowers with the petals
removed. Chaboussou (1961b) concluded that oviposit-
ing females prefer white over pink flowers. Comparing
ASF captures on traps painted with different spectral
reflectances ranging from 300 to 650 nm, Owens and
Prokopy (1978) found the highest captures on surfaces
painted with Zn-white. As Zn-white and apple flower
petals have similar reflectance patterns, i.e., white with
almost no reflectance of UV, ASF adults appear to be
specifically responsive to the colour of the blossoms on
which they feed, often mate, and oviposit (Owens and
Prokopy, 1978).
In several countries, Owens and Prokopy (1978) in-
spired research that contributed to the use of sticky traps
based on the behaviour of ASF adults (Gottwald, 1982;
Haalboom, 1983). In 1975-1979, Gottwald (1982) stud-
ied ASF behaviour with cylindrical white sticky traps in
a region west of Berlin (Germany). He found that more
males than females were captured and that most adults
were captured on the South East and South West-sides
of the traps; exposure to the sun had a positive effect.
Most activity occurred between 9:00 and 11:00, at 18-
21 °C (air temperatures), and > 50% of daily captures
occurred within 3 hours. Male captures dominated in the
morning while female captures slightly dominated in the
afternoon. It was concluded that traps should be posi-
tioned on the South side of a tree (although tree rows in
modern plantings are usually directed North-South), and
high enough to be exposed to the sun.
The white plastic ‘cross traps’ type REBELL™, origi-
nally developed by Remund and Boller (1978) and test-
ed by Wildbolz and Staub (1984; 1986), are currently
widely used in Europe. Graf et al. (1996c) found three
traps per cultivar to be the optimal number for reliable
ASF monitoring. Due to the limited range of the traps
(only 3% of released ASF were recaptured at 40 m dis-
tance), low mobility and heterogeneous distribution of
ASF, a distance of 50 m between traps is suggested.
Captured specimens should be carefully examined, be-
cause white sticky traps attract other sawfly species,
such as Hoplocampa species from nearby pear or plum
trees, visually similar species like the cabbage or turnip
sawfly (Athalia rosae L.) (Hymenoptera Tenthredini-
dae), and a number of flies and bees from nearby wild
vegetation. Unlike plum sawflies adults (Sprengel,
1930), ASF adults are not attracted by fermenting fruit
sap or wine (Böhm, 1952).
Graf et al. (1996b) recommended deploying white
sticky traps at 8-10 days before bloom. If traps are in-
stalled too early, they may lose their visual attractive-
ness by capturing too many other insects. Zijp and
Blommers (1997) found that in order to capture the first
emerging adults with a safety margin, the traps should
be deployed at 157 degree-days (DD) (> 4 °C, air tem-
perature) from March 15. Although the model was vali-
dated and found acceptable for seven different localities
in Sweden (Sjöberg et al., 2015), caution should be tak-
en when adopting the model in other geographical areas,
as Graf et al. (1996c) found that the temperature-
dependent post-diapause development of prepupae from
different European regions differed significantly, while
different artificial substrates also had some influence on
the time of emergence (Graf et al., 1996a). Graf et al.
(1996c) suggest that inclusion of winter dormancy
might improve the model, as the severity of winter af-
fects the duration of diapause.
Trap catches provide a reliable estimate of adult
emergence as > 95% of released females were caught
within 24 hours (Graf et al., 1996c). However, the relia-
bility in forecasting the risks of fruit damage is low, be-
cause the traps compete with the attractiveness of open
flowers and the attraction of ASF adults is weather de-
pendent (Haalboom, 1983). In spite of these limitations,
cumulative trap catches can be used to determine the
necessity of a pesticide application. In 19 orchards in
Massachusetts, Coli et al. (1985) reported a significant
positive relationship between the numbers caught on
fewer than one non-UV reflecting white trap per ha and
the primary damage scored on the trees shortly before
harvest. In Quebec, Vincent and Mailloux (1988) found
a similar significant relationship in 13 orchards over 5
years, when the traps were deployed after a pre-bloom
insecticide application and the primary damage scored
on 1000 fruits at harvest. However, the damage in both
studies was low, rarely > 1%, with few and extreme ex-
ceptions. Coli et al. (1985) suggested a cumulative
threshold of 4.7 ASF captures per trap, so as to attain
< 0.7% damage at harvest, while Vincent and Mailloux
(1988) reported both false negative and false positive
cases, most probably due to the pre-bloom treatment in
combination with a low trap density. In Ontario, Cana-
da, the action thresholds for post-bloom treatments are
based on trap captures, i.e. 6 ASF adults per trap if an
insecticide has been applied pre-bloom, and 3 ASF
adults per trap if no insecticide has been applied pre-
bloom (OMAFRA, 2018).
Greater action thresholds have been suggested in Eu-
rope. After several years’ experience, Höhn et al. (1993)
46
stated that 20-30 ASF adults captured per trap indicate a
risk if the flowers are abundant and the ASF flight coin-
cides with the flowering period.
When interpreting trap captures, factors such as pre-
vailing weather conditions and blooming intensity
should be considered. Activity of ASF adults increases
during sunny days (Dicker, 1953) and decreases due to
unfavourable weather conditions, e.g. rain and cloud
cover (Haalboom, 1983). Several studies have shown
that, after a steady increase, trap catches decrease during
peak bloom due to visual competition with flowers, and
increase again at petal fall (Gottwald, 1982; Haalboom,
1983; Coli et al., 1985; Noack, 1993; Graf et al., 1996c;
Zimmer, 2000; Sjöberg et al., 2015). Sjöberg et al.
(2015) found that 85% of the total oviposition, but only
60% of total female captures occurred up until full
bloom (BBCH 65). They suggest that, if this finding is
confirmed in other localities, the variation in the rela-
tionship between trap catches and damage levels might
decrease using only trap catches until full bloom. In
summary, the most important parameter to implement a
control threshold is trap captures before peak bloom be-
cause they represent the great majority of the oviposi-
tion, while captures scored during and after peak bloom
(after BBCH 64) are less reliable estimates with respect
to oviposition.
It is noteworthy that the use of these parameters de-
pends on local factors and the experience and insight of
the grower or advisor with respect to such elements as
hand thinning, premature fruit drop, or market destina-
tion of the crop. Control thresholds based on cumulative
trap catches mainly concern the decision whether to
count eggs in quasi-real time or primary damage later
on. For example, in The Netherlands a few traps are po-
sitioned in orchards and cultivars where damage is ex-
pected (Marc Trapman, personal communication). Trap
catches > 50 ASF adults per trap always require treat-
ment. When cumulative captures range between 20 and
50 ASF adults per trap, a monitoring of 50 flower clus-
ters per orchard and cultivar for eggs is performed. The
decision for treatment is based on knowledge of previ-
ous damage in the orchard, the intensity of flowering,
and is always advised when eggs are present in > 10%
of flower clusters. Using white sticky traps in northern
Germany, Noack (1993) advised counting ASF eggs
when > 2 ASF adults have been captured per trap.
Counting eggs (figure 3d) or oviposition scars (figure
3a-b) is the oldest and most direct way to determine the
threat of ASF damage (Miles, 1932). It must be done
right after bloom. It is labour intensive but was adopted
widely in Europe in the 1970s under so-called ‘Super-
vised Control’ programs. A control threshold of ten
scars (primary damage, figure 5a) per 100 flower clus-
ters was recommended in The Netherlands (van Frank-
enhuyzen and Gruys, 1978; Gruys, 1980; Blommers,
2005), and 3-5% infested flowers in Germany (Heinze,
1978; Freier et al., 1992). Noack (1993) noted that ASF
could have a useful fruit thinning effect at lower infesta-
tion levels and recommends a threshold from 15-30
scars per 100 clusters when flowering is abundant down
to 5-10 in years with flower losses due to late spring
frosts. However, the selection of apples to thin will not
be based on the same criteria as the grower would
choose (Marc Trapman and Henrik Stridh, personal
communication).
For visual observations of egg development, six stages
were described in Dutch by Kuenen and van de Vrie
(1951) (figure 3e). Trapman (2016b) provided an Eng-
lish translation of key elements of this publication as
well as practical insights. Visual observations should
focus on the most vulnerable cultivars in correlation
with intensity and duration of the flight, as indicated by
daily trap catches. As the first ASF adults usually
emerge just before the first flowering cultivars, these
cultivars tend to suffer most attack. When monitoring
for ASF eggs, the egg laying behaviour of the adults
should be considered. The first eggs should be sought
on the king flowers of older branches (Kuenen and van
de Vrie, 1951; Gottwald, 1982; Tamošiūnas, 2014;
Trapman, 2016a). Southern and top parts of the tree as
well as isolated branches and distal parts of branches are
most attacked (Soenen, 1952).
Modelling
The first attempts to improve timing of monitoring
and control of the ASF with help of biologically-based
algorithms were initiated in Switzerland and The Neth-
erlands (van den Ende et al., 1996; Graf et al., 1996a;
1996b; Zijp and Blommers, 1997). These algorithms
assume that the time spent in a developmental stage
(egg, larva, pupa, adult) is inversely related to ambient
temperature above a fixed threshold (Andrewartha and
Birch, 1954). After determining post-diapause devel-
opment times at various constant temperatures in the
laboratory, Graf et al. (1996a) constructed a soil tem-
perature-driven model for adult emergence. A threshold
of 4.5 °C and an average temperature sum (thermal con-
stant, TC) of 205 and 220 day-degrees (DD), for fe-
males and males, respectively, yielded the best fit both
in emergence cages and with captures on white sticky
traps positioned in apple trees. In a Dutch orchard, the
first trap captures of adults could be described by a sim-
ple TC based on temperatures taken at 5 cm depth in the
soil. The most accurate was 134 DD (> 4 °C) accumu-
lated from April 1st until the first capture of adults (Zijp
and Blommers, 1997). Similar figures were obtained in
two orchards (one organic and one conventional) in
Lithuania (Tamošiūnas and Valiuškaité, 2013), and in
12 assessments (i.e. orchards or years) in a few organic
orchards in Sweden (Sjöberg et al., 2015).
Graf et al. (1996c) found that the temperature-
dependent post-diapause development of prepupae from
different European regions differed significantly. The
TC increased from South to North, from 194 DD in
South Tirol (Italy) to 228 DD in Schleswig-Holstein
(Germany), while the development threshold appeared
to be the same everywhere (i.e. 4.5 °C). Inclusion of
winter dormancy to improve the models was recom-
mended by Graf et al. (1996c) because, while the lower
temperature threshold for post-diapause development is
rarely reached under natural conditions before the end
of diapause (in early March), earlier exposure to higher
temperature appeared to reduce the duration of post-
diapause development. Tauber and Tauber (1986) dis-
47
cuss this apparent conflict between the effects of low
versus elevated temperature around the end of winter
diapause.
Comparing various approaches, Tamošiūnas and Vali-
uškaité (2013) noted great differences in temperature
sums based on air temperature between years. They
found that a TC > 4 °C at a soil depth of 10 cm gave the
best fit with the flight curve based on white trap cap-
tures, while a TC of 160 DD of air temperature > 4 °C
starting on April 1st should be the best choice in prac-
tice.
Trapman (2016a) constructed a Dynamic Simulation
Model (DSM) by collecting and analysing large data
sets on temperature-related development and activity of
ASF adults in The Netherlands and Belgium, from the
emergence of ASF adults to the time of pesticide appli-
cation, notably Quassia®, targeting young larvae. The
first capture of adults on white traps varied between
April 5 and May 2 in 42 observation events in 2003-
2015 and the average temperature sum from March 15
to flight initiation was 181 DD > 4 °C (Standard devia-
tion = 4.2 days). This was slightly higher than the 177
DD reported by Zijp and Blommers (1997), and also
higher than the 169 DD > 4 °C found by Sjöberg et al.
(2015). Trapman (2016a) used life-table data for post-
diapause development, female lifespan and the duration
of the fecundity period determined by Graf et al. (2001;
2002). He also estimated and roughly validated tem-
perature sums for the migration of larvae from the ini-
tially affected fruitlet to the second one. Weather condi-
tions suitable for flight and egg deposition were as-
sumed to be similar to those for plum sawflies
(Wildbolz and Staub, 1986) and the female egg stock
was assumed to be a non-limiting factor. The simulation
model uses ‘first flowers open’ (BBCH60) as ‘cultivar-
local’ biofix for the start of egg deposition on that culti-
var.
To validate the ASF-DSM, the outcome was com-
pared with the actual situation in up to 44 orchards an-
nually in four European countries from 2010 to 2015
(Trapman, 2016b). The difference between a simulated
2% egg hatch (the suggested time for treatment) and the
application date of Quassia® as advised by an expert
was 0.69 days on average, and rarely exceeded ± 2 days.
Therefore, the modelled estimate was precise enough
for decision making and might reduce the need for field
observations of ASF egg hatching.
Chemical control
The ASF is susceptible to a broad range of pesticides.
Organic insecticides like rotenone and quassia were the
first used in the 1940s, followed by organochlorines,
notably DDT and lindane. Nicotine was demonstrated to
exert larvicidal effects by McKinlay (1950). The organ-
ophosphates and carbamates were dominant options
from the 1950s to the 2000s. For example, up to 15 of
these insecticides (azinphos-methyl, bromophos, car-
baryl, chlordimeforn + formetanate, dichlorvos, dime-
thoate, endosulfan, methidathion, parathion, phentoate,
promecarb, propoxur, trichlorphon, vamidothion) were
listed against ASF in Germany (Heinze, 1978). Some of
these insecticides became instrumental in ‘supervised
control’ in the 1970s and IPM in the 1980s, as they al-
lowed some fine tuning because of their different toxici-
ties for various pests and natural enemies (Blommers,
1994; 2005). Following the ban of organophosphates
and carbamates in the European Union in the 1990s, ne-
onicotinoids (imidacloprid, thiacloprid, acetamiprid)
became the most commonly used insecticides for ASF
control. Field experiments in organic orchards in Poland
conducted with extracts from the wood of Quassia ama-
ra and from the seeds of Azadirachta indica (commer-
cial formulation NeemAzal-T/S) gave variable results
(Danelski et al., 2014).
In general, the literature shows that the best applica-
tion time is shortly after bloom, before the eggs start to
hatch. For the most part, pesticide applications during
bloom are forbidden or not recommended because of
potential detrimental effects on pollinators. However,
some compounds have been reported to be effective
while reasonably safe for honeybees. For instance, the
nereistoxin thiocyclam hydrogen oxalate (Evisect™),
while not harmful to honey bees (Gerig, 1977), gave ad-
equate control of the ASF in field tests (Helsen and
Blommers, 1988) and is registered for this use in Swit-
zerland. In Hungary, sprays with the insecticide g-BHC
after petal fall reduced fruit damage by 82% compared
to the control (Nagy, 1954).
Applied immediately before flowering, the systemic
fungicide Topsin M (thiophanate-methyl) completely
inhibits larval hatching (Predki and Profic-Alwasiak,
1976). Its breakdown product, methyl benzimidazol-2-
yl carbamate (Vonk and Sijpestein, 1971), is accumulat-
ed in the fruit skin. This was confirmed by applications
against apple scab and powdery mildew in the rosy-bud
stage in IPM practice (Leo H. M. Blommers, personal
observation). Applied at the peak of the ASF adult flight
(i.e., at the pink bud stage), the fungicides fenarimol,
cyproconazole+captan and thiophanate-methyl were
found to be effective in reducing fruit damage (Olszak
and Maciesiak, 1996). Partial or even full control of the
ASF may also be achieved by treatments against other
pests. For instance, diflubenzuron applied against win-
termoth, Operophtera brumata (L.) (Lepidoptera Ge-
ometridae), or noctuids (Orthosia sp.) (Lepidoptera
Noctuidae) and thiacloprid against aphids will decimate
ASF populations (Erdelen, 2001; Galli and Nikusch,
2005; OMAFRA, 2017; DEFRA/ADHB, 2018).
In organic orchards in Pennsylvania, the ASF is a se-
rious concern. The best option for organic orchards is to
spray Surround (active ingredient = kaolin clay) mixed
with either Pyganic® (active ingredient = 5% pyrethrins)
or Venerate® (active ingredient = heat-killed Burkhold-
eria). These two mixtures should be applied before and
immediately after bloom (Greg Krawczyk, personal
communication).
In European organic orchards, the most commonly
used insecticide is an extract of “Quassia wood”, origi-
nating either from Quassia amara or Picrasma excelsa
(Wijnen et al., 1994; Kienzle et al., 2008). The main
active ingredient, quassin, has a short residual life and
works best on the neonate larvae, which must feed on
the product before they enter the fruit (Kienzle et al.,
2005). As a result, correct timing of the application and
48
good coverage of the receptacles is crucial to effect op-
timal larval mortality. Another obstacle to reliable effi-
cacy is the variability in active ingredient contents of
the base product, traditionally leading to erratic efficacy
of home-made extracts. Standardization of the quassin
contents in commercial products has greatly improved
the reliability of these formulations (Kienzle et al.,
2008). Quassia® was submitted for registration in the
EU in 2012.
Occasionally, natural pyrethrum, synergized with pip-
eronyl butoxide, is used for ASF management (Kienzle
et al., 2008). Self-made concoctions of common tansy
(Tanacetum vulgare), also containing pyrethrum-like
chemicals, or common wormwood (Artemisia vulgare),
are recommended against ASF larvae in France. Lack of
exclusivity precluded development, registration and
marketing of these insecticidal plant extracts (e.g.,
EFSA, 2014). Some may have a small local and tempo-
rary market, but as different plant species might be in-
volved, the quality of the plant source material is gener-
ally poorly defined in terms of insecticidal and health
properties (Zimmer, 2000; Sjöberg et al., 2015).
Side effects of insecticides on biocontrol agents
The statement that parasitism by L. ensator is higher
in orchards where less insecticide has been used
(Babendreier, 1998) is not surprising because adult
L. ensator emerge soon after flowering and may be af-
fected by post-bloom application of pesticides. In fact,
well-timed application of a selective or short-lived
compound like Quassia should be recommended, as it
resulted in high level of parasitism in The Netherlands
(L. H. M. Blommers, unpublished).
Studies suggest that applications of synthetic pyre-
throids, neonicotinoids and sulphur should be avoided
during the flight of L. ensator. In the 1990’s, the near
absence of L. ensator in organic orchards was probably
due to the application of large amounts of wettable sul-
phur against apple scab in organic orchards in The
Netherlands (Zijp and Blommers, 2002a).
Biological control
Parasitoids
In a classical biological control program from 1995 to
2001, L. ensator (figure 8a-c) was first established in
Frelighsburg, Quebec, following yearly releases of
adults (figure 8a) that emerged from parasitized cocoons
(figure 9b) collected in Western Europe (Vincent et al.,
2001; 2002). From there it has been successfully dis-
seminated in five localities of Quebec and Ontario (Vin-
cent et al., 2013; 2016) and in other orchards of south-
ern Quebec (Jacques Lasnier, personal communication).
As of 2018, it is the only documented natural enemy of
ASF in North America.
Nematodes
In Poland, Jaworska and Stanuszek (1986) applied
four doses of Heterorhabditis sp. (5 - 50 per pupa) on
filter paper rolled around ASF pupae and found infec-
tion rates of 100%.
In Quebec, Vincent and Bélair (1992) conducted bio-
assays with Steinernema carpocapsae (Weiser) DD 136
and All strains, Steinernema feltiae (Filipjev) and Het-
erorhabditis bacteriophora Poinar. The DD 136 strain
caused highest mortality of ASF larvae after 24 hours
(86% mortality), while all nematode species caused
100% larval mortality after 72 hours. A single treatment
with S. carpocapsae All strain caused significant larval
mortality (> 82% vs 5.8-9.5% control). The S. car-
pocapsae All strain applied in May-June as foliar sprays
was evaluated against the ASF and plum curculio,
C. nenuphar (Bélair et al., 1998). Inconsistency of re-
sults and high costs for production and application so
far preclude the use of this nematode against these pests
in commercial apple orchards. Nematodes can be an in-
secticide-free option to manage the ASF in small or-
chards or private gardens where the use of pesticides is
prohibited.
Fungi
Laboratory tests gave promising results for fungi as a
control agent against H. testudinea. Jaworska (1979a)
tested the pathogenicity of eight entomopathogenic fun-
gi by spraying spores on fifth instars (parasitized or not
by Lathrolestes sp.), and cocoons containing prepupae
on filter paper discs in Petri dishes. The fungi P. fu-
moso-roseus, P. farinosus, Cephalosporium lecanii
Zim., Aspergillus flavus Link ex Fries, B. bassiana,
Beauveria tenella (Delac.) Siem. and Metarrhizium an-
isopliae (Metsch.) Sorok caused greater mortality (=
58%) than the control (= 13%) among unparasitized and
parasitized fifth instars. In contrast, Scopulariopsis
brevicaulis Bainier caused no statistically greater mor-
tality than the control. Up to 100% mortality of fifth in-
stars within 7 days after treatment was caused by P. fu-
moso-roseus, P. farinosus and C. lecanii. However,
treatment of cocoons with fungal spores did not cause
significant differences in mortality compared with the
control.
During 4 years of field experiments, Jaworska (1979b)
studied the pathogenicity of eight species of entomoge-
nous fungi to the ASF in the soil. P. fumoso-roseus and
P. farinosus caused the highest mortality of ASF larvae
during their diapause. Lower mortality, but still signifi-
cantly more than in control, was caused by C. lecanii,
A. flavus, B. bassiana, B. tenella and M. anisopliae.
Scopulariopsis brevicaulis caused no greater mortality
than the control. In addition, adult female ASF that sur-
vived treatment with the fungi A. flavus, B. bassiana
and B. tenella had fewer developed eggs on the first day
of flight (Jaworska, 1979c) and their fertility and
lifespan was significantly reduced compared with con-
trol females.
In a laboratory study, B. bassiana or M. anisopliae
caused high ASF larval mortality (49.4-68.4%)
(Świergiel et al., 2016). However, Świergiel et al.
(2016) could not replicate these results in full scale field
experiments in a Swedish organic orchard using the
highest recommended soil application dose of B. bassi-
ana (5.37 × 1010 CFU per m2), as they observed only
17% mortality of the recovered cocoons. They suggest-
ed that low humidity in drip irrigated orchards, and pos-
49
sibly fungistatic effects by either antibiosis or frequent
sulphur applications, may have contributed to lower
mortality rates.
In conclusion, the effectiveness of fungi applied to the
soil to reduce ASF populations depends on soil mois-
ture, antibiosis and the period with temperatures favour-
able for infection (Jaworska, 1979a; 1979b; 1979c;
Świergiel et al., 2016). The importance of some factors
such as the critical temperature at the depth under-
ground of the descending prepupae is unclear (Zim-
mermann, 1986; Jaronski, 2007).
Little is known about pathogens applied against the
immature stages of ASF while on the tree. Prieditis and
Rituma (1974) tested a mixture of B. bassiana (1.3-1.8
kg per ha) and carbaryl or trichlorphon which resulted
in 73-86% control of H. testudinea. Bacillus thurin-
giensis applied at 0.4-0.7% mixed with carbaryl or tri-
chlorphon was ineffective. Applied before bloom, the
formulation Thuricide 90 TS (Bacillus thuringiensis ser.
kurstaki) had no significant effect on the ASF (Niez-
borala, 1972, in Jaworska, 1987). A preparation of
P. fumoso-roseus of homopteran origin and devised for
whitefly control (Preferal™), applied during both flight
and egg hatch of ASF had no effect (L. H. M. Blom-
mers, unpublished).
Other pathogens
In their review, Cross et al. (1999a) did not mention
other microbials or viruses that were researched as tools
to manage the ASF.
Concluding remarks
Published information about ASF outbreaks and man-
agement shows that H. testudinea needs to be managed
in most commercial orchard in which it has established,
both in its native area of Europe, and in regions it has
invaded like eastern North America. The explanation of
ASF outbreaks remains difficult and preventive action a
distant hope.
Consideration for the fruit is as important as the ASF
itself with respect to monitoring and damage forecast-
ing. In contrast to other pests like leafrollers or scales
which appear and attack irrespective of host phenologi-
cal stage, the ASF begins its life when the fruitlet is
available. Instead of calculating the day of first adult
appearance, one may consider, or estimate as did Trap-
man (2016b), the opening of first apple flowers as the
beginning of the new ASF generation.
At the time of adult emergence, it would be useful to
know the density of female ASF. However, this is diffi-
cult as some pupae will stay in diapause underground
for another year at least, while others have been or are
being killed underground by parasitoid, disease or both.
Observations in The Netherlands have shown that, in
absence of control measures, ASF populations may
double each year in well-managed orchards (Blommers,
2005), while observations in Denmark in unsprayed
commercial orchards indicate both smaller and larger
yearly increases possibly due to shifting local conditions
such as presence of natural enemies (Weronika
Świergiel, personal observation). This situation could be
worse in North America, where the ASF is an exotic
pest. Fortunately, adult densities estimated by means of
white sticky traps can be used to assess whether later
field counts of eggs or stings to fruitlets would be sensi-
ble.
The interpretation of trap captures tends to be compli-
cated, as commercial apple orchards are typically mixes
of cultivars positioned in particular spatial arrangement
with respect to flowering time and cross-pollination
compatibility. As flowers are abundant normally in
commercial plantings and the ASF have limited mobili-
ty, population density in any part of an orchard should
be determined mainly by the history of ASF attack and
management in that part.
As a rule, ASF adults start to emerge just before early
cultivars begin flowering, and plots of these early culti-
vars tend to remain the most infested over years. How-
ever, clear differences in susceptibility to ASF attack
between cultivars have never been shown. In fact, if
they exist, they are almost impossible to establish, as the
attack itself takes only a few days during an outburst of
flowers under otherwise unpredictable conditions, while
most eggs and young larvae disappear, due to natural
control of some kind, within about two weeks (Zijp and
Blommers, 2002b). The impossibility to relate egg pro-
duction with available protein in the food is one im-
portant handicap in field research of the ASF. This
might perhaps be partially overcome by researching the
causes of this high mortality of eggs and larvae.
As far as is known, two larval parasitoids exert most
natural control of ASF: the specialized larval parasitoid
L. ensator and, in Europe, the more polyphagous co-
coon parasitoid A. nigrocincta. These species, when
present, may eliminate substantial numbers of host, alt-
hough L. ensator has only a brief post-bloom period
available to attack its larval host. During that critical
period, L. ensator may be affected by unfavourable
weather conditions and by chemical treatments. Devel-
opment of sprayable disease agents is hindered by the
difficulty of rearing the ASF. In summary, there is cur-
rently no biological agent known that can be deliberate-
ly managed to achieve substantial control the ASF. So
far, most published information concerns situations
where ASF reached high densities. Studies in situations
where ASF densities are low and in absence of chemical
control are clearly missing.
While control of ASF in Europe was straightforward
for several decades when broad- spectrum insecticides
were in general use, development of orchard IPM as
well as the increase of organic fruit growing restored
ASF’s pre-World-War-II pest status. Moreover, due to
increased consumer awareness, increased scrutiny and
standards of regulatory agencies such as the EU, and
marketing criteria implemented by supermarkets, the
choice of broad spectrum pesticides is decreasing.
Most studies on biocontrol of ASF with entomopatho-
genic nematodes were published more than 20 years
ago. Recently, projects were undertaken in Germany to
target ASF larvae that search for pupation sites or ASF
females before they lay eggs (Ralf Udo Ehlers, personal
communication). It might also be worthwhile to re-
50
search the use of entomopathogenic fungi, following up
on Jaworska (1979b; 1992) who reported high ASF pu-
pal mortality in semi-field trials. However, as the out-
come of field studies by Świergiel et al. (2016) were
less positive, it would be interesting to test the hypothe-
sis that the fungicidal effect of sulphur accumulating in
the soil after frequent high dose applications of this el-
ement in organic orchards is a major factor for reduced
effectiveness of fungal agents.
While a decreasing choice of chemical control options
is expected to promote the ASF as major pest, recent de-
velopments towards plantings of supercolumn/columnar
apple trees in combination with mechanical/cultural pro-
tection against hail, storms and replant disease, might
open opportunities to exclude ASF from the orchards.
As the duration of adult ASF flight is less than 2-3
weeks, such a “greenhouse approach” might be promis-
ing.
Acknowledgements
An early draft of this paper has been written by Jan-Piet
Zijp, with the help of Charles Vincent and Leo Blom-
mers in 1995, but remained unfinished. We thank the
State Department of Canada for translating Tchakstynia
(1968) and Dulak-Jarworska (1976) respectively from
Russian and Polish. Benoit Rancourt and Jérémie Côté
(Agriculture and Agri-Food Canada, Saint-Jean-sur-
Richelieu, Quebec, Canada) are thanked for their tech-
nical input. We thank Greg Krawczyk (Penn State Uni-
versity, Biglerville, Pennsylvania, USA), Jacques Las-
nier (Co-Lab R & D, Granby, Quebec, Canada), Chris
Bergh (Virginia Tech, Blacksburg, Virginia, USA) and
Leslie Farmer (Pest Management Centre, Agriculture
and Agri-Food Canada, Ottawa, Ontario) for comments
of the manuscript, and Marko Prous (Senckenberg
Deutsches Entomologisches Institut, Munich, Germany)
for information on ASF identification. We have greatly
benefited from the vast experience of Marc Trapman
(Private advisor, The Netherlands) in the management
and control of ASF, also in connection with other pests
and diseases, in the context of integrated pest manage-
ment and organic pest control of pome fruit in The Neth-
erlands and neighbouring countries during three decades.
Charles Vincent acknowledges a Fellowship from the
Programme of the Netherlands Ministry of Agriculture,
Nature Management and Fisheries as well as financial
support by the Pest Management Centre, Agriculture
and Agri-Food Canada, Ottawa, Ontario, Canada.
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Authors’ addresses: Charles VINCENT (corresponding au-
thor: charles.vincent2@canada.ca), Horticultural Research and
Development Centre, Agriculture and Agri-Food Canada, 430
Gouin Blvd., Saint-Jean-sur-Richelieu, Quebec, Canada J3B
3E6; Dirk BABENDREIER (d.babendreier@cabi.org), Integrated
Crop Management Advisor, CABI, Rue des Grillons 1,
CH-2800 Delémont, Switzerland; Weronika ŚWIERGIEL
(weronika@biobasiq.se), Sveriges Lantbruksuniversitet/ Swe-
dish University of Agricultural Sciences, Institutionen för
Växtskyddsbiologi/ Department of Plant Protection Biology,
P.O. Box 102, SE-230 53 Alnarp, Sweden; Herman HELSEN
(herman.helsen@wur.nl), Wageningen University & Research,
P.O. Box 200, 6670 AE Zetten, The Netherlands; Leo H. M.
BLOMMERS (hlblomme@xs4all.nl), Willibrordweg 6, 3911CC
Rhenen, The Netherlands (Formerly: Plant Research Interna-
tional, Wageningen, The Netherlands).
Received October 16, 2018. Accepted February 4, 2019.
